36
Submitted 10 March 2019 Accepted 24 February 2020 Published 6 April 2020 Corresponding authors Jorge A. Herrera-Silveira, [email protected] Sara M. Morales-Ojeda, [email protected] Academic editor Roger Jones Additional Information and Declarations can be found on page 25 DOI 10.7717/peerj.8790 Copyright 2020 Herrera-Silveira et al. Distributed under Creative Commons CC-BY 4.0 OPEN ACCESS Blue carbon of Mexico, carbon stocks and fluxes: a systematic review Jorge A. Herrera-Silveira 1 , Monica A. Pech-Cardenas 1 , Sara M. Morales-Ojeda 1 , Siuling Cinco-Castro 1 , Andrea Camacho-Rico 1 , Juan P. Caamal Sosa 1 , Juan E. Mendoza-Martinez 1 , Eunice Y. Pech-Poot 1 , Jorge Montero 1 and Claudia Teutli-Hernandez 2 1 Departamento Recursos del Mar, Centro de Investigación y de Estudios Avanzados (CINVESTAV) del Instituto Politécnico Nacional Unidad Mérida, Mérida, Yucatán, México 2 Laboratorio de Ecología, Unidad Multidisciplinaria de Docencia e Investigación de la Facultad de Ciencias, Unidad Sisal, Universidad Nacional Autónoma de México, Mérida, Yucatán, México ABSTRACT Mexico has more than 750,000 ha of mangroves and more than 400,000 ha of seagrasses. However, approximately 200,000 ha of mangroves and an unknown area of seagrass have been lost due to coastal development associated with urban, industrial and tourist purposes. In 2018, the approved reforms to the General Law on Climate Change (LGCC) aligned the Mexican law with the international objectives established in the 2nd Article of the Paris Agreement. This action proves Mexico’s commitment to con- tributing to the global target of stabilizing the greenhouse gas emissions concentration in the planet. Thus, restoring and conserving mangrove and seagrass habitats could contribute to fulfilling this commitment. Therefore, as a first step in establishing a mitigation and adaptation plan against climate change with respect to conservation and restoration actions of these ecosystems, we evaluated Mexican blue carbon ecosystems through a systematic review of the carbon stock using the standardized method of Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). We used the data from 126 eligible studies for both ecosystems (n = 1220). The results indicated that information is missing at the regional level. However, the average above and below ground organic carbon stocks from mangroves in Mexico is 113.6 ± 5.5 (95% CI [99.3–118.4]) Mg C org ha -1 and 385.1 ± 22 (95% CI [344.5–431.9]) Mg C org ha -1 , respectively. The variability in the C org stocks for both blue carbon ecosystems in Mexico is related to variations in climate, hydrology and geomorphology observed along the country’s coasts in addition to the size and number of plots evaluated with respect to the spatial cover. The highest values for mangroves were related to humid climate conditions, although in the case of seagrasses, they were related to low levels of hydrodynamic stress. Based on the official extent of mangrove and seagrass area in Mexico, we estimate a total carbon stock of 237.7 Tg C org from mangroves and 48.1 Tg C org from seagrasses. However, mangroves and seagrasses are still being lost due to land use change despite Mexican laws meant to incorporate environmental compensation. Such losses are largely due to loopholes in the legal framework that dilute the laws’ effectiveness and thus ability to protect the ecosystem. The estimated emissions from land use change under a conservative approach in mangroves of Mexico were approximately 24 Tg CO 2 e in the last 20 years. Therefore, the incorporation of blue carbon into the carbon market as a viable source of supplemental finance for mangrove and seagrass protection is an attractive win-win opportunity. How to cite this article Herrera-Silveira JA, Pech-Cardenas MA, Morales-Ojeda SM, Cinco-Castro S, Camacho-Rico A, Caamal Sosa JP, Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic review. PeerJ 8:e8790 http://doi.org/10.7717/peerj.8790

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Page 1: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Submitted 10 March 2019Accepted 24 February 2020Published 6 April 2020

Corresponding authorsJorge A Herrera-SilveirajorgeherreracinvestavmxSara M Morales-Ojedasaramoralescinvestavmx

Academic editorRoger Jones

Additional Information andDeclarations can be found onpage 25

DOI 107717peerj8790

Copyright2020 Herrera-Silveira et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Blue carbon of Mexico carbon stocksand fluxes a systematic reviewJorge A Herrera-Silveira1 Monica A Pech-Cardenas1 Sara M Morales-Ojeda1Siuling Cinco-Castro1 Andrea Camacho-Rico1 Juan P Caamal Sosa1Juan E Mendoza-Martinez1 Eunice Y Pech-Poot1 Jorge Montero1 andClaudia Teutli-Hernandez2

1Departamento Recursos del Mar Centro de Investigacioacuten y de Estudios Avanzados (CINVESTAV) delInstituto Politeacutecnico Nacional Unidad Meacuterida Meacuterida Yucataacuten Meacutexico

2 Laboratorio de Ecologiacutea Unidad Multidisciplinaria de Docencia e Investigacioacuten de la Facultad de CienciasUnidad Sisal Universidad Nacional Autoacutenoma de Meacutexico Meacuterida Yucataacuten Meacutexico

ABSTRACTMexico hasmore than 750000 ha ofmangroves andmore than 400000 ha of seagrassesHowever approximately 200000 ha of mangroves and an unknown area of seagrasshave been lost due to coastal development associated with urban industrial and touristpurposes In 2018 the approved reforms to the General Law on Climate Change(LGCC) aligned the Mexican law with the international objectives established in the2nd Article of the Paris Agreement This action proves Mexicorsquos commitment to con-tributing to the global target of stabilizing the greenhouse gas emissions concentrationin the planet Thus restoring and conserving mangrove and seagrass habitats couldcontribute to fulfilling this commitment Therefore as a first step in establishing amitigation and adaptation plan against climate change with respect to conservation andrestoration actions of these ecosystems we evaluated Mexican blue carbon ecosystemsthrough a systematic review of the carbon stock using the standardized method ofPreferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) Weused the data from 126 eligible studies for both ecosystems (n= 1220) The resultsindicated that information is missing at the regional level However the average aboveand below ground organic carbon stocks from mangroves in Mexico is 1136 plusmn 55(95 CI [993ndash1184]) Mg Corg haminus1 and 3851 plusmn 22 (95 CI [3445ndash4319]) Mg Corghaminus1 respectively The variability in the Corg stocks for both blue carbon ecosystemsin Mexico is related to variations in climate hydrology and geomorphology observedalong the countryrsquos coasts in addition to the size and number of plots evaluated withrespect to the spatial cover The highest values for mangroves were related to humidclimate conditions although in the case of seagrasses they were related to low levelsof hydrodynamic stress Based on the official extent of mangrove and seagrass areain Mexico we estimate a total carbon stock of 2377 Tg Corg from mangroves and481 Tg Corg from seagrasses However mangroves and seagrasses are still being lostdue to land use change despite Mexican laws meant to incorporate environmentalcompensation Such losses are largely due to loopholes in the legal framework thatdilute the lawsrsquo effectiveness and thus ability to protect the ecosystem The estimatedemissions from land use change under a conservative approach inmangroves ofMexicowere approximately 24 TgCO2e in the last 20 years Therefore the incorporation of bluecarbon into the carbonmarket as a viable source of supplemental finance for mangroveand seagrass protection is an attractive win-win opportunity

How to cite this article Herrera-Silveira JA Pech-Cardenas MA Morales-Ojeda SM Cinco-Castro S Camacho-Rico A Caamal Sosa JPMendoza-Martinez JE Pech-Poot EY Montero J Teutli-Hernandez C 2020 Blue carbon of Mexico carbon stocks and fluxes a systematicreview PeerJ 8e8790 httpdoiorg107717peerj8790

Subjects Ecology Ecosystem Science Climate Change Biology Natural Resource ManagementEnvironmental ImpactsKeywords Blue carbon Mangroves Seagrasses Carbon stocks Climate change

INTRODUCTIONCoastal ecosystems are critical for the maintenance of biodiversity and human well-being by providing diverse benefits and ecosystem services including protection againststorms and mean sea level rise as well as the prevention of coastal erosion water qualityregulation nutrient recycling and provision of habitats for high diversity commercialspecies among others (Gautier Amador amp Newmark 2001 Kathiresan amp Rajendran 2005Mazda Kobashi amp Okada 2005 Alongi 2008 Bouillon amp Connolly 2009 Koch et al 2009Wang et al 2010 Yulianto Soewardi amp Adrianto 2016)

Mangroves seagrasses and salt marshes are known as blue carbon ecosystems theysequester greenhouse gases and store more organic carbon over the long term per unit areathan terrestrial forests and they are now recognized for their role in the climate changemitigation (Pendleton et al 2012) Despite these benefits blue carbon ecosystems areamong the most threatened ecosystems and their relatively low coverage lt05 (Duarteet al 2013) is the result of natural fragility and human-induced impacts

International groups such as the Intergovernmental Panel on Climate Change (IPCC)have begun to recognize the climatemitigation value of these ecosystems and included themin the 2016 update to the 2003 Wetlands Supplement (IPCC 2014) At an internationallevel it has been recognized that Corg sequestration and storage in the vegetation andsoil of blue carbon ecosystems could be a key component of mitigation strategies in theface of climate change Thus actions that conserve restore and sustainability use coastalwetlands are needed to avoid emissions and maintain (and where possible enhance) coastalwetland sequestration and storage These actions contribute to global and national carbonmanagement and increase the resilience of the socioecological ecosystem (Wolanski et al2004 Saintilan et al 2013 Sutton-Grier amp Moore 2016 Lovelock Fourqurean amp Morris2017Macreadie et al 2017)

Mexico has one of the largest extensions of blue carbon ecosystems and is among theareas with the greatest coverage in the tropical and subtropical Western HemisphereThe Mexican Federal Government reports 755555 ha of mangrove and 461059 ha ofseagrasses (Valderrama-Landeros et al 2017 CONABIO 2018) However estimationsof their extensions have varied over time according to the precision of the methods(aerial photos satellite images number of sites verified lsquolsquoin sitursquorsquo) and special attentionis required for seagrasses due to the scarce reports on their extension which differsignificantly (Table 1) For mangroves Mexicorsquos main species are Rhizophora mangleAvicennia germinans and Laguncularia racemosa (Valderrama-Landeros et al 2017) andfor seagrasses the main species are Halodule wrightii Syringodium filiforme Thalassiatestudinum and Zostera marina (CONABIO 2018)

Recently academia nongovernmental organizations and governmental groups havecreated synergies to increase scientific knowledge concerning blue carbon ecosystems and

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 236

Table 1 Reported extension for Mexicanmangroves and seagrasses in the last 48 years (1970ndash2018)

Period (decade) Mangroves extension (ha) Seagrass extension (ha) References

1970ndash1980 14200001

11240002

8564053

ndash 1 2 3

1981ndash1990 9856002

8555663ndash 23

1991ndash2000 9328004

8850002ndash 2 4

2001ndash2010 8200002

7741343

7738543

7647743

6882307 2 3 7

2011ndash2018 7419176

9395218

7755553

91930010

456059ndash461058113 6 8 10 11

NotesData from 1Flores et al (1971) 2FAO (2007) 3Valderrama-Landeros et al (2017) 4Spalding Blasco amp Field (1997) 6Giri et al (2011) 8INEGI (2014) 7Green amp Short (2003)10CCA (2016) 11CONABIO (2018)

the Corg reserves of several ecosystems have been quantified and mapped (Caamal-Sosaet al 2011 Adame et al 2013 Ramiacuterez-Ramiacuterez Medina-Goacutemez amp Herrera-Silveira 2015Adame amp Fry 2016 Ezcurra et al 2016 Kauffman et al 2016 Medina-Goacutemez et al 2016Cinco-Castro et al 2017 Ochoa-Goacutemez et al 2019) In this systematic review we checkedmore than 150 reports with data related to blue carbon stocks and fluxes in Mexico (Fig 1)

The storage and fluxes of Corg in blue carbon ecosystems mainly depend on thecommunity structural characteristics and extensions which are the result of the addition ofparticularities of climate geomorphology hydrology and human land use InMexico thereis a natural and human-induced heterogeneity along the 11592 km (De la Lanza EspinoPeacuterez amp Peacuterez 2013) of coast resulting in a mosaic of spatial and structural arrangements ofmangrove and seagrass communities Traditionally management schemes do not considerall the abovementioned criteria

In the case of seagrasses both the bathymetry gradient and coastal current velocitiesinfluence the water transparency which is one of the key variables for seagrass developmentThe variability in water transparency is a factor related to the morphometric characteristicsof the plants which determine the above ground Corg assessments of this ecosystem(Fourqurean et al 2012a) However Mexico has insufficient information on seagrasses atthe high spatial resolution required for use as a reference criterion for seagrass zonationCurrently theMexican government is requesting information frommangrove and seagrassCorg stocks under different criteria that allow for the development of conservation andrestoration policies at different scales (INECC 2018) In this context it is necessary toconsider the ecological and environmental scenarios in which mangroves and seagrassesdevelop to improve local regional and national carbon inventories

Mexico ranks 13 in the list of countries with the largest CO2 emissions (IEA 2014)derived from the use and burning of fossil fuels representing 137 of global emissionsin 2012 however and unknown amount of CO2 emissions is contributed by degraded or

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 336

Figure 1 PRISMA flow diagram of the literature selection process for the systematic review of Mexicanblue carbon stocks and fluxes FromMoher et al (2009b)

Full-size DOI 107717peerj8790fig-1

destroyed blue carbon ecosystems which are able to release the carbon they have storedfor centuries into the atmosphere and oceans and become sources of greenhouse gases(Pendleton et al 2012) It has been estimated by experts that as much as 102 billion tonsof carbon dioxide are being released annually from degraded coastal ecosystems whichis equivalent to 19 of emissions from tropical deforestation globally (Pendleton et al2012) Changes in the coverage of Mexicorsquos blue carbon ecosystems over time and theirrelation to changes in land use have been difficult to quantify due to the lack of long-termevaluation programs

Mexico is one of the 175 countries that have signed onto the Paris Agreement and it hascommitted to lsquolsquoincrease carbon capture and coastal protection with the implementation ofconservation and recovery schemes for coastal and marine ecosystems such as coral reefsmangroves seagrasses and dunesrsquorsquo throughMexicorsquos Nationally Determined Contributionwith theAdaptation category (INECC 2018)However insufficient data have been collected

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 436

inMexico andno complete synthesis of themitigation value or the greenhouse gases (GHG)emissions related to mangroves and seagrasses existed until now This comprehensivereview is a first step in providing a tool for decisionmakers to develop efficient strategiesaimed at reducing carbon emissions from the loss of these ecosystems while also protectingcurrent levels of carbon capture and storage as well the many ecosystem services providedby mangroves and seagrasses

METHODSA systematic reviewwas conducted at the country level to assess the carbon stocks and fluxesof blue carbon ecosystems in Mexico We use the Preferred Reporting Items for SystematicReviews and Meta-Analyses (PRISMA) (Fig 1) framework and protocols (Moher et al2009a)

Information sources and search strategyAn electronic literature search was performed for carbon stocks and carbon fluxes inmangroves and seagrasses fromMexico We use PubMed (MEDLINE) and Web of Scienceas the primary sources for searches and include open access publications Google Scholarwas a secondary source used to acquire additional literature (thesis technical reports)and the inclusion of gray literature is recommended for systematic reviews to minimizepublication bias (Koricheva Gurevitch amp Mengersen 2013 Pullin amp Stewart 2006)

We also include published databases on Corg stocks from Herrera-Silveira et al (2018a)and Herrera-Silveira et al (2018b) and the Mexican Carbon Program (PMC) which havebeen validated and reviewed by experts and organizations of the federal governmentand civil society (CONABIO and CONAFOR) and subjected to public consultation(httppmcarbonoorgpmc) In the initial phase titles and abstracts from network werescreened to identify potential eligible studies In the second phase full texts of the remainingarticles were read to determine if they meet the inclusion and exclusion criteria Whendisagreement emerged regarding the eligibility of studies the main author Jorge A HerreraSilveira made the final decision

The search of carbon stocks and fluxes extended from 1987 to 2018 and includedkeywords (exclusively in Spanish and English) population (lsquolsquomangroversquorsquo OR lsquolsquoseagrassrsquorsquoOR lsquolsquoSubmerged aquatic vegetationrsquorsquo OR lsquolsquowetlandsrsquorsquo OR lsquolsquocoastal basinrsquorsquo OR lsquolsquocoastrsquorsquo)AND compartments (lsquolsquoForest structurersquorsquo OR lsquolsquoecosystem structurersquorsquo OR lsquolsquoDBHrsquorsquo ORlsquolsquobiomassrsquorsquo OR lsquolsquoabove groundrsquorsquo AND lsquolsquobiomassrsquorsquo OR lsquolsquobelow groundrsquorsquo AND lsquolsquobiomassrsquorsquoOR lsquolsquolitter productivityrsquorsquo OR lsquolsquocarbonrsquorsquo AND lsquolsquofluxrsquorsquo OR lsquolsquodecompositionrsquorsquo OR lsquolsquosoilrsquorsquo ANDlsquolsquocarbonrsquorsquo OR lsquolsquosoilrsquorsquo AND lsquolsquoorganic matterrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquoorganic matterrsquorsquo ORlsquolsquosoilrsquorsquo AND lsquolsquobulk densityrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquobulk densityrsquorsquo) AND lsquolsquolocationrsquorsquo (vglsquolsquoGulf of Mexicorsquorsquo OR lsquolsquoPacificrsquorsquo OR lsquolsquoYucatan Peninsularsquorsquo) OR lsquolsquoMexican CaribbeanrsquorsquoOR state names (vg lsquolsquoYucatanrsquorsquo OR lsquolsquoCampechersquorsquo lsquolsquoQuintana Roorsquorsquo OR lsquolsquoTabascorsquorsquo ORlsquolsquoVeracruzrsquorsquo OR lsquolsquoTamaulipasrsquorsquo OR lsquolsquoBaja California Surrsquorsquo OR lsquolsquoBaja California NortersquorsquoOR lsquolsquoSinaloarsquorsquo OR lsquolsquoOaxacarsquorsquo OR lsquolsquoChiapasrsquorsquo) OR specific site names (vg lsquolsquoLagunade Terminosrsquorsquo OR lsquolsquoMagdalena Bayrsquorsquo OR lsquolsquoSian Karsquoanrsquorsquo OR lsquolsquoLa Encrucijadarsquorsquo OR lsquolsquoLa

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 536

Mancharsquorsquo OR lsquolsquoLaguna Alvaradorsquorsquo OR lsquolsquoSanQuintiacuten Bayrsquorsquo OR lsquolsquoMarismasNacionalesrsquorsquo ORlsquolsquoCelestuacutenrsquorsquo OR rsquorsquo Laguna Madrersquorsquo OR lsquolsquoBarra de Navidadrsquorsquo OR lsquolsquoLaguna Mar Muertorsquorsquo)

The searches were undertaken independently by authors with at least five years ofexperience in sampling laboratory analysis and proven experience in data analysisand redaction of technical reports on blue carbon ecosystems The five researchers formangrove review were the coauthors Andrea Camacho-Rico Monica A Pech-CardenasSiuling Cinco-Castro for sediments were Eunice Y Pech-Poot and Juan P Caamal Sosaand for seagrasses were Juan E Mendoza-Mantiacutenez and Sara M Morales-Ojeda

Eligibility criteriaWe include studies and datasets that report the biomass organic carbon stock organicmatter and bulk density in sediments per unit of area and spatially referenced or flux datafrommangroves and seagrasses For mangroves an important criterion was the plot design(including at least three replicates) to guarantee the representativeness of the data forseagrasses we looked for studies that based their results on quadrants or cylindrical coresampler along transects No conference abstracts were considered to meet the inclusioncriteria

Data extraction and analysisData extraction was independently performed by authors (Andrea Camacho Rico MonicaA Pech -Cardenas Siuling Cinco-Castro Eunice Y Pech-Poot Juan P Caamal-Sosa JuanE Mendoza-Martinez and Sara M Morales Ojeda) Study-specific variables were recordedfor each entry Many properties assessed in this review were reported as contextualenvironmental data rather than the primary outcome for their respective studies (noreplicates or dispersion measures described) which was why bias was not reported inthis study We include entries such as geographic location and region (according toValderrama-Landeros et al 2017) environmental characteristics including ecological type(Lugo amp Snedaker 1974) sample compartment (above and below ground components)mangrove fluxes by litterfall biomass andor constant decay of litter

The estimation of Corg stocks was carried out for mangroves by authors Monica APech-Cardenas Andrea Camacho-Rico Juan P Caamal-Sosa Claudia Teutli-Hernandezand for seagrasses by Juan E Mendoza-Martinez and Sara M Morales Ojeda and thesupervisor was Jorge A Herrera-Silveira The above and below ground biomass of allthe studies were converted to organic carbon using the factor 045 for mangroves and035 for seagrasses (Fourqurean et al 2012a Howard et al 2014 Kauffman amp Donato2012) The total soil Corg pool was standardized to a depth of 1 m although there arereports in mangroves of organic matter depths greater than 1 m (Caamal-Sosa et al 2011Adame amp Fry 2016 Ezcurra et al 2016) The units employed to report the Corg stocksin the coastal blue carbon ecosystems were Mg Corg haminus1 except where indicated Forboth ecosystems our lab data were used as the control for Corg and for both above andbelow ground assessments The georeferenced data were standardized and plotted andcorrections were made for inconsistencies in the location of the sites and derived from thedifferent coordinate systems used in the literature The mangrove zonation used belongs to

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 636

Figure 2 Cartographic representation of climate regions acording to humidity ranges and hydrog-raphy of Mexican coastal areas information of data number (n) for mangrove (M) and seagrass (S) ateach region is provided Reference data provided by CONABIO (2009) Based onMaderey-R amp Torres-Ruata 1990 for hydrology and Garciacutea 1990 for humidity ranges Geographic Coordinate System DatumWGS84

Full-size DOI 107717peerj8790fig-2

the national official regionalization and was proposed by a panel of scientists (CONABIO2009 based on Lugo amp Snedaker 1974) The humidity ranges were defined according toCONABIO (2009) based on Garciacutea (1988) we use humid (Am and Af variations) subhumid (Aw2 Aw1 Aw0 variations) arid (BW) and semi-arid (BS1) classifications Theecological typology criteria used were dwarf basin fringe and hammock (peten) mangrovetypes which could be of interest both for decision makers and for future research atregional and local scales (Fig 2 Table 2) We report the average carbon stored per regionand standard error as a measure of data dispersion

The estimation of the GHG emission pattern due to the loss of mangrove coverage wasperformed based on factors recommended by the IPCC (2014) and Howard et al (2014)The extension changes in mangroves for each region was taken from Valderrama-Landeroset al (2017) who accomplished a national mapping using remote sensing data validatedby more than 1000 verification points and 69000 vertical aerial photographs (Rodriacuteguez-Zuacutentildeiga et al 2013 Valderrama-Landeros et al 2017) The CO2e emissions by mangroveloss were estimated according to the average carbon stored per region and mangrove lost

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 736

Table 2 Characterization of the blue carbon ecosystems inMexico by regions

Region States Climate GT HT Mangrove species Seagrasses species Surf Salinity Int Salinity nMangrove n Seagrasses

North Pacific BC Ag

BCS VA CL Rm Rm A13 A22

Son A SM 2 Lr Zm 345 (34ndash37) 606 B28 B9

Sin SH RE Ce

Nay

Central Pacific Jal Rm

Col SH RE ND Lr ND ND 497 (35ndash78) A6 ND

Mich CL Ag B5

Ce

South Pacific Guerr Ag

Oax SH RE ND Rm ND ND 326 (8ndash38) A69 ND

Chiap H CL LrCe

B30

Gulf of Mexico Tam A Ag Hb

Ver SH RE 1 Rm Hw 331 (11ndash38) 209 (3ndash69) A170 A60

Tab H CL 2 Lr Rm B43 B45

Ce Sf

Tt

Yucatan Peninsula Camp A KS Rm Hw

Yuc SH CL 1 Lr Sf

Q Roo H RE 2 Ag Tt 377 (18ndash50) 39 (05-86) A129 A254

Ce Rm B116 B221

NotesRegions accoriding to CONABIO (2016) Climates are based on humidity ranges (HHumid SHSub-Humid SASemi-arid A Arid) Geomorphological types (GT) are Coastal lagoon (CL) Salt mash(SM) River-estuarine system (RE) and Karst system (KS) Hydrodynamic types (HT) are open (1) and closed (2) The mangrove species are Avicennia germinans (Ag) Rhizophora mangle (Rm) Lagun-cularia racemosa (Lr) Conocarpus erectus (Ce) The Seagrass species are Rupia maritima (Rm) Zostera marina (Zm) Halodule beaudettei (Hb) Halodule wrightii (Hw) Syringodium filiforme (Sf) Thalas-sia testudinum (Tt) indicate dominance ND No data n number of observations of above ground (A) and below ground (B) C stocks

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

836

area The mangroves CO2e emissions were estimated by regions during 1970 and 2015 timeperiod using a conservative approach in which a loss of 25 of the Corg store is assumedin response to land use change (Pendleton et al 2012)

To present an evaluation of the uncertainty of the data in this synthesis the authorJorge Montero analyzed the carbon stock values of mangroves and seagrasses by regionand nonparametric bootstrap confidence intervals were calculated using the method ofadjusted bootstrap percentile (BCa with B= 10000) and bootstrap variance estimatorThe BCa values were calculate using the bootci function in R software and library boots(Canty amp Ripley 2019) The uncertainty was calculated using the bootstrap standard errorand 95 confidence interval for z normal distribution and expressed as a percentage basedon the average value

RESULTS AND DISCUSSIONStudy selectionWe identified 176 articles based on the search criteria however 50 articles were deemedinappropriate and were not used in the final analysis Thus a total of 1220 data points wereextracted from 59 sources for seagrasses and 67 sources for mangroves and they were usedto assess Mexican blue carbon stocks From the first 176 articles selected 50 were screenedout remaining 126 articles whichmeets the quality and requirements for this study (Fig 1)Data on carbon fluxes were scarce evidencing the research needs in this area To improvethe accuracy of the influence from land use on ecosystem carbon dynamics studies whichinclude measurements of stocks and changes along the soil profile are required (Kauffmanamp Bhomia 2017) With respect to seagrasses difficulties involved in mapping the marineenvironment coupled with gap information in the legislative seagrassesrsquo framework ofMexico have resulted in limited knowledge regarding seagrass distribution However theresearchers and national institutions efforts in recent years entails the first official numbersfor the seagrass cover in the Gulf of Mexico

Synthesis of mangrove stocks by above ground and below groundcompartmentsThe average above ground tree biomass was 1136 plusmn 52 Mg Corg haminus1 while the averagebelow ground Corg (soils and roots) was 3852 plusmn 22 Mg Corg haminus1 for a combined total of4988 Mg Corg haminus1 The below ground mean Corg consisted of approximately 77 of thetotal Corg stock for Mexico This value is consistent with other reports for the Corg stocks inMexico which vary between 364 Mg Corg haminus1 and 442 Mg Corg haminus1 (Herrera-Silveira etal 2016 Adame et al 2018) Similar to the present work both studies used literature andoriginal data suggesting that the real value of the total Corg stock of Mexicorsquos mangroveis approximately 434 Mg Corg haminus1 which is a below global average that was reportedelsewhere as ranging from 885 to 937 Mg Corg haminus1 and less than Tier 1 default mangroversquosvalues reported by the IPCC (511 Mg Corg haminus1) Differences among reports and Tier 1estimations are largely due to the underestimation of soil carbon stocks in global studies(Donato et al 2011 Alongi 2012 Hiraishi et al 2014 Kauffman amp Bhomia 2017) In thecase of this systematic review the soil Corg content available in the literature only includes

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 936

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

1136

Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

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Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 2: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Subjects Ecology Ecosystem Science Climate Change Biology Natural Resource ManagementEnvironmental ImpactsKeywords Blue carbon Mangroves Seagrasses Carbon stocks Climate change

INTRODUCTIONCoastal ecosystems are critical for the maintenance of biodiversity and human well-being by providing diverse benefits and ecosystem services including protection againststorms and mean sea level rise as well as the prevention of coastal erosion water qualityregulation nutrient recycling and provision of habitats for high diversity commercialspecies among others (Gautier Amador amp Newmark 2001 Kathiresan amp Rajendran 2005Mazda Kobashi amp Okada 2005 Alongi 2008 Bouillon amp Connolly 2009 Koch et al 2009Wang et al 2010 Yulianto Soewardi amp Adrianto 2016)

Mangroves seagrasses and salt marshes are known as blue carbon ecosystems theysequester greenhouse gases and store more organic carbon over the long term per unit areathan terrestrial forests and they are now recognized for their role in the climate changemitigation (Pendleton et al 2012) Despite these benefits blue carbon ecosystems areamong the most threatened ecosystems and their relatively low coverage lt05 (Duarteet al 2013) is the result of natural fragility and human-induced impacts

International groups such as the Intergovernmental Panel on Climate Change (IPCC)have begun to recognize the climatemitigation value of these ecosystems and included themin the 2016 update to the 2003 Wetlands Supplement (IPCC 2014) At an internationallevel it has been recognized that Corg sequestration and storage in the vegetation andsoil of blue carbon ecosystems could be a key component of mitigation strategies in theface of climate change Thus actions that conserve restore and sustainability use coastalwetlands are needed to avoid emissions and maintain (and where possible enhance) coastalwetland sequestration and storage These actions contribute to global and national carbonmanagement and increase the resilience of the socioecological ecosystem (Wolanski et al2004 Saintilan et al 2013 Sutton-Grier amp Moore 2016 Lovelock Fourqurean amp Morris2017Macreadie et al 2017)

Mexico has one of the largest extensions of blue carbon ecosystems and is among theareas with the greatest coverage in the tropical and subtropical Western HemisphereThe Mexican Federal Government reports 755555 ha of mangrove and 461059 ha ofseagrasses (Valderrama-Landeros et al 2017 CONABIO 2018) However estimationsof their extensions have varied over time according to the precision of the methods(aerial photos satellite images number of sites verified lsquolsquoin sitursquorsquo) and special attentionis required for seagrasses due to the scarce reports on their extension which differsignificantly (Table 1) For mangroves Mexicorsquos main species are Rhizophora mangleAvicennia germinans and Laguncularia racemosa (Valderrama-Landeros et al 2017) andfor seagrasses the main species are Halodule wrightii Syringodium filiforme Thalassiatestudinum and Zostera marina (CONABIO 2018)

Recently academia nongovernmental organizations and governmental groups havecreated synergies to increase scientific knowledge concerning blue carbon ecosystems and

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 236

Table 1 Reported extension for Mexicanmangroves and seagrasses in the last 48 years (1970ndash2018)

Period (decade) Mangroves extension (ha) Seagrass extension (ha) References

1970ndash1980 14200001

11240002

8564053

ndash 1 2 3

1981ndash1990 9856002

8555663ndash 23

1991ndash2000 9328004

8850002ndash 2 4

2001ndash2010 8200002

7741343

7738543

7647743

6882307 2 3 7

2011ndash2018 7419176

9395218

7755553

91930010

456059ndash461058113 6 8 10 11

NotesData from 1Flores et al (1971) 2FAO (2007) 3Valderrama-Landeros et al (2017) 4Spalding Blasco amp Field (1997) 6Giri et al (2011) 8INEGI (2014) 7Green amp Short (2003)10CCA (2016) 11CONABIO (2018)

the Corg reserves of several ecosystems have been quantified and mapped (Caamal-Sosaet al 2011 Adame et al 2013 Ramiacuterez-Ramiacuterez Medina-Goacutemez amp Herrera-Silveira 2015Adame amp Fry 2016 Ezcurra et al 2016 Kauffman et al 2016 Medina-Goacutemez et al 2016Cinco-Castro et al 2017 Ochoa-Goacutemez et al 2019) In this systematic review we checkedmore than 150 reports with data related to blue carbon stocks and fluxes in Mexico (Fig 1)

The storage and fluxes of Corg in blue carbon ecosystems mainly depend on thecommunity structural characteristics and extensions which are the result of the addition ofparticularities of climate geomorphology hydrology and human land use InMexico thereis a natural and human-induced heterogeneity along the 11592 km (De la Lanza EspinoPeacuterez amp Peacuterez 2013) of coast resulting in a mosaic of spatial and structural arrangements ofmangrove and seagrass communities Traditionally management schemes do not considerall the abovementioned criteria

In the case of seagrasses both the bathymetry gradient and coastal current velocitiesinfluence the water transparency which is one of the key variables for seagrass developmentThe variability in water transparency is a factor related to the morphometric characteristicsof the plants which determine the above ground Corg assessments of this ecosystem(Fourqurean et al 2012a) However Mexico has insufficient information on seagrasses atthe high spatial resolution required for use as a reference criterion for seagrass zonationCurrently theMexican government is requesting information frommangrove and seagrassCorg stocks under different criteria that allow for the development of conservation andrestoration policies at different scales (INECC 2018) In this context it is necessary toconsider the ecological and environmental scenarios in which mangroves and seagrassesdevelop to improve local regional and national carbon inventories

Mexico ranks 13 in the list of countries with the largest CO2 emissions (IEA 2014)derived from the use and burning of fossil fuels representing 137 of global emissionsin 2012 however and unknown amount of CO2 emissions is contributed by degraded or

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 336

Figure 1 PRISMA flow diagram of the literature selection process for the systematic review of Mexicanblue carbon stocks and fluxes FromMoher et al (2009b)

Full-size DOI 107717peerj8790fig-1

destroyed blue carbon ecosystems which are able to release the carbon they have storedfor centuries into the atmosphere and oceans and become sources of greenhouse gases(Pendleton et al 2012) It has been estimated by experts that as much as 102 billion tonsof carbon dioxide are being released annually from degraded coastal ecosystems whichis equivalent to 19 of emissions from tropical deforestation globally (Pendleton et al2012) Changes in the coverage of Mexicorsquos blue carbon ecosystems over time and theirrelation to changes in land use have been difficult to quantify due to the lack of long-termevaluation programs

Mexico is one of the 175 countries that have signed onto the Paris Agreement and it hascommitted to lsquolsquoincrease carbon capture and coastal protection with the implementation ofconservation and recovery schemes for coastal and marine ecosystems such as coral reefsmangroves seagrasses and dunesrsquorsquo throughMexicorsquos Nationally Determined Contributionwith theAdaptation category (INECC 2018)However insufficient data have been collected

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 436

inMexico andno complete synthesis of themitigation value or the greenhouse gases (GHG)emissions related to mangroves and seagrasses existed until now This comprehensivereview is a first step in providing a tool for decisionmakers to develop efficient strategiesaimed at reducing carbon emissions from the loss of these ecosystems while also protectingcurrent levels of carbon capture and storage as well the many ecosystem services providedby mangroves and seagrasses

METHODSA systematic reviewwas conducted at the country level to assess the carbon stocks and fluxesof blue carbon ecosystems in Mexico We use the Preferred Reporting Items for SystematicReviews and Meta-Analyses (PRISMA) (Fig 1) framework and protocols (Moher et al2009a)

Information sources and search strategyAn electronic literature search was performed for carbon stocks and carbon fluxes inmangroves and seagrasses fromMexico We use PubMed (MEDLINE) and Web of Scienceas the primary sources for searches and include open access publications Google Scholarwas a secondary source used to acquire additional literature (thesis technical reports)and the inclusion of gray literature is recommended for systematic reviews to minimizepublication bias (Koricheva Gurevitch amp Mengersen 2013 Pullin amp Stewart 2006)

We also include published databases on Corg stocks from Herrera-Silveira et al (2018a)and Herrera-Silveira et al (2018b) and the Mexican Carbon Program (PMC) which havebeen validated and reviewed by experts and organizations of the federal governmentand civil society (CONABIO and CONAFOR) and subjected to public consultation(httppmcarbonoorgpmc) In the initial phase titles and abstracts from network werescreened to identify potential eligible studies In the second phase full texts of the remainingarticles were read to determine if they meet the inclusion and exclusion criteria Whendisagreement emerged regarding the eligibility of studies the main author Jorge A HerreraSilveira made the final decision

The search of carbon stocks and fluxes extended from 1987 to 2018 and includedkeywords (exclusively in Spanish and English) population (lsquolsquomangroversquorsquo OR lsquolsquoseagrassrsquorsquoOR lsquolsquoSubmerged aquatic vegetationrsquorsquo OR lsquolsquowetlandsrsquorsquo OR lsquolsquocoastal basinrsquorsquo OR lsquolsquocoastrsquorsquo)AND compartments (lsquolsquoForest structurersquorsquo OR lsquolsquoecosystem structurersquorsquo OR lsquolsquoDBHrsquorsquo ORlsquolsquobiomassrsquorsquo OR lsquolsquoabove groundrsquorsquo AND lsquolsquobiomassrsquorsquo OR lsquolsquobelow groundrsquorsquo AND lsquolsquobiomassrsquorsquoOR lsquolsquolitter productivityrsquorsquo OR lsquolsquocarbonrsquorsquo AND lsquolsquofluxrsquorsquo OR lsquolsquodecompositionrsquorsquo OR lsquolsquosoilrsquorsquo ANDlsquolsquocarbonrsquorsquo OR lsquolsquosoilrsquorsquo AND lsquolsquoorganic matterrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquoorganic matterrsquorsquo ORlsquolsquosoilrsquorsquo AND lsquolsquobulk densityrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquobulk densityrsquorsquo) AND lsquolsquolocationrsquorsquo (vglsquolsquoGulf of Mexicorsquorsquo OR lsquolsquoPacificrsquorsquo OR lsquolsquoYucatan Peninsularsquorsquo) OR lsquolsquoMexican CaribbeanrsquorsquoOR state names (vg lsquolsquoYucatanrsquorsquo OR lsquolsquoCampechersquorsquo lsquolsquoQuintana Roorsquorsquo OR lsquolsquoTabascorsquorsquo ORlsquolsquoVeracruzrsquorsquo OR lsquolsquoTamaulipasrsquorsquo OR lsquolsquoBaja California Surrsquorsquo OR lsquolsquoBaja California NortersquorsquoOR lsquolsquoSinaloarsquorsquo OR lsquolsquoOaxacarsquorsquo OR lsquolsquoChiapasrsquorsquo) OR specific site names (vg lsquolsquoLagunade Terminosrsquorsquo OR lsquolsquoMagdalena Bayrsquorsquo OR lsquolsquoSian Karsquoanrsquorsquo OR lsquolsquoLa Encrucijadarsquorsquo OR lsquolsquoLa

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 536

Mancharsquorsquo OR lsquolsquoLaguna Alvaradorsquorsquo OR lsquolsquoSanQuintiacuten Bayrsquorsquo OR lsquolsquoMarismasNacionalesrsquorsquo ORlsquolsquoCelestuacutenrsquorsquo OR rsquorsquo Laguna Madrersquorsquo OR lsquolsquoBarra de Navidadrsquorsquo OR lsquolsquoLaguna Mar Muertorsquorsquo)

The searches were undertaken independently by authors with at least five years ofexperience in sampling laboratory analysis and proven experience in data analysisand redaction of technical reports on blue carbon ecosystems The five researchers formangrove review were the coauthors Andrea Camacho-Rico Monica A Pech-CardenasSiuling Cinco-Castro for sediments were Eunice Y Pech-Poot and Juan P Caamal Sosaand for seagrasses were Juan E Mendoza-Mantiacutenez and Sara M Morales-Ojeda

Eligibility criteriaWe include studies and datasets that report the biomass organic carbon stock organicmatter and bulk density in sediments per unit of area and spatially referenced or flux datafrommangroves and seagrasses For mangroves an important criterion was the plot design(including at least three replicates) to guarantee the representativeness of the data forseagrasses we looked for studies that based their results on quadrants or cylindrical coresampler along transects No conference abstracts were considered to meet the inclusioncriteria

Data extraction and analysisData extraction was independently performed by authors (Andrea Camacho Rico MonicaA Pech -Cardenas Siuling Cinco-Castro Eunice Y Pech-Poot Juan P Caamal-Sosa JuanE Mendoza-Martinez and Sara M Morales Ojeda) Study-specific variables were recordedfor each entry Many properties assessed in this review were reported as contextualenvironmental data rather than the primary outcome for their respective studies (noreplicates or dispersion measures described) which was why bias was not reported inthis study We include entries such as geographic location and region (according toValderrama-Landeros et al 2017) environmental characteristics including ecological type(Lugo amp Snedaker 1974) sample compartment (above and below ground components)mangrove fluxes by litterfall biomass andor constant decay of litter

The estimation of Corg stocks was carried out for mangroves by authors Monica APech-Cardenas Andrea Camacho-Rico Juan P Caamal-Sosa Claudia Teutli-Hernandezand for seagrasses by Juan E Mendoza-Martinez and Sara M Morales Ojeda and thesupervisor was Jorge A Herrera-Silveira The above and below ground biomass of allthe studies were converted to organic carbon using the factor 045 for mangroves and035 for seagrasses (Fourqurean et al 2012a Howard et al 2014 Kauffman amp Donato2012) The total soil Corg pool was standardized to a depth of 1 m although there arereports in mangroves of organic matter depths greater than 1 m (Caamal-Sosa et al 2011Adame amp Fry 2016 Ezcurra et al 2016) The units employed to report the Corg stocksin the coastal blue carbon ecosystems were Mg Corg haminus1 except where indicated Forboth ecosystems our lab data were used as the control for Corg and for both above andbelow ground assessments The georeferenced data were standardized and plotted andcorrections were made for inconsistencies in the location of the sites and derived from thedifferent coordinate systems used in the literature The mangrove zonation used belongs to

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 636

Figure 2 Cartographic representation of climate regions acording to humidity ranges and hydrog-raphy of Mexican coastal areas information of data number (n) for mangrove (M) and seagrass (S) ateach region is provided Reference data provided by CONABIO (2009) Based onMaderey-R amp Torres-Ruata 1990 for hydrology and Garciacutea 1990 for humidity ranges Geographic Coordinate System DatumWGS84

Full-size DOI 107717peerj8790fig-2

the national official regionalization and was proposed by a panel of scientists (CONABIO2009 based on Lugo amp Snedaker 1974) The humidity ranges were defined according toCONABIO (2009) based on Garciacutea (1988) we use humid (Am and Af variations) subhumid (Aw2 Aw1 Aw0 variations) arid (BW) and semi-arid (BS1) classifications Theecological typology criteria used were dwarf basin fringe and hammock (peten) mangrovetypes which could be of interest both for decision makers and for future research atregional and local scales (Fig 2 Table 2) We report the average carbon stored per regionand standard error as a measure of data dispersion

The estimation of the GHG emission pattern due to the loss of mangrove coverage wasperformed based on factors recommended by the IPCC (2014) and Howard et al (2014)The extension changes in mangroves for each region was taken from Valderrama-Landeroset al (2017) who accomplished a national mapping using remote sensing data validatedby more than 1000 verification points and 69000 vertical aerial photographs (Rodriacuteguez-Zuacutentildeiga et al 2013 Valderrama-Landeros et al 2017) The CO2e emissions by mangroveloss were estimated according to the average carbon stored per region and mangrove lost

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 736

Table 2 Characterization of the blue carbon ecosystems inMexico by regions

Region States Climate GT HT Mangrove species Seagrasses species Surf Salinity Int Salinity nMangrove n Seagrasses

North Pacific BC Ag

BCS VA CL Rm Rm A13 A22

Son A SM 2 Lr Zm 345 (34ndash37) 606 B28 B9

Sin SH RE Ce

Nay

Central Pacific Jal Rm

Col SH RE ND Lr ND ND 497 (35ndash78) A6 ND

Mich CL Ag B5

Ce

South Pacific Guerr Ag

Oax SH RE ND Rm ND ND 326 (8ndash38) A69 ND

Chiap H CL LrCe

B30

Gulf of Mexico Tam A Ag Hb

Ver SH RE 1 Rm Hw 331 (11ndash38) 209 (3ndash69) A170 A60

Tab H CL 2 Lr Rm B43 B45

Ce Sf

Tt

Yucatan Peninsula Camp A KS Rm Hw

Yuc SH CL 1 Lr Sf

Q Roo H RE 2 Ag Tt 377 (18ndash50) 39 (05-86) A129 A254

Ce Rm B116 B221

NotesRegions accoriding to CONABIO (2016) Climates are based on humidity ranges (HHumid SHSub-Humid SASemi-arid A Arid) Geomorphological types (GT) are Coastal lagoon (CL) Salt mash(SM) River-estuarine system (RE) and Karst system (KS) Hydrodynamic types (HT) are open (1) and closed (2) The mangrove species are Avicennia germinans (Ag) Rhizophora mangle (Rm) Lagun-cularia racemosa (Lr) Conocarpus erectus (Ce) The Seagrass species are Rupia maritima (Rm) Zostera marina (Zm) Halodule beaudettei (Hb) Halodule wrightii (Hw) Syringodium filiforme (Sf) Thalas-sia testudinum (Tt) indicate dominance ND No data n number of observations of above ground (A) and below ground (B) C stocks

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

836

area The mangroves CO2e emissions were estimated by regions during 1970 and 2015 timeperiod using a conservative approach in which a loss of 25 of the Corg store is assumedin response to land use change (Pendleton et al 2012)

To present an evaluation of the uncertainty of the data in this synthesis the authorJorge Montero analyzed the carbon stock values of mangroves and seagrasses by regionand nonparametric bootstrap confidence intervals were calculated using the method ofadjusted bootstrap percentile (BCa with B= 10000) and bootstrap variance estimatorThe BCa values were calculate using the bootci function in R software and library boots(Canty amp Ripley 2019) The uncertainty was calculated using the bootstrap standard errorand 95 confidence interval for z normal distribution and expressed as a percentage basedon the average value

RESULTS AND DISCUSSIONStudy selectionWe identified 176 articles based on the search criteria however 50 articles were deemedinappropriate and were not used in the final analysis Thus a total of 1220 data points wereextracted from 59 sources for seagrasses and 67 sources for mangroves and they were usedto assess Mexican blue carbon stocks From the first 176 articles selected 50 were screenedout remaining 126 articles whichmeets the quality and requirements for this study (Fig 1)Data on carbon fluxes were scarce evidencing the research needs in this area To improvethe accuracy of the influence from land use on ecosystem carbon dynamics studies whichinclude measurements of stocks and changes along the soil profile are required (Kauffmanamp Bhomia 2017) With respect to seagrasses difficulties involved in mapping the marineenvironment coupled with gap information in the legislative seagrassesrsquo framework ofMexico have resulted in limited knowledge regarding seagrass distribution However theresearchers and national institutions efforts in recent years entails the first official numbersfor the seagrass cover in the Gulf of Mexico

Synthesis of mangrove stocks by above ground and below groundcompartmentsThe average above ground tree biomass was 1136 plusmn 52 Mg Corg haminus1 while the averagebelow ground Corg (soils and roots) was 3852 plusmn 22 Mg Corg haminus1 for a combined total of4988 Mg Corg haminus1 The below ground mean Corg consisted of approximately 77 of thetotal Corg stock for Mexico This value is consistent with other reports for the Corg stocks inMexico which vary between 364 Mg Corg haminus1 and 442 Mg Corg haminus1 (Herrera-Silveira etal 2016 Adame et al 2018) Similar to the present work both studies used literature andoriginal data suggesting that the real value of the total Corg stock of Mexicorsquos mangroveis approximately 434 Mg Corg haminus1 which is a below global average that was reportedelsewhere as ranging from 885 to 937 Mg Corg haminus1 and less than Tier 1 default mangroversquosvalues reported by the IPCC (511 Mg Corg haminus1) Differences among reports and Tier 1estimations are largely due to the underestimation of soil carbon stocks in global studies(Donato et al 2011 Alongi 2012 Hiraishi et al 2014 Kauffman amp Bhomia 2017) In thecase of this systematic review the soil Corg content available in the literature only includes

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 936

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

1136

Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

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INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

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Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 3: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Table 1 Reported extension for Mexicanmangroves and seagrasses in the last 48 years (1970ndash2018)

Period (decade) Mangroves extension (ha) Seagrass extension (ha) References

1970ndash1980 14200001

11240002

8564053

ndash 1 2 3

1981ndash1990 9856002

8555663ndash 23

1991ndash2000 9328004

8850002ndash 2 4

2001ndash2010 8200002

7741343

7738543

7647743

6882307 2 3 7

2011ndash2018 7419176

9395218

7755553

91930010

456059ndash461058113 6 8 10 11

NotesData from 1Flores et al (1971) 2FAO (2007) 3Valderrama-Landeros et al (2017) 4Spalding Blasco amp Field (1997) 6Giri et al (2011) 8INEGI (2014) 7Green amp Short (2003)10CCA (2016) 11CONABIO (2018)

the Corg reserves of several ecosystems have been quantified and mapped (Caamal-Sosaet al 2011 Adame et al 2013 Ramiacuterez-Ramiacuterez Medina-Goacutemez amp Herrera-Silveira 2015Adame amp Fry 2016 Ezcurra et al 2016 Kauffman et al 2016 Medina-Goacutemez et al 2016Cinco-Castro et al 2017 Ochoa-Goacutemez et al 2019) In this systematic review we checkedmore than 150 reports with data related to blue carbon stocks and fluxes in Mexico (Fig 1)

The storage and fluxes of Corg in blue carbon ecosystems mainly depend on thecommunity structural characteristics and extensions which are the result of the addition ofparticularities of climate geomorphology hydrology and human land use InMexico thereis a natural and human-induced heterogeneity along the 11592 km (De la Lanza EspinoPeacuterez amp Peacuterez 2013) of coast resulting in a mosaic of spatial and structural arrangements ofmangrove and seagrass communities Traditionally management schemes do not considerall the abovementioned criteria

In the case of seagrasses both the bathymetry gradient and coastal current velocitiesinfluence the water transparency which is one of the key variables for seagrass developmentThe variability in water transparency is a factor related to the morphometric characteristicsof the plants which determine the above ground Corg assessments of this ecosystem(Fourqurean et al 2012a) However Mexico has insufficient information on seagrasses atthe high spatial resolution required for use as a reference criterion for seagrass zonationCurrently theMexican government is requesting information frommangrove and seagrassCorg stocks under different criteria that allow for the development of conservation andrestoration policies at different scales (INECC 2018) In this context it is necessary toconsider the ecological and environmental scenarios in which mangroves and seagrassesdevelop to improve local regional and national carbon inventories

Mexico ranks 13 in the list of countries with the largest CO2 emissions (IEA 2014)derived from the use and burning of fossil fuels representing 137 of global emissionsin 2012 however and unknown amount of CO2 emissions is contributed by degraded or

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 336

Figure 1 PRISMA flow diagram of the literature selection process for the systematic review of Mexicanblue carbon stocks and fluxes FromMoher et al (2009b)

Full-size DOI 107717peerj8790fig-1

destroyed blue carbon ecosystems which are able to release the carbon they have storedfor centuries into the atmosphere and oceans and become sources of greenhouse gases(Pendleton et al 2012) It has been estimated by experts that as much as 102 billion tonsof carbon dioxide are being released annually from degraded coastal ecosystems whichis equivalent to 19 of emissions from tropical deforestation globally (Pendleton et al2012) Changes in the coverage of Mexicorsquos blue carbon ecosystems over time and theirrelation to changes in land use have been difficult to quantify due to the lack of long-termevaluation programs

Mexico is one of the 175 countries that have signed onto the Paris Agreement and it hascommitted to lsquolsquoincrease carbon capture and coastal protection with the implementation ofconservation and recovery schemes for coastal and marine ecosystems such as coral reefsmangroves seagrasses and dunesrsquorsquo throughMexicorsquos Nationally Determined Contributionwith theAdaptation category (INECC 2018)However insufficient data have been collected

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 436

inMexico andno complete synthesis of themitigation value or the greenhouse gases (GHG)emissions related to mangroves and seagrasses existed until now This comprehensivereview is a first step in providing a tool for decisionmakers to develop efficient strategiesaimed at reducing carbon emissions from the loss of these ecosystems while also protectingcurrent levels of carbon capture and storage as well the many ecosystem services providedby mangroves and seagrasses

METHODSA systematic reviewwas conducted at the country level to assess the carbon stocks and fluxesof blue carbon ecosystems in Mexico We use the Preferred Reporting Items for SystematicReviews and Meta-Analyses (PRISMA) (Fig 1) framework and protocols (Moher et al2009a)

Information sources and search strategyAn electronic literature search was performed for carbon stocks and carbon fluxes inmangroves and seagrasses fromMexico We use PubMed (MEDLINE) and Web of Scienceas the primary sources for searches and include open access publications Google Scholarwas a secondary source used to acquire additional literature (thesis technical reports)and the inclusion of gray literature is recommended for systematic reviews to minimizepublication bias (Koricheva Gurevitch amp Mengersen 2013 Pullin amp Stewart 2006)

We also include published databases on Corg stocks from Herrera-Silveira et al (2018a)and Herrera-Silveira et al (2018b) and the Mexican Carbon Program (PMC) which havebeen validated and reviewed by experts and organizations of the federal governmentand civil society (CONABIO and CONAFOR) and subjected to public consultation(httppmcarbonoorgpmc) In the initial phase titles and abstracts from network werescreened to identify potential eligible studies In the second phase full texts of the remainingarticles were read to determine if they meet the inclusion and exclusion criteria Whendisagreement emerged regarding the eligibility of studies the main author Jorge A HerreraSilveira made the final decision

The search of carbon stocks and fluxes extended from 1987 to 2018 and includedkeywords (exclusively in Spanish and English) population (lsquolsquomangroversquorsquo OR lsquolsquoseagrassrsquorsquoOR lsquolsquoSubmerged aquatic vegetationrsquorsquo OR lsquolsquowetlandsrsquorsquo OR lsquolsquocoastal basinrsquorsquo OR lsquolsquocoastrsquorsquo)AND compartments (lsquolsquoForest structurersquorsquo OR lsquolsquoecosystem structurersquorsquo OR lsquolsquoDBHrsquorsquo ORlsquolsquobiomassrsquorsquo OR lsquolsquoabove groundrsquorsquo AND lsquolsquobiomassrsquorsquo OR lsquolsquobelow groundrsquorsquo AND lsquolsquobiomassrsquorsquoOR lsquolsquolitter productivityrsquorsquo OR lsquolsquocarbonrsquorsquo AND lsquolsquofluxrsquorsquo OR lsquolsquodecompositionrsquorsquo OR lsquolsquosoilrsquorsquo ANDlsquolsquocarbonrsquorsquo OR lsquolsquosoilrsquorsquo AND lsquolsquoorganic matterrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquoorganic matterrsquorsquo ORlsquolsquosoilrsquorsquo AND lsquolsquobulk densityrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquobulk densityrsquorsquo) AND lsquolsquolocationrsquorsquo (vglsquolsquoGulf of Mexicorsquorsquo OR lsquolsquoPacificrsquorsquo OR lsquolsquoYucatan Peninsularsquorsquo) OR lsquolsquoMexican CaribbeanrsquorsquoOR state names (vg lsquolsquoYucatanrsquorsquo OR lsquolsquoCampechersquorsquo lsquolsquoQuintana Roorsquorsquo OR lsquolsquoTabascorsquorsquo ORlsquolsquoVeracruzrsquorsquo OR lsquolsquoTamaulipasrsquorsquo OR lsquolsquoBaja California Surrsquorsquo OR lsquolsquoBaja California NortersquorsquoOR lsquolsquoSinaloarsquorsquo OR lsquolsquoOaxacarsquorsquo OR lsquolsquoChiapasrsquorsquo) OR specific site names (vg lsquolsquoLagunade Terminosrsquorsquo OR lsquolsquoMagdalena Bayrsquorsquo OR lsquolsquoSian Karsquoanrsquorsquo OR lsquolsquoLa Encrucijadarsquorsquo OR lsquolsquoLa

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 536

Mancharsquorsquo OR lsquolsquoLaguna Alvaradorsquorsquo OR lsquolsquoSanQuintiacuten Bayrsquorsquo OR lsquolsquoMarismasNacionalesrsquorsquo ORlsquolsquoCelestuacutenrsquorsquo OR rsquorsquo Laguna Madrersquorsquo OR lsquolsquoBarra de Navidadrsquorsquo OR lsquolsquoLaguna Mar Muertorsquorsquo)

The searches were undertaken independently by authors with at least five years ofexperience in sampling laboratory analysis and proven experience in data analysisand redaction of technical reports on blue carbon ecosystems The five researchers formangrove review were the coauthors Andrea Camacho-Rico Monica A Pech-CardenasSiuling Cinco-Castro for sediments were Eunice Y Pech-Poot and Juan P Caamal Sosaand for seagrasses were Juan E Mendoza-Mantiacutenez and Sara M Morales-Ojeda

Eligibility criteriaWe include studies and datasets that report the biomass organic carbon stock organicmatter and bulk density in sediments per unit of area and spatially referenced or flux datafrommangroves and seagrasses For mangroves an important criterion was the plot design(including at least three replicates) to guarantee the representativeness of the data forseagrasses we looked for studies that based their results on quadrants or cylindrical coresampler along transects No conference abstracts were considered to meet the inclusioncriteria

Data extraction and analysisData extraction was independently performed by authors (Andrea Camacho Rico MonicaA Pech -Cardenas Siuling Cinco-Castro Eunice Y Pech-Poot Juan P Caamal-Sosa JuanE Mendoza-Martinez and Sara M Morales Ojeda) Study-specific variables were recordedfor each entry Many properties assessed in this review were reported as contextualenvironmental data rather than the primary outcome for their respective studies (noreplicates or dispersion measures described) which was why bias was not reported inthis study We include entries such as geographic location and region (according toValderrama-Landeros et al 2017) environmental characteristics including ecological type(Lugo amp Snedaker 1974) sample compartment (above and below ground components)mangrove fluxes by litterfall biomass andor constant decay of litter

The estimation of Corg stocks was carried out for mangroves by authors Monica APech-Cardenas Andrea Camacho-Rico Juan P Caamal-Sosa Claudia Teutli-Hernandezand for seagrasses by Juan E Mendoza-Martinez and Sara M Morales Ojeda and thesupervisor was Jorge A Herrera-Silveira The above and below ground biomass of allthe studies were converted to organic carbon using the factor 045 for mangroves and035 for seagrasses (Fourqurean et al 2012a Howard et al 2014 Kauffman amp Donato2012) The total soil Corg pool was standardized to a depth of 1 m although there arereports in mangroves of organic matter depths greater than 1 m (Caamal-Sosa et al 2011Adame amp Fry 2016 Ezcurra et al 2016) The units employed to report the Corg stocksin the coastal blue carbon ecosystems were Mg Corg haminus1 except where indicated Forboth ecosystems our lab data were used as the control for Corg and for both above andbelow ground assessments The georeferenced data were standardized and plotted andcorrections were made for inconsistencies in the location of the sites and derived from thedifferent coordinate systems used in the literature The mangrove zonation used belongs to

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 636

Figure 2 Cartographic representation of climate regions acording to humidity ranges and hydrog-raphy of Mexican coastal areas information of data number (n) for mangrove (M) and seagrass (S) ateach region is provided Reference data provided by CONABIO (2009) Based onMaderey-R amp Torres-Ruata 1990 for hydrology and Garciacutea 1990 for humidity ranges Geographic Coordinate System DatumWGS84

Full-size DOI 107717peerj8790fig-2

the national official regionalization and was proposed by a panel of scientists (CONABIO2009 based on Lugo amp Snedaker 1974) The humidity ranges were defined according toCONABIO (2009) based on Garciacutea (1988) we use humid (Am and Af variations) subhumid (Aw2 Aw1 Aw0 variations) arid (BW) and semi-arid (BS1) classifications Theecological typology criteria used were dwarf basin fringe and hammock (peten) mangrovetypes which could be of interest both for decision makers and for future research atregional and local scales (Fig 2 Table 2) We report the average carbon stored per regionand standard error as a measure of data dispersion

The estimation of the GHG emission pattern due to the loss of mangrove coverage wasperformed based on factors recommended by the IPCC (2014) and Howard et al (2014)The extension changes in mangroves for each region was taken from Valderrama-Landeroset al (2017) who accomplished a national mapping using remote sensing data validatedby more than 1000 verification points and 69000 vertical aerial photographs (Rodriacuteguez-Zuacutentildeiga et al 2013 Valderrama-Landeros et al 2017) The CO2e emissions by mangroveloss were estimated according to the average carbon stored per region and mangrove lost

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 736

Table 2 Characterization of the blue carbon ecosystems inMexico by regions

Region States Climate GT HT Mangrove species Seagrasses species Surf Salinity Int Salinity nMangrove n Seagrasses

North Pacific BC Ag

BCS VA CL Rm Rm A13 A22

Son A SM 2 Lr Zm 345 (34ndash37) 606 B28 B9

Sin SH RE Ce

Nay

Central Pacific Jal Rm

Col SH RE ND Lr ND ND 497 (35ndash78) A6 ND

Mich CL Ag B5

Ce

South Pacific Guerr Ag

Oax SH RE ND Rm ND ND 326 (8ndash38) A69 ND

Chiap H CL LrCe

B30

Gulf of Mexico Tam A Ag Hb

Ver SH RE 1 Rm Hw 331 (11ndash38) 209 (3ndash69) A170 A60

Tab H CL 2 Lr Rm B43 B45

Ce Sf

Tt

Yucatan Peninsula Camp A KS Rm Hw

Yuc SH CL 1 Lr Sf

Q Roo H RE 2 Ag Tt 377 (18ndash50) 39 (05-86) A129 A254

Ce Rm B116 B221

NotesRegions accoriding to CONABIO (2016) Climates are based on humidity ranges (HHumid SHSub-Humid SASemi-arid A Arid) Geomorphological types (GT) are Coastal lagoon (CL) Salt mash(SM) River-estuarine system (RE) and Karst system (KS) Hydrodynamic types (HT) are open (1) and closed (2) The mangrove species are Avicennia germinans (Ag) Rhizophora mangle (Rm) Lagun-cularia racemosa (Lr) Conocarpus erectus (Ce) The Seagrass species are Rupia maritima (Rm) Zostera marina (Zm) Halodule beaudettei (Hb) Halodule wrightii (Hw) Syringodium filiforme (Sf) Thalas-sia testudinum (Tt) indicate dominance ND No data n number of observations of above ground (A) and below ground (B) C stocks

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

836

area The mangroves CO2e emissions were estimated by regions during 1970 and 2015 timeperiod using a conservative approach in which a loss of 25 of the Corg store is assumedin response to land use change (Pendleton et al 2012)

To present an evaluation of the uncertainty of the data in this synthesis the authorJorge Montero analyzed the carbon stock values of mangroves and seagrasses by regionand nonparametric bootstrap confidence intervals were calculated using the method ofadjusted bootstrap percentile (BCa with B= 10000) and bootstrap variance estimatorThe BCa values were calculate using the bootci function in R software and library boots(Canty amp Ripley 2019) The uncertainty was calculated using the bootstrap standard errorand 95 confidence interval for z normal distribution and expressed as a percentage basedon the average value

RESULTS AND DISCUSSIONStudy selectionWe identified 176 articles based on the search criteria however 50 articles were deemedinappropriate and were not used in the final analysis Thus a total of 1220 data points wereextracted from 59 sources for seagrasses and 67 sources for mangroves and they were usedto assess Mexican blue carbon stocks From the first 176 articles selected 50 were screenedout remaining 126 articles whichmeets the quality and requirements for this study (Fig 1)Data on carbon fluxes were scarce evidencing the research needs in this area To improvethe accuracy of the influence from land use on ecosystem carbon dynamics studies whichinclude measurements of stocks and changes along the soil profile are required (Kauffmanamp Bhomia 2017) With respect to seagrasses difficulties involved in mapping the marineenvironment coupled with gap information in the legislative seagrassesrsquo framework ofMexico have resulted in limited knowledge regarding seagrass distribution However theresearchers and national institutions efforts in recent years entails the first official numbersfor the seagrass cover in the Gulf of Mexico

Synthesis of mangrove stocks by above ground and below groundcompartmentsThe average above ground tree biomass was 1136 plusmn 52 Mg Corg haminus1 while the averagebelow ground Corg (soils and roots) was 3852 plusmn 22 Mg Corg haminus1 for a combined total of4988 Mg Corg haminus1 The below ground mean Corg consisted of approximately 77 of thetotal Corg stock for Mexico This value is consistent with other reports for the Corg stocks inMexico which vary between 364 Mg Corg haminus1 and 442 Mg Corg haminus1 (Herrera-Silveira etal 2016 Adame et al 2018) Similar to the present work both studies used literature andoriginal data suggesting that the real value of the total Corg stock of Mexicorsquos mangroveis approximately 434 Mg Corg haminus1 which is a below global average that was reportedelsewhere as ranging from 885 to 937 Mg Corg haminus1 and less than Tier 1 default mangroversquosvalues reported by the IPCC (511 Mg Corg haminus1) Differences among reports and Tier 1estimations are largely due to the underestimation of soil carbon stocks in global studies(Donato et al 2011 Alongi 2012 Hiraishi et al 2014 Kauffman amp Bhomia 2017) In thecase of this systematic review the soil Corg content available in the literature only includes

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 936

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

1136

Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

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INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

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Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 4: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Figure 1 PRISMA flow diagram of the literature selection process for the systematic review of Mexicanblue carbon stocks and fluxes FromMoher et al (2009b)

Full-size DOI 107717peerj8790fig-1

destroyed blue carbon ecosystems which are able to release the carbon they have storedfor centuries into the atmosphere and oceans and become sources of greenhouse gases(Pendleton et al 2012) It has been estimated by experts that as much as 102 billion tonsof carbon dioxide are being released annually from degraded coastal ecosystems whichis equivalent to 19 of emissions from tropical deforestation globally (Pendleton et al2012) Changes in the coverage of Mexicorsquos blue carbon ecosystems over time and theirrelation to changes in land use have been difficult to quantify due to the lack of long-termevaluation programs

Mexico is one of the 175 countries that have signed onto the Paris Agreement and it hascommitted to lsquolsquoincrease carbon capture and coastal protection with the implementation ofconservation and recovery schemes for coastal and marine ecosystems such as coral reefsmangroves seagrasses and dunesrsquorsquo throughMexicorsquos Nationally Determined Contributionwith theAdaptation category (INECC 2018)However insufficient data have been collected

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 436

inMexico andno complete synthesis of themitigation value or the greenhouse gases (GHG)emissions related to mangroves and seagrasses existed until now This comprehensivereview is a first step in providing a tool for decisionmakers to develop efficient strategiesaimed at reducing carbon emissions from the loss of these ecosystems while also protectingcurrent levels of carbon capture and storage as well the many ecosystem services providedby mangroves and seagrasses

METHODSA systematic reviewwas conducted at the country level to assess the carbon stocks and fluxesof blue carbon ecosystems in Mexico We use the Preferred Reporting Items for SystematicReviews and Meta-Analyses (PRISMA) (Fig 1) framework and protocols (Moher et al2009a)

Information sources and search strategyAn electronic literature search was performed for carbon stocks and carbon fluxes inmangroves and seagrasses fromMexico We use PubMed (MEDLINE) and Web of Scienceas the primary sources for searches and include open access publications Google Scholarwas a secondary source used to acquire additional literature (thesis technical reports)and the inclusion of gray literature is recommended for systematic reviews to minimizepublication bias (Koricheva Gurevitch amp Mengersen 2013 Pullin amp Stewart 2006)

We also include published databases on Corg stocks from Herrera-Silveira et al (2018a)and Herrera-Silveira et al (2018b) and the Mexican Carbon Program (PMC) which havebeen validated and reviewed by experts and organizations of the federal governmentand civil society (CONABIO and CONAFOR) and subjected to public consultation(httppmcarbonoorgpmc) In the initial phase titles and abstracts from network werescreened to identify potential eligible studies In the second phase full texts of the remainingarticles were read to determine if they meet the inclusion and exclusion criteria Whendisagreement emerged regarding the eligibility of studies the main author Jorge A HerreraSilveira made the final decision

The search of carbon stocks and fluxes extended from 1987 to 2018 and includedkeywords (exclusively in Spanish and English) population (lsquolsquomangroversquorsquo OR lsquolsquoseagrassrsquorsquoOR lsquolsquoSubmerged aquatic vegetationrsquorsquo OR lsquolsquowetlandsrsquorsquo OR lsquolsquocoastal basinrsquorsquo OR lsquolsquocoastrsquorsquo)AND compartments (lsquolsquoForest structurersquorsquo OR lsquolsquoecosystem structurersquorsquo OR lsquolsquoDBHrsquorsquo ORlsquolsquobiomassrsquorsquo OR lsquolsquoabove groundrsquorsquo AND lsquolsquobiomassrsquorsquo OR lsquolsquobelow groundrsquorsquo AND lsquolsquobiomassrsquorsquoOR lsquolsquolitter productivityrsquorsquo OR lsquolsquocarbonrsquorsquo AND lsquolsquofluxrsquorsquo OR lsquolsquodecompositionrsquorsquo OR lsquolsquosoilrsquorsquo ANDlsquolsquocarbonrsquorsquo OR lsquolsquosoilrsquorsquo AND lsquolsquoorganic matterrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquoorganic matterrsquorsquo ORlsquolsquosoilrsquorsquo AND lsquolsquobulk densityrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquobulk densityrsquorsquo) AND lsquolsquolocationrsquorsquo (vglsquolsquoGulf of Mexicorsquorsquo OR lsquolsquoPacificrsquorsquo OR lsquolsquoYucatan Peninsularsquorsquo) OR lsquolsquoMexican CaribbeanrsquorsquoOR state names (vg lsquolsquoYucatanrsquorsquo OR lsquolsquoCampechersquorsquo lsquolsquoQuintana Roorsquorsquo OR lsquolsquoTabascorsquorsquo ORlsquolsquoVeracruzrsquorsquo OR lsquolsquoTamaulipasrsquorsquo OR lsquolsquoBaja California Surrsquorsquo OR lsquolsquoBaja California NortersquorsquoOR lsquolsquoSinaloarsquorsquo OR lsquolsquoOaxacarsquorsquo OR lsquolsquoChiapasrsquorsquo) OR specific site names (vg lsquolsquoLagunade Terminosrsquorsquo OR lsquolsquoMagdalena Bayrsquorsquo OR lsquolsquoSian Karsquoanrsquorsquo OR lsquolsquoLa Encrucijadarsquorsquo OR lsquolsquoLa

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 536

Mancharsquorsquo OR lsquolsquoLaguna Alvaradorsquorsquo OR lsquolsquoSanQuintiacuten Bayrsquorsquo OR lsquolsquoMarismasNacionalesrsquorsquo ORlsquolsquoCelestuacutenrsquorsquo OR rsquorsquo Laguna Madrersquorsquo OR lsquolsquoBarra de Navidadrsquorsquo OR lsquolsquoLaguna Mar Muertorsquorsquo)

The searches were undertaken independently by authors with at least five years ofexperience in sampling laboratory analysis and proven experience in data analysisand redaction of technical reports on blue carbon ecosystems The five researchers formangrove review were the coauthors Andrea Camacho-Rico Monica A Pech-CardenasSiuling Cinco-Castro for sediments were Eunice Y Pech-Poot and Juan P Caamal Sosaand for seagrasses were Juan E Mendoza-Mantiacutenez and Sara M Morales-Ojeda

Eligibility criteriaWe include studies and datasets that report the biomass organic carbon stock organicmatter and bulk density in sediments per unit of area and spatially referenced or flux datafrommangroves and seagrasses For mangroves an important criterion was the plot design(including at least three replicates) to guarantee the representativeness of the data forseagrasses we looked for studies that based their results on quadrants or cylindrical coresampler along transects No conference abstracts were considered to meet the inclusioncriteria

Data extraction and analysisData extraction was independently performed by authors (Andrea Camacho Rico MonicaA Pech -Cardenas Siuling Cinco-Castro Eunice Y Pech-Poot Juan P Caamal-Sosa JuanE Mendoza-Martinez and Sara M Morales Ojeda) Study-specific variables were recordedfor each entry Many properties assessed in this review were reported as contextualenvironmental data rather than the primary outcome for their respective studies (noreplicates or dispersion measures described) which was why bias was not reported inthis study We include entries such as geographic location and region (according toValderrama-Landeros et al 2017) environmental characteristics including ecological type(Lugo amp Snedaker 1974) sample compartment (above and below ground components)mangrove fluxes by litterfall biomass andor constant decay of litter

The estimation of Corg stocks was carried out for mangroves by authors Monica APech-Cardenas Andrea Camacho-Rico Juan P Caamal-Sosa Claudia Teutli-Hernandezand for seagrasses by Juan E Mendoza-Martinez and Sara M Morales Ojeda and thesupervisor was Jorge A Herrera-Silveira The above and below ground biomass of allthe studies were converted to organic carbon using the factor 045 for mangroves and035 for seagrasses (Fourqurean et al 2012a Howard et al 2014 Kauffman amp Donato2012) The total soil Corg pool was standardized to a depth of 1 m although there arereports in mangroves of organic matter depths greater than 1 m (Caamal-Sosa et al 2011Adame amp Fry 2016 Ezcurra et al 2016) The units employed to report the Corg stocksin the coastal blue carbon ecosystems were Mg Corg haminus1 except where indicated Forboth ecosystems our lab data were used as the control for Corg and for both above andbelow ground assessments The georeferenced data were standardized and plotted andcorrections were made for inconsistencies in the location of the sites and derived from thedifferent coordinate systems used in the literature The mangrove zonation used belongs to

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 636

Figure 2 Cartographic representation of climate regions acording to humidity ranges and hydrog-raphy of Mexican coastal areas information of data number (n) for mangrove (M) and seagrass (S) ateach region is provided Reference data provided by CONABIO (2009) Based onMaderey-R amp Torres-Ruata 1990 for hydrology and Garciacutea 1990 for humidity ranges Geographic Coordinate System DatumWGS84

Full-size DOI 107717peerj8790fig-2

the national official regionalization and was proposed by a panel of scientists (CONABIO2009 based on Lugo amp Snedaker 1974) The humidity ranges were defined according toCONABIO (2009) based on Garciacutea (1988) we use humid (Am and Af variations) subhumid (Aw2 Aw1 Aw0 variations) arid (BW) and semi-arid (BS1) classifications Theecological typology criteria used were dwarf basin fringe and hammock (peten) mangrovetypes which could be of interest both for decision makers and for future research atregional and local scales (Fig 2 Table 2) We report the average carbon stored per regionand standard error as a measure of data dispersion

The estimation of the GHG emission pattern due to the loss of mangrove coverage wasperformed based on factors recommended by the IPCC (2014) and Howard et al (2014)The extension changes in mangroves for each region was taken from Valderrama-Landeroset al (2017) who accomplished a national mapping using remote sensing data validatedby more than 1000 verification points and 69000 vertical aerial photographs (Rodriacuteguez-Zuacutentildeiga et al 2013 Valderrama-Landeros et al 2017) The CO2e emissions by mangroveloss were estimated according to the average carbon stored per region and mangrove lost

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 736

Table 2 Characterization of the blue carbon ecosystems inMexico by regions

Region States Climate GT HT Mangrove species Seagrasses species Surf Salinity Int Salinity nMangrove n Seagrasses

North Pacific BC Ag

BCS VA CL Rm Rm A13 A22

Son A SM 2 Lr Zm 345 (34ndash37) 606 B28 B9

Sin SH RE Ce

Nay

Central Pacific Jal Rm

Col SH RE ND Lr ND ND 497 (35ndash78) A6 ND

Mich CL Ag B5

Ce

South Pacific Guerr Ag

Oax SH RE ND Rm ND ND 326 (8ndash38) A69 ND

Chiap H CL LrCe

B30

Gulf of Mexico Tam A Ag Hb

Ver SH RE 1 Rm Hw 331 (11ndash38) 209 (3ndash69) A170 A60

Tab H CL 2 Lr Rm B43 B45

Ce Sf

Tt

Yucatan Peninsula Camp A KS Rm Hw

Yuc SH CL 1 Lr Sf

Q Roo H RE 2 Ag Tt 377 (18ndash50) 39 (05-86) A129 A254

Ce Rm B116 B221

NotesRegions accoriding to CONABIO (2016) Climates are based on humidity ranges (HHumid SHSub-Humid SASemi-arid A Arid) Geomorphological types (GT) are Coastal lagoon (CL) Salt mash(SM) River-estuarine system (RE) and Karst system (KS) Hydrodynamic types (HT) are open (1) and closed (2) The mangrove species are Avicennia germinans (Ag) Rhizophora mangle (Rm) Lagun-cularia racemosa (Lr) Conocarpus erectus (Ce) The Seagrass species are Rupia maritima (Rm) Zostera marina (Zm) Halodule beaudettei (Hb) Halodule wrightii (Hw) Syringodium filiforme (Sf) Thalas-sia testudinum (Tt) indicate dominance ND No data n number of observations of above ground (A) and below ground (B) C stocks

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

836

area The mangroves CO2e emissions were estimated by regions during 1970 and 2015 timeperiod using a conservative approach in which a loss of 25 of the Corg store is assumedin response to land use change (Pendleton et al 2012)

To present an evaluation of the uncertainty of the data in this synthesis the authorJorge Montero analyzed the carbon stock values of mangroves and seagrasses by regionand nonparametric bootstrap confidence intervals were calculated using the method ofadjusted bootstrap percentile (BCa with B= 10000) and bootstrap variance estimatorThe BCa values were calculate using the bootci function in R software and library boots(Canty amp Ripley 2019) The uncertainty was calculated using the bootstrap standard errorand 95 confidence interval for z normal distribution and expressed as a percentage basedon the average value

RESULTS AND DISCUSSIONStudy selectionWe identified 176 articles based on the search criteria however 50 articles were deemedinappropriate and were not used in the final analysis Thus a total of 1220 data points wereextracted from 59 sources for seagrasses and 67 sources for mangroves and they were usedto assess Mexican blue carbon stocks From the first 176 articles selected 50 were screenedout remaining 126 articles whichmeets the quality and requirements for this study (Fig 1)Data on carbon fluxes were scarce evidencing the research needs in this area To improvethe accuracy of the influence from land use on ecosystem carbon dynamics studies whichinclude measurements of stocks and changes along the soil profile are required (Kauffmanamp Bhomia 2017) With respect to seagrasses difficulties involved in mapping the marineenvironment coupled with gap information in the legislative seagrassesrsquo framework ofMexico have resulted in limited knowledge regarding seagrass distribution However theresearchers and national institutions efforts in recent years entails the first official numbersfor the seagrass cover in the Gulf of Mexico

Synthesis of mangrove stocks by above ground and below groundcompartmentsThe average above ground tree biomass was 1136 plusmn 52 Mg Corg haminus1 while the averagebelow ground Corg (soils and roots) was 3852 plusmn 22 Mg Corg haminus1 for a combined total of4988 Mg Corg haminus1 The below ground mean Corg consisted of approximately 77 of thetotal Corg stock for Mexico This value is consistent with other reports for the Corg stocks inMexico which vary between 364 Mg Corg haminus1 and 442 Mg Corg haminus1 (Herrera-Silveira etal 2016 Adame et al 2018) Similar to the present work both studies used literature andoriginal data suggesting that the real value of the total Corg stock of Mexicorsquos mangroveis approximately 434 Mg Corg haminus1 which is a below global average that was reportedelsewhere as ranging from 885 to 937 Mg Corg haminus1 and less than Tier 1 default mangroversquosvalues reported by the IPCC (511 Mg Corg haminus1) Differences among reports and Tier 1estimations are largely due to the underestimation of soil carbon stocks in global studies(Donato et al 2011 Alongi 2012 Hiraishi et al 2014 Kauffman amp Bhomia 2017) In thecase of this systematic review the soil Corg content available in the literature only includes

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 936

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

1136

Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

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Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

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Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

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INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

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Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

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Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

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Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

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Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

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Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

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Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

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Page 5: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

inMexico andno complete synthesis of themitigation value or the greenhouse gases (GHG)emissions related to mangroves and seagrasses existed until now This comprehensivereview is a first step in providing a tool for decisionmakers to develop efficient strategiesaimed at reducing carbon emissions from the loss of these ecosystems while also protectingcurrent levels of carbon capture and storage as well the many ecosystem services providedby mangroves and seagrasses

METHODSA systematic reviewwas conducted at the country level to assess the carbon stocks and fluxesof blue carbon ecosystems in Mexico We use the Preferred Reporting Items for SystematicReviews and Meta-Analyses (PRISMA) (Fig 1) framework and protocols (Moher et al2009a)

Information sources and search strategyAn electronic literature search was performed for carbon stocks and carbon fluxes inmangroves and seagrasses fromMexico We use PubMed (MEDLINE) and Web of Scienceas the primary sources for searches and include open access publications Google Scholarwas a secondary source used to acquire additional literature (thesis technical reports)and the inclusion of gray literature is recommended for systematic reviews to minimizepublication bias (Koricheva Gurevitch amp Mengersen 2013 Pullin amp Stewart 2006)

We also include published databases on Corg stocks from Herrera-Silveira et al (2018a)and Herrera-Silveira et al (2018b) and the Mexican Carbon Program (PMC) which havebeen validated and reviewed by experts and organizations of the federal governmentand civil society (CONABIO and CONAFOR) and subjected to public consultation(httppmcarbonoorgpmc) In the initial phase titles and abstracts from network werescreened to identify potential eligible studies In the second phase full texts of the remainingarticles were read to determine if they meet the inclusion and exclusion criteria Whendisagreement emerged regarding the eligibility of studies the main author Jorge A HerreraSilveira made the final decision

The search of carbon stocks and fluxes extended from 1987 to 2018 and includedkeywords (exclusively in Spanish and English) population (lsquolsquomangroversquorsquo OR lsquolsquoseagrassrsquorsquoOR lsquolsquoSubmerged aquatic vegetationrsquorsquo OR lsquolsquowetlandsrsquorsquo OR lsquolsquocoastal basinrsquorsquo OR lsquolsquocoastrsquorsquo)AND compartments (lsquolsquoForest structurersquorsquo OR lsquolsquoecosystem structurersquorsquo OR lsquolsquoDBHrsquorsquo ORlsquolsquobiomassrsquorsquo OR lsquolsquoabove groundrsquorsquo AND lsquolsquobiomassrsquorsquo OR lsquolsquobelow groundrsquorsquo AND lsquolsquobiomassrsquorsquoOR lsquolsquolitter productivityrsquorsquo OR lsquolsquocarbonrsquorsquo AND lsquolsquofluxrsquorsquo OR lsquolsquodecompositionrsquorsquo OR lsquolsquosoilrsquorsquo ANDlsquolsquocarbonrsquorsquo OR lsquolsquosoilrsquorsquo AND lsquolsquoorganic matterrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquoorganic matterrsquorsquo ORlsquolsquosoilrsquorsquo AND lsquolsquobulk densityrsquorsquo OR lsquolsquosedimentrsquorsquo AND lsquolsquobulk densityrsquorsquo) AND lsquolsquolocationrsquorsquo (vglsquolsquoGulf of Mexicorsquorsquo OR lsquolsquoPacificrsquorsquo OR lsquolsquoYucatan Peninsularsquorsquo) OR lsquolsquoMexican CaribbeanrsquorsquoOR state names (vg lsquolsquoYucatanrsquorsquo OR lsquolsquoCampechersquorsquo lsquolsquoQuintana Roorsquorsquo OR lsquolsquoTabascorsquorsquo ORlsquolsquoVeracruzrsquorsquo OR lsquolsquoTamaulipasrsquorsquo OR lsquolsquoBaja California Surrsquorsquo OR lsquolsquoBaja California NortersquorsquoOR lsquolsquoSinaloarsquorsquo OR lsquolsquoOaxacarsquorsquo OR lsquolsquoChiapasrsquorsquo) OR specific site names (vg lsquolsquoLagunade Terminosrsquorsquo OR lsquolsquoMagdalena Bayrsquorsquo OR lsquolsquoSian Karsquoanrsquorsquo OR lsquolsquoLa Encrucijadarsquorsquo OR lsquolsquoLa

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Mancharsquorsquo OR lsquolsquoLaguna Alvaradorsquorsquo OR lsquolsquoSanQuintiacuten Bayrsquorsquo OR lsquolsquoMarismasNacionalesrsquorsquo ORlsquolsquoCelestuacutenrsquorsquo OR rsquorsquo Laguna Madrersquorsquo OR lsquolsquoBarra de Navidadrsquorsquo OR lsquolsquoLaguna Mar Muertorsquorsquo)

The searches were undertaken independently by authors with at least five years ofexperience in sampling laboratory analysis and proven experience in data analysisand redaction of technical reports on blue carbon ecosystems The five researchers formangrove review were the coauthors Andrea Camacho-Rico Monica A Pech-CardenasSiuling Cinco-Castro for sediments were Eunice Y Pech-Poot and Juan P Caamal Sosaand for seagrasses were Juan E Mendoza-Mantiacutenez and Sara M Morales-Ojeda

Eligibility criteriaWe include studies and datasets that report the biomass organic carbon stock organicmatter and bulk density in sediments per unit of area and spatially referenced or flux datafrommangroves and seagrasses For mangroves an important criterion was the plot design(including at least three replicates) to guarantee the representativeness of the data forseagrasses we looked for studies that based their results on quadrants or cylindrical coresampler along transects No conference abstracts were considered to meet the inclusioncriteria

Data extraction and analysisData extraction was independently performed by authors (Andrea Camacho Rico MonicaA Pech -Cardenas Siuling Cinco-Castro Eunice Y Pech-Poot Juan P Caamal-Sosa JuanE Mendoza-Martinez and Sara M Morales Ojeda) Study-specific variables were recordedfor each entry Many properties assessed in this review were reported as contextualenvironmental data rather than the primary outcome for their respective studies (noreplicates or dispersion measures described) which was why bias was not reported inthis study We include entries such as geographic location and region (according toValderrama-Landeros et al 2017) environmental characteristics including ecological type(Lugo amp Snedaker 1974) sample compartment (above and below ground components)mangrove fluxes by litterfall biomass andor constant decay of litter

The estimation of Corg stocks was carried out for mangroves by authors Monica APech-Cardenas Andrea Camacho-Rico Juan P Caamal-Sosa Claudia Teutli-Hernandezand for seagrasses by Juan E Mendoza-Martinez and Sara M Morales Ojeda and thesupervisor was Jorge A Herrera-Silveira The above and below ground biomass of allthe studies were converted to organic carbon using the factor 045 for mangroves and035 for seagrasses (Fourqurean et al 2012a Howard et al 2014 Kauffman amp Donato2012) The total soil Corg pool was standardized to a depth of 1 m although there arereports in mangroves of organic matter depths greater than 1 m (Caamal-Sosa et al 2011Adame amp Fry 2016 Ezcurra et al 2016) The units employed to report the Corg stocksin the coastal blue carbon ecosystems were Mg Corg haminus1 except where indicated Forboth ecosystems our lab data were used as the control for Corg and for both above andbelow ground assessments The georeferenced data were standardized and plotted andcorrections were made for inconsistencies in the location of the sites and derived from thedifferent coordinate systems used in the literature The mangrove zonation used belongs to

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 636

Figure 2 Cartographic representation of climate regions acording to humidity ranges and hydrog-raphy of Mexican coastal areas information of data number (n) for mangrove (M) and seagrass (S) ateach region is provided Reference data provided by CONABIO (2009) Based onMaderey-R amp Torres-Ruata 1990 for hydrology and Garciacutea 1990 for humidity ranges Geographic Coordinate System DatumWGS84

Full-size DOI 107717peerj8790fig-2

the national official regionalization and was proposed by a panel of scientists (CONABIO2009 based on Lugo amp Snedaker 1974) The humidity ranges were defined according toCONABIO (2009) based on Garciacutea (1988) we use humid (Am and Af variations) subhumid (Aw2 Aw1 Aw0 variations) arid (BW) and semi-arid (BS1) classifications Theecological typology criteria used were dwarf basin fringe and hammock (peten) mangrovetypes which could be of interest both for decision makers and for future research atregional and local scales (Fig 2 Table 2) We report the average carbon stored per regionand standard error as a measure of data dispersion

The estimation of the GHG emission pattern due to the loss of mangrove coverage wasperformed based on factors recommended by the IPCC (2014) and Howard et al (2014)The extension changes in mangroves for each region was taken from Valderrama-Landeroset al (2017) who accomplished a national mapping using remote sensing data validatedby more than 1000 verification points and 69000 vertical aerial photographs (Rodriacuteguez-Zuacutentildeiga et al 2013 Valderrama-Landeros et al 2017) The CO2e emissions by mangroveloss were estimated according to the average carbon stored per region and mangrove lost

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 736

Table 2 Characterization of the blue carbon ecosystems inMexico by regions

Region States Climate GT HT Mangrove species Seagrasses species Surf Salinity Int Salinity nMangrove n Seagrasses

North Pacific BC Ag

BCS VA CL Rm Rm A13 A22

Son A SM 2 Lr Zm 345 (34ndash37) 606 B28 B9

Sin SH RE Ce

Nay

Central Pacific Jal Rm

Col SH RE ND Lr ND ND 497 (35ndash78) A6 ND

Mich CL Ag B5

Ce

South Pacific Guerr Ag

Oax SH RE ND Rm ND ND 326 (8ndash38) A69 ND

Chiap H CL LrCe

B30

Gulf of Mexico Tam A Ag Hb

Ver SH RE 1 Rm Hw 331 (11ndash38) 209 (3ndash69) A170 A60

Tab H CL 2 Lr Rm B43 B45

Ce Sf

Tt

Yucatan Peninsula Camp A KS Rm Hw

Yuc SH CL 1 Lr Sf

Q Roo H RE 2 Ag Tt 377 (18ndash50) 39 (05-86) A129 A254

Ce Rm B116 B221

NotesRegions accoriding to CONABIO (2016) Climates are based on humidity ranges (HHumid SHSub-Humid SASemi-arid A Arid) Geomorphological types (GT) are Coastal lagoon (CL) Salt mash(SM) River-estuarine system (RE) and Karst system (KS) Hydrodynamic types (HT) are open (1) and closed (2) The mangrove species are Avicennia germinans (Ag) Rhizophora mangle (Rm) Lagun-cularia racemosa (Lr) Conocarpus erectus (Ce) The Seagrass species are Rupia maritima (Rm) Zostera marina (Zm) Halodule beaudettei (Hb) Halodule wrightii (Hw) Syringodium filiforme (Sf) Thalas-sia testudinum (Tt) indicate dominance ND No data n number of observations of above ground (A) and below ground (B) C stocks

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area The mangroves CO2e emissions were estimated by regions during 1970 and 2015 timeperiod using a conservative approach in which a loss of 25 of the Corg store is assumedin response to land use change (Pendleton et al 2012)

To present an evaluation of the uncertainty of the data in this synthesis the authorJorge Montero analyzed the carbon stock values of mangroves and seagrasses by regionand nonparametric bootstrap confidence intervals were calculated using the method ofadjusted bootstrap percentile (BCa with B= 10000) and bootstrap variance estimatorThe BCa values were calculate using the bootci function in R software and library boots(Canty amp Ripley 2019) The uncertainty was calculated using the bootstrap standard errorand 95 confidence interval for z normal distribution and expressed as a percentage basedon the average value

RESULTS AND DISCUSSIONStudy selectionWe identified 176 articles based on the search criteria however 50 articles were deemedinappropriate and were not used in the final analysis Thus a total of 1220 data points wereextracted from 59 sources for seagrasses and 67 sources for mangroves and they were usedto assess Mexican blue carbon stocks From the first 176 articles selected 50 were screenedout remaining 126 articles whichmeets the quality and requirements for this study (Fig 1)Data on carbon fluxes were scarce evidencing the research needs in this area To improvethe accuracy of the influence from land use on ecosystem carbon dynamics studies whichinclude measurements of stocks and changes along the soil profile are required (Kauffmanamp Bhomia 2017) With respect to seagrasses difficulties involved in mapping the marineenvironment coupled with gap information in the legislative seagrassesrsquo framework ofMexico have resulted in limited knowledge regarding seagrass distribution However theresearchers and national institutions efforts in recent years entails the first official numbersfor the seagrass cover in the Gulf of Mexico

Synthesis of mangrove stocks by above ground and below groundcompartmentsThe average above ground tree biomass was 1136 plusmn 52 Mg Corg haminus1 while the averagebelow ground Corg (soils and roots) was 3852 plusmn 22 Mg Corg haminus1 for a combined total of4988 Mg Corg haminus1 The below ground mean Corg consisted of approximately 77 of thetotal Corg stock for Mexico This value is consistent with other reports for the Corg stocks inMexico which vary between 364 Mg Corg haminus1 and 442 Mg Corg haminus1 (Herrera-Silveira etal 2016 Adame et al 2018) Similar to the present work both studies used literature andoriginal data suggesting that the real value of the total Corg stock of Mexicorsquos mangroveis approximately 434 Mg Corg haminus1 which is a below global average that was reportedelsewhere as ranging from 885 to 937 Mg Corg haminus1 and less than Tier 1 default mangroversquosvalues reported by the IPCC (511 Mg Corg haminus1) Differences among reports and Tier 1estimations are largely due to the underestimation of soil carbon stocks in global studies(Donato et al 2011 Alongi 2012 Hiraishi et al 2014 Kauffman amp Bhomia 2017) In thecase of this systematic review the soil Corg content available in the literature only includes

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 936

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

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Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

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Page 6: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Mancharsquorsquo OR lsquolsquoLaguna Alvaradorsquorsquo OR lsquolsquoSanQuintiacuten Bayrsquorsquo OR lsquolsquoMarismasNacionalesrsquorsquo ORlsquolsquoCelestuacutenrsquorsquo OR rsquorsquo Laguna Madrersquorsquo OR lsquolsquoBarra de Navidadrsquorsquo OR lsquolsquoLaguna Mar Muertorsquorsquo)

The searches were undertaken independently by authors with at least five years ofexperience in sampling laboratory analysis and proven experience in data analysisand redaction of technical reports on blue carbon ecosystems The five researchers formangrove review were the coauthors Andrea Camacho-Rico Monica A Pech-CardenasSiuling Cinco-Castro for sediments were Eunice Y Pech-Poot and Juan P Caamal Sosaand for seagrasses were Juan E Mendoza-Mantiacutenez and Sara M Morales-Ojeda

Eligibility criteriaWe include studies and datasets that report the biomass organic carbon stock organicmatter and bulk density in sediments per unit of area and spatially referenced or flux datafrommangroves and seagrasses For mangroves an important criterion was the plot design(including at least three replicates) to guarantee the representativeness of the data forseagrasses we looked for studies that based their results on quadrants or cylindrical coresampler along transects No conference abstracts were considered to meet the inclusioncriteria

Data extraction and analysisData extraction was independently performed by authors (Andrea Camacho Rico MonicaA Pech -Cardenas Siuling Cinco-Castro Eunice Y Pech-Poot Juan P Caamal-Sosa JuanE Mendoza-Martinez and Sara M Morales Ojeda) Study-specific variables were recordedfor each entry Many properties assessed in this review were reported as contextualenvironmental data rather than the primary outcome for their respective studies (noreplicates or dispersion measures described) which was why bias was not reported inthis study We include entries such as geographic location and region (according toValderrama-Landeros et al 2017) environmental characteristics including ecological type(Lugo amp Snedaker 1974) sample compartment (above and below ground components)mangrove fluxes by litterfall biomass andor constant decay of litter

The estimation of Corg stocks was carried out for mangroves by authors Monica APech-Cardenas Andrea Camacho-Rico Juan P Caamal-Sosa Claudia Teutli-Hernandezand for seagrasses by Juan E Mendoza-Martinez and Sara M Morales Ojeda and thesupervisor was Jorge A Herrera-Silveira The above and below ground biomass of allthe studies were converted to organic carbon using the factor 045 for mangroves and035 for seagrasses (Fourqurean et al 2012a Howard et al 2014 Kauffman amp Donato2012) The total soil Corg pool was standardized to a depth of 1 m although there arereports in mangroves of organic matter depths greater than 1 m (Caamal-Sosa et al 2011Adame amp Fry 2016 Ezcurra et al 2016) The units employed to report the Corg stocksin the coastal blue carbon ecosystems were Mg Corg haminus1 except where indicated Forboth ecosystems our lab data were used as the control for Corg and for both above andbelow ground assessments The georeferenced data were standardized and plotted andcorrections were made for inconsistencies in the location of the sites and derived from thedifferent coordinate systems used in the literature The mangrove zonation used belongs to

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 636

Figure 2 Cartographic representation of climate regions acording to humidity ranges and hydrog-raphy of Mexican coastal areas information of data number (n) for mangrove (M) and seagrass (S) ateach region is provided Reference data provided by CONABIO (2009) Based onMaderey-R amp Torres-Ruata 1990 for hydrology and Garciacutea 1990 for humidity ranges Geographic Coordinate System DatumWGS84

Full-size DOI 107717peerj8790fig-2

the national official regionalization and was proposed by a panel of scientists (CONABIO2009 based on Lugo amp Snedaker 1974) The humidity ranges were defined according toCONABIO (2009) based on Garciacutea (1988) we use humid (Am and Af variations) subhumid (Aw2 Aw1 Aw0 variations) arid (BW) and semi-arid (BS1) classifications Theecological typology criteria used were dwarf basin fringe and hammock (peten) mangrovetypes which could be of interest both for decision makers and for future research atregional and local scales (Fig 2 Table 2) We report the average carbon stored per regionand standard error as a measure of data dispersion

The estimation of the GHG emission pattern due to the loss of mangrove coverage wasperformed based on factors recommended by the IPCC (2014) and Howard et al (2014)The extension changes in mangroves for each region was taken from Valderrama-Landeroset al (2017) who accomplished a national mapping using remote sensing data validatedby more than 1000 verification points and 69000 vertical aerial photographs (Rodriacuteguez-Zuacutentildeiga et al 2013 Valderrama-Landeros et al 2017) The CO2e emissions by mangroveloss were estimated according to the average carbon stored per region and mangrove lost

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 736

Table 2 Characterization of the blue carbon ecosystems inMexico by regions

Region States Climate GT HT Mangrove species Seagrasses species Surf Salinity Int Salinity nMangrove n Seagrasses

North Pacific BC Ag

BCS VA CL Rm Rm A13 A22

Son A SM 2 Lr Zm 345 (34ndash37) 606 B28 B9

Sin SH RE Ce

Nay

Central Pacific Jal Rm

Col SH RE ND Lr ND ND 497 (35ndash78) A6 ND

Mich CL Ag B5

Ce

South Pacific Guerr Ag

Oax SH RE ND Rm ND ND 326 (8ndash38) A69 ND

Chiap H CL LrCe

B30

Gulf of Mexico Tam A Ag Hb

Ver SH RE 1 Rm Hw 331 (11ndash38) 209 (3ndash69) A170 A60

Tab H CL 2 Lr Rm B43 B45

Ce Sf

Tt

Yucatan Peninsula Camp A KS Rm Hw

Yuc SH CL 1 Lr Sf

Q Roo H RE 2 Ag Tt 377 (18ndash50) 39 (05-86) A129 A254

Ce Rm B116 B221

NotesRegions accoriding to CONABIO (2016) Climates are based on humidity ranges (HHumid SHSub-Humid SASemi-arid A Arid) Geomorphological types (GT) are Coastal lagoon (CL) Salt mash(SM) River-estuarine system (RE) and Karst system (KS) Hydrodynamic types (HT) are open (1) and closed (2) The mangrove species are Avicennia germinans (Ag) Rhizophora mangle (Rm) Lagun-cularia racemosa (Lr) Conocarpus erectus (Ce) The Seagrass species are Rupia maritima (Rm) Zostera marina (Zm) Halodule beaudettei (Hb) Halodule wrightii (Hw) Syringodium filiforme (Sf) Thalas-sia testudinum (Tt) indicate dominance ND No data n number of observations of above ground (A) and below ground (B) C stocks

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area The mangroves CO2e emissions were estimated by regions during 1970 and 2015 timeperiod using a conservative approach in which a loss of 25 of the Corg store is assumedin response to land use change (Pendleton et al 2012)

To present an evaluation of the uncertainty of the data in this synthesis the authorJorge Montero analyzed the carbon stock values of mangroves and seagrasses by regionand nonparametric bootstrap confidence intervals were calculated using the method ofadjusted bootstrap percentile (BCa with B= 10000) and bootstrap variance estimatorThe BCa values were calculate using the bootci function in R software and library boots(Canty amp Ripley 2019) The uncertainty was calculated using the bootstrap standard errorand 95 confidence interval for z normal distribution and expressed as a percentage basedon the average value

RESULTS AND DISCUSSIONStudy selectionWe identified 176 articles based on the search criteria however 50 articles were deemedinappropriate and were not used in the final analysis Thus a total of 1220 data points wereextracted from 59 sources for seagrasses and 67 sources for mangroves and they were usedto assess Mexican blue carbon stocks From the first 176 articles selected 50 were screenedout remaining 126 articles whichmeets the quality and requirements for this study (Fig 1)Data on carbon fluxes were scarce evidencing the research needs in this area To improvethe accuracy of the influence from land use on ecosystem carbon dynamics studies whichinclude measurements of stocks and changes along the soil profile are required (Kauffmanamp Bhomia 2017) With respect to seagrasses difficulties involved in mapping the marineenvironment coupled with gap information in the legislative seagrassesrsquo framework ofMexico have resulted in limited knowledge regarding seagrass distribution However theresearchers and national institutions efforts in recent years entails the first official numbersfor the seagrass cover in the Gulf of Mexico

Synthesis of mangrove stocks by above ground and below groundcompartmentsThe average above ground tree biomass was 1136 plusmn 52 Mg Corg haminus1 while the averagebelow ground Corg (soils and roots) was 3852 plusmn 22 Mg Corg haminus1 for a combined total of4988 Mg Corg haminus1 The below ground mean Corg consisted of approximately 77 of thetotal Corg stock for Mexico This value is consistent with other reports for the Corg stocks inMexico which vary between 364 Mg Corg haminus1 and 442 Mg Corg haminus1 (Herrera-Silveira etal 2016 Adame et al 2018) Similar to the present work both studies used literature andoriginal data suggesting that the real value of the total Corg stock of Mexicorsquos mangroveis approximately 434 Mg Corg haminus1 which is a below global average that was reportedelsewhere as ranging from 885 to 937 Mg Corg haminus1 and less than Tier 1 default mangroversquosvalues reported by the IPCC (511 Mg Corg haminus1) Differences among reports and Tier 1estimations are largely due to the underestimation of soil carbon stocks in global studies(Donato et al 2011 Alongi 2012 Hiraishi et al 2014 Kauffman amp Bhomia 2017) In thecase of this systematic review the soil Corg content available in the literature only includes

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 936

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

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Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2736

ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 7: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Figure 2 Cartographic representation of climate regions acording to humidity ranges and hydrog-raphy of Mexican coastal areas information of data number (n) for mangrove (M) and seagrass (S) ateach region is provided Reference data provided by CONABIO (2009) Based onMaderey-R amp Torres-Ruata 1990 for hydrology and Garciacutea 1990 for humidity ranges Geographic Coordinate System DatumWGS84

Full-size DOI 107717peerj8790fig-2

the national official regionalization and was proposed by a panel of scientists (CONABIO2009 based on Lugo amp Snedaker 1974) The humidity ranges were defined according toCONABIO (2009) based on Garciacutea (1988) we use humid (Am and Af variations) subhumid (Aw2 Aw1 Aw0 variations) arid (BW) and semi-arid (BS1) classifications Theecological typology criteria used were dwarf basin fringe and hammock (peten) mangrovetypes which could be of interest both for decision makers and for future research atregional and local scales (Fig 2 Table 2) We report the average carbon stored per regionand standard error as a measure of data dispersion

The estimation of the GHG emission pattern due to the loss of mangrove coverage wasperformed based on factors recommended by the IPCC (2014) and Howard et al (2014)The extension changes in mangroves for each region was taken from Valderrama-Landeroset al (2017) who accomplished a national mapping using remote sensing data validatedby more than 1000 verification points and 69000 vertical aerial photographs (Rodriacuteguez-Zuacutentildeiga et al 2013 Valderrama-Landeros et al 2017) The CO2e emissions by mangroveloss were estimated according to the average carbon stored per region and mangrove lost

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 736

Table 2 Characterization of the blue carbon ecosystems inMexico by regions

Region States Climate GT HT Mangrove species Seagrasses species Surf Salinity Int Salinity nMangrove n Seagrasses

North Pacific BC Ag

BCS VA CL Rm Rm A13 A22

Son A SM 2 Lr Zm 345 (34ndash37) 606 B28 B9

Sin SH RE Ce

Nay

Central Pacific Jal Rm

Col SH RE ND Lr ND ND 497 (35ndash78) A6 ND

Mich CL Ag B5

Ce

South Pacific Guerr Ag

Oax SH RE ND Rm ND ND 326 (8ndash38) A69 ND

Chiap H CL LrCe

B30

Gulf of Mexico Tam A Ag Hb

Ver SH RE 1 Rm Hw 331 (11ndash38) 209 (3ndash69) A170 A60

Tab H CL 2 Lr Rm B43 B45

Ce Sf

Tt

Yucatan Peninsula Camp A KS Rm Hw

Yuc SH CL 1 Lr Sf

Q Roo H RE 2 Ag Tt 377 (18ndash50) 39 (05-86) A129 A254

Ce Rm B116 B221

NotesRegions accoriding to CONABIO (2016) Climates are based on humidity ranges (HHumid SHSub-Humid SASemi-arid A Arid) Geomorphological types (GT) are Coastal lagoon (CL) Salt mash(SM) River-estuarine system (RE) and Karst system (KS) Hydrodynamic types (HT) are open (1) and closed (2) The mangrove species are Avicennia germinans (Ag) Rhizophora mangle (Rm) Lagun-cularia racemosa (Lr) Conocarpus erectus (Ce) The Seagrass species are Rupia maritima (Rm) Zostera marina (Zm) Halodule beaudettei (Hb) Halodule wrightii (Hw) Syringodium filiforme (Sf) Thalas-sia testudinum (Tt) indicate dominance ND No data n number of observations of above ground (A) and below ground (B) C stocks

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

836

area The mangroves CO2e emissions were estimated by regions during 1970 and 2015 timeperiod using a conservative approach in which a loss of 25 of the Corg store is assumedin response to land use change (Pendleton et al 2012)

To present an evaluation of the uncertainty of the data in this synthesis the authorJorge Montero analyzed the carbon stock values of mangroves and seagrasses by regionand nonparametric bootstrap confidence intervals were calculated using the method ofadjusted bootstrap percentile (BCa with B= 10000) and bootstrap variance estimatorThe BCa values were calculate using the bootci function in R software and library boots(Canty amp Ripley 2019) The uncertainty was calculated using the bootstrap standard errorand 95 confidence interval for z normal distribution and expressed as a percentage basedon the average value

RESULTS AND DISCUSSIONStudy selectionWe identified 176 articles based on the search criteria however 50 articles were deemedinappropriate and were not used in the final analysis Thus a total of 1220 data points wereextracted from 59 sources for seagrasses and 67 sources for mangroves and they were usedto assess Mexican blue carbon stocks From the first 176 articles selected 50 were screenedout remaining 126 articles whichmeets the quality and requirements for this study (Fig 1)Data on carbon fluxes were scarce evidencing the research needs in this area To improvethe accuracy of the influence from land use on ecosystem carbon dynamics studies whichinclude measurements of stocks and changes along the soil profile are required (Kauffmanamp Bhomia 2017) With respect to seagrasses difficulties involved in mapping the marineenvironment coupled with gap information in the legislative seagrassesrsquo framework ofMexico have resulted in limited knowledge regarding seagrass distribution However theresearchers and national institutions efforts in recent years entails the first official numbersfor the seagrass cover in the Gulf of Mexico

Synthesis of mangrove stocks by above ground and below groundcompartmentsThe average above ground tree biomass was 1136 plusmn 52 Mg Corg haminus1 while the averagebelow ground Corg (soils and roots) was 3852 plusmn 22 Mg Corg haminus1 for a combined total of4988 Mg Corg haminus1 The below ground mean Corg consisted of approximately 77 of thetotal Corg stock for Mexico This value is consistent with other reports for the Corg stocks inMexico which vary between 364 Mg Corg haminus1 and 442 Mg Corg haminus1 (Herrera-Silveira etal 2016 Adame et al 2018) Similar to the present work both studies used literature andoriginal data suggesting that the real value of the total Corg stock of Mexicorsquos mangroveis approximately 434 Mg Corg haminus1 which is a below global average that was reportedelsewhere as ranging from 885 to 937 Mg Corg haminus1 and less than Tier 1 default mangroversquosvalues reported by the IPCC (511 Mg Corg haminus1) Differences among reports and Tier 1estimations are largely due to the underestimation of soil carbon stocks in global studies(Donato et al 2011 Alongi 2012 Hiraishi et al 2014 Kauffman amp Bhomia 2017) In thecase of this systematic review the soil Corg content available in the literature only includes

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 936

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

1136

Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

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INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

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Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

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Page 8: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Table 2 Characterization of the blue carbon ecosystems inMexico by regions

Region States Climate GT HT Mangrove species Seagrasses species Surf Salinity Int Salinity nMangrove n Seagrasses

North Pacific BC Ag

BCS VA CL Rm Rm A13 A22

Son A SM 2 Lr Zm 345 (34ndash37) 606 B28 B9

Sin SH RE Ce

Nay

Central Pacific Jal Rm

Col SH RE ND Lr ND ND 497 (35ndash78) A6 ND

Mich CL Ag B5

Ce

South Pacific Guerr Ag

Oax SH RE ND Rm ND ND 326 (8ndash38) A69 ND

Chiap H CL LrCe

B30

Gulf of Mexico Tam A Ag Hb

Ver SH RE 1 Rm Hw 331 (11ndash38) 209 (3ndash69) A170 A60

Tab H CL 2 Lr Rm B43 B45

Ce Sf

Tt

Yucatan Peninsula Camp A KS Rm Hw

Yuc SH CL 1 Lr Sf

Q Roo H RE 2 Ag Tt 377 (18ndash50) 39 (05-86) A129 A254

Ce Rm B116 B221

NotesRegions accoriding to CONABIO (2016) Climates are based on humidity ranges (HHumid SHSub-Humid SASemi-arid A Arid) Geomorphological types (GT) are Coastal lagoon (CL) Salt mash(SM) River-estuarine system (RE) and Karst system (KS) Hydrodynamic types (HT) are open (1) and closed (2) The mangrove species are Avicennia germinans (Ag) Rhizophora mangle (Rm) Lagun-cularia racemosa (Lr) Conocarpus erectus (Ce) The Seagrass species are Rupia maritima (Rm) Zostera marina (Zm) Halodule beaudettei (Hb) Halodule wrightii (Hw) Syringodium filiforme (Sf) Thalas-sia testudinum (Tt) indicate dominance ND No data n number of observations of above ground (A) and below ground (B) C stocks

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area The mangroves CO2e emissions were estimated by regions during 1970 and 2015 timeperiod using a conservative approach in which a loss of 25 of the Corg store is assumedin response to land use change (Pendleton et al 2012)

To present an evaluation of the uncertainty of the data in this synthesis the authorJorge Montero analyzed the carbon stock values of mangroves and seagrasses by regionand nonparametric bootstrap confidence intervals were calculated using the method ofadjusted bootstrap percentile (BCa with B= 10000) and bootstrap variance estimatorThe BCa values were calculate using the bootci function in R software and library boots(Canty amp Ripley 2019) The uncertainty was calculated using the bootstrap standard errorand 95 confidence interval for z normal distribution and expressed as a percentage basedon the average value

RESULTS AND DISCUSSIONStudy selectionWe identified 176 articles based on the search criteria however 50 articles were deemedinappropriate and were not used in the final analysis Thus a total of 1220 data points wereextracted from 59 sources for seagrasses and 67 sources for mangroves and they were usedto assess Mexican blue carbon stocks From the first 176 articles selected 50 were screenedout remaining 126 articles whichmeets the quality and requirements for this study (Fig 1)Data on carbon fluxes were scarce evidencing the research needs in this area To improvethe accuracy of the influence from land use on ecosystem carbon dynamics studies whichinclude measurements of stocks and changes along the soil profile are required (Kauffmanamp Bhomia 2017) With respect to seagrasses difficulties involved in mapping the marineenvironment coupled with gap information in the legislative seagrassesrsquo framework ofMexico have resulted in limited knowledge regarding seagrass distribution However theresearchers and national institutions efforts in recent years entails the first official numbersfor the seagrass cover in the Gulf of Mexico

Synthesis of mangrove stocks by above ground and below groundcompartmentsThe average above ground tree biomass was 1136 plusmn 52 Mg Corg haminus1 while the averagebelow ground Corg (soils and roots) was 3852 plusmn 22 Mg Corg haminus1 for a combined total of4988 Mg Corg haminus1 The below ground mean Corg consisted of approximately 77 of thetotal Corg stock for Mexico This value is consistent with other reports for the Corg stocks inMexico which vary between 364 Mg Corg haminus1 and 442 Mg Corg haminus1 (Herrera-Silveira etal 2016 Adame et al 2018) Similar to the present work both studies used literature andoriginal data suggesting that the real value of the total Corg stock of Mexicorsquos mangroveis approximately 434 Mg Corg haminus1 which is a below global average that was reportedelsewhere as ranging from 885 to 937 Mg Corg haminus1 and less than Tier 1 default mangroversquosvalues reported by the IPCC (511 Mg Corg haminus1) Differences among reports and Tier 1estimations are largely due to the underestimation of soil carbon stocks in global studies(Donato et al 2011 Alongi 2012 Hiraishi et al 2014 Kauffman amp Bhomia 2017) In thecase of this systematic review the soil Corg content available in the literature only includes

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 936

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

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Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

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Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

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Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2736

ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

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Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 9: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

area The mangroves CO2e emissions were estimated by regions during 1970 and 2015 timeperiod using a conservative approach in which a loss of 25 of the Corg store is assumedin response to land use change (Pendleton et al 2012)

To present an evaluation of the uncertainty of the data in this synthesis the authorJorge Montero analyzed the carbon stock values of mangroves and seagrasses by regionand nonparametric bootstrap confidence intervals were calculated using the method ofadjusted bootstrap percentile (BCa with B= 10000) and bootstrap variance estimatorThe BCa values were calculate using the bootci function in R software and library boots(Canty amp Ripley 2019) The uncertainty was calculated using the bootstrap standard errorand 95 confidence interval for z normal distribution and expressed as a percentage basedon the average value

RESULTS AND DISCUSSIONStudy selectionWe identified 176 articles based on the search criteria however 50 articles were deemedinappropriate and were not used in the final analysis Thus a total of 1220 data points wereextracted from 59 sources for seagrasses and 67 sources for mangroves and they were usedto assess Mexican blue carbon stocks From the first 176 articles selected 50 were screenedout remaining 126 articles whichmeets the quality and requirements for this study (Fig 1)Data on carbon fluxes were scarce evidencing the research needs in this area To improvethe accuracy of the influence from land use on ecosystem carbon dynamics studies whichinclude measurements of stocks and changes along the soil profile are required (Kauffmanamp Bhomia 2017) With respect to seagrasses difficulties involved in mapping the marineenvironment coupled with gap information in the legislative seagrassesrsquo framework ofMexico have resulted in limited knowledge regarding seagrass distribution However theresearchers and national institutions efforts in recent years entails the first official numbersfor the seagrass cover in the Gulf of Mexico

Synthesis of mangrove stocks by above ground and below groundcompartmentsThe average above ground tree biomass was 1136 plusmn 52 Mg Corg haminus1 while the averagebelow ground Corg (soils and roots) was 3852 plusmn 22 Mg Corg haminus1 for a combined total of4988 Mg Corg haminus1 The below ground mean Corg consisted of approximately 77 of thetotal Corg stock for Mexico This value is consistent with other reports for the Corg stocks inMexico which vary between 364 Mg Corg haminus1 and 442 Mg Corg haminus1 (Herrera-Silveira etal 2016 Adame et al 2018) Similar to the present work both studies used literature andoriginal data suggesting that the real value of the total Corg stock of Mexicorsquos mangroveis approximately 434 Mg Corg haminus1 which is a below global average that was reportedelsewhere as ranging from 885 to 937 Mg Corg haminus1 and less than Tier 1 default mangroversquosvalues reported by the IPCC (511 Mg Corg haminus1) Differences among reports and Tier 1estimations are largely due to the underestimation of soil carbon stocks in global studies(Donato et al 2011 Alongi 2012 Hiraishi et al 2014 Kauffman amp Bhomia 2017) In thecase of this systematic review the soil Corg content available in the literature only includes

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 936

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

1136

Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 10: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

the first 30 cm (soil deep) and the standardized 1 m values rank from lt10 to 2233 Mg Corg

haminus1 (Table 3) In general the low values must be taken with caution as the largest Corg

stock of those soils could be deeper than 30 cm thus more work on soil profiles is requiredaccording to the protocols in the cited studies for the diverse blue carbon environmentalsettings of Mexico

The mean downed wood stock was 1519 plusmn 41 Mg Corg haminus1 and represented up to12 of the Corg above ground reservoir The root component represented 5ndash9 of theunderground Corg stocks with an average of 266 plusmn 28 Mg Corg haminus1 Fine roots shouldbe considered as an important component of underground Corg sequestration due to thehigh productivity and decomposition rates (Adame et al 2014 Ouyang Lee amp Connolly2017) Few studies have demonstrated that the below ground fine root biomass contributesignificantly (gt20) to the below ground live Corg stock in mangrove forests (Adame et al2014 Robertson amp Alongi 2016 Santos et al 2017) This component is not just importantfor Corg inventories although their turnover rates contribute to a high Corg capture whichis why we consider them as a part of the subterranean carbon analysis

Synthesis of carbon stocks in mangroves by region and humidityrangeThe South Pacific presents the largest above ground and below ground stock means of Corg

(154 8 plusmn 15 Mg Corg haminus1 and 6631 plusmn 51 Mg Corg haminus1) the North Pacific registered thelowest stock above ground average of Corg (589plusmn 12MgCorg haminus1) and the Central Pacificpresented the lowest below ground Corg stock average (1122 Mg Corg haminus1) (Fig 3A) Inthe South Pacific region the humid climate and geomorphological features create ahydrological condition that favors the development of tall mangrove forests reaching themaximum diversity In contrast the Central Pacific and North Pacific coast account fora narrow continental shelf under arid or semi-arid conditions and few intertidal areaswhich reduces the number of habitats available for mangroves and provides less favorableconditions for Corg storage The uncertainty value recorded for the Central Pacific region(423) was associated with the scarce literature registered for this region

Meanwhile the uncertainty of the regions of the Gulf of Mexico and the YucatanPeninsula was low (Table 3) and the uncertainty results indicate that the database for theseregions is robust for country- and global-scale analyzes

The downed wood biomass for carbon estimation was considered only for the Gulfof Mexico Yucatan Peninsula and South Pacific regions (Fig 3A) due to its relevance asa source of carbon in sites exposed to hydrometeorological impacts such as hurricanesand storms Thus this component is important in these regions where the frequency andintensity of these events is expected to increase in the face of climate change (Adame et al2013b)

The undergroundmangrove Corg storage of this synthesis varies between 488 and 821of the total ecosystemic Corg The lowest values correspond to the Central Pacific regionwhile the largest comes from South Pacific region Above ground and below ground stockscould be related to high precipitation and allochthonous Corg from river inputs respectively(Adame amp Fry 2016 Ezcurra et al 2016) Additionally dominant riverine-estuarine of the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1036

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

1136

Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2736

ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

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Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 11: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Table 3 Corg stocks in mangroves and seagrasses byMexican geographic regions The values represent Corg averageplusmn SE (minimunndashmaximun) of aboveground be-lowground and total carbon per unit of area (Mg Corg ha -1) Uncertainty () for mangroves and seagrasses

Region Mangroves Seagrasses

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

Above Corg plusmn SE(MinndashMax)

Below Corg plusmn SE(MinndashMax)

Total Average Corg plusmn SE(MinndashMax)

Uncertainty95 CI

North Pacific 589plusmn 12 (38ndash162) 270plusmn 52 (453ndash893) 2049plusmn 40 (155ndash893) 396 065plusmn 049 (003ndash217) 709plusmn 96 (008 -243) 261plusmn 13 (0031ndash243) 937

Central Pacific 1170plusmn 38 (151ndash270) 1122plusmn 00 (737ndash214) 2105plusmn 50 (151ndash382) 423 ND ND ND ND

South Pacific 1548plusmn 15 (140ndash408) 6631plusmn 51 (121ndash1161) 3971plusmn 45 (141ndash1433) 222 ND ND ND ND

Gulf of Mexico 1523plusmn 15 (06ndash458) 4381plusmn 76 (98ndash2003) 2442plusmn 24 (066ndash2233) 199 104plusmn 109 (0003ndash67) 868plusmn 88 (003-299) 661plusmn 10 (0003ndash299) 645

Yucatan Peninsula 769plusmn 8 (01ndash451) 3538plusmn 18 (237ndash1085) 3489plusmn 21 (46ndash1201) 121 073plusmn 124 (000007ndash76) 1408plusmn 116 (002ndash757) 1137plusmn 7 (000007-758) 242

Herrera-Silveira

etal(2020)PeerJDOI107717peerj8790

1136

Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

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Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

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Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

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Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

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INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

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Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

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Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

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Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

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Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

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Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

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Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 12: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Figure 3 Variation in the partitioning of above and below ground contribution to the total Corg stocksinMexicanmangroves according to grouping type criteria Mexican Corg stocks for mangroves per unitof area in Mg haminus1 according to (A) Geographic regions North Pacific (NP) Central Pacific (CP) SouthPacific (SP) Gulf of Mexico (GM) and Yucatan Peninsula (YP) (B) Climate humidity ranges (C) Man-grove ecological type The stocks were divided by above (litter live and dead biomass) and below (rootsand soil) ground components Error Bars represents SE Note the different scales used in above and belowground Corg stocks

Full-size DOI 107717peerj8790fig-3

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1236

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 13: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

South Pacific region promote a greater contribution of runoff sediments (allochthonous)(Table 3) The lowest below ground Corg stocks in the Central Pacific region is related tothe small number of studies as well as the geomorphological settings which distress themangrove distribution and structure (Table 3)

According to the humidity range the largest total Corg storage was recorded for thehumid climate at 368plusmn 35 Mg Corg haminus1 the lowest value was located in the arid climate at196 plusmn 22 Mg Corg haminus1 The highest values in the below ground Corg storage was from thehumid climate at 5123 plusmn 53 Mg Corg haminus1 (Fig 3B) Regarding the ecological mangrovethe Peten (hammock) type presented the highest Corg stock (728 plusmn 230 Mg Corghaminus1) ofwhich 84 (932 plusmn 105 Mg Corg haminus1) belonged to the underground compartment (Fig3C) The freshwater inputs (springs) from karst soil fractures favored low water stress andhigh content of nitrates (Herrera-Silveira Comin amp Capurro-Filograsso 2013) In contrastdwarf mangrove exhibited the lowest Corg stock value (267 plusmn 22 Mg Corg haminus1) associatedwith locations where low phosphorus content limits the absorption of nutrients which arescarce due to the absence of external sources such as rivers and the calcareous nature of therock

According to the extension and ecosystem Corg mean (Tables 1 and 3) the mangrovesconstitute a reservoir for Mexico of approximately 2377 Tg Corg or 8723 Tg CO2e Byregion the results indicate that the Yucatan Peninsula shows the highest reservoir of Corg

(1482 Tg) (Fig 4) while the Central Pacific region accounts for the smallest Corg stocks(14 Tg) It is important to mention that the South Pacific has the highest average stockof Corg (Table 4) although its mangrove spatial cover is low (Table 4) The importance ofmangroves in the Yucatan Peninsula is not related to the forest structure although theydo cover a large area which constitutes 51 of the total area of mangroves in MexicoThis region is characterized by a low inland topography and high groundwater influencedue to the shallow water table (lt1 m) thus allowing for the creation of subterraneanestuaries that support mangrove over more than 20 km inland (Herrera-Silveira Comin ampCapurro-Filograsso 2013)

Improving and reforming the policy and legal framework for mangroves from asocioecological point of view is needed in order to restrict and regulate human activitiesthat cause the degradation of these ecosystems Such restrictions will alleviate the conflictof interest in Mexican coastal zones among conservation and economic activities (mainlyaquaculture and tourism)

Although data related to averages and regions are generally reported it is important tohighlight that basic information of Corg storage is unknown in mangrove areas Althoughaverages are used for the estimation of Corg at the ecosystem level the heterogeneity of thedata among regions indicates that site-specific evaluations are still required to represent thevariability and reduce uncertainty in the estimations (Table 3) This information is essentialfor including these ecosystems in payment mechanisms for environmental services as wellas voluntary carbon markets (Lau 2013)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1336

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 14: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Figure 4 Mangroves Corg stocks by geographic regions of Mexico Data represent the total mangrovespool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographic Coordinate System WGS 84 Referencecartography of geographic regions and mangrove extent from INEGI (2011) and CONABIO (2009)

Full-size DOI 107717peerj8790fig-4

Table 4 Summary mangrove and seagrasses Corg stocks acording to the cover extent Estimated mangrove emissions are shown with their asso-ciated land use change per geographic region Mangrove emissions were calculated for the time period 1970-2015 ussing a conservative approachof 25 loss of the total storage Main factors of change 1 Aquaculture farms and artificial ponds 2 Construction areas 3 Hydraulic infrastructure4 Communication routes 5 Industrial zones and 6 Turistic zones (from Valderrama-Landeros et al 2017)

MANGROVES SEAGRASS

Region Mangrovecover (ha)

CarbonStored(Tg Corg)

Loss of mangrovearea (1970-2015)(ha)

Emissions25 (Tg CO2e)

Main factorsof change

Seagrassescover (ha)

CarbonStored(Tg Corg)

North Pacific 187383 383 10512 19 1 4 47400 12Central Pacific 7011 14 9464 18 2 4 ND NDSouth Pacific 72187 286 26563 96 3 5 ND NDGulf of Mexico 87048 212 2602 05 1 4 3419 002Yucatan Peninsula 421926 1482 31709 101 2 6 413317 469

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1436

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2736

ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 15: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Synthesis of carbon stocks in seagrasses by regionThe extent of seagrasses considered in this study was 461058 ha distributed in three regionsof Mexico Yucatan Peninsula (896) Gulf of Mexico (01) and North Pacific (103)According to the analysis of the data collected from the Corg stocks the average aboveground stock per unit area was 078 plusmn 119 Mg Corg haminus1 and12921 plusmn 1134 Mg Corg

haminus1for below ground areas and the total Corg stock for Mexico was 130 Mg Corg haminus1This value is slightly lower than that reported by Phang Chou amp Friess (2015) for tropicalmeadows (138 plusmn 86 Mg Corg haminus1) The Corg stocks from the live biomass of seagrasseshave been estimated at 252 plusmn 048 Mg Corg haminus1 of which 75 is composed by roots andrhizomes (Fourqurean et al 2012a) For sediments the reported stocks vary from 91 to6281 Mg Corg haminus1 with a conservative average of 1397 Mg Corg haminus1 (Fourqurean et al2012a) The estimations of seagrass Corg stocks are highly variable because they dependon the species the local environment and the seasonality of the survey (Macreadie et al2014) In Mexico the average stock of Corg for living above ground (mainly leaves) was078 plusmn 119 Mg Corg haminus1 although high variability was observed (Table 3)

Regionally the largest Corg stocks per unit area were registered in the Yucatan Peninsulaand smaller ones were observed in the North Pacific (Fig 5) where the greatest valueof uncertainty was recorded (Table 3) Our results for Yucatan Peninsula were higherthan that reported by Thorhaug et al (2018) for the Yucatan Peninsula (175 Mg Corg

haminus1) The wide continental shelf and coastal geomorphology favored semiclosed orprotected water bodies (bays and coastal lagoons) and zones with a low intensity of watercurrents as in the north and west coast of the Yucatan Peninsula (Herrera-Silveira Cominamp Capurro-Filograsso 2013) where the highest total Corg stocks (1137 plusmn 7 Mg Corg haminus1)were found However the Pacific coast reported the lowest total Corg stocks (261 plusmn 13Mg Corg haminus1) which was most likely related to the physical characteristics of the regionsuch as narrow continental shelf and high discharge of rivers that are sources of sedimentsleading to high turbidity in the coastal waters (De la Lanza Espino Peacuterez amp Peacuterez 2013)The differences in the dominant hydrological conditions of each site could be playing animportant role in the carbon reservoir of this region and they also partially explain the highuncertainty values (242 -937) of the seagrasses carbon stocks (Table 3) Regarding tothe Gulf of Mexicorsquos seagrasses our study reports a total Corg stocks (661 plusmn 10 Mg Corg

haminus1) which is higher than reported by Thorhaug et al (2017) for this area (257 plusmn 177Mg Corg haminus1)

Efforts to study seagrasses in Mexico extend back to the 1950s however it has notbeen possible to determine the national extent with precision This is a crucial knowledgegap as changes in extent are required to estimate carbon stocks as well as emissions Themethodological difficulties for characterization of the marine environment in additionto the legal abandonment by the Mexican environmental authorities are reflected in thevariability of the seagrass extensions reported by different Mexican sources (Table 1)The geographic regions with the largest amount of data to estimate the blue carbonstorage were the Yucatan Peninsula and the Gulf of Mexico The Pacific Center was theregion with scarce information for blue carbon estimations The Central Pacific and SouthPacific regions did not present representative areas of seagrass distribution (CCA 2017)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1536

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2736

ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 16: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Figure 5 Partitioning of Seagrassesrsquos Corg average stocks in above and below ground for eachMexi-can geographic region Mexican seagrassesrsquos Corg stocks per unit of area in Mg haminus1 Soil stocks were stan-darized to 1m depth The stocks were divided by above and below ground components Error bars repre-sents SE Note the different scales used in above and below ground Corg stocks

Full-size DOI 107717peerj8790fig-5

In this sense regionalization allows researchers to distinguish climate geomorphologicalenvironmental seagrasses species and human use differences that have not been previouslyevaluated but certainly are drivers that impact the carbon storage capacity (Table 2) Coastallagoons and arid climate dominate the North Pacific while the Central Pacific SouthernPacific and Gulf of Mexico regions present riverine-estuarine systems with a sub-humidclimate as dominant settings finally the Yucatan Peninsula region is characterized by karstsystems with groundwater discharges (Herrera-Silveira amp Morales-Ojeda 2009De la LanzaEspino Peacuterez amp Peacuterez 2013) The information generated for blue carbon ecosystems is nothomogeneous for Corg components (above and below ground) or in the different regionsof the country and research in each region is required to reduce the estimated uncertainty(Tables 2 and 3)

Thus according to our study the estimated country stock for seagrasses is 481 Tg Corg

and the Yucatan Peninsula contribution is close to 97 (Fig 6) therefore the conservationand application of restrictive policies on activities that impact the seagrasses in this regionmust be prioritized particularly due to the conflicts of interest with the tourism sector

Mexicorsquos blue carbon in contextThe climate and geomorphology of water bodies along the coasts of each country regionhave resulted in hydrological differences related to fresh water inputs hydroperiods tidalranges hydrodynamics and nutrient supplies and the presence of stressors that couldinfluence the stocks and flux (importexport rates) of Corg in mangroves and seagrasses(Woodroffe 1992 Twilley amp Rivera-Monroy 2005 Fourqurean et al 2012a Mazarrasa etal 2018)

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1636

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2736

ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 17: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Figure 6 Seagrassesrsquos Corg stocks by geographic regions of Mexico Data represent the total seagrassesrsquospool resulting from the cover extent and regional geographic differences in Corg stocks per unit of areaData units are in Teragrams (1Tg= 1000000 Mg) Geographical Coordinates Systems Datum DWGS1984 Reference cartography of geographic regions from INEGI (2011) and seagrasses extent fromGallegos-Martiacutenez et al (2017) and Gallegos-Martiacutenez Hernaacutendez-Caacuterdenas amp Peacuterez Espinosa (2018)

Full-size DOI 107717peerj8790fig-6

For mangroves the environmental heterogeneity (Table 2) results in equally variableCorg stocks ranging from lt10 to 2233Mg Corg haminus1 This high variability has been reportedaround the world (Fig 7) Low Corg stocks characterize the arid region of Saudi Arabia(2471 Mg Corg haminus1 (Almahasheer et al 2017) while high values are often reportedfor very humid regions such as Indonesia (1691 Mg Corg haminus1 Alongi et al 2016) andMicronesia (1385Mg Corg haminus1Kauffman et al 2011) At the country level below groundCorg stocks values are up to 1300 Mg Corg haminus1 (sample depth 23 m) in arid climatessuch as the Mexican Northern Pacific region according to Ezcurra et al (2016) Isotopeanalyses of δ14C and δ13C in mangrove soil from the Pacific coast of Mexico suggestthat peat formation and vertical accretion tend to develop in topographically constrainedmangroves and most of the soil Corg of mangroves seems to derive from in situ productionin ecosystems without riverine influence (Adame amp Fry 2016 Ezcurra et al 2016) Thesefindings suggest that in addition to regional characteristics (Table 2) local variables such as

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1736

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2736

ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 18: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Figure 7 Worldwide average comparison of Corg stocks per unit of area in mangroves Data in Mg perunit of area (ha) Black bars correspond to data from Asia (data reported by Kauffman et al 2011 Liuet al 2014 Schile et al 2017 Rahman et al 2015 and Almahasheer et al 2017) Dark gray bars corre-spond to data from Africa (Jones et al 2014) Light gray bars correspond to data from America (Kauffmanet al 2014 Bhomia et al 2016 Kauffman et al 2018 and Thorhaug et al 2018) Red bar corresponds todata from Mexico obtained in this study

Full-size DOI 107717peerj8790fig-7

the hydroperiod allochthonous nutrient inputs and geomorphological history of the siteplay important roles in the sequestration and storage of below ground Corg in mangrovesTherefore considerable work is required to examine the interactions among these variablesand the Corg measurements of the entire soil profile

Regarding seagrasses Mexico ranks fourth (130 Mg Corg haminus1) in terms of carbon stockper unit area (ha) (Fig 8) which is lower than the upper boundary of the global average Corg

stock described in the literature for the Mediterranean region (375 plusmn 114 Mg Corg haminus1)and south Australia (270 Mg Corg haminus1) (Fourqurean et al 2012a) An important factor toconsider for seagrass carbon stocks at the worldwide level is the longitudinal factor ShortShort amp Novak (2016) reported four temperate regions (including the Mediterranean) andtwo tropical regions based on assemblages of taxonomic groups and physical separationThese characteristics among others such as local hydrodynamics determine the Corg

sequestration rate and stocks of seagrass meadows (both aerial and sediment) In generalMediterranean and tropical regions (western Atlantic south Australia) present optimalstorage conditions for large amounts of Corg in comparison to temperate regions (northAtlantic north Pacific) The Mediterranean is a very well-studied region that presentsvast deep meadows with a moderate diversity of a temperatetropical mix of seagrasses (9species) growing in clear water There are different factors that could favor the large stocksfor example the ecological structure or composition the architecture of the dominantendemic and deep-growing species Posidonia oceanica which forms a root and rhizomelsquolsquomatrsquorsquo that could be several meters deep and thousands of years old and is an inherent

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1836

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 19: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Figure 8 Worldwide average comparison of Corg stocks per unit of area in seagrasses Data in Mg perunit of area (ha) Black bars correspond to average data from sites located in the Atlantic sea region (con-structed from Fourqurean et al 2012a Fourqurean et al 2012b data) light gray represent data from Pa-cific Region sites (Fourqurean et al 2012a Fourqurean et al 2012b) dark gray bar represent data fromAustralia (Fourqurean et al 2012a Fourqurean et al 2012b) and finally red bar corresponds to Mexico(total result from the addition of above and below ground total averages)

Full-size DOI 107717peerj8790fig-8

characteristic in addition to the semi closed geomorphology of the Mediterranean thatfavors the large Corg stocks observed in that region

In Mexico the current extent of seagrasses must be understood as the result of additivefactors such as regional and local environmental particularities and human impacts onthe coastal zone Environmental heterogeneity represented in the country regions suchas differences in the tidal range wave energy transparency water temperature salinityand nutrient inputs from inland freshwater (rivers or groundwater) drive seagrassesdistribution composition and structure as well as soil processes that indicate the capacityfor capturing carbon by seagrasses Human activities in the Pacific Gulf of Mexico andYucatan Peninsula regions influence the Corg stocks which vary from 261 to 1137 Mg Corg

haminus1 (Table 3) The heterogeneity of Mexican seascapes and hydrogeologic characteristicsprovided along the 11000 km of coasts account for coastal lagoons bays and shallowcoastal zones which are suitable for seagrasses habitat development

In the Yucatan Peninsula a wide continental shelf with a low slope and depths ofless than 10 m away from the coast to more than 20 km represent the conditions forstoring large Corg stocks Conversely the lower Corg stocks are usually located at sites withhigh hydrodynamic energy lower transparency and greater seasonal variation in watertemperature such as those observed in the North Pacific region (Arreola-Lizaacuterraga et al2018)

These findings support the need for higher-level analyses of the variables related to thecapture and storage capacity of Corg from blue carbon ecosystems at the locality or specificsite scale and even at the global scale Factors such as climate and geomorphology havebeen previously identified to be key variables (Sanders et al 2016 Twilley Rovai amp Riul2018) However in this synthesis the local scale characteristics related to nutrient inputs

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 1936

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

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Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 20: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

and hydrology especially the time of flooding in mangroves micro climatic conditionscoast geomorphology as well as hydrodynamics dominant species and type of sedimentfor seagrasses suggested that all of these could be important characteristics favoring thevariability observed in Corg stocks of mangroves and seagrasses The evaluation of bluecarbon ecosystems at the local scale is the baseline before evaluating the feasibility ofincluding these ecosystems in a national environmental compensation scheme paymentfor ecosystem services or carbonmarkets In this work great variability of the Corg reservoirswas observed according to the region and climate and site-specific variables such as speciestemperature source of water porewater salinity and hydroperiod could be associated withtheir capacity to store and sequester Corg The addition of this information will providea better understanding of the process related to Corg sequestration and storage capabilitywhich will be a useful input for direct conservation planning as well as management andrestoration plans at country regional and local levels (Friess et al 2016)

Synthesis of the blue carbon fluxes in Mexican coastal ecosystemsFor greenhouse gas emissions due to the loss of mangroves the results showed that thehighest emissions occurred in the regions with the greatest loss of mangrove The YucatanPeninsula has contributed the most (101 Tg CO2e) followed by the South Pacific region(96 Tg CO2e) The Gulf of Mexico has the lowest contribution to CO2e emissions due tomangrove loss (05 Tg CO2e) It is important to highlight that mangrove cover in CentralPacific has shown the greatest loss over the last 45 years however its emissions are lowerdue to the low storage capacity per hectare (Table 3) According to Valderrama-Landeroset al (2017) the main factors underlying the change in the mangrove ecosystem in Mexicoare related to anthropogenic activities such as aquaculture and coastal urban development(mainly tourism) however the impact is variable according to the intensity extent andregion in which they develop (Table 4)

Studies related to emissions from mangroves to grassland conversion results in 786to 2173 Mg CO2e haminus1 (Kauffman et al 2016) which are higher than those estimatedin this study due to a more conservative approach (Table 4) However the mangroveloss due to their conversion to shrimp farms leads to an estimated emission of 2637 MgCO2e haminus1 which represents an increment up to 80 (Kauffman et al 2014) Thereforeit is important to strengthen the research on the specific impact of the activities carriedout in each region which will allow researchers and resource managers to determineestimated emission factors per activity and identify where the conservation and restorationactions are a priority in order to preserve the ecosystem service of emission avoidance(Teutli-Hernaacutendez amp Herrera-Silveira 2016) Mangrove restoration success is largelyrelated to hydrologic improvements which favor soil accretion rates The main co-benefitsassociated with restoration activities are the less vulnerable and more resilient mangrovesand human communities to sea level rise and the enhancement of biodiversity includingthe reincorporation of ecologically and commercially important species of mollusk fishand birds (Arceo-Carranza et al 2016)

For seagrasses disturbance represents a significant loss of the total carbon stockwhich contributes to CO2e emissions due to the argumentation of oxidative processes of

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2036

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

REFERENCESAdameMF Brown CJ BejaranoM Herrera-Silveira JA Ezcurra P Kauffman JB

Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 21: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

the organic matter (Moodley et al 2005) by unburied sediment (Marbagrave et al 2015) Fewstudies have been conducted to assess the contribution of CO2e emissions to the atmosphereattributed to the loss of the seagrass cover despite the high worldwide deterioration ofseagrasses (Waycott et al 2009) over recent decades Nevertheless a loss of 263 and upto 337 (Lovelock Fourqurean amp Morris 2017) of the total stock has been estimated dueto the loss of seagrass cover resulting from water quality deterioration and beach erosionrespectively

Based on the average values of CO2e emissions reported in the literature and dueto the lack of direct measures of this process in Mexican seagrasses ecosystems our firstapproach to examining potential emissions for seagrasses ranges from 581 to 744 Tg CO2econsidering the loss of 4632406 ha of seagrasses according to the extensions reported over12 years (2006-2018) however this value should be interpreted with caution due to thelack of systematic monitoring of the seagrass cover The incorporation of remote sensing inseagrass surveys and mapping methodologies (Mendoza-Martiacutenez 2017 Cerdeira-Estradaet al 2018) as well as the development of new and less expensive remote sensors orequipment such as SENTINEL 2a and unmanned aircraft system (drone) make it possibleto improve the distribution maps of marine landscapes in the near future

An important issue is the vertical and lateral carbon flux such as the capture andexchange of methane (CH4) particulate organic carbon (POC) and dissolved organiccarbon (DOC) which are currently carried out in mangroves Nevertheless carbon flux isestimated via the measurement of ecosystem productivity and despite mangroves beingkey suppliers of organic carbon to the adjacent coastal systems and being the basis of thetheory of lsquolsquooutwellingrsquorsquo proposed by Odum amp Heald (1972) the number of quantitativeestimations remains scarce

In a review of 16 studies on mangrove litterfall in Mexico the average estimated was43 plusmn 06 Mg Corg haminus1 yminus1 (Herrera-Silveira et al 2016) which is close to the estimatedinterval from global litterfall mangrove measurements ranging from 43ndash48 Mg Corg haminus1

yminus1 (Hutchison et al 2014 Zhang et al 2014) Regionally the highest average occurred inthe South Pacific (67 Mg Corg haminus1 yminus1) while the lowest was recorded in the CentralPacific (15 Mg Corg haminus1 yminus1) Air temperature and precipitation are the main variablesrelated to these regional differences as litterfall production is coupled to rain (Santini et al2015)

In Mexico predicting changes in litterfall associated with environmental variations orland use is difficult Flux studies associated with litterfall that have reported environmentalsettings that include the hydroperiod porewater or soil characteristics and macro andmicrobiota information are scarce The environmental context as well as certain biotagroups such as bacteria fungus crabs or worms could determine the litterfall Corg fluxHydroperiod is considered the main source of variation for litter in fringe mangrove forests(Odum McIvor amp Smith 1982 Twilley Lugo amp Patterson-Zucca 1986) but detritivorebiota such as crabs and bacteria play a similar role in the inland wetlands It was estimatedthat litter removal by crabs could be 33 to 77 of the total annual litterfall from the forestfloor promoting low standing stocks of litter and fast rates of leaf removal (Robertsonamp Daniel 1989) Thus in addition to the importance for Corg flux understanding the

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2136

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

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Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 22: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

environmental and biological interactions regulating litterfall decomposition will also helpus to comprehend the role of soil organic matter in accretion and accumulation processesin the face of sea level rise (Lovelock et al 2015)

Regarding mangrove swamps as a source of CH4 emissions only one study has beenconducted in tropical coastal lagoons in the Yucatan Peninsula region (Chuang et al 2017)The findings revealed diffuse fluxes of CH4 from the surface water of the lagoon to theatmosphere that varied between 13 times 10minus4 and 0876 Mg CH4haminus1 yminus1 suggesting thatcoastal lagoons surrounded by mangroves could be important natural sources of CH4Another aspect to consider is that CH4 emissions may be greater in mangroves underdisturbance conditions (Pendleton et al 2012)

In relation to the exchange of DOC and POC between the mangrove and the adjacentwater body (river coastal lagoon sea) the generated data remain scarce except for the studyby Camacho-Rico (2018) who reported exchange values between the fringe mangrove anda coastal lagoon of the Yucatan Peninsula region of 68 g DOC m2 yminus1 and 767 g DOC m2

yminus1 This range of DOC exchange values is based on values reported for karst sites (asymp 046to -108 g DOC m2 yminus1) (Adame amp Lovelock 2011) Regarding the POC the exportationvalues (591 plusmn 88 g POC mminus2 yminus1) were lower than the average estimated in a mangrovelocated in river geomorphological areas such as Papua New Guinea (285 g POC mminus2 yminus1)(Robertson amp Alongi 1995) The variability observed in the DOC and POC exchange datais related to the hydrological climatic and biotic differences that occur within the watercolumn at each site as well as the different methodologies used

Most of the studies in Mexico lack environmental information (interstitial salinity soilnutrients hydroperiod) and the role of the freshwater inputs via groundwater is poorlyunderstood Environmental information could explain geochemical processes in soil andplant exposition to stressors resulting in changes in the flux and stocks of organic carbon(Day et al 1996 Shunula amp Whittick 1999b Coronado-Molina et al 2012)

Mexican policy for blue carbon ecosystemsIn the face of climate change Mexico has joined international efforts to protect andrestore blue carbon ecosystems (UNFCCCV 2015) In this sense knowledge of the benefitsprovided by the sequestration and storage of carbon in mangroves and seagrasses as wellas the amount of environmental services they provide represents baseline information thatis required for the planning management and prioritization of activities related to theconservation and restoration of these coastal ecosystems

Mexico has ratified the United Nations Framework Convention on Climate Change(UNFCCC) the agreement which includes coastal blue carbon ecosystems as climatemitigation and adaptation solutions in its National Determined Contributions (NDCs)(Martin et al 2016) Even in Mexicorsquos NDCs the term lsquolsquoblue carbonrsquorsquo is not mentioneditself however the federal government considers coastal wetlands as part of its generalmitigation aims recognizes the benefits of coastal wetlands in themitigation and adaptationof GHGs and includes coastal wetlands as adaptation solutions Mexican NDCs actionsinclude the conservation management protection and restoration of wetlands such asmangroves seagrass and other coastal and marine ecosystems which are also considered

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2236

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

REFERENCESAdameMF Brown CJ BejaranoM Herrera-Silveira JA Ezcurra P Kauffman JB

Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2636

AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

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INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

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Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

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Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

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Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

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Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

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Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

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Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

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SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 23: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

in conservation and recovery schemes In Mexico the implications and capabilities ofreporting mangrove and seagrasses carbon storage by the official institution (ComisionNacional Forestal CONAFOR) through the national greenhouse gas inventory report iscurrently being evaluated by the federal government which would position Mexico at thelevel of Australia in the blue carbon mitigation NDCs context

At the national level mangroves and seagrasses (DOF 2010) are immersed indifferent conservation schemes and their management is controlled mainly by thefederal government via different agencies with interventions directly or indirectlyin these ecosystems such as the Ministry of Environment and Natural Resources(SEMARNAT) National Water Commission (CONAGUA) and National ForestryCommission (CONAFOR) among others Regardless mangrove and seagrasses lossescaused by anthropogenic activities are increasing due to gaps and legal contradictions thatallow land use changes mainly for road construction and the development of economicactivities of high economic impact such as aquaculture and tourism

Mexican legislation has recently established national policy instruments on climatechange (DOF 2010) which include prioritizing the sectors with the greatest emissionreduction potential The 5th Communication of Mexico to the IPCC was a precedent forblue carbon ecosystems as an important component of GHG emission reduction policiesSuch work has permeated to the research priorities in Mexico and scientific work relatedto blue carbon has grown from 2013 including the important elements included in thiswork However the first actions to harmonize the instruments of public policy based onscience and compliance at the three levels of government are just taking place The sitesaround natural protected areas seem to be natural pilot sites for the implementation ofconservation projects and restoration of blue carbon ecosystems as determined by theconsensus of authorities users academia and NGOs Studies in mangrove protected areashave revealed high Corg stocks (from 663 to 1 358 Mg Corg haminus1) (Adame et al 2013Adame et al 2013b Adame et al 2015 Kauffman et al 2016) However it is important toconsider that not all protected natural areas are effective or sufficient given the magnitudeof biological diversity competence and need to maintain other land uses (Ceccom ampMartiacutenez-Garza 2016)

A national regulatory framework offers opportunities for the creation of publicmitigation policies aimed to quantify and check the GHG emissions as well as directand promote actions to increase carbon budget stop and reverse coastal ecosystemsdeforestation and degradation The incorporation of the concept lsquolsquoblue carbon economyrsquorsquoin the public policy related to climate change through mechanisms based on the carbonmarket (credits or emissions rights) generated by restoration or conservation of wetlandsis an attractive option for the financing of blue carbon projects in Mexico (CCA 2017)

The variability in Corg stocks in mangroves and seagrasses of Mexico observed alongthe coasts and the uncertainty associated could limit their incorporation to ongoingprospections related to the setting of national baselines under REDD+ nesting andfeasibility analyses of voluntary local-regional markets (Bejarano Loacutepez amp Rosette 2018)In this sense the risk of following REDD+ strategy due to the lsquolsquoadditionalityrsquorsquo problemmust be evaluated at the national level due to Certified Emission Reductions from projects

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2336

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

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Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

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Page 24: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

which create rsquoadditionalrsquo emissions reductions to those that would otherwise have beenachieved Blue carbon offsets comewith high uncertainties and risks of reversal and becausetheir additionality (ie whether emissions reductions or removals would have happenedwithout the blue carbon project) can be difficult to prove in zones with a high occurrenceof natural impacts (ie fires hurricanes etc) such as Mexico and the Caribbean BasinPossible solutions to additionality have been largely discussed (ie use of carbon fluxesor sequestration instead of carbon storage) and the existing information of Corg fluxesfor Mexican blue carbon ecosystems could not support public policies in the short termfor the development of local regional and national strategies to achieve the internationalcommitments of Mexico

In Mexico the incorporation of alternative schemes to incentivize the protection ofblue carbon ecosystems such as the lsquolsquopayment for ecosystem servicesrsquorsquo or lsquolsquonational bluecarbon marketsrsquorsquo including concessions to communities through custody schemes couldbe better implemented and justified by the potential co-benefits from coastal ecosystemconservation and restoration Then successful and operative schemes should be designedwith the full set of ecosystem services in mind and not just carbon sequestration

CONCLUSIONSMexico has great potential to contribute to mitigating the effects of climate change throughthe conservation and restoration of blue carbon ecosystems especially mangroves andseagrasses This study contributes to the quantification of Corg stocks and CO2e emissionsestimation due to the loss of mangrove cover and it provides the first data for Corg stocksand emissions of seagrasses at the country level

According to this synthesis the total carbon storage ofMexicanmangroves and seagrassesis 4988MgCorg haminus1 and 130MgCorg haminus1 respectively Considering the official extensionof both ecosystems mangroves have a stock of 2377 Tg Corg and seagrasses have a stock of481 Tg Corg Together the blue carbon stock of Mexico compensates for the emissions ofasymp300 million hydrocarbon users in a year

Mexican mangroves exhibit great variability in organic carbon reservoirs according tothe region climate and vegetation structure According to the criteria the highest averagesfor mangroves by region were exhibited in the South Pacific (3971 plusmn 45 Mg Corg haminus1)in humid climates (3683 plusmn 35 Mg Corg haminus1) and peten vegetation (728 plusmn 230 Mg Corg

haminus1) The Yucatan Peninsula has the largest regional extension of mangroves (55) andall structural vegetation typologies are presented however this region is the most impactedby land use changes

Conservation and restoration should be prioritized in this region to avoid emissionsreduce vulnerability to sea level rises and create adaptation opportunities based onecosystemmanagement In the case of seagrasses we report only for the North Pacific Gulfof Mexico and Yucatan Peninsula with the latter presenting the highest storage records(1137 plusmn 7 Mg Corg haminus1)

Coverage loss of blue carbon ecosystems in Mexico has accounted for approximately24 Tg CO2e emissions by mangroves over the last 20 years However no coverage change

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2436

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

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Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

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el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

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Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 25: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

data are available for seagrasses although preliminary results using literature scenariosand local data indicate emissions of approximately 6 Tg CO2e over 12 years Accordingto these results and if the current loss rates are maintained the commitments of the Parisagreement signed by Mexico government will be difficult to fulfill

The results of this synthesis suggest that the policies for conservation and restorationof blue carbon ecosystems in Mexico must be improved and enforced in addition to thecurrent legal framework of protection which do not properly fulfill their purpose Officialdata report tourism agriculture and land use change as the activities with deleteriousimpacts on Mexican blue carbon ecosystems We recommend the regulation of thoseactivities according to ecohydrological approaches in order to improve conservation andconnectivity between ecosystems Such action plans should use blue carbon conservationand restoration as an umbrella to maintain andor recover environmental services at thetime synergies among government academic social and private sectors are reinforced andharmonized by win-win initiatives

ACKNOWLEDGEMENTSThis synthesis was the result of a collective efforts of many researchers without whom thiswork would not have been possible The authors give special recognition to Dra FernandaAdame and Dr Boone Kauffman for being the pioneers in studies of mangrove carbonstorage in Mexico and to Dr Rainer Ressl Executive Officer in Chief of Geoinformaticsin the National Commission for Knowledge and Use of Biodiversity (CONABIO) for allcartographic support We are grateful to the anonymous reviewers the journal editorand Jenifer Howard for their time efforts and engagement to improve the manuscriptWe thank the participation of students and field technicians to provide original datato the authors especially Ileana Osorio Javier Ramiacuterez Laura Carrillo Judith ErosaKarla Zenteno Heimy Us Oscar Peacuterez Mercy Loacutepez Julieta Gamboa Sergio Solis AngelTrasvintildea Andreacutes Canul Tania Cota Octavio Cortes Ma Teresa Andueza Silvia RamirezLeonardo Arellano Mireya Aguayo Zuemmy Chi

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by United Nations Development Programme (No CSP-2016-057) National Commission of Natural Protected Areas (Mexico) (No FN009 amp NoKN003) National Forestry Commission (Mexico) (No 137252) Ministry of Environmentand Natural Resources (Mexico) (No S0010-1108099) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUnited Nations Development Programme CSP-2016-057National Commission of Natural Protected Areas (Mexico) FN009 KN003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2536

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

REFERENCESAdameMF Brown CJ BejaranoM Herrera-Silveira JA Ezcurra P Kauffman JB

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AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

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Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

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OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 26: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

National Forestry Commission (Mexico) 137252Ministry of Environment and Natural Resources (Mexico) S0010-1108099

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Jorge A Herrera-Silveira conceived and designed the experiments analyzed the dataauthored or reviewed drafts of the paper and approved the final draftbull Monica A Pech-Cardenas Sara M Morales-Ojeda and Andrea Camacho-Rico analyzedthe data prepared figures andor tables authored or reviewed drafts of the paper andapproved the final draftbull JorgeMontero analyzed the data authored or reviewed drafts of the paper and approvedthe final draftbull Siuling Cinco-Castro and Juan P Caamal Sosa Juan E Mendoza-Martinez Eunice YPech-Poot and Claudia Teutli-Hernandez analyzed the data prepared figures andortables and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability The rawmeasurementsare available in the Supplemental Files

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj8790supplemental-information

REFERENCESAdameMF Brown CJ BejaranoM Herrera-Silveira JA Ezcurra P Kauffman JB

Birdsey R 2018 The undervalued contribution of mangrove protection in Mexicoto carbon emission targets Conservation Letters 11e12445DOI 101111conl12445

AdameMF Fry B 2016 Source and stability of soil carbon in mangrove and fresh-water wetlands of the Mexican Pacific coastWetlands Ecology and Management24129ndash137 DOI 101007s11273-015-9475-6

AdameMF Kauffman JB Medina I Gamboa JN Torres O Caamal JP RezaM Herrera-Silveira JA 2013a Carbon Stocks of Tropical Coastal Wetlandswithin the Karstic Landscape of the Mexican Caribbean PLOS ONE 8e56569DOI 101371journalpone0056569

AdameMF Lovelock CE 2011 Carbon and nutrient exchange of mangrove forests withthe coastal ocean Hydrobiologia 66323ndash50 DOI 101007s10750-010-0554-7

AdameMF Santini NS Tovilla C Vaacutezquez-Lule A Castro L Guevara M 2015 Carbonstocks and soil sequestration rates of riverine mangroves and freshwater wetlandsBiogeosciences 123805ndash3818 DOI 105194bg-12-3805-2015

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

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Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

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Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

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Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

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AdameMF Teutli C Santini NS Caamal JP Zaldiacutevar-Jimeacutenez A HernaacutendezR Herrera-Silveira JA 2014 Root biomass and production of mangrovessurrounding a karstic oligotrophic coastal lagoonWetlands 34479ndash488DOI 101007s13157-014-0514-5

AdameMF Zaldiacutevar-Jimenez A Teutli C Caamal JP AnduezaMT Loacutepez-AdameH Cano R Hernaacutendez-Arana HA Torres-Lara R Herrera-Silveira JA 2013bDrivers of mangrove litterfall within a karstic region affected by frequent hurricanesBiotropica 45147ndash154 DOI 101111btp12000

Almahasheer H Serrano O Duarte CM Arias-Ortiz A Masque P Irigoien X2017 Low carbon sink capacity of Red Sea mangroves Scientific Reports 79700DOI 101038s41598-017-10424-9

Alongi DM 2008Mangrove forests resilience protection from tsunamis and re-sponses to global climate change Estuarine Coastal and Shelf Science 761ndash13DOI 101016jecss200708024

Alongi DM 2012 Carbon sequestration in mangrove forests Carbon Management3313ndash322 DOI 104155cmt1220

Alongi DMMurdiyarso D Fourqurean JW Kauffman JB Hutahaean A CrooksS Lovelock CE Howard J Herr D Fortes M Pidgeon EWagey T 2016Indonesiarsquos blue carbon a globally significant and vulnerable sink for sea-grass and mangrove carbonWetlands Ecology and Management 243ndash13DOI 101007s11273-015-9446-y

Arceo-Carranza D Gamboa E Teutli-Hernaacutendez C Badillo-AlemaacutenM Herrera-Silveira JA 2016 Los peces como indicador de restauracioacuten de aacutereas de manglaren la costa norte de Yucataacuten Revista Mexicana de Biodiversidad 87489ndash496DOI 101016jrmb201603001

Arreola-Lizaacuterraga JA Padilla-Arredondo G Ruiz-Ruiz TM Cruz-Garciacutea LMMeacutendez-Rodriacuteguez LC Hernaacutendez-Almaraz P Vargas-Gonzaacutelez HH 2018 Estuaries andcoastal lagoons of mexico challenges for science management and conservationIn Ortega-Rubio A edMexican natural resources management and biodiversityconservation recent case studies Cham Springer International Publishing 251ndash283DOI 101007978-3-319-90584-6_12

BejaranoM Loacutepez E Rosette M 2018 Anaacutelisis de la Situacioacuten Poliacutetica y Econoacutemicadel Carbono Azul en Meacutexico PNUD CSP-2016-057 In Programa Mexicano delCarbono Pronatura Sur FMCN CEMDA CINVESTAV-IPN Meacutexico ProgramaMexicano del Carbono 126

Bhomia RK Mackenzie RA Murdiyarso D Sasmito SD Purbopuspito J 2016 Impactsof land use on indian mangrove forest carbon stocks implications for conservationand management Ecological Applications 26(5)1396ndash1408 DOI 10189015-2143

Bouillon S Connolly RM 2009 Carbon exchange among tropical coastal ecosystemsIn Nagelkerken I ed Ecological connectivity among tropical coastal ecosystemsDordrecht Springer 45ndash70 DOI 101007978-90-481-2406-0_3

Caamal-Sosa JP Zaldiacutevar A Adame-Vivanco F Teutli-Hernaacutendez C AnduezaMTPeacuterez R Herrera-Silveira JA 2011 Almacenes de carbono en diferentes tipos

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

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coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

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Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

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ecoloacutegicos de manglares en un escenario caacuterstico In Estado Actual del Conocimientodel Ciclo del Carbono y sus Interacciones en Meacutexico Siacutentesis a Texcoco Edo deMeacutexico Programa Mexicano del Carbono 478ndash483

Camacho-Rico A 2018 Dinamica de intercambio de carbono y nutrientes entre elmanglar y la Laguna costera de Celestun Yucatan Thesis Cinvestav-Merida

Canty A Ripley BD 2019 boot Bootstrap R (S-Plus) functions R package version 13-24

Commission for Environmental Cooperation (CCA) 2016 Comision para la Coopera-cion Ambiental Carbono azul en Ameacuterica del Norte evaluacioacuten de la distribucioacuten de loslechos de pasto marino marismas y manglares y su papel como sumideros de carbonoMontreal Comisioacuten para la Cooperacioacuten Ambiental 58

Commission for Environmental Cooperation (CCA) 2017 Comision para la Coopera-cion Ambiental Anaacutelisis de las oportunidades para la integracioacuten del concepto de car-bono azul en la poliacutetica puacuteblica mexicana Montreal Comisioacuten para la CooperacioacutenAmbiental 102

Ceccom E Martiacutenez-Garza C 2016 Experiencias mexicanas en la restauracion de losecosistemas Mexico City Universidad Nacional Autonoma de Mexico CentroRegional de Investigaciones Multidiscplinarias Universidad Autonoma del Estadode Morelos Comision Nacional para el Conocimiento y Uso de la Biodiversidad

Cerdeira-Estrada S Rosique-De La Cruz LO Blanchon P Uribe-Martiacutenez A Martell-Dubois R Martiacutenez-Clorio MI Cruz-LoacutepezMI Ressl R 2018 Relieve de losEcosistemas Marinos del Caribe Mexicano Cabo CatochemdashXcalak Escala 1 8000Comisioacuten Nacional para el Conocimiento y Uso de la Biodiversidad UniversidadNacional Autoacutenoma de Meacutexico Available at https simarconabiogobmx

Chuang PC YoungMB Dale AWMiller LG Herrera-Silveira JA Paytan A 2017Methane fluxes from tropical coastal lagoons surrounded by mangroves Yu-cataacuten Mexico Journal of Geophysical Research Biogeosciences 1221156ndash1174DOI 1010022017JG003761

Cinco-Castro S Camacho-Rico A Morales-Ojeda S Caamal-Sosa JP Herrera-SilveiraJA 2017 Almacenes de carbono en humedales costeros del Pacifico Norte yPeniacutensula de Yucataacuten In Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 1ndash7

CONABIO 2009Manglares de Meacutexico Extensioacuten y distribucioacuten 2nd edition MexicoCity CONABIO Available at https semadetjaliscogobmx sites semadetjaliscogobmx files manglares_de_mexicopdf

CONABIO 2016Distribucioacuten de los manglares en Meacutexico en 2015 escala 1500001st edition Mexico City CONABIO Available at http wwwconabiogobmx informacion metadata gismx_man15gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

CONABIO 2018 Comisioacuten Nacional para el Uso y Conocimiento de la Biodiversidady Universidad Autoacutenoma Metropolitana 1st edition Mexico City CONABIOAvailable at http wwwconabiogobmx informacion metadata gis pastmar17gwxml_httpcache=yesamp_xsl=db metadata xsl fgdc_htmlxslamp_indent=no

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2836

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 29: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Coronado-Molina C Alvarez-Guillen H Day JW Reyes E Perez BC Vera-HerreraF Twilley R 2012 Litterfall dynamics in carbonate and deltaic mangrove ecosys-tems in the Gulf of MexicoWetlands Ecology and Management 20123ndash136DOI 101007s11273-012-9249-3

Day JW Coronado-Molina C Vera-Herrera FR Twilley R Rivera-Monroy VHAlvarez-Guillen H Day R ConnerW 1996 A 7 year record of above-ground netprimary production in a southeastern Mexican mangrove forest Aquatic Botany5539ndash60 DOI 1010160304-3770(96)01063-7

DOF 2010 Diario Oficial de la Federacioacuten Norma Oficial Mexicana NOM-059-SEMARNAT-2010 que establece las especificaciones para la proteccioacuten ambientaly de Especies nativas de Meacutexico de flora y fauna silvestres Categoriacuteas de riesgo yespecificaciones para su inclusioacuten exclusioacuten o cambio de Lista de especies en riesgo

Donato DC Kauffman JB Murdiyarso D Kurnianto S StidhamM KanninenM 2011Mangroves among the most carbon-rich forests in the tropics Nature Geoscience4293ndash297 DOI 101038ngeo1123

Duarte CM Losada IJ Hendriks IE Mazarrasa I Marbagrave N 2013 The role of coastalplant communities for climate change mitigation and adaptation Nature ClimateChange 3961ndash968 DOI 101038nclimate1970

Ezcurra P Ezcurra E Garcillaacuten PP Costa MT Aburto-Oropeza O 2016 Coastallandforms and accumulation of mangrove peat increase carbon sequestrationand storage Proceedings of the National Academy of Sciences of the United States ofAmerica 113(16)4404ndash4409 DOI 101073pnas1519774113

Food and Agriculture Organization of the United Nations (FAO) 2007 The worldrsquosmangroves 1980-2005 FAO Forestry Paper Rome FAO 153

Flores MG Jimeacutenez J Madrigal X Moncayo F Takaki F 1971 Memorias del mapa detipos de vegetacioacuten de la Repuacuteblica Mexicana Secretaria de Recursos HidraacuteulicosSubsecretaria de planeacioacuten Direccion General de Estudios Direccioacuten de Agrologiacutea(manual and map scale 12000000) Meacutexico ISN 27151 59 Available at https librarywurnl isric fulltext isricu_i27151_001pdf

Fourqurean JW Duarte CM Kennedy H Marbagrave N HolmerMMateoMA Apos-tolaki ET Kendrick GA Krause-Jensen D McGlathery KJ 2012a Seagrassecosystems as a globally significant carbon stock Nature Geoscience 5505ndash509DOI 101038ngeo1477

Fourqurean JW Kendrick GA Collins LS Chambers RM Vanderklift MA 2012bCarbon nitrogen and phosphorus storage in subtropical seagrass meadows exam-ples from Florida Bay and Shark BayMarine and Freshwater Research 63967ndash983DOI 101071MF12101

Friess DA Thompson BS Brown B Amir AA Cameron C Koldewey HJ Sasmito SDSidik F 2016 Policy challenges and approaches for the conservation of mangroveforests in Southeast Asia Conservation Biology 30933ndash949DOI 101111cobi12784

Gallegos-Martiacutenez M Hernaacutendez-Cardenas G Espinosa IPeacuterez Andreas-Ressl R 2017Comunidad de Pastos marinos del Caribe Mexicano 2017 Comisioacuten Nacional para

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 2936

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 30: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

el Uso y Conocimiento de la Biodiversidad y Universidad Autoacutenoma MetropolitanaCONABIO-UAM Ciudad de Meacutexico Meacutexico Available at httpwwwconabiogobmx informacionmetadata gis pmver18gwxml_httpcache=yesamp_xsl=dbmetadataxsl fgdc_htmlxslamp_indent=no

Gallegos-Martiacutenez M Hernaacutendez-Caacuterdenas G Peacuterez Espinosa I 2018 Pastos marinosdel Estado de Veracruz Meacutexico escala 11 edicioacuten 1 Universidad AutoacutenomaMetropolitana Unidad Iztapalapa e Instituto Nacional de Ecologiacutea y CambioClimaacutetico Proyecto financiado por rsquoIndicadores del estado de las comunidades dePastos Marinos en la zona costera del Golfo de Meacutexico susceptible de ser impactadapor los hidrocarburos derramados por la Plataforma Horizon operada por BPrsquoINECC-SEMARNAT UAM-Iztapalapa Ciudad de Meacutexico

Garciacutea E 1988Modificacioacuten al Sistema de Clasificacioacuten Climaacutetica de KOumlPEN paraadaptarlo a las condiciones de la Repuacuteblica Mexicana Cuarta edicioacuten MeacutexicoUniversidad Autoacutenoma de Meacutexico 219

Garciacutea E 1990 Rangos de humedad Extraido de Climas IV410 Atlas Nacional deMeacutexico Vol II Escala 1 4000000 Instituto de Geografia UNAM Meacutexico

Gautier D Amador J Newmark F 2001 The use of mangrove wetland as a biofilter totreat shrimp pond effluents preliminary results of an experiment on the Caribbeancoast of Colombia Aquaculture Research 32787ndash799DOI 101046j1365-2109200100614x

Giri C Ochieng E Tieszen LL Zhu Z Singh A Loveland T Masek J Duke N 2011Status and distribution of mangrove forests of the world using earth observationsatellite data Global Ecology and Biogeography 20154ndash159DOI 101111j1466-8238201000584x

Green EP Short FT 2003World atlas of seagrasses Berkeley University of CaliforniaPress

Herrera-Silveira JA Camacho-Rico A Caamal-Sosa J Cinco-Castro S Morales-OjedaS Ramiacuterez-Ramiacuterez J Zenteno-Diacuteaz K Pech-Poot E Pech-Caacuterdenas M Carrillo-Baeza L Erosa-Angulo J Peacuterez-Martiacutenez O Teutli-Hernaacutendez C 2018a Databaseof carbon stocks in the mangroves of mexico Elementos para Poliacuteticas Puacuteblicas2(1)33ndash44

Herrera-Silveira JA Camacho Rico A Pech E PechM Ramiacuterez Ramiacuterez J TeutliHernaacutendez C 2016 Dinaacutemica del carbono (almacenes y flujos) en manglares deMeacutexico Terra Latinoamericana 3461ndash72

Herrera-Silveira JA Comin FA Capurro-Filograsso L 2013 Landscape Land-Use and Management in The Coastal Zone of Yucatan Peninsula In Day JWYaacutentildeez Arancibia A eds Gulf of Mexico origin waters and biota Ecosystem-BasedManagement Harte Research Institute for Gulf of Mexico Studies Series Texas A amp MUniversityndashCorpus Christi Volume 4 College Station Texas A amp M University Press460

Herrera-Silveira JA Mendoza-Martiacutenez J Morales-Ojeda S Camacho-Rico A Medina-Goacutemez I Ramiacuterez-Ramiacuterez I Loacutepez-Herrera M Pech-Poot E Peacuterez-Martiacutenez O

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3036

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 31: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Pech-Caacuterdenas M Cota-Lucero T Teutli-Hernaacutendez C 2018b Database of carbonstocks in seagrasses of mexico Elementos para Poliacuteticas Puacuteblicas 2(1)45ndash52

Herrera-Silveira JA Morales-Ojeda SM 2009 Evaluation of the health status ofa coastal ecosystem in southeast Mexico Assessment of water quality phyto-plankton and submerged aquatic vegetationMarine Pollution Bulletin 5972ndash86DOI 101016jmarpolbul200811017

Hiraishi T Krug T Tanabe K Srivastava N Baasansuren J FukudaM Troxler TG2014 2013 supplement to the 2006 IPCC guidelines for national greenhouse gasinventories Wetlands IPCC

Howard J Hoyt S Isensee K Telszewski M Pidgeon E (eds) 2014 Coastal BlueCarbon Methods for assessing carbon stocks and emissions factors in mangrovestidal salt marshes and seagrasses Conservation International IntergovernmentalOceanographic Commission of UNESCO International Union for Conservation ofNature Arlington Virginia USA 180

Hutchison J Manica A Swetnam R Balmford A SpaldingM 2014 Predictingglobal patterns in mangrove forest biomass Conservation Letters 7233ndash240DOI 101111conl12060

IEA 2014 The power of transformation wind sun and the economics of flexible powersystems Paris International Energy Agency OECDIEA

INECC 2018 Instituto Nacional de Ecologiacutea y Cambio Climaacutetico Sexta ComunicacioacutenNacional y Segundo Informe Bienal de Actualizacioacuten ante la Convencioacuten Marcode las Naciones Unidas sobre el Cambio Climaacutetico Meacutexico In Secretariacutea de MedioAmbiente y Recursos Naturales Meacutexico INECC-SEMARNAT 751

INEGI 2011 Instituto Nacional de Estadiacutestica Geografiacutea e Informaacutetica In Conjunto deDatos Vectoriales y Toponimias de liacutemite Nacional y entidades federativas de Meacutexicoescala 1 1000000 1 Meacutexico INEGI

INEGI 2014 Instituto Nacional de Estadiacutestica y Geografiacutea Informacioacuten de Uso del Sueloy Vegetacioacuten escala 1250 000 Serie VI 2014 Instituto Nacional de Geografiacutea eHistoria

Intergubernamental Pannel of Climate Change (IPCC) 2014 Climate Change 2014mdashSynthesis Report DOI 101017CBO9781107415324

Jones TG Ratsimba HR Ravaoarinorotsihoarana L Cripps G Bey A 2014 Ecologicalvariability and carbon stock estimates of mangrove ecosystems in northwesternMadagascar Forests 5(1)177ndash205 DOI 103390f5010177

Kathiresan K Rajendran N 2005 Coastal mangrove forests mitigated tsunami Estuar-ine Coastal and Shelf Science 65601ndash606 DOI 101016jecss200506022

Kauffman JB Bernardino AF Ferreira TO Giovannoni LR De O Gomes LE RomeroDJ Jimenez LCZ Ruiz F 2018 Carbon stocks of mangroves and salt marshes of theAmazon region Brazil Biology Letters 14(9)20180208 DOI 101098rsbl20180208

Kauffman JB Bhomia RK 2017 Ecosystem carbon stocks of mangroves across broadenvironmental gradients in West-Central Africa global and regional comparisonsPLOS ONE 12e0187749 DOI 101371journalpone0187749

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3136

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 32: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Kauffman JB Donato D 2012 Protocols for the measurement monitoring andreporting of structure biomass and carbon stocks in mangrove forests Centerfor International Forestry Working Paper 86 CIFOR Bogor Indonesia 40 ppDOI 1017528cifor003749

Kauffman JB Heider C Cole TG Dwire KA Donato DC 2011 Ecosystem carbonstocks of micronesian mangrove forestsWetlands 31343ndash352DOI 101007s13157-011-0148-9

Kauffman JB Heider C Norfolk J Payton F 2014 Carbon stocks of intact mangrovesand carbon emissions arising from their conversion in the Dominican RepublicEcological Applications 24518ndash527 DOI 10189013-06401

Kauffman JB Hernandez Trejo H Del Carmen Jesus Garcia M Heider C ContrerasWM 2016 Carbon stocks of mangroves and losses arising from their conversion tocattle pastures in the Pantanos de Centla MexicoWetlands Ecology and Management24203ndash216 DOI 101007s11273-015-9453

Koch EW Barbier EB Silliman BR Reed DJ Perillo GME Hacker SD Granek EFPrimavera JH Muthiga N Polasky S 2009 Non-linearity in ecosystem servicestemporal and spatial variability in coastal protection Frontiers in Ecology and theEnvironment 729ndash37 DOI 101890080126

Koricheva J Gurevitch J Mengersen K (eds) 2013Handbook of meta-analysis in ecologyand evolution Princeton Princeton University Press 520

De la Lanza Espino G Peacuterez MAO Peacuterez JLC 2013 Diferenciacioacuten hidrogeomorfoloacuteg-ica de los ambientes costeros del Paciacutefico del Golfo de Meacutexico y del Mar CaribeInvestigaciones Geograacuteficas Boletiacuten del Instituto de Geografiacutea 8333ndash50

LauWWY 2013 Beyond carbon conceptualizing payments for ecosystem services inblue forests on carbon and other marine and coastal ecosystem services Ocean ampCoastal Management 835ndash14 DOI 101016jocecoaman201203011

Liu J Scheuer E Dibb J Ziemba LD Thornhill KL Anderson BEWisthaler AMikoviny T Devi JJ BerginMWeber RJ 2014 Brown carbon in the continentaltroposphere Geophysical Research Letters 412191ndash2195 DOI 1010022013GL058976

Lovelock CE AdameMF Bennion V Hayes M Reef R Santini N Cahoon DR 2015Sea level and turbidity controls on mangrove soil surface elevation change EstuarineCoastal and Shelf Science 1531ndash9 DOI 101016jecss201411026

Lovelock CE Fourqurean JWMorris JT 2017Modeled CO2 emissions from coastalwetland transitions to other land uses tidal marshes mangrove forests and seagrassbeds Frontiers in Marine Science 4143 DOI 103389fmars201700143

Lugo AE Snedaker SC 1974 The ecology of mangroves Annual Review of Ecology andSystematics 539ndash64 DOI 101146annureves05110174000351

Macreadie PI BairdME Trevathan-Tackett SM Larkum AWD Ralph PJ 2014Quantifying and modelling the carbon sequestration capacity of seagrass meadowsmdasha critical assessmentMarine Pollution Bulletin 83430ndash439DOI 101016jmarpolbul201307038

Macreadie PI Nielsen DA Kelleway JJ Atwood TB Seymour JR Petrou K ConnollyRM Thomson ACG Trevathan-Tackett SM Ralph PJ 2017 Can we manage

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3236

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 33: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

coastal ecosystems to sequester more blue carbon Frontiers in Ecology and theEnvironment 15206ndash213 DOI 101002fee1484

Maderey-R LE Torres-Ruata C 1990Hidrografiacutea e hidrometriacutea IV61 (A) AtlasNacional del Meacutexico II Escala 1 Instituto de Geografiacutea UNAM 4000000

Marbagrave N Arias-Ortiz A Masqueacute P Kendrick GA Mazarrasa I Bastyan GR Garcia-Orellana J Duarte CM 2015 Impact of seagrass loss and subsequent reveg-etation on carbon sequestration and stocks Journal of Ecology 103296ndash302DOI 1011111365-274512370

MartinMA Landis E Bryson C Lynaugh S Mongeau A Lutz S 2016 Blue carbonmdashnationally determined contributions inventory appendix to coastal blue carbonecosystems In Opportunities for nationally determined contributions GRID-ArendalNorway 23

Mazarrasa I Samper-Villarreal J Serrano O Lavery PS Lovelock CE Marbagrave NDuarte CM Corteacutes J 2018Habitat characteristics provide insights of car-bon storage in seagrass meadowsMarine Pollution Bulletin 134106ndash117DOI 101016jmarpolbul201801059

Mazda Y Kobashi D Okada S 2005 Tidal-Scale Hydrodynamics within MangroveSwampsWetlands Ecology and Management 13647ndash655DOI 101007s11273-005-0613-4

Medina-Goacutemez I Madden CJ Herrera-Silveira J Kjerfve B 2016 Response of Thalassiatestudinum morphometry and distribution to environmental drivers in a pristinetropical lagoon PLOS ONE 11e0164014 DOI 101371journalpone0164014

Mendoza-Martiacutenez JE 2017 Captura y emisiones de carbono en pastos marinos sometidosa perturbaciones naturales Tesis de maestriacutea Centro de Investigacioacuten y de EstudiosAvanzados del Meacuterida Instituto Politeacutecnico Nacional 96

Moher D Liberati A Tetzaff J Altman DG 2009a Preferred reporting items forsystematic reviews and meta-analyses the PRISMA statement Annals of InternalMedicine 151(4)264ndash269 DOI 1073260003-4819-151-4-200908180-00135

Moher D Liberati A Tetzaff J Altman DG The PRISMAGroup 2009b Preferedreporting items for systematic reviews and meta analyses the prisma statementPLOS Medicine 6(7)e1000097 DOI 101371journalpmed1000097

Moodley L Middelburg JJ Herman PMJ Soetaert K De Lange GJ 2005 Oxygena-tion and organic-matter preservation in marine sediments Direct experimen-tal evidence from ancient organic carbonndashrich deposits Geology 33889ndash892DOI 101130G217311

Ochoa-Goacutemez JG Lluch-Cota SE Rivera-Monroy VH Lluch-Cota DB Troyo-DieacuteguezE OechelW Serviere-Zaragoza E 2019Mangrove wetland productivity andcarbon stocks in an arid zone of the Gulf of California (La Paz Bay Mexico) ForestEcology and Management 442135ndash147DOI 101016jforeco201903059

OdumWE Heald EJ 1972 Trophic analyses of an estuarine mangrove communityBulletin of Marine Science 22671ndash738

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3336

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 34: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

OdumWEMcIvor CC Smith TJ 1982 The ecology of the mangroves of south Floridaa community profile United States Fish and Wildlife Service Office of BiologicalServices Washington DC 144 FWSOBS-8124 Reprinted September 1985

Ouyang X Lee SY Connolly RM 2017 The role of root decomposition in globalmangrove and saltmarsh carbon budgets Earth-Science Reviews 16653ndash63DOI 101016jearscirev201701004

Pendleton L Donato DC Murray BC Crooks S JenkinsWA Sifleet S Craft CFourqurean JW Kauffman JB Marbagrave N Megonigal P Pidgeon E Herr DGordon D Baldera A 2012 Estimating global blue carbon emissions from con-version and degradation of vegetated coastal ecosystems PLOS ONE 7e43542DOI 101371journalpone0043542

Phang VXH Chou LM Friess DA 2015 Ecosystem carbon stocks across a tropicalintertidal habitat mosaic of mangrove forest seagrass meadow mudflat and sandbarEarth Surface Processes and Landforms 401387ndash1400 DOI 101002esp3745

Pullin AS Stewart GB 2006 Guidelines for systematic review in conservation andenvironmental management Conservation Biology 201647ndash1656DOI 101111j1523-1739200600485x

RahmanM Khan NI Hoque F Hamed I 2015 Carbon stock in the Sundarbansmangrove forest spatial variations in vegetation types and salinity zonesWetlandsEcology and Management 23(2)269ndash283 DOI 101007s11273-014-9379-x

Ramiacuterez-Ramiacuterez J Medina-Goacutemez I Herrera-Silveira JA 2015 Diversity and C stor-age in a submerged aquatic vegetation community of a coastal lagoon environmentIn Paz F Wong J eds Estado Actual del Conocimiento del Ciclo del Carbono y susInteracciones en Meacutexico Siacutentesis a 2014 Meacutexico Programa Mexicano del CarbonoAC 316ndash326

Robertson AI Alongi DM 1995 Role of riverine mangrove forests in organic carbonexport to the tropical coastal ocean a preliminary mass balance for the Fly Delta(Papua New Guinea) Geo-Marine Letters 15134ndash139 DOI 101007BF01204454

Robertson AI Alongi DM 2016Massive turnover rates of fine root detrital carbon intropical Australian mangroves Oecologia 180841ndash851DOI 101007s00442-015-3506-0

Robertson AI Daniel PA 1989 The influence of crabs on litter processing in highintertidal mangrove forests in tropical Australia Oecologia 78(2)191ndash198DOI 101007BF00377155

Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Vaacutezquez-Lule AD Maacuterquez-Mendoza JDVaacutezquez-Balderas B Valderrama-Landeros L Velaacutezquez-Salazar S Cruz-LoacutepezMI Ressl R Uribe-Martiacutenez A 2013Manglares de MeacutexicoExtensioacuten distribucioacuteny monitoreo Meacutexico DF Comisioacuten Nacional para el Conocimiento y Uso de labiodiversidad

Saintilan N Rogers K Mazumder DWoodroffe C 2013 Allochthonous and au-tochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands Estuarine Coastal and Shelf Science 12884ndash92DOI 101016jecss201305010

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3436

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 35: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Sanders CJ Maher DT Tait DRWilliams D Holloway C Sippo JZ Santos IR 2016Are global mangrove carbon stocks driven by rainfall Journal of Geophysical ResearchG Biogeosciences 1212600ndash2609 DOI 1010022016JG003510

Santini NS Reef R Lockington DA Lovelock CE 2015 The use of fresh and salinewater sources by the mangrove Avicennia marina Hydrobiologia 74559ndash68DOI 101007s10750-014-2091-2

Santos DMC Estrada GCD Fernandez V EstevamMRM Souza BTDE Soares MLG2017 First assessment of carbon stock in the belowground biomass of brazilianmangroves Anais da Academia Brasileira de Ciecirccias 891579ndash1589

Schile LM Kauffman JB Crooks S Fourqurean JW Glavan J Megonigal JP 2017 Lim-its on carbon sequestration in arid blue carbon ecosystems Ecological Applications27(3)859ndash874 DOI 101002eap1489

Short FT Short A Novak CA 2016 Seagrasses In Finlayson CM Milton GR PrenticeRC Davidson NC eds The Wetland Book II Distribution Description and Conserva-tion Springer Science DOI 101007978-94-007-6173-5_262-1

Shunula JP Whittick A 1999b Aspects of litter production in mangroves fromunguja island Zanzibar Tanzania Estuarine Coastal and Shelf Science 4951ndash54DOI 101016S0272-7714(99)80008-0

SpaldingMD Blasco F Field CD (eds) 1997World mangrove atlas Okinawa Interna-tional Society for Mangrove Ecosystems

Sutton-Grier AE Moore A 2016 Leveraging carbon services of coastal ecosys-tems for habitat protection and restoration Coastal Management 44259ndash277DOI 1010800892075320161160206

Teutli-Hernaacutendez C Herrera-Silveira JA 2016 Estrategias de restauracioacuten demanglares de Meacutexico el caso Yucataacuten In Ceccon Y Martiacutenez-Garza C edsExperiencias mexicanas en la restauracioacuten ecoloacutegica de ecosistemas CuernavacaCONABIO CRIM-UNAM UAEM 459ndash484

Thorhaug A Poulos HM Loacutepez-Portillo J Ku TCW Berlyn GP 2017 Seagrassblue carbon dynamics in the Gulf of Mexico Stocks losses from anthropogenicdisturbance and gains through seagrass restoration Science of The Total Environment605626ndash636

Thorhaug AL Poulos HM Loacutepez-Portillo J Barr J Lara-Domiacutenguez AL Ku TC BerlynGP 2018 Gulf of Mexico estuarine blue carbon stock extent and flux Mangrovesmarshes and seagrasses a North American hotspot Science of The Total Environment6531253ndash1261 DOI 101016jscitotenv201810011

Twilley RR Lugo AE Patterson-Zucca C 1986 Litter production and turnoverin Basin Mangrove Forests in Southwest Florida Ecology 67(3)670ndash683DOI 1023071937691

Twilley RR Rivera-Monroy VH 2005 Developing performance measures of mangrovewetlands using simulation models of hydrology nutrient biogeochemistry andcommunity dynamics Journal of Coastal Research 4079ndash93

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3536

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636

Page 36: Blue carbon of Mexico, carbon stocks and fluxes: a ...Mendoza-Martinez JE, Pech-Poot EY, Montero J, Teutli-Hernandez C. 2020. Blue carbon of Mexico, carbon stocks and fluxes: a systematic

Twilley RR Rovai AS Riul P 2018 Coastal morphology explains global blue car-bon distributions Frontiers in Ecology and the Environment 16(9)503ndash508DOI 101002fee1937

UNFCCCV 2015United Nations Framework Convention on Climate Change Adoptionof the Paris agreement I proposal by the president (Draft Decision) Geneva UnitedNations Office

Valderrama-Landeros LH Rodriacuteguez-Zuacutentildeiga MT Troche-Souza C Velaacutezquez-SalazarS Villeda-Chaacutevez E Alcaacutentara-Maya JA Vaacutezquez-Balderas B Cruz-LoacutepezMI RRessl 2017Manglares de Meacutexico actualizacioacuten y exploracioacuten de los datos del sistemade monitoreo 19701980ndash2015 Ciudad de Meacutexico Comisioacuten Nacional para elConocimiento y Uso de la Biodiversidad 128

WangM Zhang J Tu Z Gao XWangW 2010Maintenance of estuarine water qualityby mangroves occurs during flood periods a case study of a subtropical mangrovewetlandMarine Pollution Bulletin 602154ndash2160DOI 101016jmarpolbul201007025

Waycott M Duarte CM Carruthers TJB Orth RJ DennisonWC Olyarnik SCalladine A Fourqurean JW Heck KL Hughes AR 2009 Accelerating lossof seagrasses across the globe threatens coastal ecosystems Proceedings of theNational Academy of Sciences of the United States of America 10612377ndash12381DOI 101073pnas0905620106

Wolanski E Boorman LA Chiacutecharo L Langlois-Saliou E Lara R Plater AJ UnclesRJ Zalewski M 2004 Ecohydrology as a new tool for sustainable managementof estuaries and coastal watersWetlands Ecology and Management 12235ndash276DOI 101007s11273-005-4752-4

Woodroffe C 1992 Chapter 2 mangrove sediments and geomorphology In RobertsonA Alongi D eds Tropical mangrove ecosystems Coastal and estuarine series Vol 41Washington DC American Geophysical Union 7ndash41 DOI 101029CE041p0007

Yulianto G Soewardi K Adrianto L 2016 The role of mangrove in support of coastalfisheries in Indramayu Regency West Java Indonesia Aquaculture Aquarium Con-servation amp Legislation-International Journal of the Bioflux Society 9(5)1020ndash1029

Zhang H YuanW DongW Liu S 2014 Seasonal patterns of litterfall in forest ecosys-tem worldwide Ecological Complexity 20240ndash247DOI 101016jecocom201401003

Herrera-Silveira et al (2020) PeerJ DOI 107717peerj8790 3636