RED LIST ASSESSMENTGreen turtle, Chelonia mydas, South Atlantic Region

1a. Scientific name:

Chelonia mydas (Linnaeus 1758)

1b. Synonym/s:

Testudo mydas (Linnaeus, 1758)

1c. English Common Name:

Green Turtle

1d. Other Common Name:French - Tortue verte, Tortue franchePortuguese – Tartaruga verdeSpanish – Tortuga Blanca, Tortuga Verde

2a. Order 2b. Family

Testudines Cheloniidae

3. DistributionThe green turtle is globally distributed throughout the tropical and subtropical and temperate regions of the Mediterranean Sea and Pacific, Indian, and Atlantic Oceans (Wallace et al. 2010) (Fig. 1). In this assessment we have used the distinct population segment (DPS) defined in Seminoff et al. (2015) as the South Atlantic (Fig. 2), which includes the following regional management units defined by Wallace et al. (2010); Atlantic South Central; Atlantic Southwest; Atlantic South Caribbean; Atlantic East.

Countries of OccurrenceWithin the South Atlantic region, green turtles have been documented nesting in the following countries: Anguilla; Antigua and Barbuda; Aruba; Ascension Island (UK), Barbados; Bonaire; Brazil, British Virgin Islands; Cape Verde; Colombia, Curacao; Dominica; Equatorial Guinea,French Guiana; Gabon, Guadaloupe; Guinea Bissau, Guyana; Martinique; Mauritania, Montserrat; Republic of Congo; Sao Tome and Principe, St. Kitts and Nevis; St. Lucia; St. Vincent and the Grenadines; St. Maarten; Suriname, Trinidad; Tobago; Venezuela; US Virgin Islands (Girard et al. 2016, Seminoff et al. 2015).

Those listed above in bold are the index sites for which we have long term data with which to assess trends.

In addition to nesting activity, green turtles have been documented in the waters of most countries within this geographical region.

Fisheries AreasThe green turtle has been documented in the following FAO fishing area:31: Atlantic, Western Central34: Atlantic, Eastern Central41: Atlantic, Southwest47: Atlantic Southeast

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3a. Red List Assessment

3b. Red List Criteria (For threatened taxa (i.e., those assessed as CR, EN or VU) record which criteria are met (e.g., A2c+3c; B1ab (iii); D) alongside the appropriate Category. For NT taxa, record criteria nearly met):

Extinct (EX)

Extinct in the Wild (EW)

Critically Endangered (CR)

Endangered (EN)

Vulnerable (VU)

Near Threatened (NT)

X Least Concern (LC) X

Data Deficient (DD)

Not Evaluated (NE)

4. Rationale for the Red List Assessment

Rationale

The South Atlantic region as denoted by Seminoff et al. (2015; Figure 2) has been defined as the unit of assessment according to mixed stock analyses, tracking and tag returns for the Atlantic. Although previously divided into four RMUs (Wallace et al. 2010), additional data have subsequently shown that there is clear overlap and mixing of both adults and juveniles within the South Atlantic, but not with green turtles in adjacent regions. Therefore, we assessed South Atlantic Ocean green turtles as a single subpopulation.

Although there are 28 countries/dependencies included in this region, long term nesting monitoring data (≥10years) are only available for sites in Ascension Island, Brazil, Equatorial Guinea, French Guiana, Guinea Bissau, Suriname and Venezuela.

For this assessment we used annual nest counts as our index of population abundance. Collectively, these data show an overall increase of 174% from historical abundance to abundance through 2015 (see Table 1 for study periods for each population). In addition, the population is large and widely distributed across the region. However, a significant proportion (>60%) of the overall assessed population however nest at two rookeries; Ascension Island and Poilão (Guinea Bissau), which are both estimated to have in the order of 20,000 nests/yr. Both sites are relatively small and isolated islands, making them potentially vulnerable to threats such as over exploitation and local disasters (e.g. storms, oil spills, coastal erosions). In addition, their ability to respond to climate change by moving to new nesting beaches is likely to be confounded by their isolated locations, natal philopatry and high site fidelity.

Based on data from the above sites, the South Atlantic green turtle subpopulation is considered Least Concern under current IUCN Red List criteria.

JustificationThe analysis of time series datasets with ≥10 years of data (nest counts) at nine nesting sites revealed different rookery trends within the region, but an overall subpopulation increase relative to subpopulation size three generations ago (Criterion A2; Table 1). We also assessed the subpopulation under Criteria B, C, and D, but the Extent of Occurrence and Area of Occupancy exceeded the thresholds of threatened categories for Criterion B, and the number of mature individuals in this subpopulation exceeds thresholds of threatened categories for Criteria C and D.

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Assessment Procedure:

Criterion A.We used the following approach taken for the recent Red List assessments for loggerhead turtles (Casale and Tucker 2015) and leatherback turtles (Wallace et al. 2013) to apply Criterion A as follows:

For marine turtles, annual counts of nesting females and their nesting activities (more often the latter) are the most frequently recorded and reported abundance metric across index monitoring sites, species, and geographic regions (National Research Council 2010).

To apply Criterion A, three generations (or a minimum of ten years, whichever is longer) of abundance data are required (IUCN 2014). The challenges of this requirement on long-lived species like turtles—with generation lengths of 30 yr or more—are obvious (see Seminoff and Shanker 2008 for a review). Abundance data from ~135 yr ago (one generation estimated 45 yr; see Section 9d) are not available for any turtle populations anywhere in the world. Extrapolating backward using population trends based on current datasets was considered inappropriate because estimates produced would be biologically unrealistic and unsubstantiated, given what is currently known about sea turtle nesting densities on beaches and other factors (Mrosovsky 2003). In the absence of better information, we assumed that population abundance three generations ago (~135 years), was similar to the first observed abundance rather than to assume that the population has always been in a decline (or increase) of the same magnitude as in the current generation. Thus, to apply Criterion A we assumed that the abundance at the beginning of an available time series dataset had not changed significantly in the preceding three generations, and therefore used the same abundance value in trend calculations. For the green turtle global and subpopulation assessments we only considered time series datasets of ≥10 yr.

For the South Atlantic, we included time series datasets of ≥10 yr, from nine index sites (Table 1), and we assumed that these index sites were representative of the overall population trend for the entire subpopulation. It is worth noting that for six index sites the available datasets extended beyond ten years (Table 1). We estimate that a total of >72,000 nests are laid annually at these sites, with at least a further 7,000 nests laid at other sites in this region each year.

From one past and one recent abundance value (each representing the annual average of five year nest counts) we calculated annual and overall trends (past-present) for each index nesting site within the subpopulation, and then calculated the overall subpopulation past trend. The most recent year for available abundance data across all rookeries was 2015. Where time series ended prior to 2015, we estimated individual nest abundances for each rookery through 2015 based on each rookery’s population trend for existing years. Trends varied across the different rookeries, with negative trends observed at only one rookery; Bioko, Equatorial Guinea (-39%; 2001-2014; Table 1). The overall average trend – which was calculated by weighting trends from each rookery based on its abundance relative to that of the entire subpopulation – for the South Atlantic population was however positive (+174%; Table 1). In conclusion, the South Atlantic green turtle subpopulation does not qualify for a threatened category under Criterion A, and is thus classified as Least Concern.

Criterion B.Extent of occurrence for the South Atlantic green turtle subpopulation is basin-wide; therefore it exceeds the thresholds for all threatened categories (>20,000km2). Likewise, although several of the index sites used in this assessment are relatively small and isolated islands, the Area of Occupancy for this subpopulation exceeds 2,000km2, and the subpopulation does not meet any of the subcriteria for Criterion B (e.g., a: fragmented, b:decline, c: extreme fluctuations). For these reasons, this subpopulation is Least Concern under Criterion B.

Criterion C and DWe estimate that >72,000 total nests are laid at the index sites each year. It is likely that the number of breeding females is of a similar magnitude, given that on average females lay 3 clutches per season and breed every 3 years. It should be noted that for this assessment we are not estimating the number of males, for which data are extremely limited, but given that we estimate that there are >72,000 mature females, regardless of whether we include an estimate for males this sub population exceeds the threshold of >10,000 mature individuals and does not qualify under Criterion C or D.

Sources of Uncertainty

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Although monitoring of nesting activities by adult female sea turtles is the most common metric recorded and reported across sites and species, globally, there are several disadvantages to using it as a proxy for overall population dynamics, some methodological, some interpretive (National Research Council 2010). First, because nesting females are a very small proportion of a sea turtle population, using abundance of nesting females and their activities as proxies for overall population abundance and trends requires knowledge of other key demographic parameters (several mentioned below) to allow proper interpretation of cryptic trends in nesting abundance (National Research Council 2010). However, there remains great uncertainty about most of these fundamental demographic parameters for green turtles, including age at maturity, generation length, survivorship across life stages, adult and hatchling sex ratios, and conversion factors among reproductive parameters (clutch frequency, nesting success, remigration intervals, etc.). These parameters can vary among subpopulations, further complicating the process of combining them to obtain global population abundance and trend estimates, and contributing to the uncertainty in these estimates. Second, despite the prevalence of nesting abundance data for marine turtles, monitoring effort and methodologies can vary widely within and across study sites, complicating comparison of nesting count data across years within sites and across different sites as well as robust estimation of population size and trends. For further reading on sources of uncertainty in marine turtle Red List assessments, see Seminoff and Shanker (2008).

5. Reason for Change from previous Red List assessment

Genuine change in status of species New or better information available

Incorrect information used previously Taxonomic change affecting the species

Previously incorrect application of the Red List Criteria

6. Current Population Trend (cross (X) one of the following):

X Increasing Decreasing Stable Unknown

7. Date of Assessment (day/month/year): 26th July 2016

8a. Name/s of the Assessor/s

Annette Broderick and Ana Rita Patrício

8b. Names of the Evaluators - to be filled in By Red List Authority ONLY

Red List Evaluators: Nicholas Pilcher, John Musick, Bryan Wallace

Red List Authority: IUCN Marine Turtle Specialist Group

9. Text documentation

9a. Taxonomy:

Testudines, Cheloniidae, Chelonia mydas

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9b. Geographic Range

The green turtle is globally distributed throughout the tropical, subtropical and temperate regions of the Mediterranean Sea and Pacific, Indian, and Atlantic Oceans (Wallace et al. 2010) (Fig. 1).In this assessment we use the South Atlantic distinct population segments (DPS) defined by Seminoff et al. (2015; Region 3, Fig. 2) according to available molecular and movement data.

The range of the South Atlantic DPS begins at the border of Panama and Colombia at 7.5° N., 77° W., heads due north to 14° N., 77° W., then east to 14° N., 65.1° W., then north to 19° N., 65.1° W., and along 19° N. latitude to Mauritania in Africa, to include the U.S. Virgin Islands in the Caribbean. It extends along the coast of Africa to South Africa, with the southern border being 40° S. latitude.

9c. Population

The majority of nesting occurs at Poilão Island, Guinea Bissau (Catry et al. 2009), Ascension Island, UK (Weber et al. 2014) and Galibi and Matapica in Suriname (Turny pers. comm.). These three countries represent >90% of the nesting populations included in this assessment for the South Atlantic region (Table 1).

In West Africa, notable rookeries are also found on other islands of the Bijagos Archipelago in Guinea Bissau (Ferreira 2012, IBAP 2016), and in the Gulf of Guinea, in the islands of Bioko, (Equatorial Guinea, Honarvar et al. 2016), São Tomé and Príncipe (ATM 2013, ATM/MARAPA 2016).

In the southern Caribbean other important nesting sites include Aves Island, Venezuela (Garcia-Cruz et al. 2015), Guyana and the French Guiana (Seminoff et al. 2015). Additional low levels of nesting occur throughout many of the Caribbean Islands and along Colombia’s Caribbean coast.

Significant nesting is also documented in Brazil, along its mainland coast and on its offshore islands, with the major rookeries located on the remote islands of Trindade, Atol das Rocas and Fernando de Noronha (Bellini et al. 2013).

From the rookeries for which we had ≥10 years of data we estimated that >72,000 nests are laid each year (Table 1). Data for other sizeable rookeries (>100 nests per year in this region) for which we were unable to assess trends indicate that at least an additional >7,000 nests are laid in this region each year.

These sites include:

BrazilFor the island of Trindade, Brazil, estimates of the number of nests laid annually were only available for seven nesting seasons during the period 1991/92 through 2008/09, and ranged from 1333 to 6402 (mean: 3,600 nests per season), with no significant trend in the period (Almeida et al. 2011); beach monitoring and data collection have continued to be performed on Trindade since 2008, but no estimates of the annual number of nests are currently available for post-2008/09 seasons.

French GuianaChambault et al. (2016) recorded >2,100 nests in French Guiana in each of the years 2012 and 2014. Data included in our analysis for Yalimapo suggest that approximately 1,400 nests are laid at this site (Table 1.), thus a further 700+ nests may also be laid at other sites in French Guiana each year.

GuyanaNesting for the years 2010-2015 has ranged from 49-185 nests laid annually (S. Kandaswamy pers. comm. Protected Areas Commission, Guyana).

Guinea Bissau

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Besides the major rookery at Poilão Island, nesting also occurs in other islands of the Bijagós Archipelago, at much lower magnitudes. Limited monitoring has been conducted, and it is estimated that ca. 1,100 nests per season are laid (Ferreira 2012, IBAP 2016).

MauritaniaGreen turtle nesting in Mauritania has been documented in recent years and it is estimated that there are >100 nest laid each year (pers.comm J.Fretey)

São Tomé and Príncipe (STP)In Principe Island, there was an increase in nesting from 2007-2011 to 2012-2016 of 115% (Ferreira et al. 2012, ATM 2013, ATM pers. comm. and Principe Trust Foundation pers. comm.), and a mean annual number of clutches of 950 is estimated. In São Tomé Island 355 – 800 nests were laid during the 2015-2016 nesting season (ATM/MARAPA 2016).

Juveniles and SubadultsMixed-stock foraging aggregations of juvenile and subadult green turtles are further found throughout the Caribbean, and along the coastlines and offshore islands of South America and West Africa. Few of these aggregations have been monitored for over a decade (Colman et al. 2015, Vélez-Rubio et al. 2013), but for the most part very limited information is available on vital population parameters (e.g. survival, residency, abundance) and threats.

9d. Habitat and Ecology

The ecology and habitat of green turtles have recently been reviewed by Seminoff et al. (2015), where life history traits for regional populations are also presented where available. The typical life cycle for this species is similar to other species of marine turtle; females lay multiple clutches (~100 eggs/clutch) in a breeding year; eggs incubate for 6-8 weeks and sex of offspring is determined by incubation temperature, with most studies recording female biased offspring sex ratios (Seminoff et al. 2015). Upon hatching, offspring leave the nesting beach and spend the first few years in the pelagic where they are thought to associate with ocean currents before recruiting to coastal habitats where they adopt a herbivorous diet and mature. Green turtles are migratory as adults, moving between nesting and foraging sites every 2-4 years to breed and showing high site fidelity and natal philopatry. Being long-lived, there is a paucity of data on life history traits such as longevity and ageing, confounded by issues such as tag loss. Data from long term monitoring sites (e.g. French Frigate Shoals, Hawaii and Heron Island, Australia) are now providing valuable new insights into the life history of green turtles (see below).

Generation LengthThe IUCN Red List Criteria define generation length to be the average age of parents in a population, i.e. older than the age at maturity and younger than the oldest mature individual (IUCN 2014). Although different subpopulations may have different generation lengths, since this information is limited we adopted the same value for all the subpopulations.

Green turtles in the wild are estimated to attain maturity at 15-50 years (Avens and Snover 2013), and we considered here 30 years to be equal or greater than the average age at maturity. Data on reproductive longevity in green turtles are limited, owing to tag loss issues and lack of long term datasets, but are becoming available as long-term monitoring projects themselves age. Tagging studies have documented reproductive histories up to 38 years in Hawaii (Balazs et al. 2015; Humberg & Balazs 2014), 24 yrs in the Mediterranean (Broderick, unpubl. data) and 37 years at Heron Island, Australia (C. Limpus pers. comm.). We considered here 30 years to be equal or greater than the average reproductive longevity. Therefore, we considered 45 years to be equal or greater than the average generation length (i.e. average age at sexual maturity plus ½ reproductive longevity), therefore avoiding underestimation as recommended by IUCN (2014).

9e. Threats

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Being long lived, migratory and laying eggs on land makes green turtles vulnerable to many anthropogenic threats including: overexploitation; bycatch in marine fisheries; habitat degradation and loss; disease; invasive species and climate change (see Seminoff et al. 2015 for detailed review of threats in the regions).

Harvest of marine turtles remains legal in 42 countries globally and Humber et al. (2014) estimate that in excess of 33,000 green turtles are legally captured each year. Illegal harvest both at the nesting beach and in nearshore habitats, remains unquantified, typically unreported, but it represents a major threat in African countries (Catry et al. 2009, Fretey & Mint Hama, 2012, Honarvar et al. 2016). Although many marine turtle fisheries have ceased over the past century, populations are only now recovering (Broderick et al. 2006).

Bycatch of green turtles remains a major issue. Being herbivorous they are not as susceptible to long line fisheries as some other species, but are more frequently captured in net and trawl fisheries in coastal waters (Wallace et al. 2010). All stages of the life cycle are impacted by habitat degradation, in particular due to coastal development (Fuentes et al. 2016), mining and dredging, leading to loss of beach habitat and enhancing erosion. Sea-level-rise is predicted to reduce suitable habitats further (Hawkes et al. 2014). At sea, fisheries and coastal development also impact foraging habitats for this species.

Ingestion of marine debris may be a growing threat, particularly in the south west Atlantic, with studies indicating mortality rates even higher than those associated with bycatch (Alonso & Velez-Rubio 2011, Guebert-Bartholo et al. 2011).

Green Turtle Fibropapilloma (GTFP) disease is prevalent in many populations worldwide, within the South Atlantic region present in foraging areas in Brazil (Rodenbusch et al. 2014), Uruguay (López-Mendilaharsu et al. 2016), Mauritania (Mint Hama & Fretey, 2014), the Gulf of Guinea (Duarte et al. 2012), and in the Caribbean, and has been shown to be more prevalent in areas with lower water quality (Van Houtan et al. 2010), typically associated with coastal development. Although GTFP does not seem to be a current major threat, disease virulence may be enhanced with predicted climate change (Patricio et al. 2016).

As long lived reptiles with temperature-dependent sex determination, all marine turtles are vulnerable to change in climate, in particular to global warming causing skewed offspring sex ratios and lowering hatching or reducing the fitness of hatchlings (Hawkes et al. 2014).

The effective protection of in water habitats is an issue of concern, due to a greater difficulty to control the range of threats found at sea (bycatch, illegal harvesting, plastic ingestion, emerging diseases, etc.). Thus, protection granted to the nesting populations is not always extended to the foraging areas. As the green turtle is long lived with a large generation length, impacts of the depletion of younger individuals take several years to be noted in the effective population, justifying the need for more studies on the dynamics of juvenile and subadult foraging grounds, to clearly assess the trend of the green turtle in the South Atlantic region and worldwide.

9f. Conservation Actions

Green turtles are afforded legislative protection under a number of treaties and laws (Wold 2002). Annex II of the SPAW Protocol to the Cartagena Convention (a protocol concerning specially protected areas and wildlife); Appendix I of CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora); and Appendices I and II of the Convention on Migratory Species (CMS). A partial list of the International Instruments that benefit green turtles includes the Inter-American Convention for the Protection and Conservation of Sea Turtles, the Memorandum of Understanding on the Conservation and Management of Marine Turtles and their Habitats of the Indian Ocean and South-East Asia (IOSEA), the Memorandum of Understanding on ASEAN Sea Turtle Conservation and Protection, and the Memorandum of Understanding Concerning Conservation Measures for Marine Turtles of the Atlantic Coast of Africa.

As a result of these designations and agreements, many of the intentional impacts directed at

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sea turtles have been lessened: harvest of eggs and adults has been slowed at several nesting areas through nesting beach conservation efforts and an increasing number of community-based initiatives are in place to slow the take of turtles in foraging areas. In regard to incidental take, the implementation of Turtle Excluder Devices has proved to be beneficial in some areas, primarily in the United States and South and Central America (National Research Council 1990). Guidelines are available to reduce sea turtle mortality in fishing operations in coastal and high seas fisheries (FAO 2009). RFMO Recommendations are compulsory for their implementation by members, particularly within the Organizations leading with tuna fisheries. However, despite these advances, human impacts continue throughout the world. The lack of effective monitoring in fisheries operations still allows substantial direct and indirect mortality, and the uncontrolled development of coastal and marine habitats threatens to destroy the supporting ecosystems of long-lived green turtles.

This assessment only uses breeding females as an indicator of population and as such we urge caution. The rise in many populations presented here is a result of decades of positive action and a reduction of some threats. This species remains conservation dependent and we strongly recommend that conservation actions that have proved successful are continued.

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Wallace BP, DiMatteo AD, Hurley BJ, Finkbeiner EM, Bolten AB, Chaloupka MY, Hutchinson BJ, Abreu-Grobois FA, Amorocho D, Bjorndal KA, Bourjea J, Bowen BW, Duenas RB, Casale P, Choudhury BC, Costa A, Dutton PH, Fallabrino A, Girard A, Girondot M, Godfrey MH, Hamann M, Lopez-Mendilaharsu M, Marcovaldi MA, Mortimer JA, Musick JA, Nel R, Pilcher NJ, Seminoff JA, Troeng S, Witherington B, Mast RB. 2010. Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PLoS ONE 5: e15465.

Wallace BP, Lewison RL, McDonald SL, McDonald RK, Kot CY, Kelez S, Bjorkland RK, Finkbeiner EM, Crowder LB, 2010. Global patterns of marine turtle bycatch. Conservation letters 3:131-142.

Weber SB, Weber N, Ellick J, Avery A, Frauenstein R, Godley BJ, Sims J, Williams N, Broderick AC. 2014. Recovery of the South Atlantic’s largest green turtle nesting population. Biodiversity and Conservation 23:3005-3018

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Figure 1: Global distribution and nesting sites for the green turtle (Wallace et al. 2010; Figure 2a).

Figure 2. Distribution and nesting sites of the South Atlantic green turtle subpoulation, defined previously as a “distinct population segment (DPS)” under U.S. Endangered Species Act law by Seminoff et al. (2015).

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Past Estimate Recent Estimate

Site Range of Yrs

Ref year

Nests yr-1

Range of Yrs

Ref year

Nests yr-1

Estimate 3 gen. ago

Estimate to 2015

3-gen. change

Estimate to 2060

Data Source

Ascension Island, UK 1999-2003 1999 10,332

2011-2015 2015 22,969 10,332 22,969 1.22 190,353 1

Poilao, Guinea Bissau 2000-2004 2000 6,595 2011-2015 2015 23,601 6,595 23,601 2.58 851,639 2

Aves Island, Venezuela 1979-1983 1979 408 2005-2008 2008 1,365 408 1,809 3.43 11,072 3

Bioko, Equatorial Guinea 2001-2005 2001 1,128 2010-2014 2014 714 1,128 691 -0.39 159 4

Galibi, Suriname 1984-1988 1984 4,798 2006-2010 2010 12,071 4,798 14,320 1.98 66,642 5

Matapica, Suriname 2001-2006 2001 2,292 2007-2010 2010 4,782 2,292 6,907 2.01 189,053 5

Atol das Rocas, Brazil 1990-1994 1990 327 2005-2010 2010 446 327 480 0.47 934 6

Fernando de Noronha, Brazil 2006-2010 2006 118 2011-2015 2015 173 118 173 0.47 968 7

Yalimapo, French Guiana* 2002-2005 2002 374 2011-2015 2015 1409 374 1409 2.77 100,107 8

Total Index sites 26,372

67,530 26,372 72,360 1.74 1,410,927

Table 1. Summary of information on past and present nesting abundances and trends at index nesting sites of the South Atlantic subpopulation of the green turtle (Chelonia mydas). Values are average number of nests per year based on annual data from the year range indicated. Data sources: 1. Weber et al. (2014); S. Weber pers. comm. 2. Catry et al. (2009), IBAP – Guinea Bissau unpublished data. 3. Garcia-Cruz et al. (2015); Garcia-Cruz pers.comm. 4. Honarvar et al. (2016), Rader et al. (2006). 5. A.Turny pers. comm. 6. Bellini et al. (2013). 7. C. Bellini PROTAMAR pers. comm. 8. Pers comm. J. Chevalier, Réserve Naturelle de l'Amana & M. Girondot, Université Paris Sud..Gen=generation; NB where nesting season span two years, we use the year in which the season commenced. *data are track counts converted to nests using an estimate of nesting success of 40%.

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