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Biodiversity assessment

Reforestation recommendations

Dr.

Archie Carr

Wildlife Refuge

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Edited by the

Canadian Organization for Tropical Education and Rainforest Conservation (COTERC)

Caño Palma Biological Station

San Francisco de Tortuguero

Costa Rica

July 2018

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Contents

VEGETATION ...................................................................................................................................................................... 4

Introduction ................................................................................................................................................................... 5

Methods .......................................................................................................................................................................... 6

Plant species .................................................................................................................................................................. 7

LARGE MAMMALS ........................................................................................................................................................... 8

Introduction ................................................................................................................................................................... 9

Methods ......................................................................................................................................................................... 10

Mammals species ........................................................................................................................................................ 13

Discussion ...................................................................................................................................................................... 15

TENT-MAKING BATS ..................................................................................................................................................... 23

Introduction ................................................................................................................................................................. 24

Methods ........................................................................................................................................................................ 25

Bat species .................................................................................................................................................................... 26

Discussion ..................................................................................................................................................................... 27

MACAWS ........................................................................................................................................................................... 30

Introduction .................................................................................................................................................................. 31

Habitat & Ecology ...................................................................................................................................................... 32

Methods ........................................................................................................................................................................ 33

Macaws activity ........................................................................................................................................................... 34

Discussion ..................................................................................................................................................................... 36

Conclusion ........................................................................................................................................................................ 38

Complete list of recommended plant species ...................................................................................................... 40

References ..........................................................................................................................................................................41

ANNEXES ........................................................................................................................................................................... 45

1

List of abbreviations

ACER: Association for Canadian Educational Resources

ACR: Dr. Archie Carr National Wildlife Refuge

ACTo: Área de Conservación Tortuguero - Tortuguero Conservation Area

ASVO: ASsociation of VOlunteers for Protected Areas Service

Cerro: Cerro de Tortuguero

COTERC: Canadian Organization for Tropical Education and Rainforest Conservation

CPBS: Caño Palma Biological Station

IUCN: International Union for Conservation of Nature

MINAE: Ministerio del Ambiente y Energías - Ministry of Environment and Energy

P: P-value

SE: Standard Error

SINAC: Sistema Nacional de Areas de Conservación - National System of Conservation Areas

STC: Sea Turtle Conservancy

TNP: Tortuguero National Park

(*): already present on the Dr. Archie Carr National Wildlife Refuge

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The Dr. Archie Carr National Wildlife Refuge (ACR) is a 0.39 km² terrestrial wild protected area located in the Northeastern part of Costa Rica, Limón Province (Figure 1). It’s a peninsula constrained between the town of Tortuguero, the Caribbean Sea and the Tortuguero river. It is part of the Tortuguero Conservation Area (ACTo), a large protected tropical rainforest in the Atlantic lowlands. The ACR creation in 1994 was supported by the Sea Turtle Conservancy (STC) and it is now a state property [1]. This protected area is under the management of the National System of Conservation Areas (SINAC – Sistema National de Areas de Conservación), and the Ministry of Environment and Energy (MINAE – Ministerio del Ambiente y Energías). The ACR suffered logging between the 1950’s and 70’s (pers. comm.). Deforestation was reduced in the 70’s with the end of the logging industry and the creation of the Tortuguero National Park (TNP). No restoration effort has been made since. The site still witnesses human disturbances. These include locals and tourists non-motorized traffic during the day, nocturnal turtle tourism and illegal plant collection, fishing or turtle poaching. It is also usurpation of state land with illegal constructions or land management [2]. The launch of a reforestation plan has been discussed since 2017 [2]. Its goals are the improvement of the ACR biodiversity and vegetation cover to reduce erosion and facilitate marine turtle nesting, as well as the recovery of emergent trees including the mountain almond (Dipteryx panamensis). This forest conservation initiative respects Dr. Archie Carr recommendations for Tortuguero watershed protection [3]. Collaborative infrastructures such as the Association of Volunteers for Protected Areas Service (ASVO) trees nursery are already existing. If the ideal state of a primary forest ended with past logging, the ACR secondary forest still hosts potential as a “safety net” limiting the tropical biodiversity mass extinctions [4]. The ultimate goal would be to reconnect it to the landscape of the TNP, increasing the potential available home range of its inhabiting species. A delay of 70 years maximum is expected before the forest harbors similar characteristics to an old-growth forest [5].

Figure 1: The Dr. Archie Carr National Wildlife Refuge, a peninsula between the Tortuguero River and the Caribbean Sea

Tortuguero

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Ecotourism could support this reforestation effort. Thanks to its unique geography, the development of a tour connecting the town of Tortuguero and the community of San Francisco through the ACR has also been discussed in 2017 [2]. Its organization is still uncertain. The management plan proposal of the ACR reveals a lack in the ACR biodiversity knowledge [2]. According to studies, the ACR and surroundings host more than 130 birds, 34 reptiles, 21 mammals, 12 amphibians and 26 plant species. As the ACR marine turtle activity is well studied by the STC, studies on poorly known species such as macaws or plants are a management priority. It also highlights the necessity of understanding potential effect of a restauration on the ecosystem. The plan proposes studies to be conducted between 2018 and 2020 to describe the ACR species composition of plants, macaws, mammals, snakes, and tent-making bats, as well as a research on native plants to use during the restoration effort. Long-term conservation benefits can only be accomplished if local communities get involved in all of its stages, from the protection to the economical outcomes sharing [4]. This participation is anticipated in the management plan proposal and strengthens the restoration efforts while empowering the community’s position as defenders of their natural environment [6]. Giving a higher touristic value to the ACR could possibly reduce its unauthorized use, balancing the anthropogenic disturbance created by tourism. To answer these objectives, the Canadian Organization for Tropical Education and Rainforest Conservation (COTERC) edited this report. It is based on long-term survey data conducted by the Caño Palma Biological Station (CPBS) in the ACTo, including recent surveys focused within the ACR. The results are completed with bibliographic sources. It aims to assess the wildlife and forest composition as well as recommend plant species to be planted or conserved in the ACR. Focal animal taxa have been selected according to the management plan and because they increase touristic attractiveness: terrestrial large mammals, tent-making bats and macaws. The strategy is, through an ecological restoration targeting these taxa, to improve the quality for the whole ecosystem. Mainly, increasing its biodiversity level would improve the ecosystem stability, resistance to perturbations, productivity, carbon fixation, water filtering potential and nutrient cycling [7, 8, 9, 10, 11]. The surveys took place in the ACTo, in four main locations, including the ACR. The CPBS is a privately-owned swamp forest with low human disturbance. The Cerro of Tortuguero is a 119 m high ancient volcano standing beside the village of San Francisco, surrounded by a path. The Tortuguero National Park is a primary rainforest with a palm-dominated Yolillales habitat [12], visited by numerous tourists annually. The repetition of the sampling methods in these different units combined with the intensive monitoring over long periods offers a robust overview of the species composition for rare and common species in the ACTo [13].

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VEGETATION

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Plant species composition and spatial and temporal organization of vegetation drive the fauna species composition. Animals, fungi and microorganisms depend on their neighboring vegetation. Living and dead trees provide food and nesting sites for all categories of animals, for they are home to hollows and decomposition food webs [14]. Reforestation is a unique opportunity to increase the forest biodiversity and native threatened or endemic species presence. The accumulated functioning value of a forest increasing with time, the forest successional state should not be too downgraded during this delicate process [4]. A special care has to be taken with invasive species. Their introduction risk can be reduced by not planting them, avoiding uncovered with vegetation ground surfaces during the plantation, and cleaning all equipment before bringing them on the location of reforestation. Large mammals, tent-making bats and macaws use large plants such as trees, shrubs and tall grasses for nesting and feeding. Tree hollows, root systems or branches offer nests for those animals [15]. Some bats also use leaves of trees and tall grasses to roost. Many of the animals in the Neotropics are frugivores and depend on fruits for their diet. The others relate at some point on herbivores and frugivores. Thus, forest plants composition defines its hosting potential for each animal species. No consistent information exists about the ACR plant species composition [2]. Its study is part of the objectives of the local management plan [16]. In order to collect baseline information on the actual forest composition in the ACR and integrate it in the reforestation plan, identification of trees and large plants have been conducted. Due to the species richness it harbors, as well as its size, the ACR vegetation hasn’t been studied in its totality, supposing higher diversity than presented in this report.

Introduction

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Methods

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Study site The study site is a 8,400 m² (140x60 m) grid in the middle of the ACR, divided into 21 square plots of 20x20 m (Figure 2). This site is host to the global climate change effects study named the ACER (Association for Canadian Educational Resources) project [17], its protocol being adapted to tropical rainforest. Quadrats’ limits are materialized by straight cuts through the dense understory vegetation. The grid division offers an estimation of the forest and of each tree species density in the study area. This study has been conducted between February and June 2018. Survey protocol According to the ACER protocol, for each plot, all the living trees with a trunk circumference greater than 4 cm at 1.30 m height have been tagged, excluding palm trees (Aceraceae). Trees circumference is measured every six months in order to estimate species growth rate. Tree species have been identified for each tree using various documentation. Plants species identification has also been conducted on the ACR randomly and targeting the recommended plant species for reforestation, in order to record their presence before plantation.

Figure 2 : Map of the study sites focused on the Dr. Archie Carr National Wildlife Refuge biodiversity. Sites are shown for the trees, large mammals, tent-making bats and macaws species composition and activity surveys.

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Plant species

The ACR presents a continuous edge effect, with costal and riverine influence all along its length. A total of 340 broadleaved trees belonging to 36 species with different densities occupies the grid (Table 1). The total density is 405 trees/ha. Another five tree species and eight other large plant species have been identified on the ACR in or out of the ACER grid. Some tree species could not be identified due to missing elements.

Table 1: List of trees, shrubs and tall grasses species identified on the ACR. Trees species include all the trees present in study grid, along with their density (number of trees/ha) within the grid.

Other trees, shrubs and tall grasses were identified in and out of the grid.

Tree species in the ACER grid

Species Density Species Density Species Density

Amphiterna latifolia 4.8 Inga vera 15.5 Simarouba glauca 3.6

Andira inermis 7.1 Laetia procera 2.4 Solanum rovirosanum 1.2

Byrsonima crassifolia 1.2 Lonchocarpus cruentus 1.2 Spondias mombin 11.9

Calophyllum longifolium 3.6 Lonchocarpus heptaphyllus 2.4 Tabernaemontana alba 44.0

Cassipourea elliptica 46.4 Neea laetevirens 45.2 Terminalia catappa 6.0

Cecropia sp. 1.2 Octea tenerea 10.7 Xylosma sp. 13.1

Coussapoa villosa 2.4 Octea veraguensis 16.7 Zanthoxylum sp. 6.0

Coussarea impetiolaris 1.2 Pachira aquatica 9.5 Unknown 1 41.7

Dendropanax arboreus 4.8 Palicourea guianensis 6.0 Unknown 2 1.2

Hampea appendiculata 10.7 Posoqueria latifolia 6.0 Unknown 3 1.2

Hernandia dydimantha 23.8 Psychotria grandis 11.9 Unknown 4 1.2

Hibiscus pernambucensis 22.6 Pterocarpus officinalis 8.3 Unknown 5 1.2

Trees species

Cocos nucifera Pentaclethra macroloba Raphia taedigera

Dipteryx panamensis Pentagonia macrophylla

Shrubs species

Costus woodsonii Manicaria saccifera

Tall grasses species

Calathea crotalifera Heliconia irrasa Heliconia mariae

Calathea inocephala Heliconia latispatha Heliconia pogonantha

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LARGE

MAMMALS

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Costa Rica is home to ten threatened mammal species, protected under the international CITES [18]. One of the threats to land mammals is habitat fragmentation and degradation [18]. As 76% of the terrestrial mammal species have a geographic range smaller than the area of Colombia, local and global conservation initiatives are important for protecting ecosystems diversity and functions [19]. Mammals play a role the dynamic of forested ecosystems through seed dispersal, plants growth stimulation, herbivore control, nutrient cycling, and plant species composition [20]. Some, such as the Neotropical river otter (Lontra longicaudis), are considered as keystone species and ecological indicators for they regulate and depend on other animals to survive and are sensitive to changes [21]. Similar studies conducted in the ACTo found the lowest mammals diversity in areas near human settlements due to disturbances such as domestic dogs presence or hunting [18]. Beyond the anthropogenic threat, Neotropical mammals are also sensitive to natural conditions such as the floristic composition of forests. Mammals depend on their surrounding vegetation, notably for alimentation [18]. Feeding is linked to the plant phenology phases, or phenophases, displaying variations in foliage, flowers and fruits abundance [22]. Even in tropical ecosystems, most tree species have synchronized phases. The presence of trees bearing fruits during fruits scarcity periods is necessary to maintain fruits-eating species all year-long. Hence, reforestation plan should take account of the phenology of existing and forthcoming plant species to ensure a continuous food access for plant-based diet animals. The ACR mammals’ species composition is poorly known. However, species found elsewhere in the ACTo are better-documented. This documentation is partially based on the COTERC surveys. The present study targets terrestrial large mammals (species average weight greater than 1 kg). This section offers a list of mammal species identified in the ACTo and more specifically on the ACR. Based on mammal surveys and tree phenophases studies at the CPBS, this section aims to reveal the mammal species encountered and highlight their association with tree species. Finally, it proposes plant species to conserve or introduce on the ACR to increase its attractiveness for large mammals.

Introduction

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Methods

M ammal species composition Study sites Large mammal surveys have been conducted within the ACTo along four transects (Table 2) of different length through primary and secondary rainforest (Figure 2 & Figure 3). Each transect is divided into 50 m segments to facilitate evidences mapping [23] and prevent pseudo-replication [18]. Data have been collected between the monitoring start dates and June 2018.

Table 2: Large mammal survey transects characteristics

Transect name Abbreviation Length Monitoring start Number of

surveys

Dr. Archie Carr Refuge ACR 800 m February 2018 14

Caño Palma Biological Station

CPBS 1,050 m July 2012 270

Cerro of Tortuguero Cerro 1,250 m July 2012 283

Tortuguero National Park TNP 1,250 m February 2014 201

Survey protocol The monitoring protocol followed Peres [23] and MacKenzie & Royle [13] guidelines for mammal surveys. Weekly walks along each transect have been performed alternating early mornings and afternoons for maximized observation success. Surveys were canceled during extreme climatic events. To reduce inter-observer variation, the same observer or other experienced ones were leading all of the surveys [24]. Recent evidences (<24 hours) were recorded, with species identified being counted only once per 50 m segment. For each, the following data was taken: species name, estimated number of individuals, evidence type, number of the segment and GPS coordinates. Evidences included visual observations, vocalizations, tracks, trails, foraging residuals, nests, scent or feces. Species identity was confirmed using Reid’s [25] field guide. A total of 768 surveys over 308 weeks have been conducted along the four transects. For each mammal species seasonal activity, the average number of individuals encountered per month over all the study transects was calculated, with 72 months of survey.

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Methods

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T rees phenology Study site A tree phenology survey has been conducted in the forest on the property of the CPBS. It is a 100x70 m plot situated in an area adjacent to the CPBS mammal transect (Figure 3). The surveys have been conducted monthly from July 2011 to June 2018, with some exceptions. Surveys were conducted within the first 10 days of the month, ensuring that consecutive surveys were at least 20 days apart. Survey protocol A total of 160 trees have been selected within the plot and labeled. Larger trees have been favored, and palm trees excluded. From those, 136 are still alive at date (06/06/2018). Walks with binoculars were performed in the plot. For each tree, the percentage of thin branches experiencing each phenophase (flowering, fruiting, new leaves or dropped leaves) was recorded at intervals of 25, rounding up to the upper value. Trees could experience several phenophases at the same time.

Figure 3: Large mammals monitoring transects in the ACTo and trees phenology plot at the biological station. The Caño Palma Biological Station (CPBS) and the Tortuguero National Park (TNP) transects are 1,250 m long, the Cerro is 1,050 m long and the Dr. Archie Carr Refuge (ACR) is 800 m long. The tree phenology plot is adjacent to the CPBS

mammals transect.

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Methods

M ammals-trees relationship analysis Mammals species encountered during the surveys conducted at the CPBS were counted only as presence of absence, considering the variability of encounter probability between species [24]. For each tree species, the phenophases scores of all the individuals of the species have been aggregated for each survey. Only the mammals survey strictly less than four days apart from a phenology survey were used. If that condition offered more than one option, the earliest one was kept, offering a total of 55 surveys pairs. To ensure the statistical analysis strength, mammal species with at least five occurrences and tree species phenophases with at least a total score higher than 240% over the monitoring period have been used [26]. Analysis have been conducted with the software R 3.3.2 [27]. Binary logistic regression Considering the mammals presence or absence as a dichotomous outcome responding to predictors being the tree species phenophases, a binary logistic regression has been performed. This test has been run between each pair of mammal species with a tree species phenophase. The test null hypothesis was a non-association between the phenophase score and the probability of a mammal species presence during a survey. A significance level of 0.5 was stated on the Wald test. Co-correspondence analysis A predictive co-correspondence analysis has been conducted. Indeed, the number of tree species phenophases being too similar to the number of observations (71 vs 91), and none of the variables being distributed normally, the data respect its assumptions. This recent method relating on partial

least‐squares regression offers a graphical decomposition of the covariance between predictor variables and response ones [28]. The analysis was performed with the “cocorresp” package [29].

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Mammals species

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ACR composit ion Over the course of the study period, across the four transects, 32 different species or genus of large terrestrial mammals have been recorded (Table 3). A total of 9 species have been recorded on the ACR: brown-throated sloths (Bradypus variegatus), domestic dogs (Canis lupus forma familiaris), mexican hairy dwarf porcupines (Coendou mexicanus), spotted pacas (Cuniculus paca), nine-banded armadillos (Dasypus novemcinctus), opossums (Didelphis sp.), tayras (Eira Barbara), red-brocket deers (Mazama americana) and northern raccoons (Procyon lotor). These mammals usually being inconspicuous, only a brown-throated sloth and northern raccoons have been directly sighted. The nine-banded armadillo dominates the recording representing 66.3% of the evidences encountered on the ACR. The CPBS and the TNP show the highest diversity, with 28 species of large mammals. Relationship with tree species The relationship of mammal species presence with tree species phenology results from both the binary logistic regression and the co-correspondence analysis (Table 4). For the regression, tree species phenophases with a significant positive (odds ratio higher than 1) association with the presence of mammals are listed, along with their respective odd ratio defining the scale of the association. Carapa nicaraguensis, Dendropanax arboreus, Laetia procera and Pentaclethra macroloba trees are associated with the presence of 3 mammals taxa. Alchorneopsis floribunda, Apeiba membranacea, Byrsonima arthropoda, Crudia glaberrima, Cupania sp., Malouetia guatemalensis, Melastomataceae, Myristicaceae, Prioria copaifera and Rubiaceae trees are associated with the presence of 2 mammals species. C. nicaraguensis, M. guatemalensis and P. macroloba are associated mammals presence through all of their phenophases, suggesting a year-long attractiveness.

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Mammals species

According to the co-correspondence analysis results (Figure 4), Alouatta palliata, Canis lupus, Cuniculus paca, Dasyprocta punctata, Didelphis sp., Leopardus wiedii, Mazama americana, Panthera onca, Procyon lotor, Tapirus bairdii and Tayassu pecari are also associated with tree species phenophases (Table 4). Few tree species phenophases predict the set of mammal species. Alchornea costaricensis, Homalium guianense, Malouetia guatemalensis, Pachira aquatica and Pterocarpus officinalis phenophases are predictor to some mammal species presence. H. guianense is predictor to the presence of 6 mammals species during its fruiting phenophase.

Figure 4: Predictive co-correspondence analysis plot of the association of the tree species phenophases (green) and the mammal species presence (blue). The predictors (phenophases) and responses (mammals) plots are superimposed with the

same scale. The axes explain respectively 31.3% and 12.9% of the total variance for the predictors and for the responses. Phenophases are abbreviated by FL (flowers), FR (fruits) and NL (new leaves).

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Discussion ACR composit ion The ACR being a fragmented peninsula, it is not an optimum habitat for wide home range mammals. Thus, mammals such as jaguars (Panthera onca) or ocelots (Leopardus pardalis), which have an average home range of 12.8 to 54.3 km² [30] and 18.9 to 26.1 km² respectively, were seldom expected in this area [31]. Armadillos (Dasypus novemcinctus) have an approximate home range between 0.007 and 0.015 km² and are not territorial, which can explain their abundance on the 0.39 km² ACR [32]. Creating a biological corridor across Tortuguero such as a more forested and darker beach limit could allow wide home range species to expand their distribution from the TNP to the ACR. The actual ACR mammal species composition is mostly of nocturnal species, which limits its attractiveness for day-tours (Table 3). Least Concern is the highest threat status of the species present on the ACR [33]. According to the seasonal activity from the surveys data, the set of species being present in the ACTo as the potential to offer a yearlong presence of mammals. The presence of racoons was expected considering the abundance of crabs in the ACR [34]. Relationship with trees species Out of the list of tree species used by mammals (Table 4), some are more commonly used, and should be favored during the reforestation efforts. Homalium guianense is related to the presence of 6 mammals species. Carapa nicaraguensis, Dendropanax arboreus, Laetia procera, Malouetia guatemalensis and Pentaclethra macroloba are associated with the presence of 3 mammals species. C. nicaraguensis is also used by macaws. D. arboreus and L. procera are already present on the ACR with respectively 4.8 and 2.4 trees/ha. Their expansion through their own seeds should be favored. According to the bibliography, Spondias mombin, already densely present in the ACR (11.9 trees/ha), is used by 8 mammal species, while Astrocaryum standleyanum and Attalea rostrata are used by 4 and also tent-making bats and macaws. Cecropia species are used by 6 mammal species, as well as bats and are already seldom present. C. insignis is the only species naturally distributed on the Caribbean coast not considered as invasive in neighboring countries. Brosimum alicastrum, Dipteryx panamensis and Guazuma ulmifolia are used by 3 species. B. alicastrum and D. panamensis are also used by macaws, D. panamensis being considered endangered. Anacardium excelsum and Byrsonima crassifolia are used by 2 species and also by macaws.

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Large mammals recorded on the Dr. Archie Carr Refuge:

• Bradypus variegatus (Brown-throated sloth) • Canis lupus forma familiaris (Domestic dog) • Coendou mexicanus (Mexican hairy dwarf porcupine) • Cuniculus paca (Spotted paca) • Dasypus novemcinctus (Nine-banded armadillo) • Didelphis sp. (Unidentified opossum) • Eira Barbara (Tayra) • Mazama americana (Red-brocket deer) • Procyon lotor (Northern racoon)

Recommended tree species for reforestation, adapted to coastal rainforests (highly recommended are bolded):

• Astrocaryum standleyanum • Attalea rostrata • Brosimum alicastrum • Carapa nicaraguensis • Cecropia insignis • Dendropanax arboreus • Dipteryx panamensis • Homalium guianense • Laetia procera • Malouetia guatemalensis • Pentaclethra macroloba • Pterocarpus officinalis

S U M M A R Y

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MAMMALS

Table 3: Large mammals species recorded during the surveys along the Tortuguero National Park (TNP), Cerro of Tortuguero (Cerro), Caño Palma Biological Station (CPBS) and Dr. Archie Carr Refuge (ACR) transects. The daily diurnal (D) or nocturnal (N) activity of those species is specified [35]. The seasonal activity is the average

number of evidences encountered each month (1-12), through the 72 months of monitoring, across all the transects.

Mammal species Common name TNP Cerro CPBS ACR Daily

activity Seasonal activity

Alouatta palliata Mantled howler monkey

D

Ateles geoffroyi Central American spider monkey

D

Bradypus variegatus Brown-throated sloth

D/N

Canis lupus Domestic dog

D

Cebus capucinus White-throated capuchin monkey

D

Choloepus hoffmanni Hoffmann’s two-toed sloth

N

Coendou mexicanus Mexican hairy dwarf porcupine

N

Cuniculus paca Spotted paca

N

Cyclopes didactylus Silky anteater

N

Dasyprocta punctata Central American agouti

D

Dasypus novemcinctus Nine-banded armadillo

N

Didelphis marsupialis Common opossum

N

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Mammal species Common name TNP Cerro CPBS ACR Daily

activity Seasonal activity

Didelphis sp. Unidentified opossum

N

Didelphis virginiana Virginia opossum

N

Eira barbara Tayra

D

Galictis vittata Greater grison

D/N

Herpailurus yaguarondi Jaguarundi

D

Leopardus pardalis Ocelot

N

Leopardus wiedii Margay

N

Mazama americana Red-brocket deer

D/N

Mustela frenata Long-tailed weasel

D/N

Myrmecophaga tridactyla Giant anteater

D/N

Nasua narica White-nosed coati

D

Panthera onca Jaguar

D/N

Philander opossum Grey four-eyed opossum

N

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MAMMALS

Mammal species Common name TNP Cerro CPBS ACR Daily

activity Seasonal activity

Potos flavus Kinkajou

N

Procyon lotor Northern racoon

N

Sciurus granatensis Red-tailed squirrel

D

Tamandua mexicana Northern tamandula

D/N

Tapirus bairdii Baird’s tapir

D/N

Tayassu pecari White-lipped peccary

D/N

Tayassu tajacu Collared peccary

D/N

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MAMMALS

Table 4: Large mammals species recorded during the surveys, in particular along the Dr. Archie Carr Refuge (ACR) transect. The relationship with tree species phenophases is only applicable to species recorded along the CPBS transect, for the phenophases surveys area is located beside it. It is based on independent binomial logistic regressions for each pair mammal species-tree species phenophases for 55 common surveys. Only positive significant relationships with P<0.05 * and P<0.01 **

(Wald test) are presented, with their respective odd ratios. Associations are also tested with a predictive co-correspondence analysis plot interpretation (CA). Phenophases are abbreviated by FL (flowers), FR (fruits) and NL (new leaves). According to the literature, the listed tree species are used by mammals, natives, non-

cultivated and adapted to the Atlantic lowlands of Costa Rica [36, 37, 38, 39]. Tree species already on the ACR are marked (*).

Mammal species ACR Relationship with a tree species

phenophase Odd ratios

Tree species used Ref.

Alouatta palliata Homalium guianense FR (CA) Anacardium excelsum Cecropia peltata

Pithecellobium longifolium Spondias mombin (*)

[35]

Ateles geoffroyi Byrsonima arthropoda FR * 1.1

Brosimum alicastrum Cecropia sp. (*)

Pseudolmedia spuria [35]

Bradypus variegatus Cecropia obtusifolia Cordia alliodora

Coussapoa villosa (*) Leucaena leucocephala

Pterocarpus officinalis (*) Spondias mombin (*)

Trophis racemosa

[40]

Canis lupus Domestic species

Cebus capucinus Acacia collinsii Hirtella racemosa Quercus oleoides

Simarouba glauca (*) Spondias mombin (*)

Sterculia apetala

[41, 42]

Choloepus hoffmanni Same as Bradypus variegatus [40]

Coendou mexicanus Brosimum alicastrum Cecropia sp. (*) [35]

Cuniculus paca Alchorneopsis floribunda NL * Apeiba membranacea FR * Carapa nicaraguensis NL *

Crudia glaberrima FL * Cupania sp. NL *

Dendropanax arboreus NL * (*) Homalium guianense FR (CA)

Laetia procera FL * (*) Theobroma simiarum NL *

2.9 1.2 1.2 1.1 3.0 4.0

1.7 2.1

Carapa guianensis Psidium guajava [35]

Cyclopes didactylus Carnivorous [35]

Dasyprocta punctata Alchorneopsis floribunda NL ** Byrsonima arthropoda NL *

Cassipourea elliptica FL ** (*)

4.3 2.0 1.4

Astrocaryum standleyanum Attalea rostrata

Carapa guianensis

Dipteryx panamensis (*) Matisia ochrocalyx

[33, 35]

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MAMMALS

Myristicaceae FR ** Cassipourea elliptica NL ** (*)

Cupania sp. NL ** Dendropanax arboreus NL ** (*)

Hirtella NL * Laetia procera FL * (*)

Laetia procera NL ** (*) Malouetia guatemalensis FR *

Malouetia guatemalensis NL (CA) Melastomataceae FL *

Melastomataceae NL ** Pentaclethra macroloba NL ** (*)

Prioria copaifera NL * Pterocarpus officinalis NL (CA) (*)

Pterocarpus officinalis NL * (*) Rubiaceae NL **

Virola koschnyi NL * Vochysia ferruginea NL **

17.8 1.9 5.5 5.3 1.7 1.6 1.8 1.2

2.1 21.0 1.0 1.4

1.4 5.4 2.2 1.1

Dasypus novemcinctus Mostly carnivorous [35]

Didelphis marsupialis Opportunistic [43]

Didelphis sp. Dendropanax arboreus NL * (*) Heisteria concinna NL ** Laetia procera FL/NL * (*)

Malouetia guatemalensis NL (CA) Melastomataceae NL *

Pentaclethra macroloba NL * (*) Prioria copaifera NL *

Pterocarpus officinalis NL (CA) (*) Rubiaceae FR/NL *

3.4 6.2 1.5

4.4 1.0 1.4

2.9

Opportunistic [43]

Didelphis virginiana Opportunistic [43]

Eira barbara Astrocaryum standleyanum Cecropia sp. (*)

Psidium guajava Spondias mombin (*)

[35]

Galictis vittata Mostly carnivorous [35]

Herpailurus yaguarondi Mostly carnivorous [35]

Leopardus pardalis Carnivorous [35]

Leopardus wiedii Carapa nicaraguensis FR * Homalium guianense FR (CA)

1.7 Mostly carnivorous [35]

22

MAMMALS

Mazama americana Carapa nicaraguensis FL * Homalium guianense FR (CA)

1.2 Acrocomia aculeata Guazuma ulmifolia

Spondias mombin (*) [44]

Mustela frenata Carnivorous [35]

Myrmecophaga tridactyla Carnivorous [35]

Nasua narica Byrsonima crassifolia (*) Guazuma ulmifolia [35]

Panthera onca Alchornea costaricensis FL (CA) Homalium guianense FR (CA) Malouetia guatemalensis FL Pachira aquatica FL (CA) (*)

1.1

Carnivorous [35]

Panthera onca Alchornea costaricensis FL (CA) Homalium guianense FR (CA) Malouetia guatemalensis FL Pachira aquatica FL (CA) (*)

1.1

Carnivorous [35]

Philander opossum Mostly carnivorous [35]

Potos flavus Astrocaryum standleyanum Attalea rostrata

Brosimum alicastrum Cecropia sp. (*)

Dipteryx panamensis (*) Quararibea parvifolia Spondias mombin (*)

[35]

Procyon lotor Alchornea costaricensis FL (CA) Apeiba membranacea FR * Apeiba membranacea NL *

1.3 1.1

Mostly carnivorous [35]

Sciurus granatensis Attalea rostrata Dipteryx panamensis (*)

Grias cauliflora [33]

Tamandua mexicana Attalea rostrata [33]

Tapirus bairdii Crudia glaberrima NL ** Pachira aquatica FL (CA) (*)

Myristicaceae NL *

2.6

1.8

Dendropanax arboreus (*) [45]

Tayassu pecari Homalium guianense FR (CA) Pentaclethra macroloba FL * (*)

Pentaclethra macroloba FL/FR * (*)

1.0 1.1

Anacardium excelsum Astrocaryum standleyanum

Licania operculipetala

Raphia taedigera (*) Spondias mombin (*)

[35]

Tayassu tajacu Byrsonima crassifolia (*) Guazuma ulmifolia

Spondias mombin (*) [35]

23

TENT-MAKING

BATS

24

With more than 1,300 species described, the Chiroptera order represents more than 25% of the mammal species diversity [46]. Out of the 41 bats species reported around the CPBS [47], most of them roost in tree hollows (41%), caves (39%), buildings (32%), modified leaves (22%) and tree trunks (10%) [48, 33, 49, 50, 51, 52, 53]. At least 17 species reported are hollow-trees-dependent. Protecting old patches of forest reduces hollow trees loss, contributing to bats conservation. At least 17 bat species modify leaves into tents-like roosts in the Neotropics. They belong to the Phyllostomidae family, and most of them to the Stenodermatinae subfamily [54]. Chewed ribs in specific locations eventually make the leaves collapse, following recurrent architectures. Of these tent architectures, the apical one, a simple cut at the end of the main rib making the tip point downwards, is the most common, with four bat species creating it on at least 20 plant species. Some bat species show a large range of architecture types, such as Uroderma bilobatum with seven types, while others such as Ectophylla alba are restricted to one specific type. A particular architecture type of tent seems to reflect more the plant morphology than a species-specific behavior [55]. Making tents out of leaves allows bats to choose their roost location, facilitating food foraging and protecting them from rain, predators, parasites and other males [55, 56]. Indeed, they are occupied by single or small clusters of bats, mostly only females or a male with a harem, which occupy different tents depending on their activity [55]. The females’ fidelity depends on the male’s roost quality [57]. Hence, providing adapted foliage by selecting plant species permits optimized polygyny. Ecotourism initiatives based on bats can be a viable activity if the disturbance level is kept low, and the population is large enough and well-established [58]. Frequent disturbance can lead to the population displacement. A study conducted by the COTERC (unpublished) around the Cerro of Tortuguero before and after the construction of a cement path revealed lower presence of tents and observed bats after the construction. Also, tents resulted less used for roosts after the construction, reducing their sighting probability. However, recent surveys showed a recovery of the bats use of the area. It is important to note that very little touristic activity happened since the construction. This section presents the tent-making bats recorded in various sites in the ACTo and proposes plant species to introduce in the ACR in order to improve its hosting potential.

B

AT

S

Introduction

25

Methods

Study site Tent-making bats have been monitored along three transects presented in the Table 5 and Figure 2 & Figure 5. Each transect is divided into 100 m long plots with a 10 m buffer zone on both side of the transect. Tents still useable as shelter were tagged and monitored. The ACR transect is the same as the mammals transect. Data have been collected between the monitoring start dates and June 2018.

Table 5: Tent-making bats surveys transects characteristics

Transect name Abbreviation Length Monitoring

start Number of

surveys

Dr. Archie Carr Refuge ACR 800 m March 2018 14

Caño Palma Biological Station CPBS 1,000 m March 2015 29

Cerro of Tortuguero Cerro 700 m March 2015 97

Survey protocol Weekly one-way walks have been performed. New tents were marked and monitored from the encounter date until they were deemed unusable. The tent architecture, bats number and species if occupied and activity evidences (feces, fruit pulp or seeds under the tents) were recorded. Species and tent-architecture was confirmed with Rodríguez-Herrera et al. [54].

BA

TS

Figure 5: Tent-making bats monitoring transects in the ACTo. The Caño Palma Biological Station (CPBS) transect is 1,000 m long, the Cerro is 700 m long, and the Dr. Archie Carr Refuge (ACR) is 800 m long.

26

Bat species

A total of nine tent-making bats species have been encountered in the ACTo (Table 6) [47]. During the tent-making bats surveys only three species have been found: Artibeus watsoni, Ectophylla alba and Uroderma bilobatum. On the ACR, only a cluster of three adults and two juveniles of A. watsoni have been identified, using three bifid tents of Manicaria saccifera, a boat/apical tent of Heliconia latispatha and an inverted boat of Heliconia pogonantha. In the vegetation survey grid (Figure 2), 2 other tents, a bifid of M. saccifera and an inverted boat of Calathea sp., have been encountered, occupied by unidentified bat species, tents dead at date (06/06/2018). Further south, two bifid tents of M. saccifera have been encountered. E. alba has a Near Threatened status according to the IUCN Red List, the eight other species being Least Concerned [33]. Plant species normally used by those species are presented in Table 6 [54, 33, 59, 57]. Only plants present on the Caribbean lowlands (down to 0 m elevation) of Costa Rica or Nicaragua are presented [37, 36].

BA

TS

27

Discussion

BA

TS

Increasing the hosting potential of the Dr. Archie Carr Refuge Some plants used as tents by these bats are already present in the ACR (Table 1). Indeed, trees such as Cocos nucifera are used by A. watsoni. Tall grasses such as Calathea inocephala, C. crotalifera, Heliconia latispatha and H. pogonantha are used by A. watsoni and E. alba and should be conserved. If host species are already present, the actual understory vegetation, mostly of Heliconia and Calathea, is too dense for bats to use them [60]. It is due to the scarcity of trees offering large amounts of light to the understory vegetation. Hence, reforestation efforts should, as the tree cover would increase, reduce the understory density and improve its suitability to host tent-making bats. In order to enhance the attractiveness of the ACR, considering the coastal conditions, some of the species presented in Table 6 and absent on the ACR should be planted. The most recommended are Ardisia brenesii, Astrocaryum alatum, Cryosophila grayumii, C. guagara, Heliconia imbricate and H. sarapiquensis. A. brenesii and H. sarapiquensis are endemic species, respectively to the Atlantic lowlands of Costa Rica and Nicaragua, and to the lowlands between Sarapiquí, San Carlos and Tortuguero [36, 37]. C. grayumii is a critically endangered species, A. alatum and C. guagara are considered near threatened [33]. H. imbricata is used by four tent-making bats species. Other useful plant species are Heliconia latispatha and Pentagonia macrophylla, for they are used by three bats species. P. macrophylla is a critically endangered species. It’s already scarcely present on the ACR but should be planted as well. Some species are used by two bats species, such as Attalea rostrata, Cocos nucifera, Heliconia pogonantha, Manicaria saccifera, Philodendron fragrantissimum, P. mediacostatum, Sabal mauritiiformis and Rhodospatha wendlandii. A. rostrata is also used by mammal species and macaws. Individuals of C. nucifera, H. latispatha, H. pogonantha and M. saccifera are already largely present on the ACR, their plantation is not necessary.

Bats ecotourism Wildlife-oriented ecotourism requires predictable occurrences of animals on a reduced area [58]. The actual know tent-making bats population in the ACR is too scarce to represent a sustainable attraction. None of the tents being present along the path on the ocean-side of the peninsula, their sighing would involve the widening of the surveys transect path, leading to the potential destruction/desertion of the tents.

28

BA

TS

Tent-making bats on the Dr. Archie Carr Refuge:

• 3 adults and 2 juveniles Artibeus watsoni • 3 bifid tents of Manicaria saccifera, 1 boat/apical of Heliconia latispatha and 1 inverted-

boat of H. pogonantha on the survey transect • 2 tents of M. saccifera and Calathea sp. within the trees grid • 2 tents of M. saccifera south of the bats transect

Recommended plant species to introduce, adapted to coastal rainforests (highly recommended are bolded) and bats species using them:

• Ardisia brenesii U. bilobatum • Astrocaryum alatum A. watsoni • Attalea rostrata A. jamaicensis, U. bilobatum • Cryosophila grayumii A. watsoni • Cryosophila guagara A. watsoni • Heliconia imbricata A. phaeotis, A. watsoni, E. alba, U. bilobatum • Heliconia sarapiquensis E. alba • Pentagonia macrophylla A. jamaicensis, A. watsoni, E. alba • Philodendron fragrantissimum A. jamaicensis, U. bilobatum • Philodendron mediacostatum A. phaeotis, E. alba • Rhodospatha wendlandii A. watsoni, E. alba • Sabal mauritiiformis A. jamaicensis, U. bilobatum

S U M M A R Y

29

Table 6: Tent-making bats species encountered in the ACTo, and more specifically along the CPBS, Cerro and ACR transects. Tent architecture of the monitored tents are

based on descriptions by Rodríguez-Herrera et al. (2007). Plant species used by the bats, distributed on the Caribbean lowlands, according to literature [59, 33, 54, 61, 57, 37, 36]. Plants species already in the ACR (*). Highly recommended plant species are bolded.

Bat species CPBS Cerro ACR Tent

architecture Roosting plant species

Artibeus lituratus -

Artibeus jamaicensis

Attalea rostrata Pentagonia macrophylla (*)

Philodendron fragrantissimum Sabal mauritiiformis

Dermanura phaeotis Heliconia imbricata Philodendron mediacostatum

Dermanura tolteca -

Artibeus watsoni

Bifid Apical

Boat/Apical Boat

Asplundia alata Asterogyne martiana Astrocaryum alatum

A. standleyanum Bactris hondurensis

Calathea crotalifera (*) C. inocephala (*)

C. lutea Carludovica drudei

Cocos nucifera (*) Cryosophila grayumii

C. guagara Cyclanthus bipartitus Geonoma congesta Heliconia imbricata

H. latispatha (*) H. pogonantha (*)

Manicaria saccifera (*)

Monstera adansonii Myriocarpa longipes

Pentagonia macrophylla (*) Philodendron grandipes

P. pterotum P. sagittifolium

Rhodospatha wendlandii Spathiphyllum wendlandii

Ectophylla alba

Inverted boat

Calathea sp. (*) Heliconia imbricata

H. latispatha (*)

H. pogonantha (*) H. sarapiquensis

Ischnosiphon inflatus

Pentagonia macrophylla (*) Philodendron mediacostatum

Rhodospatha wendlandii

Platyrrhinus helleri -

Uroderma bilobatum

Conical

Ardisia brenesii Attalea rostrata Cecropia sp. (*)

Cocos nucifera (*) Heliconia imbricata

H. latispatha (*)

Manicaria saccifera (*) Philodendron fragrantissium

Sabal mauritiiformis

Vampyressa nymphaea Cecropia insignis

BATS

30

MACAWS

© Berryman A.

31

MA

CA

WS

The Psittacidae family contains a higher number of threatened species than the other bird families [62]. In Costa Rica, two species of macaws coexist: the great green macaw (Ara ambiguus) and the scarlet macaw (Ara macao). Macaws used to be seldom

seen in the Tortuguero until a dramatic increase of their presence during the last five years (pers. comm.) [63] They are focal elements of the management plan proposal [2]. Macaws characteristics are presented in the Table 7. The aim of this study is to present the ecological requirements for those species, understand their use of the ACR, predict their sighting potential from the ACR and edit a list of native, local and costal trees species attracting macaws [64, 37, 36, 39].

Table 7: Scarlet and Great Green Macaw populations characteristics [65, 66, 67, 68, 69, 70]

SCARLET MACAW Ara macao

GREAT GREEN MACAW Ara ambiguus

Distribution

From Peru to Mexico, until the Brazilian Atlantic coast in its easternmost distribution.

From Ecuador to Honduras.

IUCN Status

Least Concern Endangered

Species global population size

< 50,000 Decreasing

< 3,700 Decreasing

Local population

High genetic diversity suggesting a good inter-populations connectivity, explained by high population sizes and dispersion rates.

From southeastern Nicaragua to northeastern Costa Rica, about 250 individuals.

Tortuguero area at least 60 individuals.

© Kratochvil P. © Mascota y mas

Introduction

32

MA

CA

WS

© A

rias

M.

Habitat & Ecology

Both the macaw species nest in primary or secondary forests, in wet lowlands or mangrove swamps. They can also be encountered in open areas when flying or feeding. They mostly feed on fruits and seeds, and so are large-distance seed dispersers, a vital role in tropical forests [66, 67, 71]. Great green macaws In northern Costa Rica, the breeding range of this species shrank by 90% over the last decades and is now limited to about 1,120 km² [65]. A. ambiguus are highly dependant on Dipteryx panamensis, for it is their principal nesting and feeding tree. They nest mostly in its tree hollows and feed mostly on its fruits. Past logging on D. panamensis caused the population collapse. Their optimum density for macaws is between 0.5 and 2 trees/ha [59]. They nest in the same old-tree cavities year after year. They also have been seen nesting in Carapa nicaraguensis, Cavanillesia plantanifolia, Goethalsia meiantha and Vochysia ferruginea [66, 72]. They are known to feed on at least 36 plant species [72]. These include Cordia megalantha, Iriartea deltoidea, Laetia procera, Pentaclethera macroloba or Vochysia ferruginea. They can disperse over a large range for finding food, from the Atlantic forests to the volcanic ranges of Costa Rica or to the drier forests of Nicaragua. Seasonally, they migrate to higher elevations looking for Sacoglottis trichogyna trees, mostly. Along the ACTo beaches, Terminalia catappa is a common beach tree species. It is locally known to be the most attractive species for both macaw species (pers. comm.). Their seasonal activity in the lowlands presented by Chun [65] is summarized by months as follows:

J F M A M J J A S O N D

Legend: Nesting (eggs) Nesting + Nestlings Migration

Scarlet Macaws Ara macao have a broad nesting niche. They have been found nesting mostly in Ceiba pentandra, Caryocar costaricense and Schizolobium parahybum, but also in Astronium graveolens, Hura crepitans, Rhizophora mangle and Terminalia oblonga [71, 73]. Nesting trees are at least 8 m high. Their diet is partly composed of Anacardium excelsum, Attalea rostrata, Brosimum alicastrum, Cordia collococca, C. pentandra, Enterlobium cyclocarpum, Ficus insipida, H. crepitans and Schizolobium parahybum [74]. The exotic species trees Terminalia catappa are also popular feeding trees for scarlet macaws (pers. comm.) [75, 74]. They were found to have a diet consisting of 76% of non-native and cultivated species [76]. Scarlet macaws are released from breeding centers in central America. Their exotic diet could be due to a lack of native species experienced in these centers. A study conducted on the Pacific coast of Costa Rica reveals that approximately 49% of the T. catappa seeds were eaten by scarlet macaws, suggesting its potential as an exotic species for supporting native ones [77]. Being very present all along the ACR and not native, reforestation efforts should not include the plantation of T. catappa.

33

Methods

MA

CA

WS

Study site The observation site was situated on the east shore of San Francisco de Tortuguero (Figure 2). It faced the Tortuguero river, and the ACR. From this spot, the northernmost 1.5 km west shore of the refuge could be observed. This survey lasted from September 2017 to June 2018, with a total of 33 days of survey. Survey protocol The survey has been conducted weekly from 5:30 to 9:30 and from 13:30 to 17:30 on the same day. Hence, surveys cover the optimum period (6:00 to 14:00) for their observation according to Monge et al. [68] and previous COTERC researches (unpublished). Point-count surveys were used to estimate local abundance. Both audio and visual evidences were recorded, with the observation time. An individual or a group of macaws was considered as a group. For visual observation, the species, number of individuals and behavior were recorded. Behavior could be flying, feeding, resting, allofeeding, or allopreening. If flying, the cardinal or intercardinal direction from where the group came from and to where it went was noted, centered on the observation site. If resting, the tree species was identified if possible. If a group was to be heard or seen over a long time, their observation would be split in ten minutes segments, giving an estimation of the length of their stay. For audio evidences and ongoing visual observations, the cardinal direction from the observation site was noted.

Data analysis Records from flying groups were all used. Records from only heard macaws were used only if their direction of origin was comprised between the north and the south-east, for it suggests macaws are present on the ACR. Data representation were conducted using the software R (version 3.3.2). For each group resting on the ACR, the length of their stay was extrapolated from the time of their apparition to their last time of observation. The total number of individuals on the study site for each 10 minutes interval includes all observations happening during the interval as well as groups recorded before and after the interval, suggesting their presence all along.

34

Macaws activity

Seasonal activity The northernmost 1.5 km of the ACR peninsula is used by both macaw species. Great green macaws (A. ambiguus) dominate the observations, representing 88.2% of the groups of macaws seen, with 1,076 individuals over all the surveys. The Costa Rican population being estimated to 250 individuals, we can suppose that the same individuals regularly visit the ACR area. The higher numbers of macaws were counted in September, October, December, January, May and June (Figure 6)

Behavior The average group size of only-flying-by macaws is 3.7 (se = 0.3). Fortunately, the northernmost part of the ACR is also a resting site for macaws, with 51.1% of the recorded groups landing on its trees. They have an average size of 4.2 (se = 0.3). They spend an average time on the ACR of 42.0 minutes (se = 3.7). Arriving at the study site area, macaws main origins are south-east (21.0% of the groups), from the southern part of the ACR and west (17.3%), being from over San Francisco de Tortuguero. Their main directions when leaving the area are north-west (21.1%), toward the Cerro and west (20.6%).

Figure 6 : Total number of macaws observed and heard during each survey. Barplots are divided depending on the number of great green macaws (green), scarlet macaws (red), unidentified macaws (grey) and heard macaws (blue).

Num

ber

of m

acaw

s

Date of survey

35

MA

CA

WS

Macaws activity

Macaws landed mostly on the ocean side, with few landings on the river shore of the peninsula. Yet, some landing trees have been identified as being Pterocarpus officinalis and Terminalia catappa, with resting and seldom feeding behavior observed. No nests or nesting activity has been sighted from the observation site. Their actual behavior on the ACR could be missed due to the large distance between the observation spot and the peninsula Daily activity There are noticeable variations in the local activity for the great green macaws (Figure 7). Presence peaks occurred between 6:30 and 7:30 in the morning, and 13:30 and 15:50 in the afternoon. Thus, birdwatching tours during those hours are more likely to offer macaws sighting. Observed scarlet macaws and heard macaws were too seldom recorded to reveal noticeable trends.

Figure 7 : Diurnal macaws activity in the northernmost part of the Dr. Archie Carr Refuge. Lines represent the average number of observed great green macaws (green), scarlet macaws (red) or heard (blue) during survey hours (5:30-9:30 and

13:30-17:30). Vertical lines (grey) are the standard error of the mean over all surveys.

Ave

rage

num

ber

of m

acaw

s

Hours

36

Discussion

MA

CA

WS

Seasonal activity The seasonal activity of macaws around the ACR (Figure 6) is coherent with their ecology. The surveys being conducted for 9 months, from September to June 2018, they include both the critical periods of migration and nestlings care for the great green macaws [65]. Those periods are less likely to offer observations for the adults are either feeding in higher elevation areas or taking care of their nestling rather than socializing in the lowlands. As a matter of fact, higher numbers of macaws were encountered in September, October, December, January, May and June. These results suggest that either residual groups stay in the area during migration, or that the migration itself is not consistent within the population. They also emphasize the social and feeding activities happening before nestlings hatching in February and after in May. As the survey is still being conducted, year-long and multi-year results should give a more accurate estimation of the seasonal activity around the ACR. Behavior No nesting activity has been observed on the ACR. This could be explained by the lack of old trees bearing high and deep enough cavities for macaws on the ACR [78]. However, flying and resting have been recorded around and on the Refuge. These results suggest that the ACR hosts social interactions, such as mating, of feeding activity. Artificial macaws nests have been experimented in Costa Rica, with successful outcomes [71]. They consist in wooden barrels made out of local tree species or PVC pipes with entrance holes large enough for macaws. Successful outcome appeared in areas with higher macaws density, which could fit with the ACR macaws frequentation. They cross conservation and tourism benefits and could temporary fill the lack of tree hollows in the ACR.

37

MA

CA

WS

Around and on the northernmost part of the Dr. Archie Carr Refuge:

• 88.2% of observed macaws were Great Green Macaws • 6:30-7:30 and 13:30-15:50: presence peaks of macaws • September, October, December, January, May and June: higher number of macaws • Flying over/along, resting and feeding behaviors • 42.0 minutes: average time spent resting in the Refuge

Recommended tree species for reforestation, adapted to coastal rainforests (highly recommended are bolded):

• Anacardium excelsum • Attalea rostrata • Carapa nicaraguensis • Caryocar costaricense • Ceiba pentandra • Cordia megalantha • Dipteryx panamensis • Iriartea deltoidea • Laetia procera, • Pentaclethera macroloba • Rhizophora mangle • Sacoglottis trichogyna • Terminalia oblonga • Vochysia ferruginea

S U M M A R Y

38

Conclusion

The current study compiles 996 surveys over the whole period, distributed between July 2011 and June 2018 in different sites of the ACTo. On the Dr. Archie Carr National Wildlife Refuge (ACR), a total of 49 plants have been identified. From the focal taxa, nine large mammals, one tent-making bat and two macaw species have been recorded. On the ACR, Cassipourea elliptica, Neea laetevirens and Tabernaemontana alba are the most abundant tree species with respectively 46.4, 45.2 and 44.0 trees/ha within the 140x60 m study grid. The understory vegetation is very dense but dominated by few species, mostly of Heliconia and Calathea species. Reforestation is expected to reduce its density by limiting the amount of light reaching it. The nine-banded armadillo (Dasypus novemcinctus) is the most common mammal, representing 66.3% of the encounters. Its abundance is coherent for this species home range is small, and predators rare on the ACR. Considering the peninsula isolation and dimensions, the rarity of large home range terrestrial species was expected. According to relationship analysis between mammal species presence and trees phenophases, phenophases of trees such as Dendropanax arboreus, Homalium guianense, or Laetia procera are associated with the presence of various mammals. One cluster of five Artibeus watsoni has been detected, using five different tents. They are the only cluster encountered during the surveys on the ACR. Their presence could be negatively affected by increased human disturbances along the bats transect. The floristic composition of the ACR could sustain more tent-making bat species, but the current understory density seems too high to be an optimum habitat. The great green macaws form 88.2% of the macaws observations. The ACR is an important area for the ACR beach side is a meeting area and an ecological corridor for macaws daily migration. The ACR harbors less biodiversity than its surrounding areas, but various ecological functions are already represented, such as nitrogen fixation by Lonchocarpus heptaphyllus, seed dispersion by macaws and bats and underground invertebrates predation by armadillos. It forms part of the complex ecosystem of the region and its estuarine localization makes it important for the conservation of the watershed quality.

39

Conclusion

This ACR biodiversity assessment describes its biological composition, but remains incomplete, being limited to some taxa and conducted for less than a year. Further investigations are being performed to reveal its diversity and the dynamic of its populations. As presented in the management plan proposal, crustaceous, amphibians and reptiles are still to be investigated. In order to improve the attractiveness of the ACR for the focal taxa and enhance the biodiversity for all its ecosystem, a list of recommended plant species, native and distributed on the Caribbean coast of Costa Rica, to introduce or favor is presented at the end of each section, and in Table 8. Plants such as Anacardium excelsum, Attalea rostrata, Carapa nicaraguensis and Dipteryx panamensis attract more than one taxa and should be highly favored. For ensuring the sustainability and resistance of the forest, new trees of the same species should originate from different trees to provide genetic diversity. An in vivo reforestation plan experimented in a degraded site in Brazil used five native early-successional forest species directly seeded [79]. Even with a low survival rate of the planted species, planted plots showed greater rates of later colonization by species originating from surrounding remnant forests. To improve survival success, this study gives some recommendations. Old seeds should be avoided. Seeds should be collected in similar climatic and edaphic conditions as to the reforestation plot. Seeds should be planted during an abundant rainfall period. Weeding in the vicinity of the new seedlings should be performed. It also highlights the need of preliminary tests of direct seeding under field conditions for each species. Considering all this information, the launch of a reforestation plan for the ACR is now reachable. It could include a collaboration between COTERC and ASVO to test in the trees nursery and in vivo the germination success and optimal growing conditions before applying the plan to the whole ACR. The ACER grid could be used as the in vivo plot, as its composition and density are known. It’s a long-term based project, trees having to be mature to attract frugivores. The long-term benefits of the protection and restoration of the ACR are the improvement of the peninsula’s biodiversity, leading to more resistant ecological functions and services such as carbon fixation, protection against the erosion, and enhanced touristic attractiveness. Reforestation could also take place in the town of Tortuguero. Connecting the Tortuguero National Park and the ACR by restoring a forested and dark ecological corridor along the beach could permit a recolonization of the peninsula by the wildlife. Beyond reforestation, the conservation of existing large trees of the ACR would increase its hosting potential through old trees hollows and emergent trees development. Finally, the participation of local communities to the restoration effort will be necessary to ensure the durability of this project and make the ACR great again.

40

Complete list of recommended

plant species

Table 8: List of recommended plant species to introduce to the ACR for improving the habitat quality for the focal taxa large mammals, tent-making bats and macaws. Highly recommended are bolded, for they host various species or are

threatened. The threat status is based on the IUCN Red List [33]. Abbreviations stand for Critically Endangered (CE), Least Concern (LC), Near Threatened (NT) and Vulnerable (VU). The attracted bats (BA), large mammals (LM) and macaws (MA) taxa are based from the species presented in this report, but do not include all the wildlife which would benefit from the

introduction of those plant species. Tree species already on the ACR are marked (*).

Species Status Attracted taxa

Species Status Attracted taxa

Trees

Anacardium excelsum - MA Dipteryx panamensis (*) - LM, BA

Ardisia brenesii - BA Homalium guianense - LM

Astrocaryum alatum NT BA Iriartea deltoidea LC MA

Astrocaryum standleyanum - BA, LM Laetia procera (*) - LM, MA

Attalea rostrata - BA, LM, MA Malouetia guatemalensis - LM

Brosimum alicastrum LC LM, MA Pentaclethra macroloba (*) - LM, MA

Carapa nicaraguensis - LM, MA Pentagonia macrophylla (*) CE BA

Caryocar costaricense VU MA Pterocarpus officinalis (*) - LM, MA

Cecropia insignis - BA, LM Rhizophora mangle LC MA

Ceiba pentandra LC MA Sabal mauritiiformis NT BA

Cordia megalantha - MA Sacoglottis trichogyna - MA

Cryosophila grayumii CE BA Terminalia oblonga - MA

Cryosophila guagara NT BA Vochysia ferruginea - MA

Dendropanax arboreus (*) - LM

Tall grasses

Heliconia imbricata - BA Heliconia sarapiquensis - BA

Epiphytes

Philodendron mediacostatum - BA Rhodospatha wendlandii - BA

Philodendron fragrantissimum - BA

41

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ANNEXES

46

Tree phenology monitoring program at the CPBS, species l ist Alchornea costaricensis Alchorneopsis floribunda Apeiba membranacea Byrsonima arthropoda Carapa nicaraguensis Cassipourea elliptica Crudia glaberrima Cupania sp. Dendropanax arboreus Ficus sp. Heisteria concinna Hirtella sp.

Homalium guianense Inga cocleensis Inga sp. Laetia procera Lauraceae Malouetia guatemalensis Melastomataceae Myrisinaceae Myristicaceae Pachira aquatica Pentaclethra macroloba

Prioria copaifera Pterocarpus officinalis Rubiaceae Sterculia recordiana Theobroma simiarum Virola koschnyi Vismia macrophylla Vitex kuylenii Vochysia ferruginea Xylopia sericophylla Zygia latifolia

I l lustrations Front page: the ACR from the Cerro de Tortuguero platform, facing south Contents page: the ACR forest top from the inside Page 3: the ACR from the Cerro de Tortuguero platform, facing south Page 4: the Heliconia and Calathea understory of the ACR Page 5: the Heliconia and Calathea understory of the ACR Page 6: a tagged tree in the ACER plot of the ACR Page 7: beginning of the mammals transect at the ACR Page 8: a spider monkey (Ateles geoffroyi) at the CPBS Page 9: an unidentified sloth from the Cerro de Tortuguero platform Page 10-12: an Agouti (Dasyprocta punctata) track at the ACR. Page 13-14: a Tayra (Eira barbara) caught with a camera trap around the CPBS Page 15: a red-brocket deer (Mazama americana) caught with a camera trap around the CPBS Page 23: a cluster of 3 Artibeus watsoni in a bifid tent of Manicaria saccifera on the ACR Page 24: a bifid tent of Manicaria saccifera on the ACR Page 25: an inverted boat tent of Heliconia sp. on the Cerro bats transect Page 26: a cluster of Ectophylla alba in an inverted boat tent of Heliconia sp. on the Cerro transect Page 27: bifid tents of Manicaria saccifera on the ACR Page 30, 32 & 34-36: Great Green Macaws (Ara ambiguus) randomly observed Page 33: macaws observation spot of the ACR in San Francisco de Tortuguero Page 38-39: reptile observed at the ACR on a Calathea sp. leave Page 40: a patch of Heliconia pogonantha in the ACR Page 41: a hummingbird resting in the ACR Page 45: beginning of the mammals transect at the ACR

47