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COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice Cuenat Project Manager (PM) Anton Antonov Assistant Research Officer (ARO) Becky Gordon Assistant Research Officer (ARO) India Ashfield Assistant Research Officer (ARO) Nadia Jeffrey Assistant Research Officer (ARO)

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Page 1: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

COSTA RICA RESEARCH PROGRAMME (CBP)

CBP Phase 201 Science ReportJanuary 2020 - March 2020

Matthew Smart Principal Investigator (PI)Patrice Cuenat Project Manager (PM)Anton Antonov Assistant Research Officer (ARO)Becky Gordon Assistant Research Officer (ARO)India Ashfield Assistant Research Officer (ARO)Nadia Jeffrey Assistant Research Officer (ARO)

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Contents

1 Staff Members 3

2 Foreword 3

3 Introduction 53.1 Natural History of Costa Rica and its Wildlife Conservation . . . . . . . . . . . . . . . . . 53.2 Osa Peninsula . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63.3 Aims and Objectives of Frontier CBP . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

4 Training 94.1 Briefing Sessions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94.2 Science Lectures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94.3 Field Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

5 Research Work Programme 115.1 Survey Area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

6 Projects 146.1 Assessing the degree of disturbance and secondary succession on forest habitats in Carate,

Osa Peninsula . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146.1.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146.1.2 Aims of Study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156.1.3 Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156.1.4 Results and Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176.1.5 Conclusions and Implications for Future Analysis . . . . . . . . . . . . . . . . . . . 206.1.6 Limitations and Future Directions . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

6.2 The Occurrence and Forest Type Preference of Four New World Primates . . . . . . . . . 226.2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226.2.2 Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226.2.3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 246.2.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27

6.3 Investigating the Habitat Preference of the Riverside Wren (Thryothorus semibadius), anEndemic and Data Deficient Bird Species . . . . . . . . . . . . . . . . . . . . . . . . . . . 316.3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 316.3.2 Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 326.3.3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 336.3.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 346.3.5 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35

6.4 Variations in Amphibian and Reptile Abundance and Density due to Changes in Seasonand Habitat Age and the Utilization of Microhabitat by Anole Lizards. . . . . . . . . . . . 366.4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 366.4.2 Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 376.4.3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 396.4.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 446.4.5 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46

6.5 Assessing and Improving Sea Turtle Predation and Hatching Success Rates; A Study fromPlaya Carate, Costa Rica . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 486.5.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 486.5.2 Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 496.5.3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 566.5.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 626.5.5 Future research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64

6.6 Assessment of the Social Dynamics of the ACOSA Scarlet Macaw (Ara macao) Population,Situated in Carate, Costa Rica. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 666.6.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 666.6.2 Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67

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6.6.3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 686.6.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 766.6.5 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78

6.7 An Assessment of the Mammal Diversity and Distribution in Carate, Costa Rica. . . . . . 796.7.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 796.7.2 Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80

6.8 An Asessment of the Diversity and Abundance of Birds of Prey in Carate, Osa Peninsula,Costa Rica. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 816.8.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 816.8.2 Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81

6.9 Diversity and Abundance of Birds of Prey in Carate, Osa Peninsula, Costa Rica. . . . . . 836.9.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 836.9.2 Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 836.9.3 Project to Date . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84

7 References 85

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1 Staff Members

Patrice Cuenat (PC) Project Manager (PM)Matthew Smart (MS) Principal Investigator (PI)Anton Antonov (AA) Assistant Research Officer (ARO)Becky Gordon (BG) Assistant Research Officer (ARO)India Ashfield (IA) Assistant Research Officer (ARO)Nadia Jeffrey (NJ) Assistant Research Officer (ARO)Mateo Winterscheidt (MW) Assistant Research Officer (ARO)Tom Cawdron (TC) Assistant Research Officer (ARO)Tristan White (TW) Assistant Research Officer (ARO)

2 Foreword

It is with great pleasure that I present this document, which contains the results of the scientific studiesundertaken by the Frontier Costa Rica Forest (CBP) project. This report contains all the data collectionmethodologies, results, analyses along with the conclusions of the avian, habitat, herpetological, mam-malian, primate and sea turtle studies, as well as background information on the biodiversity of the OsaPeninsula and future development ideas for the project.

Like many tropical countries, Costa Rica lost a significant portion of its forests to agriculture in the 20thcentury, peaking in the 1980s at 48% of the national territory (Stan & Sanchez, 2017; Arroyo-Mora, et al.,2005). With an increase in global demand for meat in the late 1950s, Costa Rica’s demand to export beefcame primarily from the United States, supported by loans from the World Bank and other internationaldevelopment organizations (Parsons, 1983). As a result, large areas of forest were converted into farm-land and pasture, leading to the destruction and fragmentation of many forest habitats (Arroyo-Moraet al., 2005; Solorzano et al., 1991). Habitat fragmentation causes isolated areas to become overcrowdedinhibiting animals from moving to breed with other populations. This led to inbreeding, which decreasedthe heterozygosity and therefore the overall genetic fitness of the population (Keyghobadi, 2007).

Costa Rica since has been considered a global frontrunner with regards to conservation and the protec-tion of natural spaces in developing countries. Measures to aid the restoration and conservation of foresthabitats, such as the implementation of payments for environmental services (PES) and a governmentban on deforestation (Fagan et al., 2016). Despite such conservation efforts, centuries of evolution anddiversification have created the complex ecosystems that can be seen in pockets however, deforestationhas inevitably left scars and impacts which can have a wide range of effects on ecosystem services. Al-though studies have suggested considerable biodiversity can be supported it is still unknown whetherregenerating (i.e. secondary) forests are able to effectively sustain wildlife populations as well as forestsuntouched by human disturbance (i.e. primary forests) (Dent & Wright, 2009; Fagan et al., 2016; Klimeset al., 2012; Mackey et al., 2015; Ribeiro et al., 2009). Furthermore, ecosystems in regenerating forestscontinue to suffer from human activities, such as hunting, logging, and cattle grazing (Stan & Sanchez,2017). It is therefore important to conduct baseline comparison studies in areas that have been anthro-pogenically disturbed, in order to determine the full extent of damage caused by deforestation and howeffectively regenerating forests can support wildlife.

In addition to forest dwelling species, Costa Rica’s marine fauna have also suffered from populationdeclines due to anthropogenic threats, including fishing, poaching, coastal development, pollution, andclimate change (Chacon-Chaverri & Eckert, 2007 Drake, 1996; Tomillo et al., 2008; Wehrtmann & Cortes,2008). Sea turtles are particularly vulnerable to such threats, as their behaviours naturally traverse avariety of ecosystems throughout their lifespan (e.g. migration across marine ecosystems, nesting oncoastal ecosystems), exposing them to a range of pressures in all stages of their development (Fish et al.,2005). Though efforts have been made to conserve turtle populations in Costa Rica, such as increasedegg and turtle harvesting regulations, long-term studies are needed to determine the effectiveness of suchpolicies and to monitor population trends over time. In addition, monitoring the effect of climate changeon turtle nesting and hatching success rates (Campbell, 1998; Rees et al., 2016).

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Our research is aimed to contribute to the understudied and representative group of taxa within theOsa peninsula with the intention to help better inform policy makers to promote informed sustainableconservation policies. This study also evaluates the effect of anthropogenic activity on species and howthese environments and ecosystems change over time. An equally important aspect of our researchprogram is the participation of volunteers, who come from all over the world to learn and contributeto environmental conservation efforts. By providing this experience for eager volunteers, we hope tospread awareness and knowledge about the importance of this region as a biodiversity hotspot. Lastly,our project works with local community members and organizations to improve research techniques andpromote conservation strategies that are both beneficial to local businesses and help provide a moresustainable future in conservation.

I would like to thank the other staff on the project, including all previous Assistant Research Officers forthe support from the entirety of my contract, a special mention for Nadia Jeffrey finishing her contract,for her work on the beach over the last six months and positive camp attitude. Each respectively haveprovided a great deal of support and consistently endeavoured to improve this project, I would also liketo thank all the previous staff that worked on the project, all of which contributed a great deal to therunning and development of our research. A notable mention goes to a variety of individuals to acceptus as part of the community and support us whenever possible. Finally, I would like to thank the staffat Frontier HQ in London, as well as all the current and previous volunteers for their hard work andinvaluable contribution towards the research programme.

Sincerely,

Matt Smart, Principal Investigator

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3 Introduction

3.1 Natural History of Costa Rica and its Wildlife Conservation

When the Spanish conquistador Gil Gonzalez D’avile took a royal expedition on a ship from Panama toNicaragua, the country he found would soon be named Costa Rica; the title ‘rich coast’ came from theuse of gold by pre-Columbian indigenous tribes both to show rank and decoration. Ultimately, though,it was not the treasures that gave it this name; it was biological richness and variety of life piled intosuch a small country (Kappelle, 2016).

Costa Rica is situated between Nicaragua to the North and Panama to the South on a Southern stretchof the North American continent. It is one of the seven Central American nations and covers an areaof approximately 51,100km2. Enveloped by the Pacific Ocean on the West and the Caribbean Sea onthe East, it creates coastlines of 1103km and 255km respectively. Even though this small country coversonly 0.01% of the earth’s surface, it contains more than 4% of our planet’s biodiversity where around 2million described species worldwide with 95,000 found in Costa Rica accounts for approximately 5% ofthe known species on earth (Kappelle, 2016). This abundance is shared across many taxa, with around12,000 plant species, 1,239 butterfly species, 838 bird species, 440 reptile and amphibian species, and232 mammal species hailing from this country. (Butler, 2006; IUCN, 2006; Sanchez-Azofeifa et al., 2002).

There are two main factors that have led to this impressive biodiversity; the geographical location andthe climatic conditions of Costa Rica. The fact that Costa Rica is situated between the main bodies ofNorth and South America means it can serve as a species corridor between the two continents. It alsolies halfway between the Tropic of Cancer and the equator, leading to an annual average temperatureof 27◦C, with very little fluctuation throughout the year. The dry season starts around December orJanuary and continues through to April or May, after which time the rainy season begins. The SouthernPacific lowlands receive a particularly high level of annual rainfall at approximately 7,300mm per year(Baker, 2012); this consistent high temperature and rainfall both contribute to the Osa’s richness of life.

Although Costa Rica is praised for having one of the most successful protected area systems in the world(Andam et al., 2008; Sanchez-Azofeifa et al., 2003), there are many complexities within the protectedand surrounding areas that remain a mystery. The level and impact of habitat fragmentation, connec-tivity and level of protection puts into question the functionality and productivity of each protectedarea. Therefore, it is important that these areas are studied in greater detail to provide information forpolicy makers on their actions to ensure that they are being as efficient as possible with their resources,protecting and creating the most biologically beneficial areas.

Nearly half the world’s vascular plant species and one-third of terrestrial vertebrates are endemic to 25“hotspots” of biodiversity globally, each of which contain at least 1500 endemic plant species. None ofthese hotspots have more than one-third of their pristine habitat remaining. Historically, they covered12% of the land’s surface, but today their intact habitat covers only 1.4% of the land (Brooks et al.,2002). Costa Rica is a global frontrunner in environmental sustainability and conservation (Fagan etal., 2013) however, this has not always been the case. Like many other countries throughout the world,Costa Rica has been the site of extensive deforestation and human disturbance over recent centuries.Up until the 1980s, activities such as logging and hunting seriously threatened the biodiversity of theregion, resulting in over half of the country’s forests being cut down and many species being driven tothe verge of extinction (Henderson, 2002). Between 1997 and 1999 estimates of logging alone showedthat as many as 14,000 trees may have been selectively extracted from forested areas in the Peninsula(Zambrano, 2010). This rush into cattle grazing reached its maximum in 1989, when the country’sherd reached 2,131,166 heads, and pasture land increased to 2.4 million hectares, equivalent to 48% ofthe national territory (Arroyo-Mora et al., 2005). In particular, the hunting of Costa Rica’s wild catspecies, peccaries, and tapirs for their meat, skin and other body parts has significantly reduced wildpopulations. Human disturbance is also having a negative impact on marine fauna; the poaching ofturtles for the fatty calliper and the collection of turtle eggs has severely depleted populations of endan-gered Green turtles (Chelonia mydas) and vulnerable Olive Ridley turtles (Lepidochelys olivacea), both ofwhich use Costa Rica’s coastlines as nesting sites (Chacon-Chaverri & Eckert, 2007; Tomillo et al., 2008).

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Since the 1960s, some of these issues have been controlled through the implementation of several re-forestation programs, legislation, education, and the creation of protected areas, which now representalmost 27% of the country’s surface area (Andam et al., 2008). Costa Rica has also recently recordeda change from having a net loss of forests to having a net gain in forest area (Kappelle, 2016). CostaRican law currently protects 166 species from being hunted; captured, and traded, yet illegal huntingstill occurs even in protected areas (Baker, 2012). Deforestation and habitat fragmentation outside ofprotected areas and national parks is still a significant problem due to an expanding human populationand the related increases in economic pressure (Carrillo, et al., 2002; Sanchez-Azofeifa et al., 2003).Additionally, the projected impacts of climate change are likely to have significant adverse effects onCosta Rican biodiversity (Baker, 2012). Nature is being funnelled into very few pockets, therefore it isessential for us to do the best job we can to protect them (Brooks et al., 2002). Due to the high stresslevels placed on Costa Rican wildlife along with many other Tropical diversity hotspots, it is importantto conduct further research to determine the health of ecosystems and ensure that effective and con-sistent protection is delivered where necessary. Large scale deforestation and the resulting biodiversitycrisis have already increased awareness and interest in the conservation of tropical habitats worldwide(Krupnick & Knowlton, 2017). However, the actual implementation of conservation practices requiresa basic understanding of native fauna and flora. Tropical forests are not single, homogeneous, bioticformations, and therefore the biodiversity of these areas must be understood on local and regional levels(Gentry, 1988).

3.2 Osa Peninsula

The Osa Peninsula has been hailed by National Geographic as “the most biologically intense place on theplanet”. Located in the Southwest of Costa Rica and covering an area of 1093km2 (Figure 1) (Henderson,2002), the Peninsula contains the last remnants of tropical broadleaved evergreen lowland rainforest onthe Central American Pacific slope, containing approximately 50% of Costa Rica’s biodiversity (Kap-pelle, 2016). Furthermore, this area contains several endemic species such as the Cherrie’s Tanager(Ramphocelus costaricensis), the Red-backed squirrel monkey (Saimiri oerstedii), and the Golfo Dulcepoison dart frog (Phyllobates vittatus) along with a wide and diverse range of keystone and charismaticspecies from a multitude of different taxa. The presence of these endemic species and the overall highdensity of biodiversity in this region make the Osa Peninsula an ideal location for conservation research(Larsen & Toft, 2010).

Three types of forest can be found in the Osa Peninsula: Tropical Wet, Premontane Wet and TropicalMoist forest, with elevations ranging between 200 and 760m (Sanchez-Azofeifa et al., 2002). The vari-ation in topography allows for a highly variable climate, with an average annual rainfall of 2,500mm, amean temperature of 27◦C, and humidity levels almost never dropping below 90% (Cleveland et al., 2010).

There are about 12,000 people living on the Osa Peninsula, most of whom are located in small and scat-tered villages. The most important sources of income in this region are agriculture (rice, bananas, beansand corn), livestock (cattle), gold mining, logging and, the expanding eco-tourism industry (Carrillo, etal., 2000). The population in the region is increasing at a rate of 2.6% annually, which is incredibly highcompared to the 1.3% growth in the rest of the country and the global growth rate of 1.14% (Sanchez-Azofeifa et al., 2001). As a result of the growing popularity of ecotourism since the 1990s, there hasbeen a rise in the number of hospitality businesses along the road from Puerto Jimenez to Carate (Minca& Linda, 2000). This has caused growing concern for the sustainability of the region’s environmentalresource demands (Sanchez-Azofiefa et al., 2001).

Frontier’s Costa Rica Forest Research (CBP) programme began in July 2009 in collaboration with thelocal NGO ‘Osa Conservation’, based in Piro (N 08◦23.826, W 083◦20.564), Southeastern Peninsula. InOctober 2015, Frontier moved to Carate, located in the Southwest of the Osa Peninsula (Figure 1). Thesite is a prime location for carrying out both forest and shoreline surveys, as there is relatively easy accessto all variations of forest degradation, as well as pristine beach habitats. The long-term objective of thisproject is to investigate the effects of climate change, deforestation and other anthropogenic impacts onthe terrestrial communities of Costa Rica. Our research will provide information on the dispersal anddiversity of faunal communities in Corcovado National Park and their relationship with the ever-changingenvironment, with the aim of increasing protection and connectivity of these protected sites in the area.

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Currently we are conducting five core studies within CBP: primates, sea turtles, mammals, herpetofaunaand avifauna.

The Osa Peninsula has undergone considerable deforestation and fragmentation (Sanchez-Azofeifa et al.,2002) and more research is needed to understand to what degree these changing environments play arole in determining the movement, diversity and abundance of their previously resident species. TheMinistry of Agriculture and Environment (MINAE) in Costa Rica are exploring ways to increase land-scape connectivity in the region, and our project will contribute to decisions regarding the designationand location of habitat corridors and protected areas. We hope that our research will go a long way inaiding them in their decisions.

Figure 1: Map of the Osa Peninsula showing Carate (red circle), our area of study (VivaCosta Rica, 2003).

3.3 Aims and Objectives of Frontier CBP

Under the umbrella of the research program, there are two main study aims and five objectives of FrontierCBP:

� Study aim 1: Identify the habitat preferences and provide long term bio monitoring data on arange of animal taxa in Carate to help inform conservation policy implemented by MINAE, espe-cially regarding habitat protection policies and the implementation of wildlife corridors.

� Study aim 2: Participate in global efforts to conserve threatened sea turtle populations throughresearch and in-field conservation.

� Objective 1: Estimate the population density, distribution and feeding preferences of the fourprimate species present in Carate and compare these among habitats with varying levels of distur-bance.

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� Objective 2: Assess mammal species richness and abundance along various forest transects bycreating a camera trap network.

� Objective 3: Determine the habitat preference of 10 endemic and/or data deficient bird speciesby conducting point counts surveys in forest of varying levels of disturbance.

� Objective 4: Understand the density and abundance of Reptile and Amphibian species across alltrails and to better understand their habitat preference by looking at microhabitat utilization.

� Objective 5: Collect data on adult sea turtle nesting patterns, hatching success rate, and nestpredation.

� Objective 6: Investigate the behavioural ecology of the reviving population of the Ara Macaospecies in Carate.

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4 Training

All volunteers, Assistant Research Officers (AROs) and newly appointed staff members receive a numberof briefing sessions on arrival (Table 1), followed by regular science lectures and field training (Table2) throughout their deployments. The CBP research program also supports candidates completing theAdvanced Diploma in Tropical Habitat Conservation.

4.1 Briefing Sessions

Everyone arriving to CBP receives an introduction presentation on arrival. This covers the aims ofthe research program, the data collection methodologies used, and the research output of the individ-ual projects. Furthermore, they get an update on the achievements of CBP through a general sciencepresentation; this is an introduction to the Frontier Costa Rica Forest Research Program in Carate. Ad-ditionally, all volunteers and staff are given a health, safety and medical briefing, which they are testedon before participating in any field activity. Volunteers undertaking the Advanced Diploma in Tropi-cal Habitat Conservation certificate are given an introductory briefing before they begin the assessments.

Table 1: Briefing sessions conducted during Phase CBP 201.

Briefing Sessions PresenterIntroduction to the Frontier Costa Rica Forest ResearchProgramme

MS

Health and Safety Briefing and Test PCIntroduction to Surveying and Monitoring All StaffCamp Life and Duties All Staff

4.2 Science Lectures

A broad program of science lectures is offered at CBP, providing information and training on the differentaspects of research conducted in our study area. Lectures are presented using PowerPoint, providing abetter understanding of the biology and ecology of the study species. Furthermore, they give an insightinto the methods and data analysis used by CBP and the considerations made when planning researchprojects. Attendance of lectures is compulsory. We also offer optional workshops where staff membersdive into more detail on specific topics within their taxa, giving the volunteers the opportunity to becomeincreasingly engaged with what we study as well as a chance to observe each staff members’ passion andknowledge for their taxa.

Lectures are scheduled with the following objectives:

� To allow every volunteer and member of staff to attend each presentation at least once duringdeployment, regardless of length of stay.

� To avoid conflict with other activities to maximize attendance.

� To provide detailed training on specific software and applications used in conservation, such asGPS and the humidity gauge.

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Table 2: Science lectures delivered during Phase CBP 201.

Lecture PresenterScience (overall aims and background ofproject)

MS

Primates BGBirds AATurtles NJMammals BG/IAMacaws AA/IAAmphibians and Reptiles MS

4.3 Field Training

All volunteers and newly appointed staff members receive field training. Training is hands-on and pro-vides an opportunity to become familiar with the field equipment used during surveys. These sessionsare held before starting every survey to inform volunteers and new staff members about the way thesurvey is carried out and to assure accurate data collection. Identification books are present both inthe field and on the campsite to help teach participants how to identify flora and fauna species. Thisis further supplemented with taxa quizzes to help ensure the survey standard is at the high standardrequired to collect data.

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5 Research Work Programme

5.1 Survey Area

Carate is located on the Osa Peninsula adjacent to the Southeastern border of Corcovado NationalPark. The landscape is heterogeneous, composing of lowland moist primary, secondary and coastalforest, and disturbed forest. Dominant tree species include: Ficus insipida, Ceiba pentandra, Attaleabutyracea, Carapa guianensis, Castilla tunu, Spondias mombin, Hyeronima alchorneoides, Chimarrhislatifolia, Fruta dorada, Caryocar costaricense, Ocotea insularis, Pouteria torta, and Inga allenii. Meanannual rainfall and temperature for the area are 5,000-6,000mm and 26-28◦C respectively, with the dryseason extending from the end of December until March (Cleveland et al., 2010). Carate marks thebeginning of the Corcovado-Matapalo Corridor, a wildlife corridor with the potential to increase the freemovement of species that have large home ranges or require increased genetic diversity for populationsto be viable in the long term such as the Jaguar (Figure 2). This conservation initiative is incrediblyimportant for preserving biodiversity on the Osa Peninsula and can only be successful if species distri-bution patterns are closely monitored.

Figure 2: Map of the Osa Peninsula showing various land classifications (as identified bysatellite imagery) and the Corcovado-Matapalo Corridor. This map is adapted from (Dirzo etal., 2014).

Different trails have been selected for our forest surveys that encompass a range of different habitat typesand varying degrees of usage and disturbance. Most of the trails are narrow and machete-cut. The tableand map below outlines the trails that are used for study transects along with habitat classifications.The forest type classification was determined through a combination of local knowledge of forest agesand a habitat survey conducted at 200m intervals on every trail (see section 6.1 below for full analysis).

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Table 3: The names, codes (referring to Figure 3), length and age classification of each trail.

Trail Name Trail Code TrailLength

Forest Classification

3 Ajos 3AJ 1.2km UnknownAttalea ATT 1km Young SecondaryAir strip AIR 1km N/ABeach Trail BEA 1.4km Mid-secondaryCamp River CAM 1km Mix, mostly mid-

secondary with someyoung secondary

Catappa CAT 0.3km Riparian, age unknownGoldenRidge

GOL 1.2km Mix, mostly primarywith some mid/youngsecondary

LagunaVista

LAG 0.8km Young secondary

Leona LEO 1.2km PrimaryLos Aves LOS 0.6km Mid secondaryLowerGary’sLand

LWR 0.8km Unknown

Luna Trail LUN 1km Mix, mostly primarywith some mid/youngsecondary

Playa Carate(turtle patrolbeach)

TUR 2.6km N/A

Puma Creek PUM 0.8km Mid secondaryRio Carate RIO 2km Riparian, age unknownRoad ROA 1km Young secondaryShady Road SHR 0.8km Young secondaryShady Trail SHA 1.2km Mix, mostly mid-

secondary with someyoung secondary

UpperGary’s Land

UPG 1km Primary, young secondary

WaterfallRiver

WAT 1km Primary and old sec-ondary

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Figure 3: This map was created using QGIS version 2.18.15. Map shape-files were downloaded from INOGO Iniciativa Osa y Golfito at Stanford Uni-versity and Stanford Woods Institute for the Environment. Available at:http://inogo.stanford.edu/resources/INOGOMapas?language=en.

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6 Projects

6.1 Assessing the degree of disturbance and secondary succession on foresthabitats in Carate, Osa Peninsula

6.1.1 Introduction

Despite the continued global focus towards combating forest deforestation, forest degradation and im-proving forest management, primary forests continue to decline rapidly due to ongoing land-use en-croachment (Mackey et al., 2015). Of all the world’s eleven million km2 of rainforest five million km2is comprised of degraded and secondary forest (ITTO, 2002). Secondary forests, defined as a forestedhabitat regenerating from previous disturbances, have the potential to hold important ecological value(Brown & Lugo, 1990). They provide atmospheric carbon fixation, protection from erosion, and cansupport diverse fauna and flora even in fragmented landscapes (Fearnside & Guimaraes, 1996; Lamb etal., 1997). Therefore, despite often being cited as less diverse than primary forests (Barlow et al., 2007),it is essential that secondary forests are considered important for conservation. Sanchez-Azofeifa et al.(2002) documented that as of 1997, only 44% of the forest remaining on the Osa Peninsula was matureand that most of the forest located outside Corcovado National Park has been altered to some extent.Forests classed as “secondary” can contain a large range of diverse characteristics which affect the level ofbiodiversity; factors such as geographic location, taxonomic group and disturbance type make it difficultto generalize the findings of any one study (Gibson et al., 2011). Studies show that biodiversity canin fact thrive in forests recovering from disturbance (Berry et al., 2010). As many species find a newniche, developing different ecological communities, the matrix surrounding forested habitats has beenshown to influence species composition within them (Dent & Wright, 2009). There is also the potentialfor a few individual species to tolerate the disturbance much better than others and lead to a reductionin species richness. Therefore, it is important for secondary and fragmented forests to be describedand understood. Despite their potential as a conservation tool, secondary forest patterns regarding dis-turbance and succession are poorly understood. Due to the complexity of the subject, the large rangeof both biotic and abiotic factors at play, and issues relating to accessibility and resources (Murcia, 1995).

Successional changes in tropical vegetation structure have been studied extensively from a theoreticalstandpoint however, observational and experimental studies to corroborate theory have produced variedresults. This is due to the complexity and interplay of a wide range of factors that affect vegetationdynamics during secondary tropical forest succession. These include the type and intensity of previousland use, soil fertility, clearance type, edge effects and the surrounding landscape matrix (Ferguson etal., 2003; Johnson et al., 2000; Myster, 2014).

In this study, we investigated the differences between a set of parameters that have been used in previousstudies, to define the degree of succession in tropical forests. Early successional stands to be characterizedby higher tree densities, lower basal areas and shorter canopy heights (Guariguata & Ostertag, 2001),as well as lower canopy cover (Myster, 2014). Additionally, vegetation composition will be an indicatorof succession, where younger plots will have less frequently encountered lianas, large logs and large treescompared with older plots (Guariguata & Ostertag, 2001). Lastly, certain floral species are indicators ofthe disturbance level of forests.

The aim of this study is to perform an initial habitat assessment of a number of trails in Carate, OsaPeninsula, Costa Rica, on which our research is based for primates, mammals, amphibians and reptiles,birds, insects and other related projects. We will attempt over time to provide a complete descriptionof the physical habitat, and then using literature put them into distinct and appropriate categories.This will provide a great opportunity to analyse how individual taxa are utilizing the habitat on both amacro and micro scale, as well as looking at the specific use of each habitat type for example utilizationof the shrub layer. Carate has a unique history of land use; while some parts of the forest have beenpresent in this region for extensive periods of time with minimal human disturbance, other areas haveonly recently started to regenerate after they were cleared for logging and agriculture. (Kappelle, 2016;Minca & Linda, 2000). While some information on the history of the land can be obtained through localknowledge, it is important to assess patterns in habitat characteristics that could indicate what featuresof forests with varying levels of succession are most crucial for sustaining biodiversity and conservingendangered and endemic species. This initial assessment is therefore crucial for helping us understand

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patterns of abundance, diversity and behaviour of all our study species, as well as to help understandthe wildlife population trends in the Osa Peninsula. This study is important as the research area hasreceived little scientific attention and the habitat quality remains unassessed thus far. Furthermore,there is scope to develop this project further into a long-term monitoring study to investigate the rateof regeneration of tropical forests in the context of succession after anthropogenic disturbance and theseasonal variation of each habitat type.

6.1.2 Aims of Study

This study collected data on the structure and level of secondary succession of forests in this region toattempt to quantify and better understand the level and impact of disturbance present on forest trailsin Carate.

1. To provide baseline data on the structure and degree of succession of habitats in Carate so that allstudies can assess how each animal group interacts with these characteristics down to a microhab-itat scale.

2. To provide MINAE with an assessment of habitats surrounding Corcovado National Park that willhelp inform policy decisions regarding the protection and conservation of these areas, particularlywith regard to the maintenance of buffer zones surrounding Corcovado National Park along withthe potential for increased forest connectivity.

6.1.3 Methodology

Study Sites

Habitat surveys were conducted at 100m intervals on the following trails: Golden Ridge, Luna, ShadyRoad, Puma, Road, Camp river, Leona, Shady Trail, Beach Trail, Laguna Vista, and Trail Verde. Thesetrails are designed to encompass a wide range of primary and secondary habitat in various environmentsin Carate. At every survey point, a 5x5m quadrat was measured on either side of the trail path, startingone meter into the vegetation. This is to minimise skewed data due to the variation in trail width.For each plot, the following parameters were recorded: herb & shrub layers, leaf litter depth, canopycover, mid and full canopy height, number of woody plant smaller and greater than 5cm Diameter BreastHeight (DBH), DBH of woody plants greater than 5cm DBH, density of non-woody vegetation, topogra-phy, ground cover, presence of vines and lianas, logs and stumps. Elevation and GPS was also recordedfor all sites.

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Table 4: The habitat variables recorded, along with a description of the method of datacollection.

Variable Method of Data CollectionCanopy Cover Estimated at the four corners and centre point of each 5x5 plot. Esti-

mates were made to the nearest 5% by looking through a pair of binocu-lars (in the reverse viewing scope) to create a consistently sized viewingframe.

Mid and Full canopyheight

Recorded using a TONOR laser rangefinder. Full canopy height wasdefined as the height of the tallest tree in the plot. Mid canopy heightwas calculated by measuring the height of a tree representing the averageheight of the mid-level canopy. If there was no mid-level canopy, themiddle canopy height was recorded as the same as the full canopy height.If it was not possible to measure from directly beneath the tree, theheight would be calculated by standing a short distance away from thetree and measuring the person’s distance to the base of the tree and theheight of the tree. Pythagorean theorem (a2 + b2 = c2) was then usedto calculate the height of the tree. If the Canopy height was too greatfor the TONOR laser to work, a group estimation was made then theaverage was recorded.

Herb and shrub density Measured with a banded meter stick (with 11 bands, one placed every10cm) at each corner of the plot and in the centre of the plot. Forherb layer the individual starting at the bottom left point or point onewould hold the meter stick touching the ground moving up to roughlythe individuals right hip. The individual at point two or top left ofthe plot will then crouch down and state (without moving their head toadjust the position) how many bands on the meter stick they can see.For shrub layer the meter stick was held vertically from the person’s hipto above their head, the observer stands up to match the appropriateheight and repeats the same method.

Average and largest Di-ameter Breast Height(DBH).

The DBH of all trees over 5cm was measured. This was collected witha tape measure wrapped around a tree then converted to DBH fromcircumference later using D=C/. The average of these measurements,as well as the size of the largest tree in the plot, were calculated.

Stem density The plot was divided into four sections to make it easier to describe.Measured by counting all free-standing woody vegetation within threeclasses of plant size following methodology adapted from Guariguata etal., (1997): class 1: trees (stems ≥ 10cm DBH), class 2: treelets (stems≥ 5cm DBH and < 10cm DBH), and class 3: saplings and seedlings(stems < 5cm DBH). This again was measured using a tape measure atthe Breast height around the tree then converted to DBH later using asimple formula D=C/.

Non-woody vegetationdensity

All vegetation with non-woody stems were counted in the same fourdivided sections then added together.

Ground cover Estimated as a percentage; what percentage of the ground is made up ofleaf litter, bare ground, woody debris, and water (adding up to 100%).The leaf litter depth at every corner of the plot was also be taken usinga ruler.

Topography and elevation Topography was defined as a dichotomous variable: flat or steep. Eleva-tion was measured using a GPS.

Presence or absence ofvines and lianas.

1/0. This was then represented as a proportion for the trail when aver-aged out.

Presence or absence ofstumps and logs.

1/0. This was then represented as a proportion for the trail when aver-aged out.

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6.1.4 Results and Discussion

Excel was used to produce some scatter and column graphs helping describe the relationship between thevariables and across trails within the data. A principal component analysis was conducted to determinethe variables that most strongly influenced the variation across trails and to identify trail groupingsbased on the strength and directionality of these variables. RStudio was used to conduct this analysis.

Table 5: A table describing the relationship between forest age and habitat variable.

Variable Indication of Forest AgeCanopy Cover Higher cover percentage indicates older forest. Older forests tend to have

larger and taller trees that more broadly cover the canopy.Mid and Fullcanopy height

Higher canopy height indicates older forest. Older forests have largertrees and therefore taller canopies.

Herb and shrubdensity

A lower density indicates older forest. Primary forest has higher canopycover and therefore less light reaches the ground, leading one to assumethat both herb and shrub layers are not as successful in these habitattypes.

Average and largestDiameter BreastHeight (DBH)

Larger DBH indicates an older forest. Older forests will have larger treesbecause there has been more time for emergent trees to grow, so the moretrees >5 cm and the higher the ADBH and LDBH, the more likely thetrail is closer to primary forest.

Stem density Lower numbers of treelets, saplings and seedlings indicate older forests,because there is less light entering through the canopy. More trees (thelarger DBH category) indicate older forest.

Non-woody vegeta-tion density

Lower numbers indicate an older forest. Older forests have higher canopycover and therefore less light abundance, so fewer new plants can grow.The success of these plant types is more likely in increased light and lowcanopy environments as they cannot compete for light against the tallemergent trees.

Ground cover This variable does not necessarily indicate the age of the forest, howeverwe collected this data as it could be an important factor in the habitatselectivity of certain species, particularly amphibians and reptiles whomay be sensitive to alterations in microhabitats. It can also give us anindication of forest via carbon uptake and release.

Topography and el-evation

These variables do not necessarily indicate forest age, however this datawas collected as it is an indicator of the vegetation species that can besustained in a habitat. It can also be an important factor in the habitatselectivity of certain species.

Presence or absenceof vines and lianas

Older forests are less likely to have vines and lianas, as these require alot of light to grow.

Presence or absenceof stumps and logs

These variables do not necessarily indicate age of forest, however wecollected this data as it is an indicator of the condition of trees (andindirectly of soil quality), and can also be an important factor in thehabitat selectivity of certain species.

Attalea phalerataand Cryosophilaguagara

Cryosophila guagara is an indicator species for older forests, while Attaleaphalerata is an indicator of young regenerating forest.

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Principal Component Analysis

The first two Principal Components cumulatively explained 49% of the variation across trails [PC1 31.4%,SD 2.62; PC2 17.7%, SD 1.97]. A correlation of the first two principal components was calculated todetermine the strength and directionality of the association between each habitat variable and principalcomponent.

The age category of a trail was based primarily on its relationship with Principal Component 1 (PC1), asthis PC explained a larger portion of variation in the data displayed stronger correlations with featuresthat indicate habitat age (Figure 4). Specifically, as a trail has a higher value for Principal Component1, it has a lower the canopy cover, a lower leaf litter, a higher percentage of bare ground, and a lower‘largest DBH’; these are all indicators of younger secondary forest. Additionally, trails with higher valueson Principal Component 2 (PC2) displayed on average lower ‘Average DBH’ of tree larger than 5cm, asan indicator of younger secondary forest. This will be used when considering the degree to which eachtrail belongs in a particular grouping and when analysing species abundance on individual trails.

Figure 4: A biplot displaying the categorization of individual trails according to PrincipalComponent 1 (PC1) and Principal Component 2 (PC2). Red arrows represent the directionalityand strength of the relationship between each explanatory variable (habitat characteristics) inrelation to PC1 and PC2, and numbers each represent the response variable (trail).

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Habitat Variables vs Habitat Type

After using the PCA (Figure 4) to put all of the trails into habitat types, which is listed, at the end ofthe results (Table 6). We can use the averages from all of these trails to look at some important habitatvariables and how they fluctuate across habitat type (Figure 5). The three that have been selectedare leaf litter, non woody and upper canopy height. These almost all follow the expected trend thatwas described in Table 6, leaf litter has the highest depth in primary forest where the large trees haveconsistently been dropping leaves without any anthropogenic influence, as soon as the habitat has beendisturbed the leaf litter is not as dense. This drop is clear to see as we have at least 1.5cm decreasebetween primary and the secondary habitats (Figure 5a). Non woody are made up of mostly palms andother low to the ground non woody plants, these plants are notorious for needing considerable light tobe present in large numbers. Our data (Figure 5b) clearly supports this as the forest ages and the largercanopy trees become increasingly present (Figure 5c) and the available light to support the undergrowthdecreases in this case non-woody will decrease.

Figure 5: Column Charts highlighting three important habitat variables and how they fluctu-ate across different habitat types. a) The fluctuation in leaf litter depth in cm across all habitattypes, b) The number of non woody plants averaged across all habitat types and c) The uppercanopy height across all habitat types.

High levels of herb and shrub layers, which represent the first two meters of the understory, are observedin almost all of our trails implying that there is very little mature primary habitat with a complete andestablished canopy cover. There can still be high levels of herb and shrub density even in primary foresthowever, there is a lower chance of development into trees with a DBH greater than 10cm, due to thereduction in available light. With this said, Leona (Table 6 & Figure 4) is a strong representation ofprimary forest in the region as it is closest to the national park and it is not considered to have expe-rienced anthropogenic influence. Leona could therefore be used as a model for habitat variables at thatelevation. Figure 3 illustrates that the higher the height of the emergent trees, the greater percentage ofcanopy cover resulting in a dramatic drop in non-woody plants, due to the reduction of light reaching theforest floor. Therefore, this could be used to determine at what stage of succession each trail is in. Thisis confirmed by the PCA (Figure 4) and by the table describing the indication of each habitat variableon forest age (Table 5). The results are clear that there is a wide range of external variables at play,impacting our data, such as location and proximity to a body of water, etc. Each trail is recovering from

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disturbance and succession, containing different species and rates respectively, making it challengingto put them into a general bracket such as primary or secondary (both types) as they are much morecomplex and variant than that dictates.

The local classification of most of our trail show an interesting pattern; forests that are a combination ofrecently disturbed forest and completely undisturbed forest may classify themselves as “middle ground”in the habitat classification process, thus making them appear from the analysis as “mid secondary”when in fact it is more of a mixture of different ages.

Final Classification of Trails

Table 6: Final classification of each trail based on a combination of local interviews andhabitat surveys.

Trail Habitat typeLeona PrimaryLuna Trail Mix, mostly primary to old secondary with

some mid/young secondaryGolden Ridge Mix, mostly primary to old secondary with

some mid/young secondaryWaterfall Mix, primary to old secondaryUpper Gary’s land Primary, young secondaryLos Aves Mid secondaryShady Trail Mid secondaryCamp River Mid secondaryPuma Creek Mid secondaryShady Road Young secondaryAttalea Young secondaryRoad Young secondaryLaguna Vista Young secondary

6.1.5 Conclusions and Implications for Future Analysis

In conclusion, there is a lot of fluidity in the forest classifications; the lack of strong correlations betweenhabitat variables often makes it very difficult to put a trail in one distinct category as the habitat of atrail can vary considerably within, not just between trails (Gibson et al., 2011).

Continued development of the habitat data collection would only improve our knowledge of the trends inphysical and environmental characteristics between all of our trails even if they cannot easily be groupedin to well defined types. For the purposes of the study we have followed literature (Guariguata & Os-tertag, 2001; Myster, 2014) and used trends in the data from the PCA to put them into groups. In thefuture looking deeper and understanding the difference between habitat variables across trails may bemore useful for seeing how different taxa interact with the environment.

6.1.6 Limitations and Future Directions

This study has been a work in progress and has finally undergone a sufficient amount of data collectionfor analysis. However, progress is still being made and habitat surveys are currently being conducted onour other trails, including 3 Ajos and Gary’s lower. The introduction of saplings as a separate categoryinto data collection should make the distinction between woody plants < 5 cm DBH a more representa-tive data field. This is important as they play significantly different roles within each habitat. Finally,increasing the ground cover options should reduce error as some plots have had ground cover not ap-propriate for any of the current categories. Another limitation of this study is that the methodologyused to measure canopy cover can be subjective, as different individuals record canopy cover estimatesthrough the binoculars for each point. Therefore we intend to recollect data on the canopy cover of every

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point using imaging software that can formulate the foliage to sky ratio using differences in pigmentation.

An additional limitation was our inability to identify tree species. The flora in this study region is in-credibly diverse and identifying tree species often requires a level of specialization and expertise that wedid not have access to. It would greatly benefit the study to be able to identify a number of tree speciesindicative of the forest type. In the future, we intend to look into DNA barcoding, hiring local guides,or another methodology to accurately identify species within each of our 5x5 plots.

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6.2 The Occurrence and Forest Type Preference of Four New World Pri-mates

6.2.1 Introduction

The International Union for the Conservation of Nature (IUCN) classes more than one third of theworld’s primate species as threatened with about one in seven at risk of extinction. Human factors haveplayed a major role in the decline of primate populations (Wainwright, 2002) and have even caused theextinction of some species, such as the Madagascan Lemur (Wainwright, 2007). These factors includehunting, the pet trade, disease and habitat destruction (Wainwright, 2002). A species’ ability to utilisedifferent forest types (including secondary or disturbed fragments outside protected habitat); alter dietsdepending on resource availability; and inhabit a range of elevations often influences their ability toadapt to such pressures (Wainwright, 2007). Factors such as land-use change for human infrastructureor agriculture and deforestation often detrimentally impact primates with specific habitat requirements(Skrinyer, 2016). For example, arboreal movement may be restricted by poor habitat connectivity withsmaller, more isolated fragments being insufficient for sustaining populations with naturally larger homeranges (Sanchez et al., 2002).

Whilst Costa Rica is a small country, it boasts 4% of the global biodiversity including 232 mammalspecies, of which four are primates (Wainwright, 2007). Prior to 1960, more than 50% of Costa Ricanforests were cleared, but since then, a combination of legislation, protected areas and reforestation pro-grammes has resulted in 27% of the country being protected in 190 different areas. Corcovado NationalPark and Golfo Dulce Forest Reserve are two such areas on the southwest coast of the Osa Peninsula(Wainwright, 2007). This region has particularly high biodiversity and is the only part of Costa Ricawhere all four of its primates are found: Central American Squirrel Monkey (Saimirii oerstedii), White-Faced Capuchin (Cebus capuchinus), Mantled Howler Monkey (Alloutta palliate) and Geoffroy’s SpiderMonkey (Ateles geoffroyi). They are all arboreal and diurnal species who rarely move terrestrially. Theirdiet is predominantly frugivorous, although some – such as the Mantled Howler Monkey – depend lesson fruit and supplement their diet with insects, flowers, leaves and shoots (Wainwright, 2007).

The Osa Peninsula in Costa Rica has two distinct seasons: the dry season (December-April) and thewet season (May-December). The main factor that determines seasonality on the Osa Peninsula, as innearly all neotropical sites, is the annual rainfall cycle (Stone, 2007). Understanding how primates adjusttheir behaviour in response to seasonality in both continuous and fragmented forests is a fundamentalchallenge for many primatologists and conservation biologists (Boinski, 1987). Seasonal variations inboth food availability and climate may contribute to changes in primate activity patterns. During thedry season, animals in many neotropical forests are exposed to more stressful conditions than during thewet season, e.g. temporal food scarcity, drought and high temperatures (Chaves et al. 2011).

To deal with these harsh conditions, tropical primates often reduce their energy expenditure during thedry season by spending more time resting and less time travelling (Asensio et al. 2009). Since fleshly ripefruits are particularly abundant during the rainy season (Asensio et al. 2009), this season is frequentlya period of high frugivory (Felton et al. 2009; Masi et al. 2009). Moreover, some primates spend lesstime feeding during the rainy season (Masi et al. 2009), as fleshly ripe fruits are more digestible andhigher in energy than leaves (Felton et al. 2009; Lambert 1998; Milton,1981). Conversely, other studiessuggest that some primates spend more time feeding during the rainy season (Felton et al. 2009) andthey attribute this to the fact that feeding is an energetically costly activity that needs to be minimizedduring the dry season (Campos and Fedigan 2009). In addition, by increasing feeding time during therainy season, monkeys may ingest surplus energy and store it as fat in preparation for the impendingperiod of food scarcity (Felton et al. 2009).

6.2.2 Methodology

Ethical Statement

All primate and mammal studies are conducted in accordance with the legal requirements of the CostaRican Government. Data collection was solely observational and non-invasive, with observers retreatingfrom any abnormally or aggressively behaving primates.

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Study Area

Carate is an area located in the south west of the Osa Peninsula next to the southern border of CorcovadoNational Park. It is surrounded by the Golfo Dulce Forest Reserve and encompasses a variety of habitatsand elevations including disturbed areas along roads and Primary forest along ridge trails. From 2015 to2020, surveys were carried out in this area along 13 predetermined trails: La Leona, Luna, Beach, CampRiver, Puma, Shady Trail, Waterfall, 3 Ajos, Golden Ridge, Attalea, Road, Osita Road. Over the last 9months Puma, Shady Road, Waterfall and Attalea have been discontinued due to insufficiency in traillength and accessibility. However, all are included in the data analysis..

Study Species

Costa Rica is home to four species of new world primate: Central American Squirrel Monkey (Saimirioerstedii), White-Faced Capuchin (Cebus capuchinus) Mantled Howler Monkey (Allouata palliate) andGeoffroy’s Spider Monkey (Ateles geoffroyi). The Osa Peninsula provides a unique chance to study allfour species simultaneously as it is the only region in Costa Rica where all four species coexist and arecommonly seen (see Table 7).

Table 7: The four primate species studied in Carate, the Osa Peninsula. Data extractedfrom the IUCN Red List Species Assessments (Cuaron et al., 2008a-b, Wong et al., 2008).*Alternative names: Red-backed Squirrel monkey. **The White-Throated Capuchin has notyet been classified by the IUCN Red List.

MantledHowler Mon-key

Geoffrey’sSpider Mon-key

White-ThroatedCapuchin

CentralAmericanSquirrel Mon-key

Latin Name Alouatta palli-ata

Ateles geoffroyi Cebus capuci-nus

Saimiri oerste-dii

IUCN Status Least Concern Endangered ** VulnerableGroup Size 40 20-30 4-40 20-75Range Size 259-388 haElevation 2000m asl. Known popula-

tions at 600masl.

500m asl.

Diet Predominantlyleaves

Predominantlyfruits andleaves. Someinsects, barkand flowers.

Tropical ev-ergreen, drydeciduous.

Lowland rain-forest, primaryand secondarylower/midcanopy.

Sex Identifica-tion

Males have awhite scrotum.

Females havea pendulousclitoris.

Survey Protocol and Data Collection

Data was collected over a five-year period between 2015 and 2020. Surveys were conducted during boththe dry (Jan-Apr) and wet (May-Dec) seasons with single observer line surveys conducted multiple timesper week. Trails were never walked more than once per week and were randomly chosen using a randomnumber generator.

A minimum of 2 observers walked for 800m at approximately 2km/h continuously scanning the canopy.When primates were encountered the following were recorded:

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� Time

� Species

� GPS coordinates

� Group size and composition (adults, males, females, juveniles and infants)

� Behaviour (foraging, resting, travelling)

� Distance from path to central tree (m) and height of group in the central tree (m)

The latter was used to describe the position of a troop within the canopy and was recorded by estimationby eye.

Time of Day

Surveys began predominantly at 06:00 and 16:00 as these were considered the most active times of dayfor primates. Some surveys, however, were run across all daylight hours (05:00 – 17:00, excluding 12:00– 13:00) to fit with volunteer schedules as data is collected as part of a volunteer project.

6.2.3 Results

From the 11th of November 2015 to the 21st February 2020, 638 primate troops were encountered on 344of the 492 surveys conducted. Over half of these encounters were of Spider Monkeys, with 334 sightings,followed by 172 Howler Monkeys, 90 Capuchins and 68 Squirrel Monkey encounters.

Primate Detectability Frequency

The majority of surveys and thus primate encounters occurred the wet season, with 402 encountersrecorded in 525 surveys, with 244 encounters recorded in 305 surveys in the dry season. However, whenthe survey effort was considered, and the detectability probability was calculated the difference becameinsignificant (Figure 6).

Figure 6: The detectability frequency (%) of all four primate species in Carate (Geoffory’s Spi-der Monkey, Mantled Howler Monkey, White-Faced Capuchin and Central American SquirrelMonkey), across the wet and dry season.

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The detectability success across both seasons also varied between the four species. Again, the SpiderMonkey showed the highest overall detectability rates with a probability of 40.8% in both the dry season(Jan-Apr) and the wet season (May-Dec). The Howler Monkey showed a 25.5% success rate in the dryseason as opposed to a 17.4% success rate in the wet season. The Capuchin and Squirrel Monkeys showedan opposite trend to the Howler Monkey with higher success rates in the wet season (Figure 7).

Figure 7: The detection rates of the Geoffroy’s Spider Monkey, Mantled Howler Monkey,White-Faced Capuchin and Central American Squirrel Monkey, across the two distinct seasonsthe dry season (Jan-Apr) and the wet season (May-Dec).

Behaviour

Travelling and foraging were the most common behaviours observed with 256 and 253 records, respec-tively. The number of groups observed resting was considerably lower, with only 82 observations, andfar fewer groups were recorded to be aggressive, with only 2 observations. All aggressive behaviours wererecorded during the dry season.

Similar to detectability frequency, there was a variation in behaviour in each of the four primate species,between the dry and wet season. Spider Monkeys were most frequently seen travelling in the dry seasonand foraging in the wet. The Howler Monkeys and Capuchins were most frequently seen foraging acrossboth seasons and the Squirrel Monkeys were most frequently observed travelling across both seasons(Figure 8).

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Figure 8: The frequency of observed behaviours in encountered primate troops in the dry sea-son (a) and wet season (b), in Carate. Foraging, resting, travelling and aggressive behaviourswere all recorded for White-Faced Capuchin, Mantled Howler Monkey, Geoffroy’s Spider Mon-key, and Central American Squirrel Monkey.

Habitat Usage

There was very little variation in the detection rates of primates in each of the forest types, betweenthe two seasons. However, the likelihood of encountering the four different species did vary between thetwo seasons. Spider Monkeys were regularly detected in all four forest types, during both seasons, withall detection frequencies being over 27%. Across both seasons, Howler Monkeys were more frequentlydetected in Mid-Secondary with 38.7% in the dry season and 20.3% in the wet season. The Capuchinsfollowed a similar trend to that of the Howler Monkeys, favouring the Mid-Secondary forest followedby the Young Secondary. The Squirrel Monkeys showed a similar trend between the seasons, favouringPrimary or Young Secondary in the dry and wet seasons (Figure 9).

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Figure 9: The detection frequency of Geoffroy’s Spider Monkey, White-Faced Capuchin,Mantled Howler Monkey and Central American Squirrel Monkey, in the different forest types,comparing the two distinct seasons; the wet season (May-Dec, a)) and the dry season (Jan-Apr,b)). The forest types were categorized as Young secondary, Mid-Secondary, Old Secondary andPrimary.

6.2.4 Discussion

Detectability Frequency

All four primate species inhabiting Carate were encountered on surveys between 2015 and 2020 duringthe wet and dry seasons. The detectability frequency of all species varied little between the two seasons.When individually assessed, however, variations became obvious. Spider Monkeys were the most fre-quently encountered primate throughout both seasons (210 in the wet season and 120 in the dry season).This is supported by Weghorst (2007), who focused on primates at Sirena, Corcovado National Park andfound a similar result for Spider Monkeys, resulting in one of the highest population densities recordedfor the genus. Spider Monkeys are currently listed as endangered by the IUCN Red List (Cuaron et al.,2008; Spaan et al., 2017), with populations having declined by 50% since the 1970’s. Therefore, theseresults that prove their high abundances highlight the importance of continuing conservation for thisspecies.

The Mantled Howler Monkey was the second most detected species, followed by the White-Faced Ca-puchin and then the Central American Squirrel Monkey. Since the largest primate (the Spider Monkey),was detected most frequently and the smallest primate (the Central American Squirrel Monkey), wasdetected the least, this trend reflects the primate’s body size. This may be explained by the largerspecies being easier to see, and therefore easier to record. Whilst both auditory and visual aids were

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used during this survey, auditory was the most successful as we were able to hear the classic howlsof the Howler Monkeys and the movement in the trees caused by the acrobatic locomotion of SpiderMonkeys as they moved. This may explain their easier detection in comparison with the smaller, qui-eter Capuchins and Squirrel Monkeys (Cropp and Boingki, 2000), which, also use auditory signals thatare hard to distinguish from local bird species, which decreases their ease of detection (Wainwright, 2007).

The lowest detection frequency of all primate species belonged to the Squirrel Monkey, which could bedue to them having the lowest population of all the primate species in the Carate area. 1938 heraldedthe arrival of the United Fruit Company. They started massive deforestation in southwestern CostaRica, destroying the already small home range (a few hundred squared km) of the Squirrel Monkey andreplacing it with palm and banana plantation, as well as numerous small cattle and other farms (Wain-wright, 2007; Cropp and Boingki, 2000). As well as this, the pet trade also had a significant impact onthe population, with >173,000 being caught and exported to the US from 1968 to 1972 (Boingki et al.,1998). Chemicals are also a threat, those used in farming as pesticides can contaminate forest fragmentsas well as the Squirrel Monkeys’ main food sources. Many have been found dead as a result of poisoning(Henderson, 2002; Nunn and Altizer, 2006). Urban encroachment is also an issue as Squirrel Monkeymortality increases in these areas due to electrocution as they try to use electricity wires as a migrationroute between forest fragments (Wainwright, 2007). Given their small home range, habitat destructionand fragmentation has further exacerbated existing threats to the Squirrel Monkey. As forest fragmentsbecome increasingly isolated, so do Squirrel Monkey troops and migration of individuals between troops(a process needed to ensure genetic diversity) becomes increasingly impossible (Keyghobadi, 2007).

Behaviour

Squirrel Monkeys are a highly active species that typically spend a large proportion of time travelling(Pinheiro and Ferrari, 2013). This was the most common behaviour observed with very little differentia-tion across both seasons. They are highly faunivorous and can exploit insect food sources during times offruit paucity (Stone, 2007) by foraging on the ground for extended periods (Boinski, 1988). Our results,however, show very little change in the amount of time spent travelling between seasons (with it beingthe most commonly recorded behaviour), eluding to a patchy distribution of food resources which wouldincrease the amount of time spent travelling between patches. A study conducted by Stone (2007) at asite in eastern Amazonia found that the amount of time spent travelling remained the same across allseasons even though there were distinguished seasonal shifts in fruit abundance. However, this contra-dicts Boinski (1987), who found that Squirrel Monkeys in Corcovado (which Carate borders) spent <3%of their time travelling.

Spider Monkeys are highly frugivorous primates (Wallace, 2005). Our results demonstrated that theyspend most of their time travelling in the dry season due to their need for food sources that are high inenergy but are often located in patchy distributions across their territory (Wallace, 2005) and are reducedduring time of fruit scarcity. The predominant behaviour during the wet season was foraging. SpiderMonkeys are an adaptable species and during times of fruit paucity they are able to rely more on folivoryrather than frugivory. They can, however, only tolerate folivory to an extent as their digestive systemis not well adapted for a folivorous diet (Wallace, 2005). It is unlikely that the increased foraging be-haviour during the wet season is due to Spider Monkeys relying more on folivory caused by fruit paucity.Breadnut (Brosimum spp.) and Cecropia (Cecropia spp.) are favoured foods of the Spider Monkey andthese fruit and flower during the wet season (Fournier, not dated; Rocas, not dated). Rather, as theamount of available fruit increases, the Spider Monkeys may spend more time foraging in patches of highfruit abundance and less time travelling between patches.

Howler Monkeys are known as energy minimisers (species that use behavioural strategies for conservingenergy). Whilst they are known to consume fruit, leaves can constitute up to 90% of their diet (Behirand Pavelka, 2015). Foraging was by far the most commonly observed behaviour across both the dryand wet seasons, followed by resting. This may be in part due to the biology of their digestive tract.Howler Monkeys are hindgut fermenters with digestion of food occurring in the proximal colon andcecum. The amount of protein and energy extracted from the leaves is very low as these organs arelocated after the small intestine which is where the most efficient absorption of nutrients occurs. Due tothis, Howler Monkeys increase the employment of energy minimising strategies (Behie and Pavelka, 2015).

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Even though foraging was the most commonly observed behaviour across both seasons for Howler Mon-keys, there was no significant differentiation in the amount of time spent foraging between the wet anddry seasons. This is also the same for resting which was the second most observed behaviour. Therewas, however, a significant difference of 10.8% in the amount of time spent travelling with 13.1% in thedry season and 24.1% in the wet season. This is similar to the findings of Stoner (1996) who found thatthe amount of time spent foraging did not change significantly with the seasons. This is interesting asthe area in which this study was conducted (La Selva Biological Reserve) did not have a pronounced dryseason at the time of the study, whereas Carate does. Had it been studied, the results of this currentstudy may have aligned more with previous studies conducted in areas with a more pronounced dryseason than La Selva Biological Reserve.

White-Faced Capuchins were most often observed foraging across both seasons. The results for the dryseason are supported by the findings of Tarano and Lopez (2015) whose study focussed on the behaviourand time budgets of Wedge-Capped Capuchins (Cebus olivaceus) in Venezuela. Their study revealed thatwhen the amount of time spent in social interactions (resting) fell during the dry season, this coincidedwith an increase in foraging behaviour as fruit paucity increased so the Wedge-Capped Capuchins wereforced to rely on more time-consuming methods for finding invertebrates (Tarano and Lopez, 2015).Whilst there was no significant difference in the proportion of time spent resting between seasons in thecurrent study, the high proportion of time spent foraging suggests that, due to their relatively smallsize and generalist diet (Wainwright, 2007), White-Faced Capuchins may be time minimisers. Instead ofspending more time travelling between food sources of patchy distribution they choose to conserve energyduring lean times by minimising the amount of time spent obtaining resources (Stone, 2007). Their gener-alist diet also includes a range of invertebrates such as beetle larvae, ants and wasps (Wainwright, 2007).The lack of any significant change in the amount of time spent foraging, coupled with their predominantuse of Young and Mid-Secondary forests (which are highly disturbed habitats where arthropods wouldbe expected to be relatively abundant year round (Stone, 2007) throughout the wet and dry seasons,eludes to a reliance on arthropods as a main dietary component throughout both the dry and wet seasons.

Habitat Uses

As mentioned previously, Spider Monkeys were frequently observed across all four forest types duringboth the wet and dry seasons which is not surprising as they were the species with the highest num-ber of observations. They are a highly adaptable species which are able to adapt to changes in factorsincluding food sources (Chapman, 1988). Their diet is highly varied and includes fruit, leaves, bark,flowers, roots, insects and honey so Spider Monkeys are not necessarily as affected by fruit seasonalityas the other three primates. Cecropias (Cecropia spp.), figs (Ficus spp.) and breadnuts (Brosimumalicastrum) are the favoured foods of the Spider Monkey and are all indicators of Young secondaryforests (Gargiullo et al., 2008). Since their food sources range throughout most forest types, this speciesis able to thrive in habitats where the other species cannot. This is further helped by their abilityto travel long distances (using their strong fingers and prehensile tail) between food patches and theywill often move between forest types (Chapman, 1995). Due to their long life history, however, theyare vulnerable to environmental changes included habitat fragmentation so the maintenance of suitablehabitats is crucial. The importance of buffer zones outside national parks (Andam et al., 2008) has beenhighlighted by the results of both this study and the previous study conducted by Weghorst (2007) asthe high abundances of Spider Monkeys found in both studies demonstrate that the diversity of foresttypes seen in Carate is sufficient enough to support large populations of this species (Andam et al., 2008).

Throughout the wet and dry seasons, Capuchins were most frequently recorded across all secondaryforest types. Despite being rarely encountered in Primary forest during the wet season, during the dryseason (when food is scarce) they utilise all forest types in order to survive (Wainwright, 2007). Thisis one demonstration of their adaptability and increased intelligence, which has also enabled to success-fully survive outside pristine forest areas, next to farmland which has resulted in increased sightings insecondary forest (Estrada and Coates-Estrada, 1996). One of preferred food sources of the Capuchinis the Bromeliad which, in Costa Rica, are found in wet forests close to the ground in smaller trees,characteristic of second growth (Gargiullo et al., 2008). Due to their adapted ranges, some individualshave adapted to feeding on crops grown on nearby farms which brings them into conflict with farmers(Wainwright, 2007). As well as this, increased deforestation in the area has caused the extinction andisolation of many populations (Cowlinshaw and Dunbar, 2000).

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In comparison, Squirrel Monkeys were more frequently recorded in Young Secondary forest across bothseasons and were seen to tolerate and even thrive in moderate levels of forest disturbance where theyutilised the mid and lower forest levels. They also prefer to spend more time in partially logged areasand secondary forest (Boingki et al., 1998) where their preferred food sources (Cecropias (Cecropia spp.),legumes (Inga spp.) and black pepper relatives (Piper spp.) occur in abundance along forest edges androadsides (Garguillo et al., 2008). They may also feed on arthropods which are often more abundant inmore disturbed habitats such as secondary forest (Stone, 2007). These food sources may help SquirrelMonkeys thrive in secondary forest. Even though they generally prefer secondary, more built up areas,for the aforementioned reasons, the survival rate of Squirrel Monkeys in agricultural monocultures is nothigh.

Howler Monkeys were recorded most frequently in Young and Mid Secondary forest. This contrastswith a study conducted by Stoner (1996) focussing on 2 troops at La Selva Biological reserve in north-eastern Costa Rica who found preferences for primary forest and riparian habitat, not secondary forest.This was due to the troop’s spending the most time in habitats that contained the highest density oftree species most common in their diets. They specialised on particular habitats and species withintheir territories as these were resources with which they are familiar (i.e. avoidance of unpalatable/poi-sonous foods) (Stoner, 1996). This leads to the question that perhaps the troop’s observed in the currentstudy are choosing to focus on Young and Mid-Secondary forest over both seasons due to food preference.

The majority of their diet consists of Young leaves (when in season) that contain fewer toxins and morecellulose than mature leaves but higher amounts of protein (Wainwright, 2007). Even though they sup-plement their diet with flowers, older leaves and fruits, most of it consists of figs (Ficus spp.), Carneasadas (Andira inermis) and guapinols (Hymenaea courbaril) (Cristobel-Azkarate et al., 2005). Eventhough they were predominantly observed in Young and mid secondary forest, Howler Monkeys are ableto exploit all four forest types as these plant species are not specialised and occur across the range, therebyallowing the Howler Monkeys to move between forest types as different food sources come into season.As well as the ability to utilise multiple food sources, they also require less space. Despite this, however,many populations have become reduced and isolated due to habitat fragmentation (Keyghobadi, 2007).As with the Squirrel Monkey, fragmentation has also reduced the intra-group migration of individualsresulted in lowered genetic diversity (Skryinyer, 2016). It has also been eluded to that Howler Monkeysand their food plants may be negatively impacted by wind and sun within forest fragments (Wainwright,2007). This causes dirt and dust from barriers, such as roads, to accumulate on leaves. The monkeysconsume the leaves and over time the dirt/dust layer causes tooth erosion (Wainwright, 2007). Even thebiology and physiology of the Howler Monkeys themselves has been impacted by fragmentation as it hascaused them to become smaller and troops living within forest fragments have less Young than thoseliving in Primary forest (Wainwright, 2007).

Further Study

The data collected so far shows how detection frequency can be influenced by the time of day, forest typeand activity levels of the primates. More frequent surveys in the middle of the day could allow futureFrontier volunteers to further investigate the driving factors for primate sightings. In addition to thisit would be beneficial to assess the effects that other factors such as the weather, water availability andtree preference, have on primate detection.

This study did not consider the differences in the transitional phases between the wet and dry seasonswhereas Boinski (1987) suggests that this should be taken into account in future studies.

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6.3 Investigating the Habitat Preference of the Riverside Wren (Thryotho-rus semibadius), an Endemic and Data Deficient Bird Species

6.3.1 Introduction

Due to its unique location, climate zones and topography features, Costa Rica is well- known for its richbiodiversity, especially birds (Herzog et al., 2002). According to the second edition of the Birds of CostaRica (Garriguez and Dean, 2013) there are currently 903 avian species separated in 82 different families.Being part of the Southern Pacific lowlands, the Osa peninsula possess one of the largest intact stretchesof forest and is currently a home to at least 375 bird species (Barrantes et al., 1999). From them, 18species are listed as endemic. However, this exceptional avian diversity is currently facing heavy an-thropogenic pressure primarily in the form of deforestation and forest fragmentation (Sanchez- Azofeifaet al., 2002). Nowadays only 39% of the territory of Osa peninsula is protected under the authorityof Corcovado National Park, however the forests in the periphery of the park do not benefit from theprotected area status. The most severely affected zones are the primary forests. Just outside CorcovadoNational Park they are currently reduced to only 44% of their original size (Sanchez- Azofeifa et al. 2002).

Deforested and fragmented areas in tropical regions have received little attention from researchers. Oneof the few surveys conducted in such habitats were those held by Sekercioglu et al (2007) and Stiltes(1985). According to their results, it was estimated that nearly 75% of all native Costa Rican birdsmake use of heavily impacted areas to at least some extent, provided that some canopy trees and forestpatches remained. These species were classified as interior- and edge species. The former are knownto be more sensitive to forest fragmentation, while the latter benefitted from zones with anthropogenicimpact (Berg, 1997). Little is known however about how this ever- changing environment could affect theavian communities on Osa peninsula. This, coupled with the fact that many species are data deficient,highly endemic and not extensively studied makes assessment and future prediction of their populationsize extremely different.

A Typical example of a data deficient as well as endemic species is the Riverside wren (Thryothorussemibadius). The geographical range of this species runs from the Pacific slopes of Southern Costa Ricato the Chiriqui province of Western Panama. Its preferred habitats are lowlands from sea level up to 1200m (Skutch, 2001). As Dr. Skutch (2001) previously noted, Riverside wrens preferred tangled vegetationalong the edges of water bodies in disturbed areas, although rivers and streams themselves are not one oftheir food sources. Wrens tend to forage in tangled vegetation with secondary undergrowth, similarly toother species in the same genera, without showing any particular preference for streams (Skutch, 2001).T. semibadius however demonstrated great preference for vegetation patches with enough sunshine pen-etrating into the woodland.

Furthermore there is very little information about the distribution and abundance of T.semibadius globalpopulation. Stotz et al. (1996) have suggested that Riverside wrens are uncommon and not evenly dis-tributed throughout their range. However, this is difficult to prove, as there are no available studieswhich have focused on and assessed the level of anthropogenic impact on their natural habitats (IUCN2019).

Thought to be common in areas with dense vegetation within humid wetlands and forests (Cornell, 2019;IUCN 2019; Skutch, 2001), only one detailed study about Riverside wren’s ecology has been publisheduntil this day. In his study Skutch (2001) summarised the observational records spanning over a periodof over 60 years. Although this study gives us an important and detailed insight into the biology andecology of T. semibadius, it still lacks proper assessment of the habitat preference by this species. Inorder to gain a better understanding of the abundance and habitat preferences of this species withinpopulated areas, more quantitative analysis of these parameters is needed.

The main purpose of the current study is to investigate the abundance of the Riverside wren (Thryotho-rus semibadius) over a range of vegetation types and estimate if particular factors within its habitatcould be used to predict the presence of individuals. According to Temple and Wiens (1989), studyingbirds outside the borders of protected areas (in this case Corcovado National Park) would enable us toestimate the impact of long term environmental changes.

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6.3.2 Methodology

The primary target species of the Frontier’s bird survey and current report is the Riverside wren, asmall bird (13cm) listed as an endemic species to Costa Rica and Panama and continues to be frequentlyspotted on some trails within our survey area. Its striking plumage: barred black and white underparts,rufous upperparts, as well as its melodious, fast flowing song calls makes this song bird an easily identi-fiable species on surveys even by those with limited field experience, prior to joining the project.

Survey Protocols

Surveys are conducted using the point- count survey method, broadly used technique in the tropics(Bradford et al., 1998; Sanchez- Azofeifa et al., 2002; Henderson and Adams, 2010). Observers standat a single point and rotates in a circular motion, recording any birds they see. Currently, surveys areconducted on 14 trails in Corcovado National Park. Along the trails, a survey is conducted every 200mstopping at 1000m. In total, this makes up 56 different survey sites. When a bird is sighted, the surveyorwill record it as in one of three distance bands: Z1=10m from the observer, Z2=10-30 m and Z3≥30m(Figure 10).

Figure 10: Theoretical detection zones from the survey centre point (green cross) when astudy species is identified. Blue line represents Zone 1:<10m, Orange line represents Zone 2:10<30m, and Grey line represents Zone 3: ≥30m.

Surveys were run approximately 4 times per week. During a survey, research assistants would aim tomake as minimal noise as possible to prevent disturbing the target species.

Our surveys coincided with the dawn chorus to increase the likelihood of bird encounters. Once arriv-ing at a survey site, we would have three minutes settling period before beginning the survey, in orderto allow any birds to become accustomed to our presence. During the 15 minute survey effort mainlyprimary and secondary vocalisations but also visual observations were mainly taken into consideration,along with fewer/rarer visual observations. The exact time of identification, the species, the zone bandand the type of detection were also recorded. Other data, such as GPS coordinates, altitude, trail pointand names of the participants were recorded on the following sheet:

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Figure 11: Outline of datasheet used on all avifauna field surveys.

AnalysisSimilarly, to the previous bird counts, Riverside wrens were recorded in all zone bands, however indi-viduals from Zone 3 were excluded from further statistical analysis. Tropical zones are highly diverseenvironments with varying environmental conditions, where factors such as altitude, density and habitattype can vary greatly even within a very short distance. If a wren is heard anywhere near to the surveypatrol, the habitat in which the bird was recorded could be completely different than the one in whichobservers are situated. Therefore, only wrens within Zone 1(>10 m) and Zone 2 (10-30m) were consid-ered for further analysis, while individuals recorded as in Zone 3 were simply included in our tables asoverall information. In order to estimate the significance on how physical components are linked to theincreased numbers of Riverside wrens a General Linear Regression Model was run using the software forstatistical analysis ‘’R Studio”, version 3.3.2.

6.3.3 Results

Abundance

As with the previous report (CBP 194) our current work on the Riverside wren would continue to focuson its overall abundance throughout different vegetation types, rather than on total number of birdsrecorded per given transect. We adopted this approach because tropical habitats are complex systemsthat vary greatly in terms of vegetation type, landscape composition and altitude, therefore even withinthe same transect differences in all these components could occur, thus leading to a bias in our results.

The results published in this section represent the data collection from April 2018 until present. Beloware given the total number of Riverside wrens detected on all surveys throughout the main four vege-tation types. The largest numbers of T.semibadius was recorded on transects with predominantly Mid-secondary vegetation types, (n=73) closely followed by disturbed transects with Young- secondary vege-tation (n=70). Trails with Primary forests delivered the third highest abundance level (n=24). The leastnumber of recordings came from transects with vegetation cover currently listed as “Unknown” (Table 8).

Table 8: The total number of Riverside wrens recorded per vegetation type.

Vegetation Type Total N ofsurveys

Zone1

Zone2

Zone3

Total River-side Wrens

Primary 75 4 17 3 24Young Secondary 52 15 28 27 70Mid-Secondary 80 22 36 15 73Unknown 20 4 8 6 18

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Detection Rate

This section represents the overall detection rate of Riverside wrens per survey effort. To calculate thedetection rate, we divided the number of surveys with recorded wrens by the total number of surveys heldsince April 2018. Although the highest total detection rates were recorded on transects with unknowntypes of vegetation (65%), the highest values were detected on trails classified as ‘’Young- secondary”,followed by those with mid- secondary. The lowest values were recorded on transects with primary forestcover- 18.7% (Table 9).

Table 9: Detection rate across habitat type and zone.

Type of Vegetation Zone 1 & Zone 2 Total with Zone 3Primary 18.7% 20.0%Young Secondary 53.8% 63.4%Mid-Secondary 43.7% 55.0%Unknown 40.0% 65.0%

Habitat Preference

In order to estimate which factors influence the abundance of Riverside wrens, we ran a general linearregression model on R Studio version 3.3.2 in which we included transects with primary and secondarytypes of vegetation, as well as generalised values for their physical components which we believe could belinked to the habitat preference and general abundance of our target species. Transects, with vegetationcurrently listed as ‘’Unknown” were removed from further analysis, as well as all birds recorded in Zone3. Below is seen the summarised data of our regression analysis (Table 10). From all tested variables onlythree components showed significant values (P>0.1) and could be linked to the abundance of Riversidewrens on our study trails. Small trees with a diameter below 5 cm listed here as ‘’treelets” and fallen logswere the variables with the most statistically significant values (P>0.01) closely followed by canopy cover.

Table 10: Detection rate across habitat type and zone.

Model Species Physical Components p-value (chisq test)Riverside wren Canopy cover 0.078155

Treelets 0.004214Fallen logs 0.004233

6.3.4 Discussion

Total Abundance and Detection Rate

The largest number of T.semibadius (n=73) was recorded on transects where Mid- secondary type of veg-etation was in dominance, closely followed by trails with primarily young- secondary vegetation (n=70)in all zone bands. It is important to note however, that the larger number of wrens detected on tran-sects containing mid- secondary vegetation was due to the considerably higher survey effort that wascarried on trails containing Mid- secondary vegetation compared to those with Young- secondary veg-etation (see Table 8). The observed pattern clearly back the sixty years long observations of Skutch(2001) where Riverside wrens were detected in wetlands and forests with dense undergrowth. Habitatssuch as these contain great abundance of various invertebrate taxa, which in return provide an excellenttrophic base for our study species. Therefore, it is not surprising that transects with primary forests andthose with vegetation currently listed as ‘’Unknown” type yielded the least numbers of Riverside wrens.Although transects with primary forests yielded the third highest number of our target species, it is im-portant to take into consideration the high number of surveys taken on trails with this type of vegetation.

Contrary to the numbers of total abundance, detection rate produced its highest values from trails withpredominantly young- secondary type of vegetation. Our trails, falling in this category contain a largenumber of small trees and saplings, with dense undergrowth and tangled vegetation. Most importantly,

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those trails are in close proximity to water courses- rivers and a freshwater lagoon. This is anotherfinding that supports the observations of Dr. Skutch Transects listed as ‘’Unknown” type of vegetationproduced a high detection rate for Riverside wrens. However, due to the small number of surveys carriedalong those trails and the unidentified type of vegetation, the data is recorded for informative purposes,rather than as conclusive. Overall, in order to understand what role these vegetation types play in theRiverside wrens abundance, detection rate and draw conclusions we need to carry more surveys.

Habitat Preference

The highest numbers and detection rate of Thryothorus semibadius was recorded on trails with sec-ondary types of vegetation. However, it is unclear what habitat components and topographic featuresare preferred by the population of Riverside wrens, found in Carate. Although our sample size is notlarge enough, the data we have is still sufficient to run a general linear model and test different habitatvariables that are likely to attract a larger number of Riverside wrens. Our results clearly demonstratethat some of the physical components found within those transects actually play a major role in thechoice of habitat for T.semibadius. The most significant value was delivered from trees with diameterless than 5 cm, collectively respectively called, -treelets-“. Knowing what habitat types are preferredby this wren species (Skutch 2001), it is not surprising that saplings and small trees are most favoured.They provide shelter and foraging grounds for various types of arthropods, which are the preferred fooditems of Riverside wrens. Additionally, tangled undergrowth vegetation and small trees provide excellentroosting and nesting sites for T.semibadius. The conclusion stems not only from Dr. Skutch’s excellentwork, who observed them nesting 1-3 m above the ground, but also from our personal observations duringsurveys. While running an evening Amphibians and Reptiles survey we came across one of these wren’s.We spotted the sleeping bird inside and the nest itself was situated 1.5m above the ground on a shrubnext to a river, which dries out completely during the dry season.

The second most significant physical component was fallen logs (and other similar woody material). Asit is known, many invertebrates feed on and use this type of debris for shelter, but also entire life cyclesof many species also require such woody debris. Undoubtedly the Riverside wrens in Carate benefit fromthe presence of fallen logs and rotten stems for feeding.

Lastly, Riverside wrens seem to prefer habitats with a developed canopy cover. At this stage it is unclearwhat role this factor plays in the life and habitat preference of T. semibadius and why they prefer zoneswith enclosed canopies. However, as canopy cover tends to offer shelter for small birds and other animalsagainst predators, it is likely that Riverside wrens could benefit from habitats featuring this character-istic throughout their range.

6.3.5 Conclusions

While the largest number of Riverside wrens was recorded on trails with mid- secondary type of veg-etation, due to increased survey effort, the highest detection rate was observed on trails where thepredominant plant cover was young- secondary. Our results support the observations of Dr. Skutch(2001) T.semibadius are found in habitats with dense vegetation cover. The factors positively correlatedwith target species abundance are trees and saplings with diameter less than 5 cm, fallen logs/branchesand high level of canopy cover. Although our results already provide some insight into the ecology andhabitat preference of this data deficient species in the Carate area, a larger sample of birds is neededbefore being able to draw definite conclusions on the aims and objectives of this project.

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6.4 Variations in Amphibian and Reptile Abundance and Density due toChanges in Season and Habitat Age and the Utilization of Microhabitatby Anole Lizards.

6.4.1 Introduction

Herpetofauna contains all of the world’s amphibians and reptiles. Globally amphibians and reptilesplay highly important roles in ecological processes as they occupy a wide range of niches such as seeddispersers, predators and grazers therefore, herpetofauna act as bio-indicators for environmental health(Folt & Reider 2013). Amphibians and reptiles play highly important roles in ecological processes, oc-curring in high densities and are omnipresent in forest food chains (Bell & Donnely 2006 Over recentyears 43% of species within the study orders anuran and squamata have suffered population decline. Insome studies, amphibian populations have been reduced by 75% since 1970. Whitfield et al. (2016) de-scribed, in Costa Rica and Panama, a 50% decrease in species richness and 80% density decrease withinsix months. It is estimated that over 120 species of Amphibians have gone extinct within the last 50years. Pristine environments contain an overwhelming amount of biodiversity. Many of the amphibianand reptile population declines have occurred within pristine environments making these populations aconservation priority (Whitfield, 2007).

Costa Rica or the “rich coasts” deserves its name in no taxa more so than the amphibians and reptiles:retaining 147 species of frog and toad, 53 species of lungless salamander and 7 ancient creatures in theform of caecilians belonging to the amphibian family. Comparably 245 reptile species comprising of 2crocodiles, 5 marine turtles, 9 freshwater turtles, 88 lizards and 141 snakes (Leenders, 2019). Deforesta-tion is one of the biggest concerns facing tropical ecosystems. Central and South America currently havethe highest rates of deforestation. (Folt, 2013). Anthropogenic habitat modification has affected 75.2%of amphibians in Central America (Whitfield et al., 2016). Couple this with the fact that amphibianspecies are most at risk from changes in the environment due to their dependence on the immediateenvironment. The amphibian populations are expected to undergo a rapid decline in species diversityand abundance in these areas (Folt & Reider, 2013). Both groups have been compared to “canaries ofthe coal mines” due to their supposed susceptibility to environmental change (Urban et al., 2014). Thereis a large concern as all this is occurring in an area with high levels of biodiversity, with roughly 55%more endemic species in Central America than Mexico despite being 3 times the size (Bohm, 2013).

It has been shown using Environmental Service measures (Johnson et al., 2015) that one in five reptilespecies are threatened with extinction. Moreover, a similar percentage of reptiles are data deficientmeaning a vast amount of research and conservation action is still needed (Johnson et al., 2015, Whit-field et al., 2007). Several species in this group are indicators of a healthy ecosystem as they have veryspecific environmental and habitat requirements. Salamanders for example, are extremely vulnerable tosubtle changes in the environment such as temperature and soil pH (Caruso, 2014). This one would hopewould shift funding and focus into the most valuable indicator species to better understand and provideevidence for climate change and best protect ecosystems not just individual species.

Our study of herpetofauna density, abundance and diversity aims to understand the population trendand any potential causes of population decline. Costa Rica has undergone significant environmentalchange over the last 50 years. To acquire an understanding on whether herpetofauna are able to adaptto the environmental changes creates the ideal study system to illustrate the biological and evolutionaryprocesses underlying speciation (Folt & Reider, 2013). Wildlife inventories are an essential conservationtool and are important for selecting priority sites for potential population extinctions, understandingconservation status of certain species, aiding in conservation planning and prioritising areas that needeither conserving or restoration (Santos-Barrera et al., 2008). The study takes place on the Pacific Coastof the Osa Peninsula on the Southern edge of Corcovado National Park. The trails used in the studyinclude disturbed forests, secondary forests, primary forests and roads lined with degraded forest. Ourseparate habitat study enabled us to classify the habitat surrounding the trails. (Project 6.1).

Climate change is a major concern for reptiles and amphibians. Whitfield et al. (2016) explained the“climate-linked epidemic hypothesis”, suggesting severe outbreaks of diseases, such as the Chytrid fun-gus, causing the extinction of species like the famous Monteverdi Golden frog in 1989 (Leender, 2016).The temporal part of the study will provide an insight into seasonal, yearly and even monthly changes

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in temperature, humidity and weather patterns. This study has the potential to provide importantinformation on the impact of climate change on herpetofauna populations. Due to the unique naturalhistory of the Osa Peninsula it is extremely important to understand any changes in the environment sothat effective and efficient measures can be taken to preserve the animals and ecosystems.

The ability to take a closer look at how individual species utilize their habitat provides a much clearerunderstanding on what habitat variables play influential roles in the abundance of various species. It isnot only very important in the locomotory behaviour of the lizards as different structural elements posedifferent functional demand influencing ability to escape predation for example but more relevant to thisreport is the ability to understand what habitat elements are most relevant to certain species indicatingwhat and how they use preferred habitats (Vanhooydonk et al., 2006). This report will focus on the Osaanole as this endemic species is data deficient and the most frequently encountered species on the surveys.

6.4.2 Methodology

Survey Area

Surveys were carried out on our thirteen different trails: 3 Ajos Beach, Camp Trail, Trail Verde (inthis report the name ‘Gary’s Land’ is also used), Gary’s Lower, Golden Ridge, Laguna Vista, Leona,Los Aves, Luna, Puma Creek, Road, Shady Road, Shady Trail, Waterfall see Table 3. Visual encountersurveys (VES) were used, as this is the most efficient and one of the most widely used methods forsurveying tropical herpetofauna (Laurencio, 2009).

Survey Protocols

Surveys began from 07:00 in the morning and 20:00 onwards and consisted of a 400 meter transects withthe survey paused at each amphibian or reptile sighting for data recording. At least two individualsparticipated in each survey. If possible, the survey would be conducted in a single file and all observerswould look at both sides of the trail. In some circumstances, due to the variation of trail width, the groupwas required to split into two, covering each side separately. Due to observing camouflaged and elusivespecies, surveyors were encouraged to walk at a slow pace, and in addition, to minimise disturbance,scanning leaf litter, shrubbery and trees for any Herpetofauna. The following data points are recorded onsite; Time, Species, Group size, GPS, Distance from trail (m), Height off ground (m), Substrate type anddiameter. Following the survey, any animal that could not be identified in the field were photographedand identified using field manuals on camp.

Climate

Costa Rica has two seasons. The driest months of the year in the Osa Peninsula are January, Februaryand March, with the wetter ones being May through to December, with September and October gen-erally being the wettest months of the year, despite this 2019 was a relatively dry year with the el Nioeffect reducing the amount of rainfall. Temperatures are always high: the hottest month tending to beMarch where temperatures can reach 30; the cooler ones October and November where they hover justunder 25 (Figure 12). On average, March is the sunniest time of year; while June experiences the leastsunshine (Figure 13).

The temperature and sunlight hours in Carate, Puntarenas, Costa Rica, does not vary dramatically allyear round. The average temperature in the hottest month does not exceed the average temperature inthe coldest month by more than 5 degrees centigrade (Leenders, 2016). They do not have the typicaltemperate four seasons; their relative changes in weather, temperature and hours of light don’t fluctuateto the same degree. A dry season and a wet season however have a significant impact on the quantity ofmonthly rainfall (Figure 14). This can have a dramatic impact on the flora and fauna in the region asthe sudden heavy rains refill dried rivers, lagoons, lakes and other wetland environments and ecosystems(Alho, 2008). With this in mind, it could be expected that separate sets of flora and fauna could beseen with strikingly different adaptations for the dry environment and then separately for the wet envi-ronment. It would also be expected that the transitional periods would show the most diversity (Junk,2013; Shvidenko, 2013).

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Figure 12: The maximum and minimum temperature between January 2018 andDecember 2018 in the Puntarenas area of Costa Rica that includes the Osa Penin-sula where all surveys are carried out. This graph has been taken. Available fromhttps://www.worldweatheronline.com/carate-weather-history/puntarenas/cr.aspx.

Figure 13: The average hours of sunlight in Puntarenas, Costa Rica between January2019 and December 2019. This graph has been taken. Available from https://weather-and-climate.com/average-monthly-Rainfall-Temperature-Sunshine,Puntarenas,Costa-Rica

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Figure 14: The average rainfall in mm within Carate between July 2019 and January2020. This graph has been taken. Available from https://www.worldweatheronline.com/carate-weather-history/puntarenas/cr.aspx

Data Analysis

This report uses an extract from our long-term datasets, only from the 8th Augustl 2019 until 13th Febru-ary 2020 will be used for the results. This dataset has been selected to compliment previous reports butalso provide a stronger understanding of the seasonal variation for both animal groups. Results of am-phibian and reptile surveys were analysed separately, as their ecology, physiology, behaviour and habitatpreferences differ. For the amphibian taxa we found Anura species (frogs and toads) and an individualsalamander. For reptiles we found only Squamata species (snakes and lizards). The total encounter rate,and Simpson’s diversity index were calculated for each of the forest types and each taxa (amphibians andreptiles separately). A Simpson’s diversity index is a method of calculating species diversity that takesinto account both the number of species present and the relative abundance of each species (Morris,2014). It is calculated using the formula D =

∑(n/N)2, where n is the number of individual species

found, N is the total number of all encounters, and D represents a diversity index. D can take any valuebetween 0 and 1, where zero represents lower levels of diversity and 1 represents complete diversity (thereis an equal number of all species detected). The average diameter of substrate utilised was collected forall arboreal amphibians and reptiles. This substrate analysis for this report will focus on the Osa Anole(Anolis osa) as a commonly encountered species, this species has previously been analysed in reports butthere is now a considerable pool of data to draw some accurate conclusions about the specific roostingutilization of this anole species. These habitat values were taken across all surveys of each particularforest or group and used for statistical analysis. All data analysis was completed using Microsoft Excel.

6.4.3 Results

Total Encounters

Across the study period between 8/08/19 and 11/02/20, 806 herpetofauna were found, 200 more thanthe previous report in December. Throughout the study period 452 encounters were reptiles and 354encounters were amphibian. There were a total of 40 species of herpetofauna consisting of 23 reptilespecies and 17 anuran species. Figures 15 & 16 and 17 & 18 show the number of encounters for reptilesand amphibians respectively. The most frequently encountered species was the Osa Anole with 316 ofthe 806 encounters.

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Figure 15: Total number of amphibian encounters from August 2019 to February 2020 acrossall of the amphibian and reptile trails.

Figure 16: Total number of amphibian encounters from August 2019 to February 2020 acrossall of the amphibian and reptile trails.

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Figure 17: Total number of Reptile encounters from August 2019 to February 2020 across allof the amphibian and reptile trails. Describe using a logarithmic scale to account for the highproportion of Osa anole encounters.

Figure 18: Total number of Reptile encounters from August 2019 to February 2020 across allof the amphibian and reptile trails.

The Simpson’s diversity index (SDI) shows a lower diversity in reptile than amphibian populations.Amphibians have a 0.3 higher diversity which is considerably higher compared to the previous reports(Figure 19).

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Figure 19: Simpson’s diversity index for all encounters of amphibian and reptile species acrossthe study site, using all 13 trails over the 6 month study period.

Encounters and Diversity Across Forest Type

The highest amphibian and reptile densities were observed in the mid secondary forest trails (Figure 19).Amphibians showed a more significant decrease in Mid secondary trails compared to reptiles, but bothhave the lowest density in Primary forests (Figure 20). The Simpson diversity index displays a peakvalue in mid secondary. However, amphibians displayed an almost equal value, highlighting that thesehabitats are our most evenly distributed and biodiverse habitats compared to the young forest. Reptilesillustrate a much more comparable level of biodiversity in both primary and Young secondary habitats.There is a significant increase in biodiversity in Mid secondary habitats. (Figure 20).

Figure 20: Density per meter for both amphibians and reptiles per trail within each differenthabitat type; young secondary forest, mid secondary forest and primary forest.

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Figure 21: Simpson’s diversity for both amphibians and reptiles across all habitat types. Avalue between 0 and 1 visually describes the differences in diversity between each other acrossall degradation levels.

Substrate Utilization and Average Diameters

This substrate analysis focuses on the Osa anole (Anolis osa). The majority of encounters are arborealbetween both stem and leaf making the two most commonly observed substrates (Figure 21). The leafwas the most commonly used substrate with 104 Osa anole encounters.

Figure 22: Number of encounters for each substrate type utilized by Osa Anoles.

The tree represents the greatest diameter averaging 41.8cm compared to the smallest being the vineaveraging 0.2cm. They make up the least and second least encountered substrates (Figure 22 & 23). Themost commonly encountered substrate leaf had an average diameter of 7.1cm, a significant difference tothe second most popular substrate stem, which was on average 6.3cm smaller.

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Figure 23: Average substrate diameter in centimetres m across the most commonly utilizedarboreal substrates by the Osa Anoles.

6.4.4 Discussion

Costa Rica’s diverse and abundant herpetofauna has endured significant pressures from habitat destruc-tion, climate change, water and air pollution and the presence of non-native species. This along withcollateral damage from an increasing human population and economic pressures on a developing country(Leenders, 2016). Consequently, having potentially devastating effects on animal populations, as seen inmany examples throughout a variety of vectors, most notably in the form of the chytrid fungus (Whitfieldet al., 2016; Leender, 2016). With this being said, Corcovado and the surrounding areas such as Carateare providing a stronghold as there are abundant and diverse endemic species populations (Figures 15-18). Amphibians and reptiles are highly vulnerable to environmental change. 43% of all amphibians arein a state of population decline due to their high sensitivity to environmental change.

During the course of the study two more amphibian species were encountered compared to the previousreport. However, there was a decrease in reptile species richness as one less species was encountered.Pacific litter frogs being one example of a increased density than described in previous reports (Figures15-18). This is potentially down to the ability for us to observe some of the rain dependant canopydwelling species that usually are much harder to observe outside the rainy season such as the glass frogfamily. The Osa anole is thriving within Carate and Costa Rica due to its generalist nature givingthem the ability to adapt to a changing environment; deforestation and fragmentation (Figure 17). Thishighlights the productivity of successional forests for some species that normally wouldn’t occur in suchdensities, this is positive, as it is clear to see an abundance of certain species in secondary habitats ofwhich most of our trails are. Despite this the potential for monopolization from certain species hasbecome increasingly apparent. Monopolization can be a sign of a new or imbalanced ecosystem withgeneralists dominating the available niches most likely caused from anthropogenic interference. Evenwithin anoles, highly territorial family that are comfortably the most commonly encountered reptileson our trails (Bohn et al., 2013). Some charismatic and updated identification described in this reportincludes; the introduction of the Pygmy Rain Frog that may have previously been misidentified as ajuvenile Slim-fingered Tree Frog but now is a valuable part out our total encounter charts (Figure 16).From a reptile perspective the charismatic introductions for the Red-eyed Tree Snake and the PacificTree Boa have been personal favourites as two snakes that are not commonly encountered and make thelate night for volunteers and staff increasingly worthwhile.

The Simpson Diversity Index has seen a significant increase in the gap between reptiles and amphibians.Reptile diversity has decreased in the wetter months compared to amphibians which had an increase indiversity with 2 more species included in the data. This is most likely explained with the beginning of

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some elusive species that are much easier to observe during the rainy season. The species descend fromhigher latitudes to lay egg clutches next to fresh water sources which are located near some of the studytransects. The continued proportional increase in Osa anole observations compared to the last reporthas reduced the SDI value for reptiles significantly.

Density per Meter and Diversity Across Forest Type

Costa Rica is unique in its recovery story of anthropogenically-altered habitats. It is estimated that 40%of its land was being utilised for agriculture in the 60s Sanchez-Azofeifa et al. (2002). It is documentedthat as of 1997, only 44% of the forest remaining on the Peninsula was mature and the majority ofthe forest located outside Corcovado National Park has been altered by anthropogenic activity. As aresult, large amounts of forest fragmentation have occurred causing significant changes in the ecosystemcomposition. Over recent years, there has been a huge focus to restore Costa Rica’s natural spaces

Certain species have had to adapt to the surrounding pressures arising from the changes of a succes-sional forest (Murcia, 1995). The highest density per m of amphibian and reptiles in Carate were inmid secondary forests. Density decreased for both groups in Primary and young secondary forests (Fig-ure 21). The relationship shown in Table 5 in the habitat section (Project 6.1) of this report betweenyounger forests and greater density of vegetation in the first 2 meters in the herb and shrub layers, thisprovides more available substrate for species such as the Osa anole which are commonly encountered inthe secondary forest types. This decline may also be partially due to survey limitations, the number ofcanopy and leaf litter species that are notoriously found in primary forest are considerably harder to ob-serve and encounter. Furthermore, the lack of available understory substrate and unobserved individualscontribute to the significantly lower encounter rate within this habitat type. There was a reduced efforton nocturnal survey efforts on the primary forest transect (Leona). Encounter rates of amphibian andreptiles were higher during nocturnal surveys across the other study transects. If nocturnal surveys wereto increase on primary forest transects then we would expect to see a much higher density and diversityvalue for the herpetofauna data set.

Certain generalist amphibian species, such as Cane toads and Common rain frogs have monopolizedthese young secondary habitats and out compete other species. This could explain the higher densitiescompared to other species recorded in this study (Figure 20). Simpson’s Diversity Index describes thehighest values for amphibians in both primary and mid secondary habitat (Figure 21). This may be dueto certain limitations such as elevation and reduced nocturnal surveys as mentioned previously. However,young secondary habitat has a significantly lower biodiversity with only a few species dominating thehabitat. With a wide variety of organisms coexisting with one another and occupying every availableniche. It is probable that there is a high amount of interspecific and intraspecific competition resultingin a great equilibrium of fluctuating population sizes in mid secondary habitats. This notable changefrom previous observation in amphibians is almost certainly linked to their reliance on bodies of waterand the center of the study period fall in the wettest months of the year (Figure 14).

The Reptile diversity results are what we would expect to see across the forest types, as mid secondaryhas the widest range of niches and microhabitat environments providing the greatest potential to accom-modate a large number of species (Scheffers et al., 2014). The vast majority of the common species wefind are highly generalized and highly adaptive to subtle changes in the environment (Cates & Orians.,1975). Secondary succession is very much involved within this forest type meaning that a wide range ofplants can become established in the community. A combination of colonist species and climax speciescreates a wide range of niches and substrate types for species to exploit (Horn, 1974). The majority ofencounters recorded were found in the leaf litter. Amphibian species seem less territorial in these areascompared to lizard species. Male dominance is generally considered important in controlling a territorywithin lizard species. In contrast to amphibians, which are more comfortable, inhabiting smaller spacesin much larger numbers.

Substrate Utilisation and Average Substrate Diameters

Anoles are one of the most common reptilian inhabitants across all of Costa Rica, occupying many dif-ferent niches across the majority of the eco-regions from leaf litter species to canopy dwellers all fulfillingimportant roles in ecological processes (Bell & Donnelly 2006, Folt & Reider 2013). The Osa anole is a

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medium sized cryptic species. In addition to its wide range of morphologies for its effective camouflage,the Osa anole also has colour changing abilities, which makes it challenging to identify. A distinctivelylarge dewlap with striking red and yellow colorations is a great morphological feature, which aids theidentification of this species (Leender, 2019).

This substrate analysis gives us a better insight into the species’ ability to adapt to the changes inmicrohabitats and whether secondary forests can still provide diverse communities. Anoles typicallyuse explosive bursts of locomotion to escape predators and capture prey (Vanhooydonck et al., 2006)The Osa anole has become specialized for the secondary habitat and is thriving in great numbers withlittle predation (Figure 20). It spends the days hunting in leaf litter for invertebrates. The majority ofour arboreal observations occur during nocturnal transects when the anoles are utilizing small substratediameters to avoid predation (Figure 23). The most encounters occurred on stem and leaf substrates.This is aligned with our habitat data as greater shrub and herb layers are found in secondly habitattrails and decreases in primary (Project 6.1) where there is lower density of reptiles.

Claws alone are known to increase potential substrate utilization (Cartmill, 1974). The anoles utilise acombination of claws and adhesive toe pads to allow them to access a much wider variety of habitatswhich other reptilian competitors cannot access (Crandell et al. 2014). The van der waals force is thesame one utilized by geckos. The combination provides optimal adhesive properties when on smoothsurfaces but when on irregular surfaces the claw comes into its own interlocking against the surface. Leafand stem were the two most commonly observed substrates (Figure 23). One explanation for this is thatthe majority of anole encounters occur in secondary forest where there are high levels of herb and shrublayers (Table 6). These layers give them perfect roosting locations. The small substrate diameter meansthat the branches and stems cannot support the weight of a predator, comparable to the chameleons ofMadagascar being able to escape predation due to the hand morphology allowing them to roost in safetyon small stems. The leaf has a very low load capacity making it hard to hold the predator and preyhowever, this makes predation avoidance much harder for the prey (Figure 22).

6.4.5 Conclusion

Due to the fluctuation of both biotic and abiotic factors influencing amphibian and reptile populationsin the successional forest. The dominant species tend to be generalist species that have adapted tomonopolize a particular ecosystem. This generally results in a lower diversity being observed. Moreniche and specialist species, those are ideal for primary forest being more evenly distributed in speciesrichness density. We have observed a wide range of species in this time frame and the datasets continueto highlight the importance of these trails irrespective of its degradation level.

Mid secondary has produced the most densely populated habitat for both amphibian & reptiles provid-ing an ideal habitat for those generalist species but also having a greater enough variation in habitat toprevent monopolisation from certain species which are common in degraded habitats. A great exampleof this is seen in Cane Toads, which represents a large proportion of encounters within young secondaryhabitats. Cane Toads are documented as being very dominant in degraded habitats. Although bothamphibians and reptiles are dominated by some generalist species, there are still wide varieties of nichesfor species to inhabit.

The Osa anole is a perfect generalist species, perfectly adapted for successional forests and as the foresttends to age, trees grow higher and the amount of dense undergrowth vegetation seems to decrease. Inturn the Osa anole allows the predator prey balance to be restored and less dominance of one species isobserved. The substrate analysis suggests that herpetofauna rely heavily on shrubbery. The herb layersin the habitat provide shelter at night for diurnal species and for the medium-small sized anuran species;there is a heavy reliance on leaf litter and decomposing organic matter camouflage (Ernst and R odel,2006). Although the effect of substrate diameter on many biomechanical performances may be especiallyrelevant in arboreal habitats. There is currently no available data on substrate utilization and preferenceof the Osa anole. Furthermore, there is data deficiency on reptile and amphibian populations of the OsaPeninsula. Data collection on these species will continue to further the understanding of these speciesand study sites.

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For future work, more variables should be included into habitat data collection. Variables such as dis-tance from bodies of water this is one of the major factors that influences amphibian abundances asat some point in almost all of their life cycles they will need to interact with a body of water. Thiscan also be monitored annually and seasonally with regards to fluctuations in water level and thereforespecies abundances. Once all these habitat variables are taken into account monitoring this changingenvironment will provide a good example of a species model. The model can then be translated to otherareas attempting to re-establish forest habitats so there is a better understanding on the prediction ofbio-composition change during different levels of succession.

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6.5 Assessing and Improving Sea Turtle Predation and Hatching SuccessRates; A Study from Playa Carate, Costa Rica

6.5.1 Introduction

Sea turtles inhabit all of the world’s oceans and are considered integral to the ecosystems that theyassociated with (Eckert et al., 1999; Ossmann, 2019). They alter important habitats, such as seagrassmeadows, through foraging; act as source of prey and also maintain the balance of nutrient cycles (Bjorn-dal et al., 1999). Sea turtles are keystone species in their ecosystems whilst also being good indicatorsof coastal and marine environments. The oldest turtles are thought to have evolved 220 million yearsago in the Jurassic era and they remain some of the most primitive extant reptilians (Leenders, 2019).They have proven to be a resilient clade having withstood considerable environmental changes (Honarvaret al., 2008), something that is often contributed to their relatively unchanged morphology (Leenders,2019). Although at the height of their diversity over 30 species existed, only 7 are found today, all ofwhich are classified from vulnerable to critically endangered by the IUCN Red List (Abreu-Grobois &Plotkin 2007; Mortimer et al., 2007; Wallace et al., 2011). All sea turtle populations have recently seena rapid decrease due to many factors that limit their ability to sustain stable populations. The threatsinclude exploitation of eggs, climate change driven effects, marine pollution and increased coastal devel-opments (Honarvar et al., 2008; Fuentes et al., 2011; Tripathy & Rajasekhar, 2009; Dudley & Porter,2014; Camacho et al., 2017). Turtles are central to many beliefs and religions, such as Hinduism, andprovide income to many local communities through the up and coming trend of ecotourism (Ossmann,2019). In this way, the protection and conservation of sea turtles is in all of our best interests given notonly their ecological importance but also their socioeconomic value. Given the global distribution of thisthreatened group, international cooperation to ensure the survival of sea turtles is required.

Whilst the ultimate aim for any conservation programme is for the long-term survival of the populations,first and foremost, the major threats must be identified (Eckert et al., 1999). Three of the largest threatsto turtles are poaching for the illegal trade, climate change driven effects and predation of turtle eggs byintroduced species (Donlan et al., 2010).

Poaching of sea turtle adults, hatchlings and eggs is not uncommon in many parts of the world. Whilstthe eggs of all species are subject to poaching for consumption (Ossmann, 2019), it is the Greens andHawksbills that are most threatened at adulthood by poachers. Green turtles have traditionally beenhunted for their meat whilst Hawksbill shells are the most desired for making jewellery and ornaments(Campbell, 1998). This hunting has driven populations of both of these species to the brink of extinctionin the past and now both species are classified as critically endangered (Abreu-Grobois & Plotkin, 2007).All sea turtles are now internationally protected by law under part of the Convention on InternationalTrade in Endangered Species (CITES) meaning these practices are illegal in most places without excep-tional permits, and unethical everywhere (Chacon-Chaverri & Eckert, 2007; Eckert, 1999; Tomillo et al.,2008). Having said this, due to the limited resources and funds associated with sea turtle conservation,enforcement of these laws are difficult to enforce (Eckert et al., 1999) and therefore poaching still occursat unacceptable rates.

Unfortunately, the impact caused by poaching on sea turtle population is further exacerbated by preda-tion of sea turtle nests. Whilst predator-prey cycles are, obviously, natural and essential in all ecosystems,the problem arises from over-predation of natural species by introduced species. In the case of sea turtles,predation from foxes, badgers and domesticated dogs has drastically impacted the hatching success ofnests of all species (Fowler, 1979). In Costa Rica dogs from communities close to nesting beaches arethe largest consumer of turtle eggs, eating entire nests and if not, exposing eggs for secondary predatorssuch as birds (Burger & Gochfeld, 2014).

Climate change is by far one of the most concerning threats to sea turtle populations. Sea level rise andtemperature increases are affecting multiple aspects of sea turtle ecology (Korein et al., 2019). Nestinghabitats have already been lost for several populations such as the pacific Green turtles who nestedon low-lying beaches on the Maldives (Fish et al., 2005). This habitat loss forces nests to be laid inunfavourable nesting locations that more prone to tidal inundation, erosion or predation (Burger &Gochfeld, 2014). Increase of sand temperature affects the hatching success of sea turtles. This is becauseany sand temperature outside of the critical range, 22-35◦C, will always lead to stunted development oregg mortality (Wibbels et al., 1998). Sand temperatures above 35◦C have been seen all over the world on

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nesting beaches and are expected to be more common (Bezy et al., 2015; Santos et al., 2017; Howard etal., 2014; Pike, 2014). In those that are able to hatch in warmer sand, we expect to see a skewed sex ratioin turtle population due to temperature dependent sex determination in these reptiles. The higher thetemperature, the greater proportion of female sea turtles making future breeding more difficult (Hawkeset al., 2007; Valverde et al., 2010) as demographics become skewed.

All these negative impacts affect the 6 sea turtle species of Costa Rica, however the efforts for conser-vation projects have increased nationwide. Alongside international law, Costa Rica also enforces theFish & Maritimes Law of 1948, which prohibits the commercial capture and sale of marine turtles andeggs and the destruction of turtle nests (Campbell, 1998). Additionally the Promotion of AgriculturalProduction Law states that in during the mass nesting events exhibited by Ridley turtles known as the‘arribada’, eggs can be commercially harvested but restrictions are in place to mitigate the impact thishas on turtle populations (Campbell, 1998). Ecotourism drives government interest and funding for seaturtle conservation and has also increased the work between multiple organisations and local communi-ties (Fennell & Eagles, 1990; Chacon-Chaverri & Eckert, 2007). Given the time lag that is associatedwith sea turtles between intervention and population response (Bjorndal et al., 1999) it will be decadesbefore the effectiveness of these strategies can be truly evaluated both in and out of Costa Rica. A largeproportion of sea turtle conservation comes from protecting nesting females, their eggs and hatchlingson nesting beaches (Ossmann, 2019).

The study area, Playa Carate on the Osa Peninsula, Costa Rica has had relatively few sea turtle nestingstudies in comparison to other major nesting beaches further North in the Peninsula. Four species areknown to nest in the study area; Green turtles (Chelonia mydas), Hawksbills (Eretmochelys imbricata),Olive Ridleys (Lepidochelys olivacea) and Leatherbacks (Dermochelys coriacea). The primary threats toturtles on Playa Carate are predation, poaching and overheating.

In addition to sustaining the successes of the previous research conducted here, the primary aims of thisproject are:

� To utilise relocation techniques to increase the number of nests hatching.

� To investigate how an increased patrol effort can reduce predation and poaching rates.

� To observe changes in nesting between and throughout seasons.

� To determine the effect of temeprature on hatching success and incubation times.

� To assess patterns in activity to best predict peaks in nesting and improve monintoring strategies.

6.5.2 Methodology

Survey Protocol

Both morning and night patrols were carried out on Playa Carate beach from June 1st 2017 to February15th 2020. The beach is approximately 2.6km in length and is divided into 100m sectors (numbered1-26), each with four 25m sub-sectors (i.e. 1, 1.25. 1.5, 1.75). Morning patrols began every morningbetween 4:30am and 5:30am and night patrols took place 4 hours before high tide, giving the highestchance for turtle encounters. To minimise the disturbance to nesting females, survey teams were limitedto 6 people and only red lights were used when needed. Gloves were always worn when directly touchingeggs and turtles to prevent diseases or harmful substances being transferred from people to turtles andvice versa.

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Patrols

For every turtle track encountered during night patrols, the following data was collected:

� Patrol date.

� Start and end time of the patrol.

� Name of the patrol leader.

� The time the track was encountered.

� Sector number, always taking the lowest number (e.g. if observers are between sector 11 and 11.25,they will write down sector 11).

� Zone:

– Zone 1; Tidal inundation zone.

– Zone 2; Beach area, still within reach of the high tide.

– Zone 3; Vegetation areas, safely away from the high tide.

� GPS coordinates of the nest.

� Species: Identified either by turtle sighting or track.

� Activity (what the turtle was doing when first seen):

– Emerging

– Digging and egg chamber

– Laying

– Covering

– Returning

– No turtle

� Nest type:

– False Crawl – The turtle makes no attempt to lay and returns to the sea.

– False Nest – The turtle has made at least one attempt to dig a nest but does not lay.

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– Semi Predated – The nests had been partially predated but some eggs are remaining.

– Fully Predated/Poached – All eggs are predated/removed by poachers.

– Relocated to the beach.

– Relocated to the hatchery.

– In Situ – Nest laid in a good location with zero eggs predated.

� The number of attempts, if any, she took to lay.

� If the nest was predated, what animal was the predator.

� Nest cover type; either logs or bamboo (see Nest Covers section below).

� Depth; both to the top of the egg chamber, and if possible (during relocations or excavations) thebottom of the nest.

� The number of eggs:

– If the turtle was encountered before she started laying and the eggs could be counted as theywere laid.

– Eggs were also counted whenever a relocation occurred.

– The number of eggs predated were also recorded is a nest was semi predated.

� Triangulation points; distance in meter from each of the two sector posts the nest lies between.

� Distance in meters from the nest to the vegetation line.

In the absence of a turtle, the exact location of the nest was determined by inserting a stick into thesand to locate the egg chamber (indicated by change in resistance when pressure was applied), followedby careful digging to confirm the presence of eggs. Every nest found was given an identification tag,which was written on a small piece of bamboo placed inside the nest (to be picked up later during ex-cavation). Since we work on the beach with several other partnering organisations simultaneously andcommunication can be difficult, we developed a system to ensure that tags would be unique. Each taghad written on it;

� The date of the encounter.

� The time of the encounter, corresponding to the time recorded in the data book.

� The leader of the patrol

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If a turtle was encountered whilst she was emerging or digging her eggs chamber, we waited quietly atthe bottom of the beach to avoid disturbance. A turtle was only approached when it was certain that shehad started laying her eggs. This is because once she has laid around 20 eggs, the turtle becomes fullycommitted to laying the full clutch and it is very hard to disturb her past this point. When approachingthe turtle, all surveyors were extremely quiet and interacted with the turtle as minimally as possible. Ifa turtle was found laying eggs, the following additional data was collected:

� Carapace length (cm).

� The health of the turtle; flipper/carapace damage, scars, barnacles, algae, fungal infections.

� Whether or not a flipper tag was present, and if so, the prefix and tag number.

Once a nest was fully processed and all data collected, the track was crossed out by drawing a line inthe sand to avoid the track being recorded twice.

Relocations

Nests were only relocated if they were laid in a location on the beach where they would otherwise beat risk, meaning we believe the benefits of relocating the nest to a more secure location are worth theinherent risks of relocating a nest. These locations include:

1. Nests in zone 1 or 2. This is because high tides frequently wash away the sand covering any nestslocated in zones 1 and 2, making them more exposed and vulnerable to predation and extremeheat (Burger & Gochfeld, 2014).

2. Nests located in areas where local dogs are more abundant (e.g. outside lodges).

3. Nests located near a river or cliff edge, as these regions are particularly prone to sand erosion andthus increased risk of a nest being washed away.

4. Nests located near the lagoon on the east side of Playa Carate, as in the wet season the lagoonoften opens up into the ocean, leading to nest damage or exposure.

In order to relocate a nest, the eggs were first dug up and carefully placed into a bucket lined witha plastic bag. The number of eggs laid by the turtle was recorded, the time at which the eggs wereremoved, and the time they were placed into the new nest. Eggs were either relocated to a safer locationon the beach or to the hatchery. Previous studies on Playa Carate have shown that zone 3 has thehighest hatching success and that the optimum depth for a successful nest is 45cm deep, therefore anynests needing relocated were moved to zone 3 and dug to 45cm.

Relocations were done on night and morning patrols. More than 20% of the nests encountered on morn-ing patrols were in locations that would require relocating. Even further care was taken when handlingthe eggs in the morning to ensure no eggs were lost due to movement induced mortality, a risk which issignificantly greater between 10 hours and 14 days from laying (Limpus et al., 1979).

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Hatched Nests

Patrollers would also scan the beach for predated or hatched nests. Hatched nests were identified by thepresence of hatchlings or hatchling tracks which were traced back to a small crater in the sand at thesite of the nest, caused by soft sand collapsing into the nest when the hatchlings emerged. If only a fewhatchlings or hatchling tracks were present, the nest would be left for 48 hours, ensuring all hatchlingshave been given a chance to emerge.

After the appropriate incubation time, the nest is excavated. This process involves digging up the nestand recording the following information:

� Patrol date.

� Patrol leader.

� Whether the nest had a tag inside and if not; GPS coordinates and sector were recorded so wecould find the relevant nest in our data set.

� Nest Type:

– Hatched.

– Unhatched/Undeveloped.

– Semi Predated.

– Fully Predated/Poached.

� Hatch date, if known.

� Number of:

– Live hatchlings.

– Dead hatchlings.

– Pipped hatchlings – hatchlings that have broken the egg but are still in the shell.

– Empty shells.

– Unhatched eggs (see below).

� Predator, if applicable, identified by animal tracks.

� Nest protection (cage or logs), if any.

� Depth of the nest.

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Extreme care was taken during the entire excavation process to ensure as few eggshells as possible werebroken, as anything less than 50% of an eggshell was not counted. To excavate a nest, the top of the eggmass was found first. The person excavating then gently made the hole larger, gently brushing sand outuntil the entire egg mass was distinguishable. The eggs were then removed in as few attempts as possible,again to avoid breaking shells. Once the chamber was empty, eggshells were then carefully separatedand counted to determine the number of hatched eggs. Any unhatched eggs and dead hatchlings wereplaced to the side and counted separately.

If either a live hatchling or a large number of unhatched eggs (>10) were found in the nest, the nest wasre-covered and another 24 hours was given so the hatchlings had a chance to hatch and emerge naturally.If less than 10 unhatched eggs were present, or if the unhatched eggs were still present after waiting theadditional 24 hours, they were broken open to determine their stage of development. Figure 27 belowshows images of the 4 stages of embryo that are recorded during excavations. Five different stages of eggdevelopment in unhatched eggs were recorded. These were:

� No visible embryo: only an egg yolk can be seen.

� Stage One: Eyespot – signs of an embryo can be seen as a tiny white dot within the yolk sack.

� Stage Two: A small hatchling has begun to develop which may be either white or just starting toturn black.

� Stage Three: The hatchling has begun to visibly take shape and is dark in colour. The hatchlingwill be hugging the yolk sack, but the yolk sack remains larger than the hatchling.

� Stage Four: A fully developed hatchling – the yolk sack that it is hugging is noticeably smallerthan the hatchling.

Figure 24: Image depicting the stages 1-4, from left to right, of turtle embryo described above.

Notes were made in the comments section if there was anything unusual about the nest, such as thepresence of roots, maggots, bacteria or fungus. Fungus often occurs in sea turtle eggs and is easiest tosee in eggs with no visible embryo, identified by a pale yolk with a slightly solidified texture. Bacteria ismost easily identified from the strong odour it gives off.

After an excavation was completed, all shells, eggs and dead hatchlings were buried below the high tideline to ensure dogs did not subsequently dig them up.

Predation

Only freshly predated nests were recorded. They were identified based on the shape and colour of theeggshells, as newly predated eggs were still soft and white, whilst old eggs were drier and more yellowin colour. Predated nests were looked to see if they still contained any viable eggs. If none were found,the location of the nest was taken and recorded as fully predated. If viable eggs were present, we then

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determined the number of eggs that were predated counting the shells that were scattered around thenest. If more than 50% of the shell was intact, it was counted as one whole egg. Viable eggs wereleft in the nest to be reburied. However, if less than 20 viable eggs remained in the predated nest, werelocated them to a new egg chamber since the structural integrity of the original nest is often jeopardised.

In these scenarios, any eggs and pieces of shell that were predated on were reburied below the highwater mark to avoid predators smelling the open eggs and re-digging up the nest. Once all relevant datawas taken, the nest was then treated as normal, with a nest cover placed on top and the location recorded.

Nest Covers

Every single nest laid on Carate was left covered either by a bamboo cage or logs in order to deterpredators (Figure 28). Covers were constructed using fourteen 1 meter bamboo sticks, tied togetherwith rope to create a 7x7 mesh cage. If a bamboo nest cover was not available, logs were placed ontop of a nest in a criss-cross fashion (to mimic the bamboo cover design) as an alternative method ofpreventing predation. Preference was always given to bamboo cages since previous data shows that theyare less likely to be washed away by the tide.

Tide Level

Tide measuring transects were conducted on Playa Carate at every spring tide (full moon and newmoon). Tide-measuring sessions would take place 15 minutes after high tide, when the high tide linewas easily identifiable by observing the water line in the sand. At each sector post, the location ofthe high tide mark is recorded with GPS coordinates, as well as the vegetation line. Tide-measuringsessions will be conducted every fortnight over the coming years in order to track long-term changes intide-levels which can be visually mapped with GIS and provide insight into the future availability of suit-able beach habitat for sea turtles to lay their eggs without risking their nests being inundated by the tide.

Figure 25: An image of a bamboo nest cover. Sticks were dug into the corners of the nestand in some cases logs were placed on top of the cover to further stabilize it and prevent dogsfrom moving it to dig up a nest.

Sand Temperature

Sand temperature was taken along Playa Carate once a week at 6am and 2pm in the 2019 study seasonusing a temperature probe. The temperature was recorded at sectors 6, 12, 18, 24 at 0, 8, 16, 24 and36m from the sector post towards the ocean. The average temperature across the year and between dryand wet seasons was then analysed to estimate nest incubation temperature.

Analysis

All statistical analyses were conducted using Microsoft Excel and RStudio. One-way ANOVAs, Tukeytests and t-tests were used to estimate statistical difference between data.A result was considered statistically significant if p≤0.05. The risk ratio with 95% confidence intervalswas also calculated to determine the relative probability of a nest being predated with versus without

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a nest cover. A risk ratio of 1 would indicate no difference in probability of predation across the twoconditions, so the result was considered statistically significant if the confidence interval did not straddle1. R squared values were used to estimate the strength of correlation.

6.5.3 Results

As the season is not quite complete on Playa Carate, only corresponding data from previous seasons(2017/18-2018/19) was analysed. Therefore, the total sampling period analysed in this section is be-tween June 1st and February 15th for these seasons.

Nesting Patterns and Preferences

During the total sampling period, 3728 adult turtle tracks were identified along Playa Carate. Of these,2701 were identified as being nests. Olive Ridleys laid the vast majority (97%), 95 Greens and 8 Hawks-bills also nested in the study area during the sampling period.

Table 11: Comparing the number of different nest types on Playa Carate across the samplingyears.

2017 2018 2019

SuccessfulLays

In Situ 758 740 704Beach Relocation 45 6 198

Hatchery Relocation 79 15 54Poached 56 29 14

Semi Predated 38 50 70Fully Predated 48 10 45

No LayFalse Nest 20 58 145

False Crawl 243 185 118Total 1287 1093 1348

Figure 26: Pie chart showing proportion of activity by species from June 1st 2017- February15th 2020.

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Effect of Nest Covers on Predation

During the sampling period, a total of 261 nests have been identified as predated to some degree. Ofthese, 158 were recorded as semi predated (5.85%), and 103 were fully predated (3.81%).

Since the beginning of the 2018 phase, bamboo nest covers were placed on 718 nests. Of these, 30 weresubsequently predated. This gives a lower predation rate of 4.18% with a bamboo cage in comparison to14.4% when no cover was present. Additionally, a total of 893 nests had logs placed on them, 74 (8.29%)of which were predated. Figure 27 below shows the average predation rate for each nest type. A one-wayANOVA revealed that there was no significant difference between the presence of logs or bamboo on nestpredation rate however both protection types significantly reduced predation rates (Z=4.21, P<0.001) Acalculation of the risk ratio found that the probability of a nest being predated without a nest cover was1.67 times greater than the probability of predation with a nest cover (95% CI: 1.63, 4.48). However,this does not account for any of the nests, which were predated by crabs, since they are able to burrowinto the nest and this cannot be prevented either by logs or bamboo.

Figure 27: Bar chart displaying predation rates on nests with different cover types (bamboocages, logs and no protection).

Predation and Hatching Success

The average hatching success of nests that had undergone semi predation by dogs, vultures, raccoons orcoatis before a cage could be placed over the nest was compared to nests with a bamboo cage or log cover.Accounting for the eggs that had been lost in the predated nests, the subsequent hatching success waslowest among nests that had previously been predated, averaging 61.70% (See Figure 28). Nests that wereexcavated with no cover but were not predated had a hatching success of 81.72%. Bamboo caged nestshad an average hatching success of 86.55% and nests with logs averaged 83.27%. A one-way ANOVArevealed that there was no significant difference in hatching success between nests covered with logs orbamboo (p=0.2952). A Tukey Test of honest significant difference showed that there was, however, a sig-nificant difference in hatching successes between nests covered by bamboo cages and no cover (p=0.0313).

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Figure 28: Average hatching success (%) of nests that underwent different nest cover typesin 2019/20 study season.

24% of all semi-predated nests were relocated based on the number of viable eggs remaining in thenest. The hatching success of these relocated nests was 74.8%, compared to the semi-predated neststhat remained in their original location, which had an average success of 61.7%. An unpaired two-tailedt-test determined there to be no significant difference between in situ and relocated semi-predated nests(p=0.146).

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Figure 29: Average hatching success (%) of semi-predated nests that were relocated and thosethat were not in 2019/20 study season.

Effect of Relocations on Hatching Success

In an effort to increase the number of hatching nests, 252 nests in the 2019/20 season that would other-wise have been unviable have been relocated either to a safer location on the beach or to the hatchery.In order to determine whether this is successful, both in situ and relocated nests have been excavatedpost-hatching and examined to evaluate hatching success. Hatching success is defined as the proportionof eggs in a nest that hatch a fully developed turtle. Figure 30 below compares the average hatchingsuccess of nests left in situ, beach-relocated nests and hatchery-relocated nests. A one-way ANOVA de-termined there to be a significant difference between the three nest types (p=0.0137) however, a Tukeytest of honest significant difference showed that there was no significant difference in hatching successesbetween in situ nests and beach relocations (p=0.874) but relocations to the hatchery were significantlysuccessful (p=0.0104).

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Figure 30: Bar chart comparing average hatching success (%) of different nest types: In situnests, those relocated on the beach and those relocated to the hatchery.

Effect of Time of Year on Incubation Period, Hatching Success and Temperature.

The study site, Playa Carate, is considered as in the wet season from May to November. The dry season,lasting from December to April, has significantly less rain and higher air temperatures. Figure 31 showsthe relationship between the time of year and time taken for the eggs to hatch. An unpaired two-tailedt-test determined that the month had a significant effect on incubation period (p=0.000322). Averagesand temperature in the wet season was 32.73◦C compared with 34.79◦C in the dry season. Figure 31also shows this relationship. This difference was determined significantly by an unpaired two-tailed t-test(p=3e−4).

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Figure 31: Bar chart showing the effect month on average incubation period (days). Lineshows relationship between sand temperature (◦C) per month and incubation time.

Additionally, to investigate whether the sand temperature had a significant impact on the hatching suc-cess, the R value of the two variables was calculated (R=-0.55), showing there was a negative correlationbetween sand temperature and hatching success (See Figure 32).

Figure 32: Graph showing the negative correlation between mean sand temperature (◦C) ina month with the mean hatching success (%). (R=-0.55).

Effect of Month and Lunar Phase on Turtle Activity

A total of 1348 activities were documented in the 2019/20 study season. The month and lunar phase peractivity was compared. The most popular months were between August and November, yielding 72% ofall activities (Figure 33). 28.2% and 23.0% of all activities were, respectively, yielded during the WaxingGibbous and Waning Crescent lunar phases (Figure 34).

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Figure 33: Graph showing the number of activities per month in 2019/20 study season.

Figure 34: Radar graph showing number of activities per lunar phase in 2019/20 study period.

6.5.4 Discussion

Effect of Nest Covers on Predation

With 9.66% of nests still subjected to some form of predation prior to being covered, it is clear thatpredation remains the largest threat to sea turtles on Playa Carate. Domestic dogs over all three studyperiods were accountable for the majority of predations, digging out both covered and uncovered nestson the beach. Whilst vultures and crabs predated on a large proportion of nests, these are secondaryor burrowing predators and therefore cannot be avoided. Vultures predate on nests that have alreadybeen dug up by dogs, coatis or raccoons and therefore the impact of said primary predators is exacerbated.

The relationship found in this study of bamboo cages reducing predation rate supports the literaturefound in the Osa, other parts of Costa Rica and other parts of the world (Korein et al., 2019; O’Connoret al., 2017; Lei & Booth, 2017). Alongside its proven ability to protect nests from predators the bamboocage is sustainable, lightweight and resilient. Both logs and bamboo cages are environmentally friendly,unlike plastic or metal covers, and do not prevent hatchlings emerging (Ossmann, 2019; Mascarenhas etal., 2004). These qualities make bamboo cages the ideal nest covers in terms of practicality and func-tionality.

As with any predation-prevention method, bamboo cages are not perfect - 4.18% of nests covered withbamboo cages were subsequently predated. The predation rate of nests with logs on was slightly higher,

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8.29%, and this difference was statistically different most likely because of the greater proportion of logcover washed by the tide. Both types of cover were susceptible to being dug up by dogs if they were notbuilt or placed correctly, and this likely explains the percentage of covered nests that were predated. Afurther limitation is, simply, availability of either nest cover type. Suitable driftwood is plentiful at timesand scarce at others depending on what has washed in with the tide. Similarly, bamboo cage distributionis not always even along the beach. This can lead to unsatisfactory nest covers at times making nestsmore susceptible to predation though this is not recorded any differently in the data and so cannot beaccounted for. In preparation for the future, more cages are needed to be made before the peak nestingperiod of the 2020/21 seasons.

Effects and Benefits of Relocations

This season saw 198 relocations, four times the number of relocations than in the past two seasonscombined. Turtle egg relocation is a delicate task and requires extreme care. Movement induced mor-tality occurs when the orientation of eggs is altered significantly between approximately 10 hours and14 days from laying (Miller & Limpus, 1973). 126 relocated nests were excavated on the beach and theyshowed that the hatching success of the relocated nests was not compromised when compared with insitu nests. This should not be undermined, as it is a skilful and risky operation. The reduction of nightpatrols over the season has increased the proportion of risky, morning patrols however, there did notappear to be a change in hatching success. The 54 hatchery relocations consistently had a high hatchingsuccess, averaging 91.3%. Known benefits of hatcheries include guaranteed protection from predatorsand poaching, as well as the ability to get exact estimates of hatching success (Tisdell & Wilson, 2005).Additionally, hatcheries allow for consistent temperature monitoring and manipulation, using artificialshading, to reduce egg mortality (Maulany et al., 2012). The cost and manpower associated with themaintenance of a hatchery is a disadvantage (Tisdell & Wilson, 2005), but thanks to co-operation withCOPROT, Planet Conservation and COTORCO this workload was distributed. Unfortunately, due toa withdrawal of involvement from the ADI, who helped set up the hatchery, it was closed at the end ofDecember 2019. This was a direct loss for the beach in terms of ensured protection and control of nesttemperature as we go further into the dry season and sand temperatures continue to increase.

Finally, the relocation of semi-predated nests did improve the hatching success of remaining eggs by13.1%. Though this was not found to be significant it is likely due to the small sample size of semi-predated relocated nests. Having said this, almost 50% of these nests were from the past three months.An increased effort to do this in the future will help to prove the importance of this task and shouldimprove overall hatching success significantly. This relationship is supported by research that provedthat the most successful method for improving hatching success is removing and replacing nest sand(Bezy et al., 2015). Old nest sand of a semi-predated nest tends to increase crab predation and antinfestation (Bezy et al., 2015). Additionally, semi-predated nests often lose the structural integrity ofthe egg chamber meaning any later hatchlings may not be able to emerge (Bustard & Greenham, 1968).Damp sand or roots are the two most common ways to maintain structure, however these are both lostwhen the nest is dug or its sand is exposed to the sun (Bustard & Greenham, 1968). This is an importantdirection for us to move in the future.

Effect of Month on Hatching Success, Sand Temperature and Incubation Times

Previous reports from past seasons have proved the effect of sector and zone on hatching success (CBP193, CBP194) – sectors with mainly trees for vegetation and zone 3 were the most successful. Havingwitnessed the shift in hatching success first hand from the wet season into the dry, the effect of monthseemed an important factor to analyse.

The results showed a strong correlation between the time of year and sand temperatures. In the wetseason, May to November, Playa Carate had significantly lower sand temperatures which coincided withhigher hatching success and longer incubation times. Hatching success decreased with increased tem-perature, something that is in line with all literature. Temperatures above 34◦C for three consecutivedays are known to consistently reduce hatching success in Olive Ridley’s (Maulany et al., 2012). Highesthatching success in Greens has been documented between 27◦C and 32◦C but anything above 38◦C willresult in mortality (Bustard & Greenham, 1968). Whilst the average temperature, even in the warmestpart of the beach was only 33◦C there were over 20 weeks with recorded sand temperatures above 35◦C

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and at least 3 weeks with sand temperatures over 39◦C. This highlights how the nest temperature maydirectly be influencing egg mortality on Playa Carate.

Even in the successful nests on the beach, we expect that the sand temperatures seen will cause askewed sex ratio in the sea turtle populations emerging from Playa Carate. It has been determined byprevious studies that the incubation temperature at which a 1:1 male to female sex ratio is produced,or pivotal temperature, for Olive Ridley populations in Costa Rica is between 30-31◦C (McCoy et al.,1983; Wibbels et al., 1998). Anything above 30.5◦C and 32◦C is expected to have a female bias inGreens and Olive Ridley’s, respectively (Hawkes et al., 2007). Due to their long life history and the lackof non-invasive methods to sex sea turtles it is difficult to estimate how strong the female bias for decades.

6.5.5 Future research

The protection of nests as soon after nesting as possible is our priority. The relocation of “doomed” nestsis also essential for increasing the hatching success and it was achieved through co-operation with the lo-cal turtle conservation group COPROT, as well as Planet Conservation. Thus far, in the 2019/20 seasonhas seen over 933 patrol hours on the beach however, due to safety concerns night patrols significantlydecreased since September 2019. 85 patrols are estimated to have been missed for this reason. This hascoincided with an increase in overall predation rate of almost 9%. Increased patrol hours, specificallynight patrols, will ensure relocations can take place as safely to avoid movement induced mortality andminimise nests or tracks lost by the tides. Additionally, patrol hours undoubtedly reduce poaching andpredation, the two major threats which we are able to prevent directly.

Increasing patrol hours requires the adequate amount of manpower and this can be a limitation basedon the number of staff, volunteers or assisting organisations present at any time in the season. Analysisof activity showed there to be the most turtle activity between August and November and during theWaning Crescent moon and Waxing Gibbous. These results are conducive with previous studies loggingactivity patterns of sea turtles in Costa Rica (Pinou et al., 2009). Based on this information, an emphasison night patrols especially during these months at these lunar phases should ensure as little activity ismissed as possible, if any at all, in coming seasons. This overall can help predict peaks in activity andimprove our conservation strategies.

Secondly, the introduction of a new hatchery is a necessity to ensure the success of the nesting populationon Playa Carate. There is approximately four months until the start of the next season and preparationsfor a hatchery on the adjacent beach, Rio Oro, are underway. The hatching success from nests in thehatchery was an unquestionable triumph for Playa Carate this season and it will be a huge loss to nothave one functioning on our beach. A hatchery in the dry season is even more essential as beach temper-atures rocket and implementation of artificial shading could be used to cool the sand (Ossman, 2019).In the dry season Carate is on average 3◦C hotter than in the wet season (Barquero-Edge, 2013) and ourresults proved the negative impact this has on hatching success. Monitoring of the nest temperaturescan also ensure for a sustainable population of sea turtles in the next generations.

Finally, the most exciting prospect I would like to propose for the future research on Playa Carate is aninvestigation into the hybridisation of Olive Ridley nests. It is known that female sea turtles will matewith multiple males in any one mating season and therefore producing a degree of variation within asingle nest (Pearse & Avise, 2001). However, though it has not been recorded in previous seasons, in thepast six months, on various occasions, hatchlings from Olive Ridley nests have emerged with atypicalcharacteristics. These hatchlings are often larger in size than the average Olive Ridley hatchlings, darkerin colour and present a white margin along their flippers and carapace (See Figure 35); all of which aresimilar to that of the Green turtle, or in this case, the Black turtle (a subspecies of Green found in theEastern Pacific).

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Figure 35: Photograph on the left shows a typical Olive Ridley hatchling. Photograph onthe right shows a putative hybrid with atypical features such as the white margins on carapaceand darker colouration from the same Olive Ridley nest.

Hybridisation between different species of sea turtle has been recorded on several instances: betweenLoggerheads and Hawksbills, Loggerheads and Kemp’s Ridleys, Greens and Hawksbills, Greens and Log-gerheads and Olive Ridleys and Hawksbills (Kelez et al., 2016). However, only one peer-reviewed paperby Hart et al. (2019) currently exists documenting the hybridisation between Olive Ridley and EasternPacific Greens in northwest Mexico. For all putative hybrids the paper recorded features including, butnot limited to: number of various scales or scutes, carapace or plastron colour and beak shape. A futurestudy on Playa Carate next season should use a similar format as Hart et al., (2019) to accurately builda database and record the possibility of these hybrids existing here.

To conclude, as there is relatively minimal amount of literature of nesting trends in the Osa Peninsula,the data collected over past and present seasons on Playa Carate is extremely important. Long-termrecords of tide levels, temperature and weather help to track not only important ecological data relat-ing to sea turtles, but also important changes in climate in the region that may impact multiple otherecosystems. This season has seen more nests than 2017 or 2018; 1008, 882 and 811, respectively. Morerelocations have been done than in previous years combined and 584 nests have been excavated, averag-ing a success of 86.0%, an increase on past years. These numbers reflect the success of this season andprovide excellent groundwork for the same conservation work to continue on Playa Carate.

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6.6 Assessment of the Social Dynamics of the ACOSA Scarlet Macaw (Aramacao) Population, Situated in Carate, Costa Rica.

6.6.1 Introduction

With a geographical range once expanding from Mexico through Central America to Bolivia in SouthAmerica, the current global population of this charismatic and iconic large parrot is fragmented andgreatly reduced in numbers due to habitat loss throughout its range and active poaching for the pettrade (Marineros and Vaughan 1995; Snyder et al., 1992; Vaughan et al., 2003a). Not surprisingly, Scar-let macaws are currently listed as ‘’Endangered” species on CITES, Appendix 1 (Marineros and Vaughan1995). Additional strain on their global population is caused by the fact that Ara macao has a very lowreproductive rate and low breeding success. In a survey carried out in a Peruvian floodplain forest, only10%-20% of the local population nested in any given year. From those, 33% were unsuccessful attempts(Guitar et al., 2008).

The Scarlet macaws were once on the brink of extinction in Costa Rica, nowadays their numbers areincreasing thanks to their reintroduction to territories that were formerly occupied by this species. Asa result, there are currently two viable populations of Ara macao that are established in Costa Rica.The first one is located in the ACOPAC (Central Pacific Conservation Area), with a population sizeof approximately 432 individuals. This population has been a subject of many studies for nearly twodecades (Marineros and Vaughan 1995, Vaughan et al., 2003a, Myers and Vaughan 2004, Vaughan et al.,2005). The second one, which is the larger of the two, is located in the Osa Peninsula Conservation Area(ACOSA), and currently numbers 800- 1200 individuals. Despite of its greater numerical abundance,the ACOSA’s population is virtually unstudied (Dear et al., 2010).

The ACOSA’s Scarlet macaws population has been studied by Frontier since November 2017, whena project regarding the feeding ecology and tree preference was launched in Carate, Costa Rica. Thisproject managed to reveal some important aspects of the feeding and roosting trees preferences. However,like everywhere else, nothing was known about their behaviour and social structure in the wild (Dearet al., 2010). What is currently known is that Scarlet macaws are highly sociable psittacids with groupsizes reaching up to 30 individuals. Also, the expanded telencephalic region of their brains allows themto form complex social networks, perform high levels of communication and the ability to form strongbonds with conspecifics (Chappel, 2017: Olkowicz et al., 2016). Although communal roosts with largenumbers of birds were observed in many places throughout Central America, Scarlet macaws developeda monogamous mating system with biparental care, lasting up to two years (Vigo et al., 2011). Anothervery prominent feature is the familial socialisation (further referred as in- group socialisation), which iscommon with mated adults who only separate in order to feed during the breeding season. In- flight orgrounded families that include adult male, a female and up to two juvenile offspring will always maintaina close proximity, either by flying wing-tip to wing-tip or perched on the same tree branch (Vigo et al.,2011).

Keeping strong familial bonds is essential not only for the successful reproduction of adult Scarlet macawsbut also for the survival of their offspring. However, socialisation outside of the family is also equallyimportant. This behavioural pattern, further referred to as out- group socialisation is not only crucialfor the successful integration of every individual within a conspecifics group, but it also greatly increasesthe chance to find a mating partner, leading to successful reproduction. Out-groups socialisation holdsbenefits to an individual’s survival (Brown et al., 2016), such as reduced predation rate (safety in num-bers) and provides information about availability of seasonal food resources. In addition, some group-living species are thought to be able to anticipate seasonal climate changes and adjust their group sizein order to maximise their survival rate (Thogmartin & McCann, 2014).

Observing communal roosting species would surely allow for better understanding of their ecology andsocial dynamics. However, this can prove difficult, because roosting sites are very often found high upin the canopies of large trees, or in the dense mangrove forests (Masello et al.,2006). Therefore, ourcurrent aim is to investigate the social behaviour and group dynamics of the ACOSA’s Scarlet macawpopulation during daylight activity. As the population in Osa peninsula is new, we are unable to makecomparisons with other populations found in Central or south America. The results of our previousproject support the study made by Dear, Vaughan and Polanco (2010), which suggest that socialisationduring daylight hours is mostly in-group. The current project is focused on group dynamics (both in

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flight and grounded), group composition, behaviour and communicatory calls between individual birds.This new study allows us to assess and understand the social structure and behavioural composition ofthe ACOSA Scarlet macaw population, as well as any patterns in their behaviour.

6.6.2 Methodology

The local population of Scarlet macaws in the Carate area has been a subject of study by Frontier sinceNovember 2017, when a project regarding the feeding ecology of this large psittacid species was launched.The data collection on this topic continued until August 2019 and the results were last published in CBP194 Science Report. Since then the main focus on this species shifted from feeding ecology to an as-sessment of the social dynamics of the local Ara macao’s population. The current abundance marks therevival of this species not only on Osa peninsula but in Costa Rica in general, however little is knownabout many aspects of their social behaviour.

Study Area

As with the previous reports on the ecology of Ara macao, surveys were conducted on the same study trailsand for the same duration of time. The transects show a marked difference in regard to anthropogenicimpact and types of vegetation cover, therefore we would be able to understand how adaptable Scarletmacaws are to environmental heterogeneity. Surprisingly, this species can be found on all the surveyedtrails.Protocol

Surveys are carried at any of the four timepoints (6am, 10am, 2pm and 4pm). The trail and start timeused for each survey is chosen via a randomisation generator. Surveys are held approximately three timesper week. Every survey effort lasts for up to 40 minutes. Once the beginning of the chosen transect isreached, the start time is recorded, as well as the number of all survey participants. Then, at a steadybut slow pace the survey team starts to scan the surroundings for any macaws. Once individuals from thetarget species are identified, the group stops and records the time of sighting and whether the macawsare grounded or in flight.

Grounded Individuals

In this category, birds are only recorded as grounded individuals if they are perched on a tree. At thetime of recording, if the same tree is used by multiple individuals, all macaws are recorded as a singlegroup. If this is the only group of Ara macao within 20m, then they are recorded as a lone group. Thenext step of the research protocol is to determine how many subgroups are present within the spottedflock. A given number of individuals is considered a subgroup if individuals are within 1 m distancefrom each other. Social behaviour and communication were also recorded. Typical behavioural patternsinclude feeding (when actively foraging), resting, preening (singly or mutually between a bonded pair),travelling (moving from one branch or tree to the next) and hanging (upside-down posture from a branchbefore taking flight), or a mixture of two or more behavioural patterns among the listed above. Com-munication between individual birds was also recorded on the data sheet. Vocalisations between Scarletmacaws have two types: loud and quiet. The former are squawks with a high volume, that are clearlyheard by the surveyors, even at a great distance. They are used for communication between relatedconspecifics within a larger group. The latter are quiet mumbles, acting as a tool of communicationbetween conspecifics within a subgroup.

Birds in Flight

In this category, Scarlet macaws are recorded as in flight when they are flying in front of the observer.This approach eliminates the possibility of recording the same bird twice. If all birds are flying at thesame height and follow the same direction, then they are recorded as a single group. The next step ofthe protocol is to estimate how many subgroups are presented within the flock. Individuals are recordedas a subgroup only when they are flying within 1 m of each other. As with the previous activity, loudand soft calls were recorded for the same purpose.

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When all the required data is collected, the survey continues until another individual or a group is found,or until the final point of the trail is reached.

Figure 36: The recording sheet, used for data collection.

6.6.3 Results

Total Abundance

The results in this section represent the total abundance of Scarlet macaws, recorded between late August2019- late February 2020. During this period, a total of 434 Ara macao were observed on all three surveytrails. In regard to sightings frequency, the survey trails follow the same trend as the previous report(CBP 194), where the largest number of macaws seen on the ‘’Beach” transect, with a total number of292 individuals, followed by ‘’Rio Carate” with 102 recorded individuals. The ‘’Road ‘’ transect producedthe lowest number of sightings- only 40 individuals were observed over the last six months (Figure 37).

Figure 37: Total number of Scarlet macaws (Ara macao) delivered from all transects.

In Flight vs Grounded Birds

Of all recorded individuals, the majority were birds in flight (n=267) vs 167 grounded birds, representing61.5% and 38.5% respectively. On the ‘’Beach” trail the total number of flying birds was slightly highercompared to the grounded ones 164 vs 128 individuals (Figure 38). ‘’Rio Carate” produced much highernumbers of flying birds (n=95), compared to grounded birds (n=7). The reverse tendency however wasobserved on the ‘’Road” trail, where only 8 Scarlet macaws were observed in flight, while 32 macawswere recorded as grounded (Figure 39).

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Figure 38: Total number of Scarlet macaws- In Flight vs. Grounded birds.

Figure 39: In Flight vs. Grounded Birds per Transect.

Social Structure and Group Composition

As a highly social species, Scarlet macaws have been observed to form flocks of up to 30 individuals inthe wild. The smallest group size recorded by Frontier so far were those consisting of a single individual,whereas the highest numbers were delivered by groups containing 5 individuals. From all transects,single birds formed a total number of 113 individuals, making up 26% of all recorded birds Similar tothe results from the previous report, groups consisting of two individuals delivered the highest number(n=246) and percentage (56.7%) in total, thus forming more than half of all observed Ara macao. Asmaller percentage came from the groups consisting of 3 individuals (n=48;16 groups), making 11.5%of the total number of all birds. The lowest group numbers recorded were groups of 4 (n=12; 3 sub-groups) and 5 individuals (n=15; 3 subgroups), representing 2.8% and 3.5% respectively (Figure 40 & 41).

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Figure 40: Subgroups composition in relation of the total number of recorded A. macao.

Figure 41: Group composition’s percentage in relation to the total number of observed A.macao.

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Communication

Being a highly sociable species, communication between group members and conspecifics undoubtedlyplay a vital role in the life of A. macao. The type of communication (loud or quiet calls) depends onfactors such as group size and relation between its members. From all 343 individuals, types of commu-nication were recorded in 296 birds, while 113 macaws did not make any calls during the time of theirobservation. The level of communication for another 25 macaws was marked as ‘’Unknown” on the datarecording sheets, therefore they are excluded from further analysis (Figure 42).

Figure 42: Presence and absence of communication- total numbers.

Group Size and Presence of Communication

Over the last six months, 75 Scarlet macaws (referred here as groups of 1 individual), showed differentforms of communication, thus representing 18.3% of the total number of observed birds. The largestnumber of birds showing communication was derived from groups containing two individuals (n=174;87 groups). In total this makes 42.5% of all observed birds during the last six months. Groups of 3individuals yielded considerably smaller numbers of communicating birds (n=24), contributing 5.9% ofall Ara macao. Two groups of 4 individuals (n=8) and three groups of 5 individuals (n=15), showeddifferent levels of communication, representing 2.0% and 3.7% of all sampled birds (Figure 43 & 44).

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Figure 43: Total number of communicating Ara macao.

Figure 44: Total percentage of communicating Ara macao.

Group Size and Lack of Communication

During the data collection process, 113 Scarlet macaws did not show any signs of communication duringthe time of recording. Of these, 33 were groups of 1 individual, making up 8.1% of all observed indi-viduals. Similar to the previous subchapter sections, groups of two birds produced the highest numberof non- communicating birds (n=70; 35 groups), staying at 17.1% in total. Communication was notpresent in two groups of three individuals and a single group of 4 birds, representing 1.5% and 0.9%of the total number of birds. No groups of 5 birds were observed in this category (Figure 45 & Figure 46).

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Figure 45: Total number of non- communicating Ara macao.

Figure 46: Total percentage of non- communicating Ara macao.

Communication vs Non Communication

Our results clearly demonstrate that communication plays an important role in the life of the Carate’sScarlet macaw population. Currently, two- thirds of all recorded individuals (n=296; 68.2%) showed aclear level of communication. This is a slight decrease compared to the numbers from late August- lateNovember period, when communication was present in 72.8% of all observed individuals. In addition, thenumber of non- communicating birds marked an increase- of 26% over the last three months, comparedwith those registered during the first three months of the project where only 16.2% of all Scarlet macawswere considered as non- communicating (Figure 47).

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Figure 47: Total percentage of communicating vs non- communicating Ara macao.

Behaviour

Due to the extended telencephalon sector of their brains and complex cognitive functions, Scarlet macawsare highly intelligent birds demonstrating varied types of behaviour. Since the start of this project wehave observed different behavioural patterns in a total of 163 birds. The most frequently observed typeof activity among the Carate’s population was ‘’feeding”, which was registered in 69 individuals sincethe start of this project, thus forming a total of 16.9% of all registered individuals. The second mostcommonly detected activity was ‘’resting”, observed in 9% of all birds (n=39). Another 32 birds showed‘’mixed” type of behaviour when two or more behavioural patterns were observed at the same time.These included feeding and travelling (moving from one branch to another while searching for food),thus making 7.3% of all observed individuals. Less commonly observed were preening (both singly ormutually between two conspecific individuals), recorded in 12 birds (2.8%) and hanging (upside-downposition from a perch, prior taking off) observed in only 3 individuals (0.7%) (Figure 48).

Figure 48: Total percentage of different behavioural patterns recorded in Ara macao.

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Seasonal Variability

Although the following project is still in its early stages (six months survey effort), the results havealready started to reveal some insight into the social dynamics of Ara macao. Moreover, the projectcoincided with the overlap between both the wet and dry seasons, therefore we are able to compare theseasonal differences in total abundance and group composition of A. macao.

Total Abundance

Figure 49 shows the differences in total abundance of Scarlet macaws observed during the wet and dryseasons. During the dry season the total number of observed birds (n=139) dropped significantly on alltransects. In contrast, during the wet season the numbers of recorded individuals was higher, reachinga total number of 295 individuals.

Figure 49: Total numbers of Ara macao recorded during wet and dry seasons.

Abundance by Transect

Although in significantly lower numbers during the dry season, the majority of sightings was recordedfrom the ‘’Beach” trail- 62 birds, which compared to the numbers from the wet season is four times less.The second highest number of this study species was observed on the ‘’Rio Carate” transect- 56 birds,which is slightly higher compared to the sightings during the wet season, when only 46 A. macao wererecorded. Again, the smallest abundance was derived from the ‘’Road” trail- 21 individuals, which issimilar to the numbers observed during the rainy season (n=19) (Figure 49).

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Figure 50: Seasonal variation of Ara macao per transect.

In regard to the frequency of sightings, the three transects followed the same trend, the overall sightingspercentage revealed a completely different pattern. The dry season (considered as Jan- may, produced atotal of 44.6% of all macaws. In comparison, the same transect produced 78% of all sightings during therainy season. ‘’Rio Carate” produced 40% of all sightings during the dry season, in comparison with thewet season, when the numbers from this transect contributed only 15.6% of all sightings. Although thenumber of Scarlet macaws from the ‘’Road ‘’ transect was the same during both seasons, the percentagechanged, due to the lower overall total number of observed birds. During the wet season this transectproduced 6.4% of all observed birds, while the dry season numbers shifted to 15.2% due to the overalldetection rate of Scarlet macaws.

Social Structure and Group Composition

Although the sample of birds was significantly lower during the dry season, it is still possible to see dif-ferences in their group composition. Groups of two individuals formed the largest group size, consisting84 Scarlet macaws, making a total of 60% of all observed birds. In comparison, during the late Aug- Febperiod, groups of two Ara macao comprised 55% of all birds. The second most abundant group size wasthe one containing single individuals (n=23). Solo birds contributed 23.2% to all recorded individuals,compared to wet season, when this group size stood at 27.5%. A steady downward trend was registeredin groups containing three individuals (n=9; 3 groups), compared to the wet season, (n=39; 13 groups)where this size class contributed 6.5% and 13.2% of all observed individuals. No differences were recordedin the groups containing 4 individuals- the wet and dry seasons produced 2.7% and 2.9% of all birdsrespectively. However, there is a marked increase in relation to the groups containing 5 individuals. Thisgroup size contained 7.5% of all observed birds, compared to 1.7% during the wet season. (Figure 50).

6.6.4 Discussion

Total Abundance

As mentioned in the results, the period December-April (referred here as dry season), produced a consid-erably lower number of Scarlet macaws compared to the first three months from the start of the project.Previously, the ‘’Beach” trail produced 78% of all A.macao sightings. A possible explanation of thispattern is the fact that large number of Indian Beach almonds (Terminalia catappa) are growing in highnumbers along this trail. When you consider the abundance of this mid- height tree and its ability to

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produce seeds all year round it is not surprising that this trail attracts the highest numbers of the targetspecies.

During the last three months the number of birds recorded on this transect dropped to only 44%. Thereason behind this shift is most likely due to the changes between wet and dry seasons. Food suppliesare getting scarcer and the overall fruits and seeds productivity is dropping significantly. To compen-sate for the shortage of food supplies, animals are forced to travel greater distances in order to reachmore abundant food resources. Known to roost in high canopy trees in primary forests and mangroves,Scarlet macaws have been observed to fly inland to feed. This behaviour fully explains the decreaseof recorded individuals on a transect, where A. macao are generally considered to be abundant. Birdsare forced to look for alternative feeding grounds in order to compensate for the seasonal shortage of food.

On the other hand, the ‘’Rio Carate” transect is showing quite the opposite trend in comparison withthe ‘’Beach” transect. During the wet season, the total number of recorded birds was 46 individuals,thus making up 15.6% of all individuals observed. The dry season marked a slight increase in the totalabundance of A.macao staying at 56 individuals, while the total percentage of birds increased to 40.2%.The majority of all individuals were observed in flight at the time of their recording, which supports ourconclusion that Scarlet macaws use the high trees along ‘’Rio Carate” for a roosting site and travel toother areas to feed on a daily basis.

There is no change in the numbers of macaws recorded on the ‘’Road” transect during both seasons. Thelarger percentage value recorded during the dry season is due to the overall lower number of observedmacaws, rather than significant changes in their social dynamics.

Group Composition

There are minimal changes recorded in the overall group composition. Similar to the results from theprevious season, groups of two individuals were the most abundant social unit, followed by groups ofsingle birds, thus contributing 55% and 27% to all sightings. The given numbers mark an insignificantdecrease in the groups of two individuals and a slight increase in the groups containing one bird. Thereis also a clear drop in the numbers of groups formed by three birds- 13.5% during the wet season toonly 6.5% during the dry season. There were no changes observed in groups of 4 birds, as both seasonsproduced the same values. On the other hand, groups of 5 individuals marked an increase in their overallpercentage- from 1.7% during the wet season to 7.2% during the current three months period. However,this shift is unlikely to represent any upward trend due to the overall low numbers of macaws recordedin general. Despite the little fluctuations, our results revealed that seasonal changes do not have a directinfluence on the social structure of the studied population in Carate.

Communication

As with the previous report, the results from the last three months support the fact that the populationof Scarlet macaws in Carate rely heavily on communication. Despite the slight numerical differencesbetween communicating and non- communicating birds observed during both seasons, it could be con-cluded that seasonal changes do not negatively affect the level of communication between birds. Again,the change in numbers is because of the lower number of Scarlet macaws observed between December2019 and February 2020.

Behaviour

From all behavioural patterns, feeding was the most frequently detected activity. Most of those sight-ings were recorded on the ‘’Beach” transect. Parrots were observed foraging on the seeds of Terminaliacatappa. Although Scarlet macaws were undoubtedly moving more actively between feeding grounds,the dry season did not seem to alter the typical behavioural patterns, published in the previous report.The second most common detected activity was resting, which was observed in roosting birds from the‘’Beach” and ‘’Road” transects. The less commonly observed behavioural patterns were preening, travel-ling and hanging. As the total number of all observed activities is still low, more prolonged observationsand a higher number of surveyors would be required before drawing certain conclusions on the behaviourand social structure of Ara macao.

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6.6.5 Conclusions

Although this project is still at its early stages, the collected data already reveals fluctuations in thesocial dynamics of A. macao in Carate. The total abundance of Scarlet macaws is directly influencedby the dry season, resulting in numbers four times lower compared to the wet season. As food resourcesare becoming less abundant, birds are compelled to move to different foraging grounds in order to com-pensate for shortages, caused by the dry season.

Drastic changes were not observed in regard to group composition, with two birds being the most fre-quently seen social unit, followed by groups of 1 individual. The seasonal change did not seem to alterthe natural behaviour of the target species. Foraging continues to be the most frequently observed pat-tern, followed by resting and preening. As a future recommendation, surveyors should spend more timeobserving, when birds are detected, in order to extract more details on their behaviour. In addition, alarger sample size is required to complete the aims and objectives required from this project.

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6.7 An Assessment of the Mammal Diversity and Distribution in Carate,Costa Rica.

6.7.1 Introduction

Tropical forests represent over half of the 36 global biodiversity hotspots (Mittermneier et al., 2004).However, these valuable ecosystems are currently threatened by deforestation and fragmentation in or-der to make space for human activities, infrastructure and agriculture (DeFries et al., 2005; Fisher &Christopher, 2007). To date, more than 75% of Earth’s biodiversity has been pushed to extinction, witha further 3.5% expected to be lost by 2100, particularly in tropical ecosystems (Newbold et al., 2015).Protected areas are a vital conservation strategy implemented to preserve the remaining forest fragmentsand the species inhabiting them (Hansen & DeFries, 2007). However, species are often forced to migrateout of these regions, due to competition for resources and limited availability of reproductive individualswithin the isolated areas (Wainwright, 2007; Crooks et al., 2011).

Costa Rica is considered to be one of the most biodiverse regions on Earth, boasting 6% of global mammalspecies (Baltensperger & Brown, 2015) and 4% of all extant species (IUCN, 2006), despite only covering0.03% of the world’s land surface (Baltensperger & Brown, 2015). Although over half of the country’sforest has been depleted, 27% of the country is now preserved through a system of approximately 190protected areas. The Osa Peninsula, located on the country’s Southern Pacific coastline, is considered apriority area for conservation. It has numerous protected areas set up, including Corcovado and PiedrasBlancas National Parks, the National Terraba Wetlands, and the Golfo Dulce Forest Reserve (GDFR).Approximately half of the country’s biodiversity can be found within Corcovado National Park on theSouthwest of the peninsula (Kappelle, 2016). The protected lowland wet forests are home to severalcharismatic species, including the Baird’s Tapir, Jaguar and Puma (Carrillo et al., 2002; Garcia et al.,2016; Nielsen et al., 2015), which attract considerable ecotourism to the region.

Although Costa Rica is praised for having one of the most successful protected area systems in the world(Andam et al., 2008), there are many complexities within the protected and surrounding areas thatremain understudied. Therefore, gathering additional data and understanding of these ecosystems andtheir dynamics is key to better inform policymakers and improve local policymaking. Insuring efficientuse of resources, as well as protection and creation of the most biologically beneficial areas possible. Ul-timately avoiding isolation of populations and the subsequent limited sustainability/viability of (animal)populations.

Frontier has been running a volunteer mammal programme on the Osa Peninsula since 2015 specificallyfocussing on the Big Cats and their prey populations. Camera traps have become an essential tool forstudying many mammals to monitor the use of non-protected areas of these often-elusive species. Manyspecies of mammals are very rare, secretive, and move around mostly at night in thick vegetation and/ordifficult terrain, making direct observation in the wild very difficult (Di Bitetti & De Angelo, 2006).Once set up at a specific location, camera traps act as a 24-hour vigilance system. They are designed toturn themselves on every time an animal triggers their motion sensors. They will snap a photo or recorda video of any animal that moves in their line of sight (Foster & Harmsen, 2012). This results in largecollections of photos and videos, some of them showing very interesting behaviour, this data can then beused for many wildlife studies. Developing the use of this technology will allow Frontier to investigatethe mammal diversity across larger areas, without unachievable efforts in the field by project volunteers.

Research Questions

� What is the abundance of Mammal species using the buffer zone that encompasses Carate, OsaPeninsula?

� How diverse are Mammals in the buffer zone that encompasses Carate, Osa Peninsula?

� Do the Mammal species that inhabit Carate, Osa Peninsula, prefer different habitat types? And ifso, which species prefer which habitat types?

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� Are factors such as human disturbance and climate change affecting the activity patterns of mam-mal species within Carate, Osa Peninsula? And if so, How?

6.7.2 Methodology

We are proposing the use of a new methodology based on video records of individuals collected usingcamera traps. Camera traps have recently been used with great success in similar studies, to studythe population densities of wild cats, including Tigers (Panthera tigris) (Karanth, 1995, Carbone et al.,2001), Jaguars (Pathera onca) ( Wallace et al., 2003; Maffei, Cuellar & Noss, 2004; Silver et al., 2004)and Ocelots (Leopardus pardalis) (Trolle & Kery, 2003, 2005; Maffei et al., 2005; Di Bitetti et al., 2006).

Due to the nature of camera traps, the study area has been divided into two time periods (as illustratedin figure 4), and half of the stations will be operating during each sampling period. Each survey willconsist of 2 month long sampling periods, separated by 2-3 days, during which time we will bring thecameras back into base camp and assess them ready for redeployment and shift the cameras to thecamera sites assigned to the second period. Thus, the survey will last 4 months.

Each camera will be active 24 hours a day, capturing videos at both day and night, and will be set upto record the date and time of each trigger event. Motion sensors will be set to medium and an infraredLED flash will be used to produce monochrome videos in the dark, to reduce disruption to the capturedspecies. The cameras will be programmed so that at each trigger event a 13 second video (resolution1080P HD) is recorded, with a 30 second interval between trigger events. The cameras will be checkedevery month for water damage from the heavy rains and humidity, and in order to replace batteries andswap SD cards when necessary.

Figure 51: A map of Carate created using GIS then a grid overlaid to provide equal spacings.The circles represent the acceptable deployment radius around the cameras (250m) to allow forphysical limitations when deploying the cameras.

Project to Date

There are already 5 cameras out in the field, 1 of which was deployed on the 27th of February 2020,another of which was deployed on the 29th of February 2020 and the other 3 of which were deployed onthe 5th March 2020 (as seen in Figure 51). The other 3 cameras of the first sampling period are set to bedeployed on the 10th of March 2020. Each of the cameras will then be checked, batteries and SD cardschanged 1 month after their initial deployment date.

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6.8 An Asessment of the Diversity and Abundance of Birds of Prey inCarate, Osa Peninsula, Costa Rica.

6.8.1 Introduction

Ecological indicators are of utmost importance for detecting environmental change and have widespreadappeal to scientists and the general public (Niemi and McDonald, 2004; Council for Environmental Ed-ucation, 1992). Abundance and diversity of species can be used to measure environmental health e.g.an environment’s amount of resources will be reflected by the number of species/individuals (Councilfor Environmental Education, 1992). As well as assessing environmental health, ecological indicatorscan also be used as barometers assessing ecological resource trends and warning against future ecolog-ical problems (Niemi and McDonald, 2004). Birds of Prey (BoP) are high on the food chain and theirpresence is an indicator of the variety of wildlife in the area and therefore the health of the environment(Council for Environmental Education, 1992). Whilst BoP population changes may largely be due tonatural causes, these can also be man made. Chemicals build up in the environment and are ingested,sometimes resulting in mass die-offs, signalling an ecological problem. Dichlorodiphenyltrichloroethane,an insecticide, thinned the eggshells of the Mauritius kestrel (Falco punctatus) causing the population todecline to just 4 wild birds by 1974 (Jones et al., 1995) and during the 1990’s the Oriental White-BackedVulture (Gyps begalensis) declined by >95% in Pakistan due to the use of diclofenac, a medicinal drug,in Cattle (Bos indicus) and Water Buffalo (Bubalus bubalis) (Green et al., 2004). These examples showthe importance and relevance of measuring the abundance and diversity of BoP over time to deduce thehealth of the environment and detect any changes or potential future problems.

Raptor Migration

A large series of inter-branching migration flyways creates the Mesoamerican Land Corridor whichstretches a total of 4000km from southern Texas to north-western Colombia. This is the largest andone of the most important raptor migration flyways’ in the world (>3 million individuals counted)(Porras-Penaranda et al., 2004). So not only does this study have the potential to contribute towards en-vironmental monitoring (see above) but also towards the knowledge of the Mesoamerican Land Corridoras a raptor migration flyway as the study will occur during raptor migration season in Spring (Garriguesand Dean, 2014).

6.8.2 Methodology

Bildstein and Saborio (2000) conducted research between 07:45 and 16:45 and Porras-Penaranda et al.,(2004) noticed that daily migration activity peaked at 10:00 (Kekoldi) and 12:00 (Bribri); therefore,surveys will be conducted at 10:00am and 15:00 to coincide with peak activity (Thiollay, 1989). Therewill be 2 morning and 2 afternoon surveys per week which will last 40 minutes each.

Transect Surveys

During transect surveys, observers will walk along a randomly selected trail at a pace of 2km/hour stop-ping every 200m to scan the canopy and sky. BoP will only be recorded from a sighting and will not berecorded if seen behind the survey (to avoid survey bias). When a BoP is sighted, we will record the timein 24hrs; species; GPS N and W; and number of individuals. Individuals with the highest probability ofbeing sighted are most likely to be species which do not fly above the canopy, but there is also a chancethat soaring species may be sighted above the canopy where it is open (Thiollay, 1989).

Transect surveys will be used to survey BoP on Gary’s Upper, 3 Ajos, La Leona, Rio Carate, BeachRoad and Road. See the appendix for the transect survey datasheet.

Point Counts

Point count will be used on Lagoon and Playa Carate as these are singular locations that do not requirea walkable transect to survey BoP. These surveys will occur on randomly selected vantage points andthe observers will record all the raptors that are seen. See appendix for the point count datasheet.

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Project to Date

Since the start of the study Black Vultures (Coragyps atratus) have been found to be by far the mostabundant of the 8 sighted species with 155 individuals being counted. The least abundant of the surveyedspecies was the Osprey (Pandion heliaetus) with only one sighting of an individual. Figure 3 shows theaverage abundance for each species since the start of the study.

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6.9 Diversity and Abundance of Birds of Prey in Carate, Osa Peninsula,Costa Rica.

6.9.1 Introduction

Wetlands are considered to be one of the most important ecosystems on Earth; they form a vital compo-nent in key environmental processes, such as the control of flooding, surface water filtration and regulationof global levels of carbon dioxide in the atmosphere. The biodiversity associated with an ecosystem isdependent on the health of the ecosystem itself and wetlands are no exception. If the condition of thewetland is degraded, then the ecosystem resources that it provides to its associated fauna & flora will bein short supply or simply lost. As the wetlands associated species depend on these ecosystem resourcesfor their own survival, it naturally follows that in locations where these ecosystems have been degradedthe associated species will be found in lower abundance and in some cases will be absent altogether. Assuch by monitoring the associated species of the wetland it is possible to evaluate the current state ofhealth for that ecosystem. It is also important to note that wetlands also have a significant value tohuman society for cultural and recreational activities, which will also be lost as these key habitats aredegraded.

Despite the significant value that wetlands have, many are severely impacted by anthropogenic activi-ties. Since the first European settlers arrived in New Zealand many wetlands were greatly diminishedand currently only 10% remain (Clarkston, et al., 2003). Similarly, the wetlands of Florida experiencedheavy habitat loss and degradation due to active harvesting of numerous plants and heavy hunting ofanimals throughout the 19th century (Ogden et al., 1978; Frohring et al., 1988; Ogden, 1994). Manyof the affected species managed to recover due to legal protection however this protection ended in the1930s. A steady decline in species abundance & biodiversity followed due to the extensive alteration andexploitation of the Florida wetlands (Ogden, 1994). Many populations of various species of heron andegret have shown a marked decrease (Ogden, 1996a, Ogden, 1996b). The loss of the many species thatare closely associated with wetlands continues to be a major global problem. Similar trends have beenobserved in over half of all North American shorebird species the majority of which are long distancemigrants (Brown et al., 2001). Migratory birds have very high energy demands and in order to meetthese, they must frequently land in mudflats and shallow wetlands to forage and rest (Skagen and Knoppf1993., Clarkson et al., 2003, Helmers 2003). It has been shown that populations of migratory birds arestruggling in the continental United States due to vast wetland losses and destruction (Brown et al.,2001, Clarkson et al., 2003).

One method of assessing the current condition of a wetland is to assess key indicator species utilisingthe ecosystem and the number of individuals that the ecosystem supports, in order to truly understandthe dynamics of a population long term monitoring programmes are required. Such programmes havebeen shown to provide crucial data that underpins and promotes the conservation of biological groupsand habitats. Avian taxa are well known indicators of the quality and condition of wetland ecosystems(Clarkson et al., 2003). In addition, aquatic birds are relatively easy to survey without collection oranalysing of samples, nor working with complex taxonomic keys (Clarkston et al., 2003).

In terms of biodiversity, Costa Rica is one of the richest nations in the world; it also has a very highlevel of endemism. It is because of this that Costa Rica has attracted significant attention from scientificresearchers. Certain groups within taxon, such as large mammals and endemic terrestrial birds havebeen studied in detail. However, little is known about the life history and ecology of various wading andaquatic birds species in Costa Rica. There is currently little or no data on the wading and shore birdpopulations within Carate, Osa Peninsula, Costa Rica. The results of this project will therefore form avaluable contribution towards the better understanding of the local populations of wetland avian speciesas well as an understanding of the various habitats health and value to migratory species.

6.9.2 Methodology

PCS is a monitoring technique widely used in scientific research of bird species and offers possibilities foroptimal and effective data collection with minimal anthropogenic impact. Each PCS will be conductedby a trained bird observer along with several volunteer assistants. PCS are a simple survey techniquewith an easy to follow method for survey personnel with minimal field experience.

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Each PCS will consist of one point per survey location and each survey will take a total of 30 minutesto complete. At each point the survey team will allow for 5 minutes for the bird activity to return tonormal following the anthropogenic disturbance caused by the arrival of the survey team. Surveys willstart 30 minutes before sunset, allowing surveyors to monitor both roosting & foraging behaviour.

For each sighting the following data was recorded:

� Species

� No. of individuals

� Time of sighting

� Behaviour – Flight, Feeding, Nesting

� Location

� Direction of flight

6.9.3 Project to Date

The first data collection survey on this project was held on 20th January 2020 and currently the projectcompleted its seventh week. Surveys are run three times on a weekly basis with survey points beingvisited once per week. Although the project is still at its very early stages, our observations started togive some results. The most abundant and frequently detected species is the Northern jacana (Jacanaspinosa). The constant presence of adult and juvenile birds gives a hint that this species is residentand breeding throughout the year. The same conclusion could be drawn for the closely related Purplegallinule (Gallinula galeata). Although recorded in considerably smaller numbers, the presence of adultand juvenile birds suggest that this rail is a resident breeder in the area. The same is valid for the localpopulations of Brown pelicans (Pelecanus occidentalis), regularly seen on our surveys. Both adults andjuveniles are present at all times and forage actively in the shallow waters, as the lagoon is shrinking itsvolume throughout the dry season. Different wader species, listed as migrants regularly use the lagoonas a feeding ground. Undoubtedly this place is an import wintering ground for Whimbrels (Numeniusphaeopus), Spotted sandpipers (Actitis macularius) and Semipalmated plovers (Charadrius semipalma-tus), however we need longer field observations in order to support this conclusion. Family Ardeidae-herons and egrets is currently the most diverse avian taxa recorded in the study area. Until present, 9different species are detected on our surveys. All ardeid species except one are recorded in low numbers.The most abundant is the Cattle egret (Bubulculus ibis), using the lagoon as a night roosting site withnumbers fluctuating between 30 and 80 individuals on a daily basis. Other species include Great Blueheron (Ardea heroidalis), the largest heron in the Americas, Tricolored heron (Egretta tricolor), Great(Ardea alba) and Snowy egrets (Egretta thula).

We need more surveys over all seasons of the year in order to assess fully what role the lagoon plays intothe lives of all observed species.

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7 References

Alho, C. 2008. Biodiversity of the Pantanal: response to seasonal flooding regime and to environmentaldegradation. Brazilian Journal of Biology. 68(4), pp. 957-966.

Andam, K.S., Ferraro, P.J., Pfaff, A., Sanchez-Azofeifa, G.A., and Robalino, J.A. 2008. Measuring theeffectiveness of protected area networks in reducing deforestation. Proceedings of the National Academyof Sciences. 105(42), pp. 16089-16094.

Arroyo-Mora, J.P., Sanchez-Azofeifa, G.A., Rivard, B., Calvo, J.C. and Janzen, D.H. 2005. Dynamicsin landscape structure and composition for the Chorotega region, Costa Rica from 1960 to 2000. Agri-culture, Ecosystems & Environment. 106(1), pp. 27-39.

Baker, C.P. 2012. Eye Witness Travel Costa Rica. Dorling Kindersley Limited, London.

Baltensperger, A.P. and Brown, C.L. 2015. Mammalian Biodiversity Conservation at Two Biological Sta-tions in Nicaragua and Costa Rica. In Central American Biodiversity, pp. 351-389. Springer. New York.

Barlow, J., Gardner, T. A., Araujo, I. S., Avila-Pires, T. C., Bonaldo, A. B., Costa, J. E., Esposito, M.C., Ferreira, L. V., Hawes, J., Hernandez, M. I. M., S.Hoogmoed, M., Leite, R. N., Lo-Man-Hung, N. F.,Malcolm, J. R., Martins, M. B., Mestre, L. A. M., Miranda-Santos, R., Nunes-Gutjahr, A. L., Overal,W. L., Parry, L., Peters, S. L., Ribeiro-Junior, M. A., da Silva, M. N. F., da Silva Motta, C. and Peres,C. A. 2007. Quantifying the biodiversity value of tropical primary, secondary, and plantation forests.PNAS, 104 (47), pp. 18555-18560.

Barquero-Edge, P. 2013. Trends in Marine Turtle Nesting and Egg Predation on the Osa Peninsula,Costa Rica. Marine Turtle Newsletter, 138, pp.7-10.

Barrantes, G., Jimenez, Q., Lobo, J., Maldonado, T., Quesada, M. and Quesada, R. 1999. Manejoforestal y realidad nacional en la penınsula de Osa. San Jose, The Cecropia Foundation, Costa Rica.

Behie, A, M., Pavelka, M, S, M. 2015. Chapter 13: Fruit as a Key Factor in Howler Monkey PopulationDensity: Conservation Implications. In: Kowalewski, M, M. Howler Monkeys. Developments in Prima-tology: Progress and Prospects. Springer, New York. pp. 357 – 382.

Bell, K.E. and Donnelly, M.A 2006. Influenced forest fragmentation on structure of frogs and lizards innortheastern Costa Rica. Conservation Biology. 20 (6), pp. 1750-1760.

Berg, A. 1997. Diversity and abundance of birds in relation to forest fragmentation, habitat quality andheterogeneity. Bird Study. 44(3), pp. 355-366.

Berry, N.J., Phillips, O.L., Lewis, S.L., Hill, J.K., Edwards, D.P., Tawatao, T.B., Ahmad, N., Magintan,D., Khen, C.V., Maryati, M., Ong, R.C. and Hamer, K.C. (2010) The high value of logged tropicalforests: lessons from northern Borneo. Biodiversity Conservation. /textbf19(4), pp. 985–997.

Bezy, V.S., Valverde, R.A. and Plante, C.J. 2015. Turtle hatching success as a function of the microbialabundance in nest sand at Ostional, Costa Rica. PloS one. 10(2).

Bildstein. K. L., Saborio. M. 2000. Spring Migration Counts Of Raptors And New World Vultures InCosta Rica. Ornitologia Neotropical. 11. pp. 197-205.

Bird. D. M., Bildstein. D. R. 2007. Raptor Research and Management Techniques. 1st edition. Wash-ington: Institute for Wildlife Research, National Wildlife Federation.

Bohm, M., Collen, B., Baillie, J.E., Bowles, P., Chanson, J., Cox, N., Hammerson, G., Hoffmann, M.,Livingstone, S.R., Ram, M. and Rhodin, A.G. 2013 . The conservation status of the world’s reptiles.Biological Conservation. 157, pp. 372-385.

85

Page 87: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Boinski, S. 1988. The positional behaviour and substrate use of squirrel monkeys: ecological implica-tions. Journal of Human Evolution. 18, pp. 639 – 677.

Boinski, S. 1987. Habitat Use by Squirrel Monkeys (Saimiri oerstedi) in Costa Rica. Folia primatol. 49,pp. 151 – 167.

Boinski, S., Jack, K., Lamarsh, C. and Coltrane, J.A. 1998. Squirrel monkeys in Costa Rica: drifting toextinction. Oryx. 32(1), pp. 45-58.

Bradford, D.F., Franson, S.E., Neale, A.C., Heggem, D.T., Miller, G.R. and Canterbury, G.E. 1998.Bird species assemblages as indicators of biological integrity in Great Basin rangeland. EnvironmentalMonitoring and Assessment. 49(1), pp.1-22.

Brodie, J., Giodano, A., & Ambu, L., 2015. Differential Respones of Large Mammals to Logging andEdge Effects. Mammalian Biology. 80, pp. 7-13.

Brook, B.W., Sodhi, N.S. and Ng, P.K. 2003. Catastrophic extinctions follow deforestation in Singapore.Nature. 424(6947), pp. 420-426.

Brooks, T.M., Mittermeier, R.A., Mittermeier, C.G., Da Fonseca, G.A., Rylands, A.B., Konstant, W.R.and Hilton-Taylor, C. 2002. Habitat loss and extinction in the hotspots of biodiversity. ConservationBiology. 16(4), pp. 909-923.

Brown, C.R., Brown, M.B., Roche, E.A., O’Brien, V.A. and Page, C.E. 2016. Fluctuating survival se-lection explains variation in avian group size. PNAS. 113(18), pp. 5113-5118.

Brown, S. and Lugo, A. E. 1990. Tropical secondary forests. Journal of Tropical Ecology. 6(1), pp. 1–32.

Burger, J. and Gochfeld, M. 2003. Parrot behavior at a Rio Manu (Peru) clay lick: temporal patterns,associations, and antipredator responses. Acta ethol. 6, pp. 23-34.

Burger, J. and Gochfeld, M. 2014. Avian predation on olive ridley (Lepidochelys olivacea) sea turtle eggsand hatchlings: avian opportunities, turtle avoidance, and human protection. Copeia, pp. 109-122.

Butler, R.A. 2006. Tropical Rainforests: Costa Rica. Available from: https://rainforests.mongabay.com/20costarica.htm.

Bustard, H.R. and Greenham, P. 1968. Physical and chemical factors affecting hatching in the green seaturtle, Chelonia mydas (L.). Ecology, 49(2), pp. 269-276.

Campbell, L.M. 1998. Use them or lose them? Conservation and the consumptive use of marine turtleeggs at Ostional, Costa Rica. Environmental Conservation. 25(4), pp. 305-319.

Carbone, C., Christie, S., Conforti, K., Coulson, T., Franklin, N., Ginsberg, J.R., Griffiths, M., Holden,J., Kawanishi, K., Kinnaird, M., Laidlaw, R., Lynam, A., MacDonald, D.W., Martyr, D., McDougal,C., Nath, L., O’Brien, T., Seidensticker, J., Smith, D.J.L., Sunquist, M., Tilson, R. & Wan Shahruddin,W.N. (2001). The use of photographic rates to estimate densities of tigers and other cryptic mammals.Anim. Conserv. 4, pp. 75–79.

Carrillo, E., Saenz, J.C. and Fuller, T.K. 2002. Movements and activities of white-lipped peccaries inCorcovado National Park, Costa Rica. Biological Conservation. 108(3), pp. 317-324.

Carrillo, E., Wong, G. and Cuaron, A.D. 2000. Monitoring mammal populations in Costa Rican pro-tected areas under different hunting restrictions. Conservation Biology. 14(6), pp. 1580-1591.

Cartmill, M., 1974. Pads and claws in arboreal locomotion. In Primate Locomotion. Jenkins, F.A. (Ed.)Academic Press, New York.

86

Page 88: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Caruso, N.M., Sears, M.W., Adams, D.C. and Lips, K.R. 2014. Widespread rapid reductions in bodysize of adult salamanders in response to climate change. Global Change Biology. 6(20), pp. 1751-1759.

Cates, R.G. and Orians, G.H. 1975. Successional status and the palatability of plants to generalizedherbivores. Ecology. 2(56), pp. 410-418.

Chacon-Chaverri, D. and Eckert, K.L. 2007. Leatherback sea turtle nesting at Gandoca Beach inCaribbean Costa Rica: management recommendations from fifteen years of conservation. ChelonianConservation and Biology. 61, pp. 101-110.

Chapman, C.A. 1995. Primate seed dispersal: coevolution and conservation implications. EvolutionaryAnthropology. 4(3), pp. 74-82.

Chapman, A.C. 1988 Patterns of foraging and range use by three species of Neotropical primates. Pri-mates. 29, pp. 177-194.

Chaves, O, M., Stoner, K, E., Arroyo-Rodriguez, V. 2011. Seasonal Difference in Activity Patterns ofGeoffroyi’s Spider Monkeys (Ateles geoffroyi) Living in continuous and Fragmented Forests in SouthernMexico. International Journal of Primatology. 32, pp. 960 – 973.

Clarckson R.B., Sorrel B., Reeves N., Champion P., Partridge T., Clarckson B., 2003. Handbook formonitoring wetland condition.

Cleveland, C.C., Wieder, W.R., Reed, S.C. and Townsend, A.R. 2010. Experimental drought in a trop-ical rain forest increases soil carbon dioxide losses to the atmosphere. Ecology. 91(8), pp. 2313-2323.

Cornell, 2019. Riverside Wren (Cantorchilus semibadius), In Neotropical Birds Online (T. S. Schulen-berg, Editor). Cornell Lab of Ornithology, Ithaca, NY, USA. Retrieved from Neotropical Birds Online:https://neotropical.birds.cornell.edu/Species-Account/nb/species/rivwre1

Council for Environmental Education. 1992. Environmental Barometer. [Accessed: 29th January 2020].Available from: https://www.fws.gov/uploadedFiles/Region 1/NWRS/Zone 2/Inland Northwest Complex/Turnbull/Documents/EE/Animal Tracks/Environmental%20Barometer%281%29.pdf

Cowlishaw, G. and Dunbar, R.I. 2000. Primate conservation biology, University of Chicago Press.

Crandell, K, E., Herrel, A., Sasa, M., Losos, J. B., Autumn, K. 2014. Stick or grip? Co-evolution ofadhesive toepads and claws in Anois lizards. Zoology, 117(2014) pp. 363–369

Cristobal-Azkarate, J., Vea, J., Asensio, N. and Rodrıgues-Luna, E. 2005. Biogeographical and florisiticpredictors of the presence and abundance of mantled howlers (Alouatta palliata mexiacana) in rainforestfragments at Los Tuxtlas, Mexico. Am. J. Primatol. 67, pp. 209-222.

Crooks, K.R., Burdett, C.L., Theobald, D.M., Rondinini, C. and Boitani, L. 2011, Global patterns offragmentation and connectivity of mammalian carnivore habitat. Biological sciences. 366(1578), pp.2642-2651.

Cropp, S. and Boingki, S. 2000. The Central American squirrel monkey (Saimiri oerstedii): introducedhybrid or endemic species? Molecular Phylogenetics and Evolution. 16(3), pp. 350-365.

Cuaron, A.D., Helgen, K. and Reid, F. 2016. Conepatus semistriatus. The IUCN Red List of ThreatenedSpecies 2016: e.T41633A45210987. Available at: https://www.iucnredlist.org/species/41633/45210987[Accessed 5 Aug. 2019].

Cuaron, A.D., Helgen, K., Reid, F., Pino, J. and Gonzalez-Maya, J.F. 2016. Nasua narica. The IUCNRed List of Threatened Species 2016: e.T41683A45216060. Available at: https://www.iucnredlist.org/species/41683/45216060[Accessed 5 Aug. 2019].

87

Page 89: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Cuaron, A.D., Morales, A., Shedden, A., Rodrıguez-Luna, E., de Grammont, P.C. and Cortes- Ortiz, L.2008. Ateles geoffroyi. The IUCN Red List of Threatened Species 2008: e.T2279A9387270. Availableat: https://www.iucnredlist.org/species/2279/9387270 [Accessed 5 Aug. 2019].

Cuaron, A.D., Reid, F., Helgen, K. and Gonzalez-Maya, J.F. 2016. Peira barbara. The IUCN Red List ofThreatened Species 2016: e.T41644A45212151. Available at: https://www.iucnredlist.org/species/41644/45212151[Accessed 5 Aug. 2019].

Cuaron, A.D., Shedden, A., Rodrıguez-Luna, E., de Grammont, P.C., Link, A., Palacios, E., Morales,A. and Cortes-Ortiz, L. 2008. Alouatta palliata. The IUCN Red List of Threatened Species 2008:e.T39960A10280447. Available at: https://www.iucnredlist.org/fr/species/39960/10280447 [Accessed 5Aug. 2019].

Dear, F., Vaughan, C. and Polanco, A. M. 2010. Current status and conservation of the scarlet macaw(Ara macao) in the Osa Conservation Area (ACOSA), Costa Rica. UNED Research Journal. 2(1).

De-Azevedo. 2008. Food Habits and Livestock Depredation of Sympatric Jaguars and Pumas in theIguacu National Park Area, South Brazil. Biotropica. 40, pp. 494 – 500.

DeFries, R., Hansen, A., Newton, A.C., and Hansen, M.C. 2005. Increasing isolation of protected areasin tropical forests over the past twenty years. Ecological applications. 15, pp. 19-26.

Dent, D.H., and Wright, S.J. 2009. The future of tropical species in secondary forests: a quantitativereview. Biological conservation. 142(12), pp. 2833-2843.

Di Bitetti, M. & De Angelo, C. 2006. Density, Habitat Use and Activity Patterns of Ocelots (Leoparduspardalis) in the Atlantic Forest of Misiones, Argentina. Journal of Zoology.

Dirzo, R., Young, H.S., Galetti, M., Ceballos, G., Isaac, N.J.B. and Collen, B. 2014. Defaunation in theAnthropocene. Science. 345(6195), pp. 401–406.

Donlan, C.J., Wingfield, D.K., Crowder, L.B. and Wilcox, C. 2010. Using expert opinion surveys to rankthreats to endangered species: a case study with sea turtles. Conservation Biology. 24(6), pp. 1586-1595.

Drake, D.L. 1996. Marine turtle nesting, nest predation, hatch frequency and nesting seasonality on theOsa Peninsula, Costa Rica. Chelonian Conservation and Biology. 2, pp. 89-92.

Dudley, P.N. and Porter, W.P. 2014. Using emperical and mechanistic models to assess global warmingthreats to leatherback sea turtles. Marine Ecology Progress Series. 501, pp. 265-278.

Ernst, R. and Rodel, M.O. 2006. Community assembly and structure of tropical leaf-litter anurans.Ecotropica. 12, pp. 113-129.

Estrada, A. and Coates-Estrada, R. 1996. Tropical rain forest fragmentation and wild populations ofprimates at Los Tuxrlas, Mexico. International journal of primatology. 17(5), pp. 759-783.

Fagan, M.E., DeFries, R.S., Sesnie, S.E., Arroyo, J.P., Walker, W., Soto, C., Chazdon, R.L. and Sanchun,A. 2013. Land cover dynamics following a deforestation ban in northern Costa Rica. Environmental Re-search Letter. 8(3).

Fagan, M.E., DeFries, R.S., Sesnie, S.E., Arroyo-Mora, J.P. and Chazdon, R.L. 2016. Targeted reforesta-tion could reverse declines in connectivity for understory birds in a tropical habitat corridor. EcologicalApplications. 26(5), pp. 1456-1474.

Fennell, D.A. and Eagles, P.F. 1990. Ecotourism in Costa Rica: a conceptual framework. Journal ofpark and recreation administration. 8, pp. 23-34.

88

Page 90: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Ferguson, B. G., Vandermeer, J. , Morales, H. and Griffith, D. M. 2003. Post-Agricultural Succession inEl Peten, Guatemala. Conservation Biology. 17, pp. 818-828.

Fearnside, P.M. and Guimaraes, W.M. 1996. Carbon uptake by secondary forests in Brazilian Amazonia.Forest Ecology and Management. 80(1–3), pp. 35-46.

Fish, M.E., Cote, I.M., Gill, J.A., Jones, A.P., Renshoff, S. and Watkinson, A.R. 2005. Predicting theimpact of sea-level rise on the Caribbean Sea turtle nesting habitat. Conservation biology. 19(2), pp.482-491.

Fisher, B. and Christopher, T. 2007. Poverty and biodiversity: measuring the overlap of human povertyand biodiversity hotspots. Ecological Economic. 62(1), pp. 93-101.

Flora and Fauna International. 2019. Costa Rica. Available from: https://www.fauna-flora.org/countries/costa-rica. [Accessed: 12 Dec 2019].

Folt, B. and Reider, K.E. 2013. Leaf-litter herpetofaunal richness, abundance, and community assemblyin mono-dominant plantations and primary forest of northeastern Costa Rica. Biodiversity and conser-vation. 22(9), pp. 2057-2070.

Foster, R. & Harmsen, B. 2012. A Critique of Density Estimation from Camera-Trap Data. Journal ofWildlife Management.

Fournier, L, A. Not dated. Cecropia obtusifolia Bertol. In: Tropical Tree Seed Manual. No publicationdetails available.

Fowler, L.E. 1979. Hatching success and nest predation in the green sea turtle, Chelonia mydas, atTortuguero, Costa Rica. Ecology. 60(5), pp. 946-955.

Frohring, P.C., D.P. Voorhees and J.A. Kushlan 1998. History of wading bird populations in the FloridaEverglades: a lesson in the use of historical information. Colonia waterbirds. 11, pp. 328-335.

Fuentes, M.M.P.B., Limpus, C.J. and Haman, M. 2011. Vulnerability of sea turtle nesting grounds toclimate change. Global Change Biology. 17, pp. 140-153.

Garriguez R., Dean R., 2014. The Birds of Costa Rica. A Field Guide. A Zona Tropical Publication.Cornell University Press, Ithaca, New York.

Garcıa, M., Jordan, C., O’Farril, G., Poot, C., Meyer, N., Estrada, N., Leonardo, R., Naranjo, E., Simons,A., Herrera, A., Urgiles, C., Schank, C., Boshoff, L. and Ruiz-Galeano, M. 2016. Tapirus bairdii. TheIUCN Red List of Threatened Species 2016: e.T21471A45173340. Available at: https://www.iucnredlist.org/species/21471/45173340[Accessed 5 Aug. 2019].

Gargiullo, M. B., Magnuson, B. and Kimball, L. 2008. A Field Guide to Plants of Costa Rica. Oxford,Oxford University Press.

Gentry, A.H., 1988. Tree species richness of upper Amazonian forests. Proceedings of the NationalAcademy of Sciences. 85, pp. 156-159.

Gibson, L., Lee, T.M., Koh, L.P., Brook, B.W., Gardner, T.A., Barlow, J., Peres, C.A., Bradshaw, C.J.,Laurance, W.F., Lovejoy, T.E. and Sodhi, N.S. 2011. Primary forests are irreplaceable for sustainingbiodiversity. Nature. 478(7369), pp. 378-391.

Government, C.R., 2003. Costa Rican Government Decree No. 31514-MINAE, Normas Generales parael acceso a los elementos y Recursos Geneticos y Bioquımicos de la Biodiversidad. Gaceta 214, del 15 dediciembre del 2003., Avaliable at: http://www.minae.go.cr/index.php/es/”.

89

Page 91: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Green. R. E., Newton. I., Shultz. S., Cunningham. A. A., Gilbert. M., Pain. D. J., Prakash. V. 2004.Diclofenac poisoning as a cause of vulture population declines across the Indian subcontinent. Journalof Applied Ecology. 41(5).

Guariguata, M. R., Rheingans, R. and Montagnini, F. 1995. Early Woody Invasion Under Tree Planta-tions in Costa Rica: Implications for Forest Restoration. Restoration Ecology. 3, pp. 252-260.

Guariguata, M.R. and Ostertag, R. 2001. Neotropical secondary forest succession: changes in structuraland functional characteristics. Forest Ecology and Management. 148(1–3), pp. 185-206.

Gutierrez B. L., Allmeyda Zambrano, A. M., Almeyda Zambrano, S. L., Quispe Gil, C. A., Bohlman,S., Avellan Arias, E., Mulder, G., Ols, C., Dirzo, R., DeLuycker, A. M., Lewis, K. and Broadbent, E. N.2019 An island of wildlife in a human-dominated landscape: The last fragment of primary forest on theOsa Peninsula’s Golfo Dulce coastline, Costa Rica. Plos One. 14(3), pp. 1-19.

Hansen, A.J. and DeFries, R. 2007. Ecological mechanisms linking protected areas to surrounding lands.Ecological Applications. 17(4), pp. 974-988.

Hart, C.E., Ley-Qunonez, C.P., Abreu-Grobois, F.A., Plata-Rosas, L.J., Llamas-Gonzalez, I., Oceguera-Camacho, D.K.E. and Zavala-Norzagaray, A.A., 2019. Possible hybridization between East Pacific GreenChelonia mydas and Olive Ridley Lepidochelys olivacea sea turtles in northwest Mexico. Amphibian &Reptile Conservation, 13(2), pp.174-180.

Hawkes, L.A., Broderick, A.C., Godfrey, M.H. and Godley, B.J. 2007. Investigating the potential im-pacts of climate change on the marine turtle population. Global Change Biodiversity. 13(5), pp. 923-932.

Helmers D.L., (1992) Shorebird management manual. Western Hemisphere Shorebird Reserve Network,Manoment.

Henderson, C.L. and Adams, S. 2010. Birds of Costa Rica: a field guide. 64th ed. University of TexasPress, Texas.

Henderson, C.L. 2002. Field guide to the wildlife of Costa Rica. 51st ed. University of Texas Press, Texas.

Herzog, S.K., Kessler, M. and Cahill, T.M. 2002. Estimating species richness of tropical bird communi-ties from rapid assessment data. The Au. 119(3), pp. 749-769.

Honarvar, S., O’Connor, M. and Spotilla, J. 2008. Density-dependent effects on hatching success of theolive ridley turtle, Lepidochelys olivacea. Oecologia. 157(2), pp. 221-230.

Horn, H.S. 1974. The ecology of secondary succession. Annual review of ecology and systematics. 1(5),pp. 25-37.

Howard, R., Bell, I. and Pike, D.A. 2014. Thermal tolerances of sea turtle embryos: current understand-ing and future directions. Endangered Species Research. 26, pp. 75-86.

ITTO. 2002. International Tropical Timber Organisation Guidelines for the Restoration, Managementand Rehabilitation of Degraded and Secondary Tropical Forests. Policy Development Series 13.

IUCN, 2019. Red List of Threatened Species, Retrieved from: www.iucnredlist.org.

Johnson, J.D., Mata-Silva, V. and Wilson, L.D. 2015. A conservation reassessment of the Central Amer-ican herpetofauna based on the EVS measure. Amphibian & Reptile Conservation. 2(9), pp. 1-94.

Jones, G., Jacobs, D.S., Kunz, T.H., Wilig, M.R. and Racey, P.A. 2009. Carpe noctem: The importanceof bats as bioindicators. Endangered Species Research. 8, pp. 93-115.

90

Page 92: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Junk, W. E. (Ed.). 2013. The central Amazon floodplain: ecology of a pulsing system. Springer-VerlagBerlin Heidelberg.

Kappelle, M. 2016. Costa Rica’s Ecosystems: Setting the stage. Costa Rican Ecosystems. University ofChicago Press, pp. 3.

Karanth, K.U. (1995). Estimating tiger Panthera tigris populations from camera trap data using cap-ture–recapture models. Biol. Conserv. 71, pp. 333–338.

Kelez, S., Velez-Zuazo, X. and Pacheco, A.S., 2016. First record of hybridization between green Che-lonia mydas and hawksbill Eretmochelys imbricata sea turtles in the Southeast Pacific. PeerJ, 4, p.e1712.

Keuroghlian, A., Desbiez, A., Reyna-Hurtado, R., Altrichter, M., Beck, H., Taber, A. and Fragoso,J.M.V. 2013. Tayassu pecari. The IUCN Red List of Threatened Species 2013: e.T41778A44051115.Available at: https://www.iucnredlist.org/species/41778/44051115 [Accessed 5 Aug. 2019].

Keyghobadi, N. 2007. The genetic implications of habitat fragmentation for animals. Canadian Journalof Zoology. 85(10), pp. 1049-1064.

Klimes, P., Idigel, C., Rimandai, M., Fayle, T.M., Janda, M., Weiblen, G.D. and Novotny, V. 2012. Whyare there more arboreal ant species in primary than in secondary tropical forests? Journal of AnimalEcology. 81(5), pp. 1103-1112.

Korein, E., Caballol, A., Lovell, P., Exley, L., Porras Marin, C., Carrillo, J., Bond, G. Capria, L., Earl,S., Ferrari, O.M., Hamm, J., Johnson-Gutierrez, S., King, C., Malmierca, A., McAnally, L. Price, E.Riddick, E. and Stokes, L. 2019. Using Bamboo Nest Covers to Prevent Predation on Sea Turtle Eggs.Marine Turtle Newsletter. 156, pp. 33-37.

Krupnick, G. and Knowlton, N. 2017. Earth Optimism: success stories in plant conservation. Annals ofthe Missouri Botanical Garden. 102(2), pp. 331-340.

Lamb, D., Laurence, W.F. and Bierregaard, R.O. 1997. Rejoining habitat remnants: Restoring degradedrainforest lands. Tropical Forest Remnants: Ecology, Management, and Conservation of FragmentedCommunities. University of Chicago press, pp. 366-385.

Larsen, T. and Toft, R. 2010. Osa: Where the rainforest meets the sea. Zona Tropical Publications.

Laurencio, D. and Malone, J.H. 2009. Amphibians and reptiles of Parque Nacional Carara, a transi-tional herpetofaunal assemblage in Costa Rica. Herpetological Conservation and Biology. 4, pp. 120-131.

Lei, J. and Booth, D.T. 2017. How best to protect the nests of the endangered loggerhead turtle Carettacaretta from monitor lizard predation. Chelonian Conservation and Biology 16(2), pp. 246-249.

Leenders, T. 2016. Amphibians of Costa Rica: A Field Guide. Cornell University Press.

Leenders, T. 2019. Reptiles of Costa Rica: A Field Guide. Comstock Publishing Associates.

Limpus, C.J., Baker, V. and Miller, J.D. 1979. Movement induced mortality of loggerhead eggs. Her-petologica. 35(4), pp.335-338.

Mackey, B., DellaSala, D.A., Kormos, C., Lindenmayer, D., Kumpel, N., Zimmerman, B., Hugh, S.,Young, V., Foley, S., Arsenis, K. and Watson, J.E., 2015. Policy options for the world’s primary forestsin multilateral environmental agreements. Conservation letters. 8(2), pp. 139-147.

Maffei, L., Cuellar, E. & Noss, A. (2004). One thousand jaguars (Panthera onca) in Bolivia’s Chaco?Camera trapping in the Kaa-Iya National Park. J. Zool. (Lond.) 262, pp. 295–304.

91

Page 93: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Maffei, L., Noss, A.J., Cue´ llar, E. & Rumiz, D.I. (2005). Ocelot (Felis pardalis) population densities,activity, and ranging behaviour in the dry forests of eastern Bolivia: data from camera trapping. J.Trop. Ecol. 21, pp. 1–6.Manosa. S., Mateos. E., Pedrocchi. V. 2003. Abundance Of Soaring Raptors In The Brazilian AtlanticRainforest. J. Raptor. Res. 37(1). pp. 19 – 30.

Marineros L. and Vaughan C. 1995. Scarlet macaws of Carara, p.445- 467. In: Abramson, J., Speer,B.L., and Thomsen, J.B. (Eds). The large macaws: their care, breeding and conservation. Raintreepublications California.

Marques. T., Rexstad. E., Miller. D. Not dated. What is distance sampling? [Accessed: 30th January2020]. Available from: distancesampling.org/whatisds.html

Mascarenhas, R., Santos, R. and Zeppelini, D. 2004. Plastic debris ingestion by sea turtle in Paraıba,Brazil. Marine pollution bulletin. 49(4), pp. 354-355.

Masello, J., Pagnossin, M., Sommer, C. and Quillfeldt, P. 2006. Population size, provisioning frequency,flock size and foraging range at the largest known colony of Psittaciformes: the Burrowing Parrots ofthe north-eastern Patagonian coastal cliffs. Emu - Austral Ornithology. 106, pp. 69-79.

Maulany, R.I., Booth, D.T. and Baxter, G.S. 2012. Emergence success and sex ratio of natural andrelocated nests of olive ridley turtles from Alas Purwo National Park, East Java, Indonesia. Copeia,2012(4), pp.738-747.

McCoy, C.J., Vogt, R.C. and Censky, E.J. 1983. Temperature-controlled sex determination in the seaturtle Lepidochelys olivacea. Journal of Herpetology. 17, pp. 404–406.

Miller, J.D. and Limpus, C.J. 1983. A method for reducing movement-induced mortality in turtle eggs.Marine Turtle Newsletter. 26, pp. 10-11.

Milton, K. 1981. Food choice and digestive strategies of two sympatric primate species. The AmericanNaturalist. 117, pp. 496-505.

Minca, C. and Linda, M. 2000. Forest tourism and recreation. Case studies in environmental manage-ment. Ecotourism on the edge: the case of Corcovado National Park, Costa Rica. CABI Publishing,Wallingford, Oxon, pp. 103-126.

Mittermeier, R. A., Robles Gil, P., Hoffman, M., Pilgrim, J., Brooks, T., Mittermeier, C. G., Lamoreuz,J. and Da Fonseca, G. A. B. 2004. Hotspots Revisited. Earth’s Biologically Richest and Most EndangeredTerrestrial Ecoregions. Conservation international, CEMEX, Mexico City.

Morris E.K, Caruso T., Buscot F., Fischer M., Hancock C., Maier T.S, Meiners T., Muller C., Ober-maier E., Prati D., Socher S.A., Sonnemann I., Waschke T., Wurst S., Rillig M.C. 2014. Choosing andusing diversity indices: insights for ecological applications from the German Biodiversity Exploratories.Ecology and Evolution. 4(18), pp. 3514-3524.

Mortimer, J.A., Meylan, P.A. and Donnelly, M. 2007. Whose turtles are they,anyway? Molecular Ecol-ogy. 16(1), pp. 17-18.

Murcia, C. 1995. Edge effects in fragmented forests: Implications for conservation. Trends in Ecologyand Evolution. 10(2), pp. 58-62.

Myster, R. W. 2014. Primary vs. secondary forests in the Neotropics: two case studies after Agriculture.New York, Nova Science Publishers, Inc.

Nationalgeographic.com. 2019. Four places where humans are living in sync with the natural world. [on-line] Available at: https://www.nationageographic.com/environment/2019/07/partner-content-living-in-sync-with-the-natural-world/ [Accessed 2 Dec. 2019]

92

Page 94: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Newbold, T., Hudson, L. N., Hill, S. L., Contu, S., Lysenko, I., Senior, R. A. 2015. Global effects of landuse on local terrestrial biodiversity. Nature. 520(7545), pp. 45-50.

Nielsen, C., Thompson, D., Kelly, M. and Lopez-Gonzalez, C.A. 2015. Puma concolor. The IUCN RedList of Threatened Species 2015: e.T18868A97216466. Available at: https://www.iucnredlist.org/species/18868/97216466[Accessed 5 Aug. 2019].

Niemi. G. J., McDonald. M. E. 2004. Application of ecological indicators. Annual Review of Ecology,Evolution and Systematics. 35, pp. 89-111.

Nunn, C. and Altizer, S.M. 2006. Infectious diseases in primates: behaviour ecology and evolution, Ox-ford University Press, Oxford.

O’Connor, J.M., Limpus, C.J., Hofmeister, K.M., Allen, B.L. and Burnett, S.E. 2017. Anti-predatormeshing may provide greater protection for sea turtle nests than predator removal. PloS one. 12(2), pp.1-11.

Oliveira, T., Paviolo, A., Schipper, J., Bianchi, R., Payan, E. and Carvajal, S.V. 2015. Leopar-dus wiedi i. The IUCN Red List of Threatened Species 2015: e.T11511A50654216. Available at:https://www.iucnredlist.org/species/11511/50654216 [Accessed 10 Dec. 2019].

Olkowicz, S., Kocourek, M., Lucan, R.K., Portes, M., Fitch, W.T., Herculano-Houzel, S. and Nemec, P.2016. Birds have primate-like numbers of neurons in the forebrain. Proceedings of the National Academyof Sciences. 113(26), pp. 7255–7260.

Ogden J.C 1994. A comparison of wading bird nesting colony dynamics (1931- 1946 and 1974-1989) asan indication of ecosystem conditions in the southern Everglades. pp. 533-570 in S.M.Davis and J.C.Ogden editors. Everglades: the ecosystem and its restoration. St. Lucie press, Delray beach, Florida,USA.

Ogden J.C., 1996a- Snowy egret. Pages 420-431 in J.A. Rodgers, Jr., H.W. Kale, II, and H.T. Smith,editors. Rare and endangered biota of Florida. Volume V. Birds. University Press of Florida, Gainesville,USA.

Ogden J.C., 1996b- Tricolored heron. Pages 432- 441 in J.A. Rodgers, JR., H.W. Kalle II, and H.T.Smitheditors. Rare and endangered biota of Florida. Volume V. Birds. University press of Florida, Gainesville,USA.

Osa Conservation, 2016. Osa Conservation, viewed 16 November 2016, Available at: http://psaconservation.org/projects/wildlife/birds/.

Ossmann, M. 2019. Sea turtle nesting trends from 2011-2017 on the Osa Peninsula, Costa Rica. (Doc-toral dissertation, Duke University).

Parsons, J. 1983. Costa Rican Natural History, University of Chicago Press, Chicago, IL.

Pearse, D.E. and Avise, J.C., 2001. Turtle mating systems: behavior, sperm storage, and genetic pater-nity. Journal of Heredity, 92(2), pp. 206-211.

Pike, D.A. 2014. Forecasting the viability of sea turtle eggs in a warming world. Global change biology.20, pp. 7-15.

Pinheiro, T., Ferrari, S, F. 2013. Activity budget, diet, and use of space by two groups of squirrelmonkeys (Saimiri sciureus) in eastern Amazonia. Primates. DOI: 10.1007/s10329-013-0351-9.

Pinou, T., Pacete, K.J., De Niz, A.P., Gall, L. and Lazo-Wasem, E, 2009. Lunar illumination and seaturtle nesting. Herpetol. Rev, 40, pp. 409-410.

93

Page 95: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Plotkin, P., Wicksten, M. and Amos, A. 1993. Feeding ecology of the loggerhead sea turtle Carettacaretta in the Northwestern Gulf of Mexico. Marine Biology. 115, pp. 1-5.

Porras-Penaranda. P., Robichaud. L., Branch. R. 2004. New Full-Season Count Sites For Raptor Mi-gration In Talamanca, Costa Rica. Ornitologie Neotropical. 15. pp. 267-278.

R Core Team. R: A Language and Environment for Statistical Computing. In: R Foundation for Statis-tical Computing. Vienna, Austria; 2016. Available from: https://www.r-project.org/[Accessed 5 Aug.2019].

Rees, A.F., Alfaro-Shigueto, J., Barata, P., Bjorndal, K.A., Bolten, A.B., Bourjea, J., Broderick, A.C.,Campbell, L.M., Cardona, L., Carreras, C. and Casale, P. 2016. Are we working towards global researchpriorities for management and conservation of sea turtles?. Endangered Species Research. 31, pp. 337-382.

Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J. and Hirota, M.M. 2009. The BrazilianAtlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conser-vation. Biological conservation. 142(6), pp. 1141-1153.

Salom-Perez, R., Carrillo, E., Saenz, J.C. and Mora, J.M. 2007. Critical condition of the jaguar Pantheraonca population in Corcovado National Park, Costa Rica. Oryx. 41, pp. 51-56.

Sanchez-Azofeifa, G., Rivard, B., Calvo, J. and Moorthy, I. 2002. Dynamics of tropical deforestationaround national parks: remote sensing of forest change on the Osa Peninsula of Costa Rica. MountainResearch and Development. 22(4), pp. 352-358.

Sanchez-Azofeifa, G.A., Daily, G.C., Pfaff, A.S. and Busch, C. 2003. Integrity and isolation of CostaRica’s national parks and biological reserves: examining the dynamics of land-cover change. BiologicalConservation. 109, pp. 123-135.

Sanchez-Azofeifa, G.A., Harriss, R.C. and Skole, D.L. 2001. Deforestation in Costa Rica: a quantitativeanalysis using remote sensing imagery. Biotropica. 33(3), pp. 378-384.

Santos, K.C., Livesey, M., Fish, M. and Lorences, A.C. 2017. Climate change implications for the nestsite selection process and subsequent hatching success of a green turtle population. Mitigation and Adap-tation Strategies for Global Change. 22, pp. 121-135.

Scheffers, B.R., Edwards, D.P., Diesmos, A., Williams, S.E. and Evans, T.A. 2014. Microhabitats reduceanimal’s exposure to climate extremes. Global change biology. 2(20), pp. 495-503.

Sekercioglu, C.H., Loarie, S.R., Brenes, F.O., Ehrlich, P.R. and Daily, G.C. 2007. Persistence of forestbirds in the Costa Rican agricultural countryside. Conservation Biology. 21(2), pp. 482-494.

Shvidenko, A.Z., Gustafson, E., McGuire, A.D., Kharuk, V.I., Schepaschenko, D.G., Shugart, H.H.,Tchebakova, N.M., Vygodskaya, N.N., Onuchin, A.A., Hayes, D.J. and McCallum, I. 2013. Terrestrialecosystems and their change. In Regional environmental change in Siberia and their global consequences.Springer Environmental Science and Engineering pp. 171-249.

Silver, S.C., Ostro, L.E.T., Marsh, L.K., Maffei, L., Noss, A.J., Kelly, M.J., Wallace, R.B., G ´omez, H.& Ayala, G. 2004. The use of camera traps for estimating jaguar Panthera onca abundance and densityusing capture/ recapture analysis. Oryx. 38, pp. 148–154.

Skagen S.K., Knopf F.L., 1993. Toward conservation of mid- continental shorebird migrations. Conserv.Biol. 7, pp. 533- 541.

Skrinyer, A. 2016. Living on the edge: An Assessment of Habitat Disturbance and Primate Use on theOSA Peninsula, Costa Rica. Kent University Thesis.

94

Page 96: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Skutch, A.F. 2001. Life history of the Riverside Wren. Journal of Field Ornithology. 72, pp. 1-12.

Snyder, N. and Beissinger, G. 1992. New World Parrots in Crisis: Solutions from Conservation Biology.Smithsonian Institution Press, Washington, D.C., USA.

Solorzano, R., de Camino, R., Woodward, R., Tosi, J. and Watson, V. 1991. Accounts Overdue: NaturalResource Depreciation in Costa Rica, World Resources Institute, Washington, DC.

Spaan, D., Ramos-Fernandez, G., Schaffner, C. M., Pinacho-Guendulain, B. and Aureli, F. 2017. Howsurvey design affects monkey counts: a case study on individually recognized spider monkeys (Atelesgeoffroyi). Folia Primatologica. 88, pp. 409-420.

Stan, K. and Sanchez, A. 2017. Modelling deforestation trends in Costa Rica and predicting future forestsustainability. In EGU General Assembly Conference Abstracts. 19, pp. 556.

Stone, A, I. 2007. Responses of Squirrel Monkeys to Seasonal changes in Food Availability in an EasternAmazonian Forest. American Journal of Primatology. 69, pp. 142 – 157.

Stoner. K. E., 1996. Habitat Selection and Seasonal Patterns of Activity and Foraging of Mantled Howl-ing Monkeys (Alouatta Palliata) in Northeastern Costa Rica. International Journal of Primatology. 17.

Stotz, D.F., Fitzpatrick, J.W., Parker, T.A. and Moskovits, D.K. 1996. Neotropical Birds: Ecology andConservation. University of Chicago Press, Chicago.

Tarano, Z., Lopez, M, C. 2015. Behavioural Repertoires and Time Budgets of Semi-Free-Ranging andCaptive Groups of Wedge-Capped Capuchin Monkeys, Cebus olivaceus, in Zoo Exhibits in Venezuela.Folia Primatol. 86, pp. 203 – 222.

Temple, S.A. and Wiens, J.A. 1989. Bird populations and environmental changes: can birds be bio-indicators. American Birds. 43(2), pp. 260-270.

Thiollay. J. 1989. Censusing Of Diurnal Raptors In A Primary Rain Forest: Comparative Methods AndSpecies Detectability. J. Raptor Res. 23(3). pp. 72-84.

Thogmartin, W.E. and McKann, P.C. 2014. Large-scale climate variation modifies the winter groupingbehavior of endangered Indiana bats. J Mammal. 95, pp. 117-127.

Tisdell, C. and Wilson, C. 2005. Do open-cycle hatcheries relying on tourism conserve sea turtles? Srilankan developments and economic–ecological considerations. Environmental management. 35(4), pp.441-452.

Tomillo, P.S., Saba, V.S., Piedra, R., Paladino, F.V. and Spotila, J.R. 2008. Effects of illegal harvest ofeggs on the population decline of leatherback turtles in Las Baulas Marine National Park, Costa Rica.Conservation biology. 22(5), pp. 1216-1224.

Tripathy, B. and Rajasekhar, P.S. 2009. Natural and anthropogenic threats to olive ridley sea turtles(Lepidochelys olivacea) at the rushikulya rookery of Orissa coast, India. Indian Journal of Geo-MarineSciences. 38(4), pp. 439-443.

Trolle, M. & Kery, M. (2003). Estimation of ocelot density in the Pantanal using capture–recaptureanalysis of camera trapping data. J. Mammal. 84, pp. 607–614.

United Nations Environment Programme. 2019. Costa Rica named ‘UN Champion of the Earth’ forpioneering role in fighting climate change. Available at: https://www.unenvironment.org/news-and-stories/press-release/costa-rica-named-un-champion-earth-pioneering-role-fighting-climate. [Accessed 12Dec. 2019].

95

Page 97: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

Urban, M.C., Richardson, J.L. and Freindenfelds, N.A. 2014. Plasticity and genetic adaptations mediateamphibian and reptile responses to climate change. Evolutionary applications. 7, pp. 88-103.

Valverde, R.A., Wingard, S., Gomez, F., Tordoir, M.T and Orrego, C.M. 2010. Field lethal incubationtemperature of olive ridley sea turtle Lepidochelys olivacea embryos at a mass nesting rookery. Endan-gered Species Research. 12, pp. 77-86.

Vanhooydonck, B., Herrel, A., Irschick, D.J., 2006. Out on a limb: the differential effect of substratediameter on acceleration capacity in Anolis lizards. The journal of experimental biology, 9, pp. 4515-4523.

Vaughan, C., Nemeth, N. and Marineros, L. 2003. Ecology and management of natural and artificialScarlet Macaw (Ara macao) nest cavities in Costa Rica. Ornitologia Neotropical. 14, pp. 381-396.

Vaughan, C., Nemeth, N., Cary, J. and Temple, S. 2005. Conservation strategies for a Scarlet Macaw(Ara macao) population in Costa Rica. Birdlife International. 15, pp. 119-130.

Vigo, G., Williams, M. and Brightsmith, D.J. 2011. Growth of scarlet macaw (Ara macao) chicks inSoutheastern Peru. Ornitologia Neotropical. 22, pp. 143-153.

Wainwright, M. 2002. The Natural History of Costa Rican Mammals. Zona Tropical. Journal of Mam-mology. 85(1), pp. 171-172.

Wainwright, M., 2007. The Mammals of Costa Rica: A Natural History and Field Guide, Cornell Uni-versity Press.

Wallace, B.P., DiMatteo, A.D., Bolten, A.B., Chaloupka, M.Y., Hutchinson, B.J., Abreu-Grobois, F.A.,Mortimer, J.A., Seminoff, J.A., Amorocho, D., Bjorndal, K.A. and Bourjea, J. 2011. Global conservationpriorities for marine turtles. PloS one, 6(9).

Wearn, O.R. (2015). Mammalian community responses to a gradient of land-use intensity on the islandof Borneo. Imperial College London (PhD thesis).

Wearn, O. and Glover-Kapfer, P. 2017. Camera-trapping for conservation: a guide to best-practices.WWF Conservation Technology Series 1(1). Woking, UK: WWF-UK.

Weather-and-climate.com. 2019. Climate and average monthly weather in Puntarenas (Puntarenas),Costa Rica. [online] Available at: https://weather-and-climate.com/average-monthly-Rainfall-Temperature-Sunshine,Puntarenas,Costa-Rica [Accessed 7 Aug. 2019].bezy

Weghorst, J. A. 2007. High population density of black-handed spider monkeys (Ateles geoffroyi) inCosta Rican lowland wet forest. Primates, 48, pp. 108-116.

Wehrtmann, I.S. and Cortes, J. 2008. Marine Biodiversity of Costa Rica, Central America, 86th ed.Springer Science & Business Media.

Whitfield, S.M., Lips, K.M. and Donnelly, M.A. 2016. Amphibian decline and conservation in centralAmerica. Copeia. 104(2), pp. 351-379.

Whitfield, S.M., Bell, K.E., Philippi, T., Sasa, M., Bolanos, F., Chaves, G., Savage, J.M. and Donnelly,M.A. 2007. Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proceedings of theNational Academy of Sciences. 104(20), pp. 8352-8356.

Wibbels, T., Rostal, D. and Byles, R. 1998. High pivotal temperature in the sex determination of the oliveridley sea turtle, Lepidochelys olivacea, from Playa Nancite Costa Rica. Copeia. 1998(4), pp. 1086-1088.

Wong, G., Cuaron, A.D., Rodriguez-Luna, E. and de Grammont, P.C. 2008. Saimiri oerstedii. The IUCNRed List of Threatened Species 2008: e.T19836A9022609. Available at: https://www.iucnredlist.org/species/19836/9022609

96

Page 98: COSTA RICA RESEARCH PROGRAMME (CBP) · COSTA RICA RESEARCH PROGRAMME (CBP) CBP Phase 201 Science Report January 2020 - March 2020 Matthew Smart Principal Investigator (PI) Patrice

[Accessed 5 Aug. 2019].

Zambrano, A., Broadbent, E. and Durham, W. 2010. Social and environmental effects of BarrantesEcotourism in the Osa Peninsula of Costa Rica: the Lapa Rios case. Journal of Ecotourism. 9, pp.62-83.

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