COSTA RICA FOREST RESEARCH PROGRAMME (CRF ......Frontier’s Costa Rica Forest Research (CRF) programme began in July 2009 in collaboration with the local non-governmental organisation

COSTA RICA FOREST RESEARCH

PROGRAMME (CRF)

Osa Peninsula, Costa Rica

Eretmochelys imbricata (LINNÉ, 1766)

CRF Phase 153 Science Report

15 June 2015 – 14 September 2015

Peter Brakels, Charlotte Armitage, Rachel Curran, Eleanor Flatt, Emily Neville

& Charles Wheeler

Staff Members

Alex Foulkes (AF) Project Manager (PM) – Until July

Peter Brakels (PB) Principal Investigator (PI)

Charlotte Armitage (CA) Assistant Research Officer (ARO)

Jackson Shanks (JS) Assistant Research Officer (ARO)

Rachel Curran (RC) Assistant Research Officer (ARO)

Eleanor Flatt (EF) Assistant Research Officer (ARO)

Emily Neville (EN) Assistant Research Officer (ARO)

George Shankar (GS) Field Communication Officer (FCO)

Charles Wheeler (CW) Conservation Apprentice (CA)

CRF151

Brakels P, Armintage, C., Shanks, J., Rachel, C., Duszynski, N., Flatt, E., Neville, E. &

C. Wheeler

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Table of Contents

1. Introduction ............................................................................................. 4

1.1 Natural History of Costa Rica and Wildlife Conservation ...................................... 4

1.2 Osa Peninsula .......................................................................................................... 4

1.3 Aims and Objectives of Frontier CRF ..................................................................... 5

2. Training .................................................................................................... 7

2.1 Briefing Sessions ..................................................................................................... 7

2.2 Science Lectures ...................................................................................................... 7

2.3 Field Training .......................................................................................................... 8

2.4 BTECs ...................................................................................................................... 8

3. Research Work Programme ................................................................... 9

3.1 Survey Areas ............................................................................................................ 9

3.2 Local Population Density of the Four Primate Species Coexisting in Costa Rica 12

3.2.1 Introduction .................................................................................................. 12

3.2.2 Methodology ................................................................................................ 12

3.2.3 Results .......................................................................................................... 13

3.2.4 Discussion .................................................................................................... 18

3.4 Neotropical River Otter Habitat Preferences of Reutilised Latrine Sites and the

Role of Scat Deposition in Intra-Specific Communication ............................... 20

3.4.1 Introduction .................................................................................................. 20

3.4.2 Methodology ................................................................................................ 21

3.4.3 Results .......................................................................................................... 21

3.4.4 Discussion ..................................................................................................... 22

3.5 A baseline study assessing the impacts of habitat disturbance on the distribution

and abundance of six focus species (including four endemic) of the Osa

Peninsula: .......................................................................................................... 22

3.5.1 Introduction .................................................................................................. 22

3.6.2 Methodology ................................................................................................ 24

3.6.3 Results ...............................................................................................................

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

3.7 CRF and the Osa Conservation Sea Turtle Conservation Programme .................. 29

3.7.1 Introduction .................................................................................................. 29

3.7.2 Methodology ................................................................................................ 30

3.7.3 Results .......................................................................................................... 34

3.7.4 Discussion .................................................................................................... 35

Additional Projects .................................................................................... 36

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C. Wheeler

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5. Proposed Work Programme for Next Phase ..................................... 37

6. References ............................................................................................ 37

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1. Introduction

1.1 Natural History of Costa Rica and Wildlife Conservation

Despite covering an area of just 50,000 km2, the Central American country of Costa Rica has

high levels of biological diversity, with some 12,000 species of plants, 1,239 species of

butterflies, 838 species of birds, 440 species of reptiles and amphibians, and 232 species of

mammals, which represent around 5% of the world’s species, with only 0.1% of the worlds land

mass (Sánchez-Azofeifa et al., 2002). The extraordinary biodiversity observed here has been

attributed to two main factors; the geographical location and climatic conditions of the region.

Costa Rica lies about halfway between the Tropic of Cancer and the equator, with an annual

average temperature of 27 °C, fluctuating little throughout the year. This small variance means

that seasons in the tropics are defined by the amount of rainfall, which is much more variable

than temperature, providing distinct wet and dry seasons, particularly in the southern Pacific

lowlands, which receive an average annual rainfall of 7,300 mm . The dry season begins around

November/December and continues through to April/May, after which the rainy season

commences (Baker, 2012).

Costa Rica is one of the world’s leading countries in environmental sustainability and

conservation (Fagan et al., 2013), however, this has not always been the case. Up until the

1960s, activities such as logging and hunting seriously threatened biodiversity in this region,

resulting in over half of the country’s forests being cut down and many species being driven to

the verge of extinction (Henderson, 2002). The poaching of turtles for the fatty calipee and

collection of turtle eggs, has severely depleted populations of endangered black turtles

(Chelonia mydas) and vulnerable olive ridley turtles (Lepidochelys olivacea) that use Costa

Rica’s coastlines as nesting sites. Similarly, the hunting of Costa Rica’s wild cat species,

peccaries and tapirs for their meat, skins and other body parts, has significantly reduced wild

populations.

Since the 1960s, some of these issues have been controlled through the implementation of

several reforestation programmes, legislation, education and the creation of protected areas,

representing almost 27% of the country’s surface area (The World Bank Group, 2015). Costa

Rican law currently protects 166 species from hunting, capture and sale, yet illegal hunting still

occurs, including in protected areas (Baker, 2012). Deforestation and habitat fragmentation

outside of the country’s protected areas and national parks is still a significant problem, due to

expanding human populations and related increases in economic pressure. Additionally, the

projected impacts of climate change are also likely to have significant adverse effects on Costa

Rican biodiversity (Baker, 2012). Due to the high levels of biodiversity and multiple threats

placed on Costa Rica it is important to conduct research to determine the health of the

ecosystem and its encapsulated species.

1.2 Osa Peninsula

The Osa Peninsula is located at the southern end of the Southern Pacific lowlands and covers an

area of 1093 km² (Henderson, 2002). It is the region where the last remnants of tropical

broadleaved evergreen lowland rainforest on the Pacific slope in Central America are found

(Kappelle et al. 2002). It is a unique ecosystem in terms of endemic species like the Cherrie’s

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C. Wheeler

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Tanager (Ramphocelus costaricensis), the Red-backed squirrel monkey (Saimiri oerstedii)), the

Golfo Dulce poison dart frog (Phyllobates vittatus) as well as possessing rich biodiversity, with

over 2.5% of the planets species, making this peninsula an ideal location for scientific research

(Larsen & Toft 2010).

The Osa Peninsula consists of Tropical Wet, Premontane Wet and Tropical Moist forest types,

with elevations ranging between 200 and 760 m (Santchez-Azofeifa et al., 2002). Due to its

diverse topography, the peninsula has a variable climate, with an average annual rainfall of 5500

mm, a mean temperature of around 27°C and humidity levels almost never falling below 90%

(Cleveland et al, 2010).

The Osa Peninsula has a population of around 12,000 people, mainly located in small scattered

settlements. The major sources of income in the region are agriculture (rice, bananas, beans and

corn), livestock (cattle), gold mining, logging and more recently, the expanding eco-tourism

industry (Carrillo et al., 2000). The peninsula’s population is increasing at a rate of 2.6%

annually, compared to 1.3% in the rest o the country and 1.14% globally (Sánchez-Azofeifa et

al., 2001). Since the 1990s, there has also been a dramatic rise in the number of hospitality

businesses opening along the road, from Puerto Jimenez to Carate, as a result of the growing

popularity of ecotourism (Minca and Linda, 2002). This has caused growing concern for the

sustainability of the region’s environmental resource demands (Sánchez-Azofeifa et al., 2001).

Frontier’s Costa Rica Forest Research (CRF) programme began in July 2009 in collaboration

with the local non-governmental organisation Osa Conservation at the Piro site (N 08°23.826,

W 083°20.564) in the southeast of the Osa Peninsula. The site is located within a 1700 ha

private forest reserve, managed by the administrative unit of ACOSA (Osa Conservation Area)

within the National System of Conservation Areas (SINAC). The site is a prime location for

carrying out both forest and shoreline surveys, as there is relatively easy access to both the

primary and secondary forest, as well as pristine beach habitat. The long term objectives of the

project are to investigate the effects of climate change, deforestation and other anthropogenic

impacts on the terrestrial communities of Costa Rica and on the country’s network of protected

areas. There are five core faunal study groups within CRF; primates, sea turtles, wildcats,

neotropical otters and birds.

1.3 Aims and Objectives of Frontier CRF

Under the umbrella of the research programme, the specific aims and objectives of Frontier

CRF are:

1. To estimate the density of the four primate species within the Osa Conservation site at

Piro and its boundaries.

2. To compare primate behaviour between different forest types throughout Piro

3. To assess Neotropical river otter habitat preferences of reutilised latrine sites and

investigate the role of scat deposition in intra-specific communication.

4. To compare the abundance of six endemic birds species between young secondary and

mature primary forest of the Osa Peninsula.

5. To monitor the activity and health of nesting marine turtles on Piro and Pejeperro

beaches and to support the management of the hatchery under the Osa Conservation

Sea Turtle Conservation Programme.

CRF151 Brakels, P., Armitage, C., Curran, R., Flatt, E., Neville, E., Wheeler, C.

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2. Training Volunteer Research Assistants (RAs) and newly appointed staff receive a number of briefing

sessions on arrival (Table 1), followed by regular science lectures (Table 2) and field training

(Table 3) throughout their deployments. The CRF research programme also supports candidates

completing the BTEC Advanced Certificate and Advanced Diploma in Tropical Habitat

Conservation and the Certificate of Personal Effectiveness (CoPE) (Table 4).

2.1 Briefing Sessions

All new arrivals to CRF are introduced to the aims of the research programme, the

methodologies and the research output of the individual projects. They are also provided with an

update on the achievements of CRF. This information is delivered via the ‘Introduction to the

Frontier Costa Rica Forest Research Programme presentation’. Additionally, all volunteers and

staff are given a full health, safety and medical briefing, which they are tested on before

participating in field activities. Volunteers undertaking a BTEC and/or CoPE qualification are

given an introductory briefing before they begin the assessments.

Table 1. Briefing sessions conducted during Phase CRF151

Briefing Session Presenter

Introduction to the Frontier Costa Rica Forest Research

Programme

PB

Health and Safety Briefing and Test ALL

Medical Briefing and Test ALL

Introduction to the BTEC and CoPE Qualifications ALL

Introduction to Surveying and Monitoring PB

Camp Life and Duties ALL

2.2 Science Lectures

A broad programme of science lectures is offered at CRF providing information and

training in various aspects of research. Lectures are typically presented utilising

PowerPoint and give an opportunity for greater understanding of the ecology and

identification of focal species, methods of data analysis used by CRF and considerations

when planning research projects.

Lectures are scheduled with the following objectives:

To allow every volunteer and member of staff to attend each presentation at least

once during deployment, regardless of length of stay.

To meet the time requirements for BTEC assessments.

To avoid conflict with other activities, maximizing attendance.

Workshops provide detailed training on specific software and applications used

in conservation.

Attendance of lectures is compulsory.


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Table 2. Science lectures delivered during Phase CRF153

Science Lecture Presenter

Survey Planning: BTEC E07 Preparation ALL

Surveying and Monitoring: BTEC E09

Preparation

ALL

Bird Call Identification CA

Primates of the Osa, identification,

ecology and behaviour

PB

Mammal track survey workshop PB

GPS workshop PB

2.3 Field Training

All volunteers and newly appointed staff receive field training. Training is hands-on and

provides an opportunity for participants to become familiar with field equipment.

The following topics are covered:

Specific training sessions to prepare volunteers and staff for accurate data collection

Identification of flora and fauna

Survey method training

Skills and tools used for research

- Turtle tagging

- Proper maintenance of equipment

Table 3. Field training provided during Phase CRF152

Field Training Provider

Turtle Patrol Data Collection ALL

Primate Surveys by total counts PB

Bird Surveys by Point Surveys CA, EF

Field Equipment: GPS PB

Identification of Neotropical Otters and their Signs,

and Recording River Attributes

ALL

Studying Primate Behaviour ALL

Staff Turtle Training Osa Conservation

Wildlife Track Recording and Identification PB

2.4 BTECs

Frontier offers volunteer Research Assistants an opportunity to gain internationally recognised

qualifications based around teamwork, survey techniques, environmental conservation and

effective communication of results. The BTEC in Tropical Habitat Conservation may be studied

as an Advanced Certificate (four week program) or Advanced Diploma (ten week program). See

Table 4 for the BTECs undertaken during this phase.


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Table 4. BTECs Undertaken in Tropical Habitat Conservation during Phase CRF152

Name BTEC Title and Type Mentor

Holly Coleman Primate behaviour – Comparison between

habituation levels and behavioural profiles of all four

primate species on the Osa Peninsula between two

locations, Carate & Piro.

RC

Thomas Humphreys Turtle beach patrols and community awareness in

Carate

PB

3. Research Work Programme

3.1 Survey Areas

Field research is conducted within an 11.83 km2 privately-owned property in Piro, Osa

Peninsula and its boundaries (8°23’-8°26’N, 83°18’-83°25’W) (Figure 1). Located largely

within the Golfo Dulce Forest Reserve and Osa Conservation Area (ACOSA) Wildlife Refuge,

this property is owned by NGO Osa Conservation (OC). The landscape is heterogeneous,

composed of lowland moist primary, secondary and coastal forest. Dominant tree species

include; Ficus insipida, Ceiba pentandra, Attalea butyracea, Carapa guianensis, Castilla tunu,

Spondias mombin, Hyeronima alchorneoides, Chimarrhis latifolia, Fruta dorada, Caryocar

costaricense, Ocotea insularis, Pouteria torta, and Inga allenii. The property also borders dense

forest and pastoral properties to the southeast and encompasses pochote (Pachira quinata) and

teak (Tectona grandis) plantations in the north and northeast, each occupying 0.4 km2. There are

two biological research stations within the survey area, Cerro Osa station in the northwest and

Piro station in the southern region of the property. Mean annual rainfall and temperature for the

area is 5,000-6,000 mm and 26-28 °C respectively; the dry season extends from the end of

December until March.


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Figure 1. The Frontier Costa Rica Forest Research Programme study area with

research: beaches, rivers and trails marked. LS: Laguna Silvestre; FD: Rain Forest

Discovery; AL: Attalea; LT: Las Tortugas; CO: Ocelote ; AT: Ajo; TA: Tangara; CO:

Cerro Osa; NB: Northern Border; CT: Chicle.

A forest trail network covers most of the southern and north eastern portions of the site. The

majority of the trails are narrow and machete-cut. Exceptions to this are Cerro Osa, which is an

old logging road, and the north-south segment of Northern Border and Laguna Silvestre, which

are both 5 m wide cleared tracks. Attalea is the most recently cut trail and is approximately one

year old, while all other trails are more than five years old with the Rainforest discovery trail

over 2 years old.

The property is bordered to the south by the Pacific Ocean and the coastline is separated into

two beaches – Playa Piro (2 km) and Playa Pejeperro (4.5 km). The primary rivers intersecting

the property are the Rio Piro and the adjoining Quebrada Coyunda; the mouth of the former is at

approximately the centre of Playa Piro.

The trails run to a diversity of habitats with different degrees of usage and disturbance (table 5).

The forest trails are used as survey transect for the different monitoring projects.


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Table 5. Current trails present in Piro with description on habitat and frequency of use

Transect

Name (code)

Transect

Length (km)

Habitat Description,

Trail Type and disturbance

Ajo (AT) 2.0 Trail through secondary and mature, primary broad-

leaved evergreen lowland forest. Frequently used by

researchers and volunteers.

Ocelot (OC) 1.4 Trail through secondary and mature primary broad-


researcher and volunteers.

Cerro Osa

(CO)

1.4 Old logging road and forest trail through secondary

and mature, primary broad-leaved evergreen lowland

forest, abandoned pochote (Pachira quinata)

plantation and across a branch of the Quebrada

Coyunda River

Laguna

Silvestre

(LS)

2.6 Access road through secondary and primary broad-

leaved evergreen lowland forest. Road used by local

farmers, transport by horse and occasionally by truck

(dry season)

Las Tortugas

(LA)

1.6 Trail through secondary riparian and coastal forest

with a variety of palm species and main access road

dissecting secondary forest. Daily use by researchers

and volunteers.

Tangara

(TA)

1.3 Trail through secondary and mature, primary broad-


researchers and volunteers.

Chicle (CT) 1.9 Forest ridge trail through primary broad-leaved

evergreen lowland forest and across Quebrada

Coyunda River.

Northern

Border (NB)

4.9 Old logging road through a pochote (Pachira

quinata) plantation and trail through mature, primary

broad-leaved evergreen lowland forest. Trail along

border is used by locals, hunting likely present.

Forest

discovery

(FD)

2.5 Trail through secondary forest and main access road

dissecting secondary forest. Trail in close vicinity

parallel to the mean access road Puerto Jimenez –

Carate. Frequently used by researchers and

volunteers.

Attalea (AL) 1.8 Trail through secondary coastal broad-leaved

evergreen lowland forest dominated by palms of the

species Attalea butyracea (Royal Palm) &

Astrocaryum standleyanum (Black Palm) and

pasture.

Total 21.4


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3.2 Local Population Density of the Four Primate Species Coexisting in Costa Rica

3.2.1 Introduction

There are four species of primate found in Costa Rica; the Central American squirrel monkey

(Saimiri oerstedii), mantled howler monkey (Alouatta palliata), geoffroy’s spider monkey

(Ateles geoffroyi) and white-faced capuchin (Cebus capucinus). All four species are present at

the study site in Piro. A. geoffroyi is listed as Endangered and S. oerstedii as Vulnerable (IUCN

2015). Population declines exceeding 50% over 45 years have been reported for A. geoffroyi,

principally driven by stress-induced habitat loss (Cuarón et al., 2008b). S. oerstedii has a limited

distribution, restricted to Panama and Costa Rica, this makes populations which are exploited

for the pet trade and those experiencing habitat loss and degradation more vulnerable to

stochastic events. Land conversion for agriculture and development, clear cutting, selective

logging, hunting and the pet trade have implications for all four Costa Rican primate species

(Cropp and Boinski, 2000). Populations of A. palliata and C. capucinus are thought to be stable

and not in declined, they are therefore listed as least concern, however monitoring is necessary

as they are exposed to the same threats as other, more endangered primates (IUCN, 2015).

The primate guild in Costa Rica is vital to forest structural integrity. All four species perform

important roles as seed dispersers (Julliot, 1997; Garber et al., 2006) and the Osa Peninsula is

the only part of Costa Rica where all four species occur together (Carrillo et al., 2000).

Frontier CRF has been surveying the presence and abundance of all four species in

collaboration with Osa Conservation since March 2010. The overall aim of this research is to

provide an insight into the habitat use and behaviour of primates in the area to better inform

management and policy decisions at a local level. The principal and foremost objective of this

project is to produce estimates of population density for each of the four species. Density

estimates are lacking for two of the four primate species, the Central American squirrel monkey

and the white-faced capuchin, which are therefore key to survey, however focus is also on the

red listed spider monkey and squirrel monkey. This phase we aimed to conduct a total count of

the species, identify the different groups and their minimum (sub) group size in order to

estimate the density of all the species within the protected area of Piro (Burgiere & Fleury

2000). The long term monitoring of home range size and primate total counts are considered the

most reliable method in deriving primate densities (Hassel-Finnegan et al. 2008; Marshall et al.

2008; Plumptre & Cox 2006; Burgiere & Fleury 2000; Fashing & Cords 2000). This method is

especially effective working in areas of small fragmented forest with habituated primates

(Pruetz & Leasor 2002).

3.2.2 Methodology

Data is collected by walking transects and conducting total counts of all primates encountered

(Hassel-Finnegan et al. 2008; Marshall et al. 2008; Plumptre & Cox 2006; Burgiere & Fleury

2000; Fashing & Cords 2000). The transects are sampled equally across times of day. Surveys

started between 6:00-7:00am hours to cover peak primate activity, increasing the detection

probability. Transects include, for the most part, combinations of different forest trails.

Transects sampled (Table 5) are walked by two observers at a constant speed of 1.5 – 2 km per

hour including regular stops between every 100-200m as recommended by Peres (1999). No

transect is surveyed more than once on the same day and sampling is only conducted in fair

weather due to the reduction in detection probability in adverse weather conditions. Transects

were surveyed evenly once a month. To assure reliable total count a minimum observation time

of 30 minutes was set to assure that all individuals within the (sub)group could be counted


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(Pruetz & Leasor 2003). The research was non-invasive and adhered to the legal requirements

of Costa Rica (Costa Rican Government Decree 31514-MINAE). Any and all aggressive

behaviour towards the observers by individual primates was responded to by moving on as

quickly as possible.

All primates observed were recorded and the spatial location noted using GPS. The number of

individuals within the target group was recorded. All individuals visible at the same time and

exhibiting the same general behaviour (e.g., resting, moving or foraging) were considered to be

part of the same group (Chapman et al., 1995). Agreement upon group size was made between

the observers where the group could be counted together; otherwise the observers split their

search effort into non-overlapping areas (e.g., left and right of the trail) and made independent

counts which were then summed. Where possible, secondary data on group composition (i.e.

gender and age group; adult, juvenile, infant) was also recorded, however vocal detections were

not included. Furthermore, the behaviour upon encounter, duration of observation and distance

from the trail and direction travelling was noted. Primate home ranges are based on field

observations, where primates are encountered and the direction they travel. Data on group

composition as well as the occurrence of identifiable individuals (scars, missing limbs,

pigmentation etc.) is collected making it possible to identify different groups. When primate

troops are 'recaptured' it will be included in the spatial database and minimal home ranges per

troops are drawn in google earth on the basis of habitat availability and the average home ranges

of the species known from previous studies. For spider monkeys this ranges between 0.73 – 2.2

km2 (Fedigan et al. 1988), Central American squirrel monkey range is on average 2 km

2, white-

faced capuchin up to 1 km2 (but usually less

) and mantled howler monkeys have the smallest

home range ranging between 0.27 – 0.6 km2

on average. Primate minimum density was

calculated as the total number of individuals for the different groups encountered divided by the

surface area of the study site (11.83 km2).

3.2.3 Results

Primate total counts data was collected since the start of this phase. All trails are surveyed at

least once a month, resulting in a total of 3 surveys for this phase. Primate encounters from

previous phases were added to compile a map with all primate records and the identification of

the different troops and their size. This will result in a reliable actual minimum density of the

primates present in Piro Conservation Area. By surveying evenly and thoroughly throughout the

whole study area with an emphasis on primate group composition, we were able to identify and

map previously unrecorded primate groups. Below, the different primate groups within each

species are listed with home ranges displayed on the accompanying maps (Figures 2-5). These

represent the groups that have only been encountered once and 'total' numbers have not been

confirmed yet, or of situations where total counts were not possible because of the conditions in

the field (e.g. distance or dense foliage) and the behaviour of the group (e.g. fleeing or group

spread).

Central American Spider monkey (SP)

In total a minimum number of nine different groups are estimated to occur within the property

of Piro (see fig 2 and table 6). The largest minimum subgroup (based on not knowing if an

entire family has been observed) count was 23 individuals from a group that occurs on the

northern border. Four new groups were identified during this phase; G1, G4, G6 & G9.

http://soltiscentercostarica.tamu.edu/sites/default/files/NormasGenerales.pdf


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Table 6. Number of Spider monkey groups, group size, characteristics and location

SP Group ID Minimum

subgroup size

Characteristics, location and estimated home range size

(small/average/large)

Group 1 8 Attalea forest (small)

Group 2 20 Habituated group, field station and camp (small)

Group 3 20 Ocelot group, group size underestimated (average)

Group 4 14 Chicle group (large/ unknown)

Group 5 12 Discovery/Laguna Silvestre group (average)

Group 6 8 Upstream Quebrada coyunda/ Cerro Osa group

(unknown)

Group 7 18 Laguna Silvestre group (large), likely more than one

group

Group 8 >10 Upstream Piro river group

Group 9 23 Northern Border group (average)

Total: 133

Density:

11,2/km2

Figure 2. Map with spider monkey encounters (pin points), and estimated home ranges

(circles) per group (numbers). Red line represents boundary of study area. Yellow line

main road Puerto Jimenez - Carate


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Central American Squirrel Monkey (SQ)

In total 11 possible different groups have been identified (see table 7). The groups appear to be

highly variable in size, with two large (>30) groups visiting the two different field stations of

OC. Five new groups were recorded this phase; G1, G8, G9, G10 & G11. Squirrel monkeys

represent the highest density of all four species of primates in Piro, with 19 individuals per km2.

Table .7 Number of Squirrel monkey groups, group size, characteristics and location

SQ Group ID Minimum

subgroup size



Group 1 16 Attalea forest (average)

Group 2 32-52 Habituated group visit Frontier camp (small)

Group 3 23 Tortugas trail and nearby road (small)

Group 4 >15 Possible same group as 3 (average)

Group 5 25 Possible same habituated group as 2, Visits OC site east

side (small)

Group 6 >10 Possible same group as 5, Ocelot group (small)

Group 7 20 Possible same group as 2, Discovery trail, along road

Group 8 10 Reforestation area group (average)

Figure 3. Map with squirrel monkey encounters (pin points), and estimated home

ranges (circles) per group (number). Red line represents boundary of study area.

Yellow line main road Puerto Jimenez - Carate


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Group 9 15 Laguna Silvestre group (large)

Group 10 >30 Cerro Osa group, visit CO field station (large)

Group 11 >10 Northern border group (large)

Total: 226

Density:

19,1/km2

White-faced capuchin (CA)

Capuchins are the least encountered primate species in Piro and they appear to present

the lowest primate density for all species, although have been found to occur throughout

the whole study area. In total nine different groups have so far been identified

representing a total density of 8.3/km2.

Table 8. Number of Capuchin monkey groups, group size, characteristics and location

CA Group ID Minimum

subgroup size



Group 1 15 Tortugas trail group, crossing road (average)

Group 2 10 Habituated group, visits Frontier camp (average)

Group 3 10 Ocelot group (unknown)

Figure 4. Map with capuchin encounters (pin points), and estimated home ranges

(circles) per group (number). Red line represents boundary of study area. Yellow line



17

Group 4 >10 Chicle group (unknown)

Group 5 12 Discovery trail group near road (unknown)

Group 6 >10 Cerro Osa group, visits field station (unknown)

Group 7 10 Upstream Piro river group (unknown)

Group 8 10 Norther border group (unknown)

Group 9 >10 Attalea group (unknown)

Total: 98

Density:

8,3/km2

Mantled howler monkey (HO)

This species represents the highest group density within the study area; so far at least 18

distinct groups have been identified, although this is likely to be an underestimation (see

table 9). With 16 individuals per km2

howler monkeys are well represented within the

study area.

Figure 5. Map with howler monkey encounters (pin points), and estimated home ranges

(circles) per group (number). Red line represents boundary of study area. Yellow line



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Table 9. Number of Howler monkey groups, group size, characteristics and location

HO Group ID Minimum

subgroup size



Group 1 27 Attalea group (at least 2 groups)

Group 2 ? >5 Beach group south of road

Group 3 13 Tortugas group, beach group 2

Group 4 11 Tangara trail, near field station

Group 5 24 Behind Frontier camp

Group 6 13 Ajo group

Group 7 10 Ocelot – Cerro Osa junction group

Group 8 9 Chicle group

Group 9 13 Discovery group

Group 10 16 Possible same group as 9

Group 11 ? >3 Cerro Osa group, Quebrada Coyunda valley

Group 12 A=15 B=7 Laguna silvestre groups, likely more than one group

Group 13 9 Northern border east group

Group 14 > 5 Laguna silvestre upper part

Group 15 A= > 5 B= > 5 Northern border west group, two distinct groups

Total: 190

Density:

16,1/km2

3.2.4 Discussion

Group counts for Spider monkeys are very hard since this species lives in fission-fusion

societies where the whole group is hardly ever complete (Di Fiore, A. & Campbell C.

2007) Spider monkeys split up in several sub groups (2-6 individuals on average) in the

early morning when leaving the sleeping tree and return to the same tree to join the rest

of the group before nightfall. Sometimes however, subgroups stay separate from the rest

of the group for more than a day (Youlatos 2008). Therefore, total counts might not be

the ideal measure to calculate the population density of spider monkeys in an area.

Squirrel monkey group composition is also very difficult to determine, because of the

difficulty in distinguishing males from females, and the fact that troops are large, the

animals move rapidly, and are widely spread (Boinski 1992). For this reason the

estimations of these two species surveyed in this study need to be regarded as relative

minimum numbers and are likely to be underestimated.

In order to conduct a total count for a large group of squirrel monkeys, ideally,

researchers would be split into several survey teams, spread out depending on the

spread of the squirrel monkey group. For spider monkeys, distance-sampling might be

an alternative method, as although it is an extrapolation of a sample of encounters,


19

density numbers can be derived relatively quickly. The accuracy of these numbers

should obviously be critically assessed. For all four species, but especially the squirrel

and spider monkeys, the number of groups and their home ranges need to be more

precisely mapped.

The number of groups for the two latter species is likely to be overestimated, since both

species can occupy large home ranges and travel over relatively large distances of up to

2-4 km per day. A solution to this problem would be to have several survey teams and

to survey simultaneously in different part of the study area. The density estimation in

this study is considerably less than that of our previous study using line-transect

sampling, which was 34.36 individuals/km2. Obviously, both methods can't be

compared one on one, as they are meant to be used complementary to each other to

derive more accurate estimations (Plumptre 2000, Plumptre & Cox 2006). Distance

density estimates are likely to overestimate the primate density since numbers will be

extrapolated from a sample throughout the whole area. Assuming that the sample is

representative for the study site and suitable habitat is continuous, the primates are

present throughout the whole area.

The home ranges depicted per species are indicative and have to be regarded as rough

boundaries and are by no means accurate. Furthermore, home ranges of our primate

study species are likely to overlap to a considerable degree. Since we are restricted to

the trails, troops cannot be followed and therefore home ranges cannot be accurately

mapped.

Group size of spider monkeys can be in the range of 20-40 (Campbell 2008). The

biggest group count in this study is 23 individuals. The minimum density of spider

monkeys in Piro, based on subgroup counts, was calculated to be 11.2 individuals/km2.

However, if the spider monkey density is calculated based on a minimum group size of

20 individuals, this would result in a density of over 15 individuals/km2. The squirrel

monkeys occur in groups of 23-54 and have been recorded to be over 65 in some areas

(Boinski 1988). Research staff counted only two large groups and one average sized

group (see table 7), there are potentially more large groups (>20) in the study area,

however, group counts for the other groups are based on only a few and some a single

encounter(s). White-faced capuchins live in smaller family groups than their smaller

relatives, ranging from 10-20 on average. All groups identified in this study, except one,

have the minimum count of +/- 10 individuals. White-faced capuchins were the least

encountered species and total counts for most groups are based on only a single

encounter. This could possibly result in an underestimation of the group size, since with

several encounters of the same group different counts can be averaged. Mantled howler

monkey group size, like capuchins, range between 10-20, with an average of 12,9

individuals (Chapman & Pavelka 2005). Two large groups have been encountered with

24 and 27 individuals, these groups are likely to consist of the two different groups. It is

not uncommon for mantled howler monkeys to have overlapping home ranges. Howler

monkeys are territorial primates, males set their home range boundaries by howling

before sunset, which would cease of any other males entering their home range. No

aggression or any other signs of a dispute was observed within the group; why these

howler monkeys are so tolerable at these sites needs further studying. Howler monkey

density in Piro was estimated to be 30.8 individuals/km2, that's almost 50% more than


20

the estimate based the total counts. The total count estimation is clearly underestimated,

since only a fragment of the howler population within the property has likely been

encountered. Certain parts of the area cannot be accessed due to the lack of trails (NW

part of the property).

Overall this pilot can be considered a success, the first results are promising with

several new groups identified this phase. Some group counts are not complete however,

and are based only on a few sightings, therefore more survey work is required to

complete some group counts and distinguish groups from each other in order map their

home ranges more precisely. It is likely that more howler monkey groups will be

discovered/identified in the future. Howler monkeys are probably the most difficult to

detect since they spent most of the time motionless in the canopy of the forest and are

therefore easily missed. This possibly explains why we haven't recorded any howler

monkeys in the Piro river valley upstream from Frontier camp so far.

3.4 Neotropical River Otter Habitat Preferences of Reutilised Latrine Sites and the

Role of Scat Deposition in Intra-Specific Communication

3.4.1 Introduction

The Neotropical River Otter (Lontra longicaudis) is a solitary species that can be found

in a variety of habitats including swamps, streams and lagoons from Mexico to Uruguay

(Emmons and Feer, 1997; Quadros et al., 2002; Gori et al., 2003; Santos et al., 2012).

Despite this, otters are an adaptive species and have been reported to inhabit irrigation

ditches in rice and sugar cane plantations in Guyana (IOSF, 2012). Their low

reproductive potential and dependence on healthy aquatic environments means that the

species cannot respond quickly to population crashes and are sensitive to environmental

change (Cezare et al., 2002; Waldemarin and Alvarez, 2008). Despite their wide

distribution, little is known about the species’ ecology, local distribution and population

status, hindering the development of appropriate conservation strategies; the

Neotropical river otter is currently listed as “Data Deficient” on the IUCN Red List of

Threatened Species (Waldemarin and Alvarez, 2008). This is because relatively little

research effort has been devoted to the study of the species throughout its range, and

detailed habitat and ecology information is lacking.

Otters are secretive and difficult to observe, thus necessitating alternative methods to

monitor their status and distribution. In contrast, otter latrines or haul-outs; places along

the shoreline where otters eat, defecate, urinate, roll and deposit anal sac secretions, are

often obvious evidence of otter activity (Bowyer et al., 1995; Crowley et al., 2012).

Latrines are located several meters from the water on high ground (e.g. logs, rocks)

(Quadros and Montiero-Filho, 2002; Stevens and Serfass, 2008; Depue and Ben-David,

2010) and mark territorial boundaries within otter home ranges (Melquist and

Hornocker, 1983; Remonti et al., 2011). The exact purpose of latrines is not

conclusively known, but they are believed to play a role in intraspecific communication

(Melquist and Hornocker, 1983; Rostain et al., 2004; Kasper et al., 2008), signalling

reproductive state to the opposite sex (Rostain et al., 2004), marking areas of key

resource use (Kruuk et al., 1986; Kruuk, 1992) and conveying the social status of males

(Rostain et al., 2004).


21

Numerous environmental characteristics such as water depth (Anoop and Hussain,

2004; Depue and Ben-David, 2010; Remonti et al., 2011; Carrillo-Rubio and Lafón,

2004), water edge topography (Swimley et al., 1998; Bowyer et al., 1995; Anoop and

Hussain, 2004) and vegetation structure (Prenda and Granada-Lorencio, 1996), are

reported to influence latrine site selection, however, discrepancies exist regarding the

importance of each factor. Therefore, habitat preference studies are essential to better

comprehend the distribution, abundance, and requirements of the Neotropical Otter.

3.4.2 Methodology

Two linear transects were established along the course of the Rio Piro and Quebrada

Coyunda measuring 5.2 km and 2.8 km respectively (Fig.5). Each river was surveyed

once a week, typically as two distinct transects. One began at CRF camp and ran 3.5 km

north on the Rio Piro. The other began at CRF camp and started 1.7 km south on the

Rio Piro to the river mouth and then ran 2.8 km east of the Quebrada Coyunda from the

intersection with Rio Piro. Surveyors walked within the river course and typically began

sampling early morning.

Figure 5. Map of otter transects along Rio Piro and Quebrada Coyunda.

During the course of the survey all reutilised sites such as rocks, logs, fallen trees, roots

and river margins were actively searched for otter spraints. Research staff defined

reutilised latrines as sites having two or more scats present. The substrate diameter

where the spraint was deposited, stream depth adjacent to the substrate and distance to

the waterline was recorded. At each site, GPS data was collected and river width and

river depth at 1 m intervals of the river cross-section was measured. The

presence/absence of mucous in spraint was also recorded and escape cover distance,

defined as the distance from the water’s edge to the point where the undergrowth

started, was collected for both river margins.


22

3.4.3 Results

Data collection still progress

3.4.4 Discussion

Data collection still progress

3.5 A baseline study assessing the impacts of habitat disturbance on the distribution

and abundance of six focus bird species (including four endemic) of the Osa

Peninsula:

3.5.1 Introduction

The highly multifaceted and heterogeneous environments of Costa Rica have many

species-rich communities; particularly those within the avian families (Herzog et al.,

2002). Due to their sensitivity to change, birds are well known as important indicators

of the ecosystem health in which they reside. The avifauna of Costa Rica are infamous

for their wealth in diversity, with over 800 species documented (Henderson, 2010),

however, populations are becoming more threatened with pervasive human influences.

The complex myriad of interactions between trees and the birds that destroy or disperse

their seeds play crucial roles in these ecosystems (Howe, 1980), yet reductions in bird

population levels show a correlation to falling pollination and seed dispersal rates, both

process that are fundamental to any stable ecosystem (Pejchar et al., 2008). This,

combined with high levels of endemism within Costa Rica highlights the need to

regularly and closely monitor the bird communities. Trends are impossible to measure

unless some baseline is first established (Bibby et al., 1998), followed by the

assessment of biotic and abiotic factors on bird distribution, which has been

successfully undertaken by many authors (Blake & Loiselle, 2000). Therefore, by

conducting a study in the Osa Pennisula of focus bird species we can begin to establish

the health of bird populations here and therefore the ecosystem as a whole. This study

also aims to identify the potential effects of disturbance on these endemic bird species,

which little information is known.

Due to population growth in Costa Rica, large areas of forest have been cleared to allow

the expansion of agriculture and other industries. This has resulted in Costa Rica

currently suffering from one of the world’s highest rates of deforestation of unprotected

forest (Powell et al. 2000), creating dramatic alterations to the ecosystems. With this in

mind, and the fact that there are knowledge gaps in the understanding of tropical bird

communities (Herzog et al. 2002), this project aims to support the ongoing assessment

of tropical bird communities of the Osa Peninsula. The project started in early October

2014, after some initial pilot studies, with the intention of assessing the species

distribution of six focus species of the Osa Peninsula in order to start a baseline survey.

In order to provide a more concise study we selected six individual bird species as focus

species unique to this study, with four being endemic to the area. The six focus species


23

are listed in Table 6 with additional details of their conservation status and species

range taken from IUCN Red List (2014) and Henderson (2010). Four of these, the

Fiery-billed Aracari (Pteroglossus frantzii), Riverside Wren (Thryothorus semibadius),

Cherries Tanager (Ramphocelus costaricensis) and Orange-Collared Manakin (Manacus

aurantiacus) are endemic to the region of South West Costa Rica and western Panama.

It was determined that those species of the Manakin family found in the region,

including the Blue Crowned (Lepidothrix coronate) and Red Capped Manakin (Pipra

mentalis), should also be assessed over the course of the study. Focal species were

chosen to eliminate bias that was present in past studies when researching all bird

species. This bias arises as some calls are much more distinct than others, leading to

particular species of bird being recorded more than others; focal species allow a more

succinct and accurate analysis. The specific focal species were chosen as they allow a

study of endemic birds in the region but also allow the analysis of different members of

the same family (Manakins).

Table 6. Six Focus Species IUCN Red List (2014) and Henderson (2010)

Species Endemic Range IUCN

Status

Pop Trend

Fiery-billed Aracari

(Pteroglossus frantzii)

SW Costa Rica to W

Panama

Least

Concern Decreasing

Riverside Wren

(Thryothorus

semibadius)

SW Costa Rica to W

Panama

Least

Concern Unknown

Cherries Tanager

(Ramphocelus

costaricensis)

SW Costa Rica to W

Panama

Least

Concern Stable

Red-Capped Manakin

(Pipra mentalis) Belize to Panama

Least

Concern Decreasing

Blue-Crowned Manakin

(Lepidothrix coronate) Costa Rica to Brazil

Least

Concern Decreasing

Orange Collared

Manakin (Manacus

aurantiacus)

SW Costa Rica to W

Panama

Least

Concern Decreasing

The aim of this project is to be the start of many feeder projects assessing differences in

the communities of the six focus species across different habitat gradients, particularly

human created gaps, using the definition of Levey (1988), whereby a gap is a “vertical

hole in the forest extending through all levels down to within an average of 2 m above

ground” (Levey 1988:252). By selecting points which are effected by human

disturbance our study can begin to establish how bird species are responding to these

changes and subsequently the wider ecosystem. It is hoped the project can focus on

sampling the populations at dawn, and possibly dusk in the future over the coming

phase. Trails examined encompass primary and secondary forest as well as swamp and

river habitats (Table7).


24

Table 7. Overview of point counts with habitat type

Trail Point Description

Ajo

1 Forest Edge

2 Secondary Forest

3 Secondary Forest

Ocelot

1 Forest Edge

2 Gallery Forest

3 Primary Forest

Tangara

1 Secondary Forest

2 Secondary Forest

3 Primary Forest

Discovery

trail

1 Secondary Forest

2 Secondary Forest

3 Swamp

Northern

Border

1 Secondary Forest

2 Secondary Forest

3 Secondary Forest

Cerro Osa

1 Secondary Forest

2 Primary Forest

3 Forest Edge

Rio Piro (S)

1 Gallery forest

2 Gallery forest

3 Gallery forest

Tortugas

Trail

1 Forest Edge

2 Secondary Forest

3 Forest Edge

3.6.2 Methodology

Point counts were conducted along six trails/transects (Tortugas trail, Discovery trail,

Cerro Osa, Ajo, Tangara, Ocelot, Northern Border and a river transect down Rio Piro)

and consist of four different habitat types; primary forest, secondary forest, gallery

forest and forest edge. Point counts were conducted in a similar manner to Blake &

Loiselle (2000). Observers visited set points where they listened and watched for the

focal species, as well as noting additional species. Volunteers were trained to recognise

the calls and physical characteristics of the selected target species, as well as other

species, in order to increase the accuracy of data collection during each survey. Each

point count lasted 10 minutes at each of the marked points, which included a minute

settling period prior to starting. Points were marked prior to data collection along each

of the trails using a handheld GPS, selected in order to assess different habitat types.

Surveys were conducted in the morning, with the three point counts undertaken at 0530,

0600 and 0630am, to coincide with the dawn chorus. All birds seen or heard were noted

down with particular attention paid on the six focal species highlighted above.


25

When noting down the species name and whether it was heard or seen, distance bands

were also used in order to ascertain where the bird lay in relation to the trail. This will

aid in establishing whether birds are found near or further away from man-made gaps in

the forest canopy layers. Distance band 1 encompassed a bird sighted or heard within 2

m of the trail, band 2 was between 2 and 10 m of the trail, and band 3 was beyond 10 m

(Figure 6).

Figure 6. Survey distance bands to established the location of the bird in relation to the point count

It is noted within the literature that even highly experienced observers can introduce a

variety of bias into the results due to varying identification skills between species, as

well as differences in observation technique (Herzog et al. 2002). In order to avoid this,

observer bias was minimised with the same trail leader conducting the survey each time.

All volunteers are made familiar with the calls and physical characteristics of each of

the target species before conducting a survey. The potential for the birds to have

different calls from those learnt is also an important point to recognise, which could be

mitigated against by taking recordings for further analysis. Baldo & Mennill (2011)

found that Great Curassow birds had many different calls and it is highly likely that the

species under focus on this study also possess many variants of the calls learnt to

identify them, potentially introducing error and the chance of missing certain birds. Due

to the dense canopies overhead birds can also go unnoticed if they are not seen or heard,

especially when there is heavy rain, which is accounted for by cancelling surveys under

these conditions .

3.6.3. Results

In total 155 point counts were conducted since the 24th

of October 2014, which started

during the previous phase. The number of points counts conducted among different

forest types were uneven, with 16 in primary forest, 52 in secondary forest, 31 at the

forest edge, and 56 along gallery forest. These include point counts conducted by a

BTEC candidate that was studying 5 different species including Riverside Wren, Blue-


26

Crowned manakin and yet another endemic species the Blue-black grosbeak but also

two red listed species the Great Currasow and the Great Tinamou.

The highest species richness was found in gallery and secondary forest, while the lowest

was found in primary forest and at the edge of the forest .The riverside wren was

recorded in all four forest types but most frequently within the gallery forest. The blue

crowned manakin was recorded in gallery, secondary and primary forest and was the

most frequently observed bird in primary forest among the focal birds. The red capped

manakin was only recorded once, in gallery forest. Cherries tanagers were heard and

seen in gallery, secondary and forest edge habitat. The Fiery-billed araḉari has been

recorded in secondary forest and gallery forest. The Orange collared manakin has not

yet been recorded so far in any point count. Three IUCN red listed bird species were

also recorded during the point counts, the Vulnerable Great Currasow (Crax rubra) and

the two Near threatened birds the Baird's Trogon (Trogon bairdii) and the Great

Tinamou (Tinamus major). The Great Currasow was recorded only five times and the

two latter species 17 times and 42 times respectively. All three red list species were

found in a range of forest types, especially the Great Tinamou, which appeared to be

versatile as it was recorded in primary, secondary and gallery forest habitats.

3.6.4. Discussion

All of the focal species, with an exception of the cherries tanager, mainly occur in

mature and tall wet second growth forest and not at the forest edge. The cherries tanager

however, is said to be more common in open areas, often in disturbed habitats with

thickets & shrubs (Stiles & Skutch 1989). The riverside wren was seen in all forest

types, as stated in Stiles & Skutch 1989. This particular wren is known to forage low in

dense vegetation inside mature wet forests and at forest edges, despite the name, which

0 5 10 15 20 25

Forest Edge (N=25)

Primary Forest (N=10)

Secondary Forest (N=30)

Gallery (N=30)

Frequency of Focus Bird Species found at Different Habitat Types

Riverside Wren Blue Crowned Manakin Red Capped Manakin

Cherries Tanager Fierey Billed Aracari Orange Collared Manakin

Figure 11. Frequency of focus bird species found at different habitat types


27

is conclusive with our results. The blue crowned manakin is said to be a typical forest

bird, which frequents the understory of humid mature forest and tall secondary forest

(Stiles & Skutch 1989). The secondary forest within our study area is generally tall and

regarded as old secondary forest, where blue crowned manakins were frequently

encountered. Not much is known about the ecology of this bird so with the continuation

of this study we hope to able to obtain information on this. The red capped manakin was

not as frequently encountered as the blue crowned manakins, which may be related to

their tendency to stay in upper understory and sub-canopy habitat (Stiles & Skutch

1989). The fiery-billed araḉari is commonly found in the middle to upper level of semi

open second growth forest often adjacent to clearings (Stiles & Skutch 1989). This

corresponds to our findings, where 50% of the point counts in secondary forest were

located at natural clearings

The blue-black Grosbeak was only recorded once in Primary forest, which could

suggest a preference for this forest and as low numbers were sited, that deforestation has

impacted this species in this area. However more point counts are required to draw any

conclusions for this species. The few sightings of Great Currasow could be explained by

the fact that they are generally uncommon, especially in areas that were previously

unprotected like this study site. However, this species is also hard to survey since it

possess a large variety of different calls (Baldo & Mennill 2011) and can therefore be

easily missed by the inexperienced surveyor.

The Great Tinamou (Tinamus major) was recorded quite frequently in this study and

during the BTEC study, with no obvious habitat preference found. The Great Tinamou

is heavily targeted for its meat throughout its range, mainly outside protected areas and

tt is likely that this bird profits from the fact that there is no hunting present in the study

site. The Baird’s trogon (Trogon bairdii) doesn’t appear to be as common, however, it is

a species that frequents the canopy in tall forests (Stiles & Skutch 1989) and since only

a few point counts were conducted in tall mature primary forests, this could partially

explain the few recordings of Baird’s trogon.

The point counts are uneven amongst the different types of forest, with primary forest

being underrepresented. The number of point counts conducted so far is not sufficient to

determine the presence or absence and habitat preference of the focal species. The

orange collared manakin was regularly seen within our study site and is considered

quite common by local residents, although it has not yet been recorded in our study

(Pers. Comm. Sanchez. M). More point counts need to be conducted to evenly cover the

different forest types, thereby increasing the representativeness of the whole study site.

Having undertaken this project in its pilot stage some changes have been suggested

moving onto the next phase. Very little is known about these endemic birds so before

trying to understand the effects of humans on these populations it has been decided that

increasing our knowledge of their ecology is our primary concern. Once we begin to

understand the bird’s preferences we can begin to establish a baseline which will then

allow us to study factors such as human disturbance more thoroughly. In light of this,

the six focal species will remain the same but point counts will be conducted at

locations which allow better habitat comparison; more points will be chosen in primary

forest habitat types to diminish the current bias in the point counts and allow us to more


28

accurately compare different forest types. There are also plans to expand the project to

focus on other threatened species in the area, such as the Great Currasow and the Great

Tinamou.

3.7 CRF and the Osa Conservation Sea Turtle Conservation Programme

3.7.1 Introduction

Sea turtles are a flagship species for conservation, due to their iconic nature, and being

an excellent indicator species for climate change. This is due to their temperature-

dependant sex determination, whereby increased temperatures create a sex bias skewed

toward females, which could cause entire populations to collapse. Additionally,

temperature-induced changes in plant community composition, together with rising sea

levels, may result in increased incidences of beach erosion and inundation of nests

(Janzen, 1994). Late maturation in conjunction with anthropogenic threats, such as

beach development, long line fishing and pollution, mean that turtle populations are

highly vulnerable and often unstable (Govan, 1998). Poaching, and the illegal trade of

turtle eggs causes further reductions in turtle populations, which may result in entire

clutches being destroyed. Turtle hunting was widespread between the 1950s and 70s,

with half of the world’s turtle catches being conducted in Mexico, where as many as

350,000 turtles were harvested annually (Marquez et al., 1996).

A number of conservation strategies have been established throughout Costa Rica,

including limited legal commercial egg harvesting on a nesting beach in Ostional during

the first 36 hours of wet season arribadas (mass arrival of turtles) (Campbell, 1998) and

an annual catch of 1,800 black turtles being granted to fishermen in Limόn (Troëng and

Rankin, 2004). Though the latter may have increased extractive use along with illegal

hunting in the mid 1990s, the ban on black turtle fishing and increased law enforcement

since 1999 may have increased female turtle survivorship (Troëng and Rankin, 2004).

In other regions such as Tortuguero, the Costa Rican government has made egg

poaching illegal, in addition to prohibiting the trade of calipee, the edible part of the

shell (Government of Costa Rica 1963 and 1969; Troëng and Rankin, 2004).

Meanwhile, the growing ecotourism industry in Costa Rica has provided locals with an

alternative source of income and has promoted conservation throughout the country. To

evaluate the effectiveness of such strategies, it is imperative that monitoring

programmes are long term as it can take decades for species with late maturity to show a

population response (Troëng and Rankin 2004; Bjorndal et al., 1999).

On the Osa Peninsula where turtles are threatened primarily from predation by dogs,

coastal development, illegal trade of eggs and, to a lesser extent, turtle meat (Drake,

1996), NGO Osa Conservation have been patrolling Piro and Pejeperro beaches since

2003. Their aim is to monitor the frequency and health of the local nesting turtle

population and manage nest relocations to the associated hatchery. The Frontier Costa

Rica Forest research programme works in partnership with the Osa Conservation Sea

Turtle Conservation programme, protecting the four species which nest here: olive

ridley (Lepidochelys olivacea), Pacific black turtle (Chelonia mydas agassizii),

leatherback (Dermochelys coriacea) and hawksbill (Eretmochelys imbricata). The latter

two rarely nest on these two beaches. The olive ridley is most commonly found nesting


29

here and is listed by the IUCN as ‘vulnerable’, whilst the black turtle is listed as

‘globally endangered’ (Troëng and Rankin 2004; Honarvar et al., 2008; IUCN, 2013).

3.7.2. Methodology

Now in peak olive ridley season, night and morning patrols were conducted on both

Playa Piro and Playa Pejeperro, managed between Frontier and Osa Conservation.

Morning patrols commenced at 04:00 am on Playa Piro and 03:00 am on Pejeperro

(high tide permitting) to minimise surveyor exposure to direct sunlight and high

temperatures. Night patrols typically started at 19:30 pm on both beaches. To minimise

disturbance to nesting females, surveyors used red lights during night patrols and survey

teams were limited to six people.

The survey area for both beaches was divided into 100 m sectors; this constituted a 2

km stretch of Playa Piro and 4.4 km stretch of Playa Pejeperro. For every turtle track

encountered, data such as patrol date, name of data recorder, beach sector number and

time were recorded. Nest data was also collected, for example; the nest type associated

with the tracks (in situ IS, false crawl FC; i.e., turtle returned to sea without nesting or

NA when the nest type could not be determined) and track symmetry (symmetrical S or

asymmetrical A) and the nest distance to the vegetation. The track was then crossed

through with a deep heel drag in the sand to avoid the track being recorded again in

subsequent patrols. Track characteristics were used as an indicator of species where the

turtle was absent (i.e., asymmetrical tracks suggest olive ridley, symmetrical tracks

suggest black). If a turtle was encountered, the species and distance to the tide was

recorded, a health assessment conducted and tagging of both the individual’s flippers

completed.

In-situ nests were confirmed by inserting a stick into the sand to locate the egg chamber

(indicated by a marked change in resistance when pressure applied) followed by careful

digging to confirm the presence of eggs. A false crawl was defined by the absence of a

nest or where it was clear that the turtle returned to sea without digging a nest. In the

case of predated nests, typically evident by the presence of predator tracks, egg shells

and signs that the nest had been dug up, the predator was identified by the tracks and

number of egg shells recorded.

Flipper Tagging and Health Assessments

All turtles encountered pre- or mid-nesting were tagged whilst they were laying, during

which time the female enters a haze and therefore associated stress is reduced. To

reduce the risk of infection during tagging, the tag sites were washed firstly with water,

then alcohol and iodine before applying the alcohol-cleaned tag. National’s ear tags

(National Band and Tag Co., KY, USA), each with a unique identifying number

engraved, were used. Two tags were used, one on each front flipper; both through the

third nail from the body (Figure 7).


30

Figure 7. Diagram of Turtle flipper tag placement

While the turtle was laying (or at latest when returning to the ocean, stopping the turtle

en route by covering the eyes and kneeling in front of her), a health assessment was

completed. In addition to the date, flipper tag number and beach sector number, the

following health parameters were assessed; head (including the eyes, ears and nostrils),

front and rear flippers, carapace and skin, fibropapillomas (e.g., barnacles) and body

fat.

i) The features of the head are checked for swelling, cuts, lesions, sunken in eyes,

wounds and other deformities.

ii) The flippers are checked for symmetry, wounds, deformities; such as missing digits,

cuts, missing limbs, scars from tags torn out, and fibropapillomatosis, a form of the

herpes virus which has a cauliflower-like appearance and may, in addition to being

commonly found on the skin, be found on the eyes.

iii) The carapace is also noted for wounds, mating scars, boat strike wounds, defects and

any exposed bones or flesh. Any epibionts such as barnacles, leeches and algae on the

carapace are also counted.

iv) A body condition score is given, using integers from 1-3 where 1 indicates a thin and

emaciated turtle and 3 indicates one which is overweight. The condition can most

clearly be determined by inspecting the area around the neck and shoulder area.

Nest Triangulation

Nest triangulation was carried out only on those nests between sector 10 and 20 on

Playa Piro for the close monitoring of individual nests and their respective incubation

periods and hatchling success. When a nest was in situ the egg chamber was located

through probing the sand with a stick, as above, and in effect a chimney was then dug to

reach the surface of the eggs. In this chamber, a piece of flagging tape noting the date

and a unique nest number to identify it was placed inside before the nest was covered

again with the sand originally removed. From the point on the sand surface directly

above the centre of the egg chamber, the distance to the three nearest trees was


31

measured, one central, i.e., approximately 90° relative to the nest, and one each to the

east and west of this point. These trees were also marked with flagging tape noting the

date, nest number and whether they are central (C), east (E) or west (W) of the nest. The

height of the tape in the tree from the ground was also recorded for precise nest location

referencing. Finally, the angle from the tree to the nest was recorded, again for C, E, and

W.

Nest Relocations and Hatchery Management

Osa Conservation has restored the use of the hatchery to be included in the programme.

Turtle nests that are at risk of flooding or erosion by the ocean’s tide are relocated to the

hatchery. These were deemed to be found between sector one and 10 of Playa Piro.

Considering this, the hatchery is located in sector 16 of Playa Piro. The hatchery is

divided into 300 quadrats, lettered from A-O on one axis and 1-20 on the other. Each

quadrat has a specific marker (e.g., A1, A2, and so on) in order to identify individual

nests.

A maximum of three nests are to be relocated to the hatchery per day. Any additional

nests may be relocated to sectors 11 and greater of Playa Piro, where they are not at risk

of high tides. When relocations away from one of the at-risk sectors are necessary, but

the time of day means that the ambient temperature becomes too high, or in the case that

three nests have already been relocated to the hatchery that day, nests may also be

relocated to these ‘safe’ sectors in order to avoid heat damage whilst transferring eggs.

When an in situ nest is found, the first step is to locate the egg chamber by probing the

sand. Next, wearing latex gloves, the surveyor digs out the eggs very carefully. Wet

sand found in the nest is placed into a clean bucket, to provide cushioning for the eggs

to be relocated. One by one the eggs are taken out of the nest and placed into the bucket,

in the same upright position they were found in to avoid any damage to the embryo. The

eggs are then covered by wet sand from the nest, again to avoid damage. The egg

chamber’s depth and width are measured so that a new egg chamber, approximately

identical in size and depth, can be dug during relocation. Date, sector in which the nest

was found, number of eggs and time of relocation are to be noted on a ticket allocated to

each nest, accompanied by the chamber measurements. Place of relocation is noted on

the nest ticket by circling either ‘Relocated to A’ (hatchery) or ‘B’ (other, e.g., sector

11). In either case, the egg buckets are carefully carried to their new location.

In the case of the hatchery, a pre-appointed quadrat is marked with red flagging tape by

the previous surveyor, following a chequered pattern to allow space for working and for

hatchlings between nests. The nest code (e.g., A1) is noted on the nest ticket, and all its

information is transferred to a data sheet along with the time of arrival at the hatchery.

A new egg chamber is dug, again whilst wearing latex gloves, in accordance with the

stated procedure.

The sex of hatchlings has been shown to be determined by the temperature in the nest.

Therefore, a plastic tube perforated with holes - to allow for air exchange, and long

enough to reach the top of the nest - is inserted into the middle of the chamber of each

new nest to house the thermometer inserted after egg deposition. This is in order to


32

record temperatures in the nests and to estimate the percentage of male and female

hatchlings at the end of the season. The same process of transferring the eggs to the

bucket is reversed to fill the nest. The wet sand from the bottom of the bucket is initially

used to cover the eggs and is patted down. More wet sand is then used to cover the rest

of the hole and patted down, and the remaining exposed pipe is covered with a bottle

cap so that air exchange does not occur between the nest and the ambient air. Finally, a

mesh is placed on top of the sand around the egg chamber. A ring around the nest is dug

out to approximately 10cm depth to insert the bottom edges of the mesh. The top is tied

with string in order to allow for easy opening when taking nest temperatures and to

protect the nest from flies or predators. The red flagging tape is moved to the next

quadrate to be used for relocation.

The temperature in each nest was checked three times per day: at 0600, 1400 and 2200

hours. Slowly, the thermometer is pulled out and the temperature read immediately, to

allow for an accurate recording, before being carefully replaced in its original position.

A rain gauge is also set up at the hatchery to be checked every morning at 0600, and

emptied thereafter. Nest codes and temperatures (°C) as well as rain measurements

(mm) are kept on a separate spreadsheet managed by Osa Conservation.

Whenever a surveyor visited the hatchery for temperature readings, all nests were

checked for hatchlings that had emerged from the nest and were on the surface of the

sand. When hatchlings were present, the nest code is noted and a total of 20 hatchlings

are measured. The mesh is removed and with gloves the hatchlings are placed in a clean

bucket. The mesh was replaced if any eggs or live pipped hatchlings remained in the

nest. A clean Ziploc bag was clipped onto a handheld microscale (50g). The scale was

calibrated to 0g. One by one each hatchling was placed in the bag and its weight was

noted. Next, the hatchlings’ carapace length and width is measured using a calliper and

noted. Once all necessary hatchlings were measured, they were re-placed into the bucket

and all were released on the beach. If the necessary number of hatchlings was not

obtained from a single emergence, the next hatchlings to emerge from the same nest

were measured until this number was obtained. This data is managed by Osa

Conservation.

When relocating to sector 11 of Playa Piro, a new chamber was dug according to the

previous measurements that were taken. Eggs were transferred from the bucket into the

nest, as described above, as soon as possible to reduce any effect of egg temperature

change whilst eggs remained in the bucket. This was particularly important during

warmer hours of the morning. Once the chamber was full, wet sand from the bottom of

the bucket was packed over the eggs, and the remaining space filled with more wet

sand. The nest is then triangulated according to the triangulation procedure above. No

temperature measurements were taken for nests outside of the hatchery.

Nest Excavations

Triangulated nests were excavated after the expected hatch date to determine hatch

success, emergence success and embryology. This data was combined with the data

collected at the time of nesting, and where possible linking with data of individual

turtles (i.e., tagging and health assessment). These data are essential for quantifying


33

hatching and emergence success, which are integral components in understanding

population trends. Excavations, as described below, were also performed for non-

triangulated nests when the hatchlings emerged; indicated by the presence of hatchling

tracks or emerging hatchlings.

Any egg shells on the surface (greater than 50% of the entire shell) were counted and

recorded as predated. The area was searched for any live or dead hatchlings outside of

nests and these were recorded separately before beginning the excavation. If a live

hatchling was found in the nest, it was removed and put on the surface of the sand to

make its own way to the sea. The hatchling could be assisted by moving it closer to the

sea if the sand was very hot, but as it is believed that for the hatchling to become

imprinted on its natal beach to which it will return to nest as an adult (Lohmann et al.,

2008) , the hatchling must enter the water on its own. All of the remaining contents of

the nest were removed separating unhatched eggs from empty egg shells. Unhatched

eggs which varied from the normal white colouration and/or had large impressions

present and were very soft-shelled were deemed dead - a lesson learned from years of

professional experience gained by Osa Conservation and other expert parties - and were

opened to ascertain the stage of development; white unhatched eggs were returned to

the nest. There were five developmental stages which were determined by the

percentage that the embryo occupied within the egg, graduated at 25% intervals

whereby a Stage 1 occupied 0-25% of the egg (and had blood vessels and an eye spot

present), Stage 2 occupied 26-50% and so on. The fifth category was for undeveloped

eggs which were identified as an egg yolk with no signs of an embryo or eye spot.

Protective latex gloves were worn at all times.

3.7.3. Results

This phase, a total of 89 turtle patrols was conducted at Piro beach and 47 patrols on

Pejeperro beach by Frontier and Osa Conservation. On Piro beach 41 night patrols were

conducted during this period and 22 in Pejeperro beach. Oliver Ridley turtles largely

outnumbered the Black Pacific sea turtles this phase. On Pejeperro beach a third more

turtle tracks were found oppose to Piro while the patrol effort on Piro was double as

much (see table). This phase a critically endangered Hawksbill turtle laid 3 nests on Piro

beach on the 23th

of June, 5th

of July and her last nest on the 17th

of July.

Table 8. Summary of all turtle data collected this phase. LO: Lepidochelys olivacea;

CM: Chelonia mydas agassiz; S: symmetrical tracks; AS: asymmetrical tracks, FC:

False crawls.

Piro (LO-AS) Peje (LO-AS) Piro (CM-S) Peje (CM-S)

Tracks (FC) 117 141 11 19

Nests 326 536 5 17

Total tracks 443 677 16 36


34

Hatchling success hatchery

In total 159 nests have been relocated to the turtle hatchery at the time of writing. The

first nest being moved on the 9th

of June and the latest nest moved (at the time of

writing) on the 13th

of September. Hatchling success for the first 38 nests is 89%; these

represent all the nests laid up until the first of August. In total 3275 hatchlings (N=38)

have been released successfully. Hatchling success for August and September has yet to

be analysed.

3.7.4 Discussion

The peak of the nesting season of the Pacific Green turtle is December – March and of

the Olive Ridley turtle August – October in Piro and Pejeperro (Pers. Comm. Manual

Sanchez, Osa Conservation). Although there can be yearly variation in the nesting

activity of the sea turtles and an overlap between the species, with the first turtles

arriving 2-3 months before the ‘peak’ of the nesting season (Pers. Comm. Manual

Sanchez, Osa Conservation). At Playa Naranjo, Guanacaste, Costa Rica, the peak of

Green turtles is October-March (Cornelius 1986). This phase largely overlaps with the

nesting season of the Olive Ridley turtles, which explains the higher numbers of this

species found during this time of the year. On beaches shared with other nesting turtles

species, Pacific green turtle nesting occurs after the nesting peak of the Olive Ridley

turtle (Alvarado et al. 1985). This may reduce competition for nesting space. Both

species can’t be compared based on their numbers. Olive Ridley turtles are known to be

the most abundant sea turtle species globally, especially in the Eastern Pacific ocean,

where they are known to outnumber the Pacific green turtles. (Cliffton et al. 1982,

Alvarado-Díaz et al. 2001, Márquez et al. 1976, Solís et al. 2007) This is also reflected

by their different global status, Vulnerable for the former and Endangered for the latter

(Seminoff 2004, Abreu-Grobois & Plotkin 2008).

Hatchling success from the ex-situ nests in the hatchery will be discussed when all data

has been compiled.

CRF151 Brakels P, Armintage, C., Stanish, T., Shanks, J., Curran, R. & Duszynski, N.

35

Additional Projects

N/A

CRF151

Brakels P, Armintage, C., Stanish, T., Shanks, J., Rachel, C. & Natalie D.

36

5. Proposed Work Programme for Next Phase

Primate surveys will continue, sampling evenly across all trails and times of day until

sufficient data (group composition, home range boundaries) is collected for all four primate

species. Hopefully we can pick up the line-transect sampling again next phase so accurate

density estimates can be made of spider monkeys and squirrel monkeys (in particular) with

the complementary data of actual group counts.

The monitoring program of the otter project will continue until there is sufficient data to

analyse. This will provide a greater insight into the distribution and habitat selection of the

species in Piro river. Next phase we aim to report our first findings of this year’s otter data.

Next phase we will be approaching the end of the nesting season of the Olive Ridley turtles

and we will get the first Pacific green turtles to come nest on the beaches.

The bird project will carry on collecting point count data to analyse the encounters and

abundance of endemic birds between different types of habitats across the trail.

Track surveys will be continued next phase, with the main focus on the distribution and

abundance of wild cats and their prey throughout the Piro property.

6. References

Abreu-Grobois, A & Plotkin, P. (IUCN SSC Marine Turtle Specialist Group). 2008.

Lepidochelys olivacea. The IUCN Red List of Threatened Species 2008

Alvarado, J., A. Figueroa, and H. Gallardo. 1985. Ecologia y conservacion de las tortugas

marinas de Michoacan, Mexico. Cuadernos de Investigacion, UMSNH, Mexico, 4:44 pp.

Alvarado-Díaz, J., Delgado-Trejo, C. and Suazo-Ortuño, I. 2001. Evaluation of black turtle

project in Michoacán, México. Marine Turtle Newsletter 92: 4-7.

Anoop, K. R. & Hussain, S. A. (2004). Factors affecting habitat-selection by smooth-coated

otters (Lutra perspecillata) in Kerala, India. Journal of Zoology, 263, 417-423.

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

Baldo, S., & D.J., Mennill. (2011). Vocal behaviour of Great Curassows, a vulnerable

Neotropical bird. Journal of Field Ornithology, 82 (3), 249-258.

Balme, G. A., Hunter, L. T. B., & Slotow, R. (2009). Evaluating Methods for Counting

Cryptic Carnivores. Journal of Wildlife Management, 73, 433-441.

Bibby, C., Jones, M., & Marsden, S. (1998) Expedition Field Techniques: Bird Surveys.

Royal Geographical Society, London.

Bibby, C. J., Burgess, N. D., Hill, D. A., & Mustoe, S. H. (2000). Bird Census Techniques,

CRF151


37

2nd edn. Academic Press, London.

Bjorndal, K. A., Wetherall, J. A., Bolten, A. B. & Mortimer, J. A. (1999). Twenty-six years

of Green Turtle Nesting at Tortuguero, Costa Rica: An encouraging trend. Conservation

Biology, 13, 126-134.

Blake, J.G., & Loiselle, B.A. (2000) Diversity of birds along an elevational gradient in the

Cordillera Central, Costa Rica. The Auk, 117(3), 663-686.

Blake, J.G., & Loiselle, B.A. (2001) Bird assemblages in second-growth and old-growth

forests, Costa Rica: Perspectives from mist nets and point counts. The Auk, 118(2), 304-326

Boinski, S. (1992). "Monkeys with Inflated Sex Appeal". In Ciochon, R. & Nisbett, R. The

Primate Anthology. Prentice-Hall. pp. 174–179.

Bowyer, R. T., Testa, J. W., & Faro, J. B. (1995). Habitat selection and home ranges of

river otters in a marine environment: Effects of the Exxon Valdez oil spill. Journal of

Mammalogy, 76, 1-11.

Byrne, R. & Whiten, A. (1988). Machiavellian intelligence: social expertise and the

evolution of intellect in monkeys, apes, and humans. Oxford University Press. pp. 289–294

Buckland, S. T., Anderson, D. R., Burnham, K. P., Laake, J. L., Borchers, D. L., &

Thomas, L. (2001). Introduction to Distance Sampling. Oxford, UK: Oxford University

Press.

Buckland, S. T., Anderson, D. R., Burnham, K. P. & Laake, J. L. (1993). Distance

sampling: estimating abundance of biological populations. Chapman & Hall, London.

Buckland, S. T., Plumptre, A. J., Thomas, L., & Rexstad, E. A. (2010). Design and

Analysis of Line Transect Surveys for Primates. International Journal of Primatology, 31,

883-847.

Brugiere, D., & Fleury, M. C. (2000). Estimating primate densities using home range and

line transect methods: A comparative test with the black colobus monkey Colobus satanas.

Primates, 41, 373–382.

Calzada, J., Delibes-Mateos, M., Clavero, M., & Delibes, M. (2010). If drink coffee at the

coffee-shop is the answer, what is the question? Some comments on the use of sprainting

index to monitor otters. Ecological Indicators, 10, 560-561.

Campbell, L. M. (1998). Use them or lose them? Conservation and the consumptive use of

marine turtle eggs at Ostional, Costa Rica. Environmental Conservation, 25, 305-319.

Campbell, C. J. 2008 Spider Monkeys: The Biology, Behavior and Ecology of the Genus

Ateles. Cambridge University Press. p.352

Carrillo, E., Wong, G. & Cuaron. A. D. (2000). Monitoring mammal populations in Costa

Rican protected areas under differing hunting restrictions. Conservation Biology, 14, 1580-

1591.

Carrillo-Rubio, E., & Lafón, A. (2004). Neotropical river otter micro-habitat preference in

West-central Chihuahua, Mexico. IUCN Otter Specialist Group Bulletin, 21, 10-15.

CRF151


38

Cezare, C.H.G., Brandt, A.P., Pianca, C., and C.F. Josef. 2002. Some observations on the

southern river otter (Lontra longicaudis, Mammalia: Mustelidae): status and biology. Pages

149-155 in Mateos, E., Guix, J.C., Serra, A. and K. Pisciotta, editors. Censuses of

vertebrates in a Brazilian Atlantic rainforest área: the Paranapiacaba fragment. Centre de

Recursos de Biodiversitat Animal. Universitat de Barcelona. Barcelona, Spain.

Chanin, P. (2003). Monitoring the Otter Lutra lutra. Conserving Natura 2000 Rivers

Monitoring Series No. 10. English Nature, Peterborough, UK.

Chapman, C. A. 1990. Ecological constraints on group size in three species of Neotropical

primates. Folia Primatologica, 55, 1-9.

Chapman, C. A. & Balcomb, S. R. (1998). Population characteristics of howlers: ecological

conditions or group history. International Journal of Primatology, 19, 385-403.

Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1995). Ecological constraints on

group size: analysis of spider monkey and chimpanzee subgroups. Behavioural Ecology

and Sociobiology, 36, 59-70.

Cleveland, C.C., Wieder, W.R., Reed, S.C. & Townsend, A.R. (2010). Experimental

drought in a tropical rain forest increases soil carbon dioxide losses to the atmosphere.

Ecology, 91, 2313-2323.

Cliffton, K., Cornejo, D.O. and Felger, R.S. 1982. Sea turtles of the Pacific coast of

México. In: K.A. Bjorndal (ed.) Biology and Conservation of Sea Turtles, pp. 199-209.

Smithsonian Institution Press, Washington, D.C.

Cornelius, S.E. 1986. The sea turtles of Santa Rosa National Park. Fundacion de Parques

Nacionales Costa Rica. 64 pp.

Cropp, S. & Boinski, S. (2000). The Central American Squirrel Monkey (Saimiri

oerstedii): Introduced Hybrid or Endemic Species? Molecular Phylogenetics and

Evolution, 16, 350-365.

Crowley, S., Johnson, C. J. & Hodder, D. (2012). Spatial and behavioural scales of habitat

selection and activity by river otters at latrine sites. Journal of Mammalogy, 93, 170-182.

Cuarón, A. D., Morales, A., Shedden, A., Rodriguez-Luna, E. & de Grammont, P. C.

(2008a). Ateles geoffroyi. In: IUCN 2010. IUCN Red List of Threatened Species. Version

2010.4. Available at: www.iucnredlist.org. [Accessed: 14th June, 2012].

Cuarón, A. D., Shedden, A., Rodríguez-Luna, E., de Grammont, P. C., Link, A., Palacios,

E., Morales, A. & Cortés-Ortiz, L. (2008b). Alouatta palliata. In: IUCN 2013. IUCN Red

List of Threatened Species. Version 2013.2. Available at: www.iucnredlist.org. [Accessed:

25th May, 2013].

Davison, A., Birks, J. D. S., Brookes, R. C., Braithwaite, T. C., & Messenger, J. E. (2002).

On the origin of faeces: morphological versus molecular methods for surveying rare

carnivores and their scats. Journal of Zoology, London, 257, 141-144.

Defler, T. (2004). Primates of Colombia. Conservation International. p. 234.

Depue, J. E. & Ben-David, M. (2010). River otter latrine site selection in arid habitats of

CRF151


39

western Colorado, USA. Journal of Wildlife Management, 74, 1763-1767.

Di Fiore, A. & Campbell, C. J. (2007). The Atelines: variation in ecology, behaviour, and

social organization. In: Campbell, C. J., Fuentes, A., MacKinnon, K. C., Panger, M., &

Bearder, S. K. (Eds.), Primates in perspective. Oxford University Press, Oxford, 155-185.

Drake, D. L. (1996). Marine turtle nesting, nest predation, hatch frequency, and nesting

seasonality on the Osa Peninsula, Costa Rica. Chelonian Conservation and Biology, 2, 89-

92.

Dunn, J. C., Cristóbal-Azkarate, J. & Veá, J. J. (2009). Differences in diet and activity

pattern between two groups of Aloutta palliata associated with the availability of big trees

and fruit of top food taxa. American Journal of Primatology, 71, 654-662.

Emmons, L., & Feer, F. (1997). Neotropical rainforest mammals: a field guide. The

University of Chicago Press, Chicago.

Fedigan, L. M., Rose, L. M., & Morera Avila, R. (1998). Growth of mantled howler

groups in a regenerating Costa Rican dry forest. International Journal of Primatology,

19(3), 405–432.

Fagan, M. E., DeFries, R. S., Sesnie, S. E., Arroyo, J. P., Walker, W., Soto, C., Chazdon,

R. L. & Sanchun, A. (2013). Land cover dynamics following a deforestation ban in

northern Costa Rica. Environmental Research Letters, 8, 1-9.

Fashing, P. J., & Cords, M. (2000). Diurnal primate densities and biomass in the Kakamega

Forest: An evaluation of census methods and a comparison with other forests. American

Journal of Primatology, 50, 139–152.

Foster, R. & Harmsen, B. (2012). A critique of density estimation from camera-trap data.

The Journal of Wildlife Management, 76, 224-236.

Garber, P. A., Estrada, A. & Pavelka, M. S. (2006). New perspectives in the study of

Mesoamerican primates: Distribution, Ecology, Behaviour, and Conservation. Springer,

US.

Garrigues, R. & Dean, R. (2007). The Birds of Costa Rica. Zona Tropical, Costa Rica.

Glander, K. E. (1980). Reproduction and population growth in free-ranging mantled

howling monkeys. American Journal Physical Anthropology, 53, 25-36.

Gori, M., Carpaneto, G.M. & Ottino, P. (2003). Spatial distribution and diet of the

Neotropical otter Lontra longicaudis in the Ibera Lake (northern Argentina). Acta

Theriologica, 48, 495-504.

Govan, H. (1998). Community turtle conservation at Río Oro on the Pacific coast of Costa

Rica. Marine Turtle Newsletter, 80, 10-11.

Graham, K. E., Bulloch, M. J., & Lewis, T. R. (2013). Foraging behaviour of three primate

species in a Costa Rican coastal lowland tropical wet forest. Biodiversity Journal, 4 (2):

327-334.

Guter, A., Dolev, A., Saltz, D. & Kronfeld-Schor, N. (2008). Using videotaping to validate

the use of spraints as an index of Eurasian otter (Lutra lutra) activity. Ecological

CRF151


40

Indicators, 8, 462-465.

Hájková, P., Zemanová, B., Roche, K. & Hájek, B. (2009). An evaluation of field and

noninvasive genetic methods for estimating Eurasian otter population size. Conservation

Genetics, 10, 1667-1681

Hassel-Finnegan, H. M., Borries, C., Larney, E., Umponjan, M., & Koenig, A. (2008). How

reliable are density estimates for diurnal primates?. International Journal of Primatology,

29(5), 1175-1187.

Henderson, C. L. (2002). Field Guide to the wildlife of Costa Rica, 1-36. University of

Texas Press, Austin, USA

Henderson, C. L. (2010). Birds of Costa Rica: a Field Guide. 2nd Ed. University of Texas

Press, Singapore.

Herzog, S.K., Kessler, M., & Cahill, T.M. (2002). Estimating species richness of tropical

bird communities from rapid assessment data. The Auk, 119 (3), 749-769.

Holden, J., Yanuar, A. & Martyr, D. J. (2003). The Asian Tapir in Kerinci Seblat National

Park, Sumatra: evidence collected through photo-trapping. Oryx, 37, 34-40.

Honarvar S., O'Connor, M. P. & Spotila, J. R. (2008). Density-dependent effects on

hatching success of the olive ridley turtle, Lepidochelys olivacea. Oecologia 157, 221-230.

IUCN Red List of Threatened Species. (2013). Version 2013.1. Available at:

www.iucnredlist.org. [Accessed: 5th September 2013.

IUCN Red List of Threatened Species. (2014). Version 2014.1. Available at:

www.iucnredlist.org. [Accessed: 10th December 2014].

IOSF. (2012). The International Otter Survival Fund. Available at:

http://www.otter.org/otterSpecies.aspx [Accessed: 15th September 2014]

Janzen, F. J. (1994). Climate change and temperature-dependent sex determination in

reptiles. Population Biology, 91, 7487-7490.

Jongsma, J., Pieterse, S., Planqué, B. & Vellinga, W. (2005). Xeno-canto, Sharing Bird

Sounds Around the World. Available at: www.xeno-canto.org [Accessed: 11th September

2014]

Julliot, C. (1997). Impact of seed dispersal by red howler monkeys, Alouatta seniculus, on

the seedling population in the understorey of tropical rain forest. Journal of Ecology, 85, 431-440.

Kappelle, M., Castro, M., Acevedo, H., González, L. & Monge Huberth (2002) Ecosystems of the Osa

Conservation Area (ACOSA). 1st ed . Santo Domingo de Heredia, Costa Rica: Institudo Nacional de

Biodiversidad, INBio. 500p.

Karanth, K. U. (1995). Estimating tiger Panther tigris populations from camera-trap data

using capture-recapture models. Biological Conservation, 71, 333-338.

CRF151


41

Kasper, CB., Bastazini, VAG., Salvi, J. & Grillo, HCZ. (2008). Trophic ecology and the

use of shelters and latrines by the Neotropical otter (Lontra longicaudis) in the Taquari

Valley, Southern Brazil. Iheringia, Série Zoologia, 98, 469-474.

Kelly, M. J., Noss, A. J., Di Bitetti, M. S., Maffei, L., Arisp R. L., Paviolo A., De Angelo,

C. & di Blanco, Y. E. (2008). Estimating puma densities from camera trapping across three

study sites: Bolivia, Argentina, and Belize. Journal of Mammalogy, 89, 408-418.

Kruuk, H., Conroy, J.W.H., Glimmerveen, U. & Ouwerkerk, E.J. (1986). The Use of

Spraints to Survey Populations of Otters Lutra lutra. Biological Conservation, 35, 187-194.

Kruuk, H. (1992). Scent marking by otters (Lutra lutra): signalling the use of resources.

Behavioural Ecology, 3, 133-140. In Remonti, L., Balestrieri, A., Smiroldo, G. & Prigioni,

C. (2011). Scent marking of key food sources in the Eurasian otter. Annales Zoologici

Fennici, 48, 287-294.

Langbein, J., Hutchings, M. R., Harris, S., Stoate, C., Tapper, S. C. & Wray, S. (1999).

Techniques for assessing the abundance of Brown Hares Lepus europaeus. Mammal

Review, 29, 93-116.

Larrucea, E. S., Brussard, P. F., Jaeger, M. M. & Barrett, R. H. (2007). Cameras, Coyotes,

and the Assumption of Equal Detectability. The Journal of Wildlife Management, 71, 1682-

1689.

Larsen, T & Toft, R. (2010) OSA where the rainforest meets the sea. Zona Tropical

Publications; 1st edition. 222 p.

Leca, J. B., Gunst, N., Rompis, A., Soma, G., Arta Putra, I. G. A., & Wandia, I. N. (2013).

Population density and abundance of ebony leaf monkeys (Trachypithecus auratus) in West

Bali National Park, Indonesia. Primate Conservation 26, 133-144.

Lohmann, K. J., Putman, N.F. & Lohmann, C.M.F. (2008). Geomagnetic imprinting: A

unifying hypothesis of long-distance natal homing in salmon and sea turtles. Proceedings of

the National Academy of Sciences of the United States of America , 105, 19096-19101.

Quadros, J. & Monteiro-Filho, V. (2002). Sprainting sites of the Neotropical otter, Lontra

longicaudis, in and Atlantic forest area of Southern Brazil. Journal of Tropical

Mammalogy, 9, 39-46.

Link, A., Gabriela de Luna, A., Alfonso, F., Giraldo-Beltran, P., & Ramirez, F. (2010).

Initial effects of fragmentation on the density of three neotropical primate species in two

lowland forests of Colombia. Endangered Species Research, 13, 41-50.

Mackenzie, D. I. (2005). What are the issues with 'presence/absence' data for wildlife

managers? Journal of Wildlife Management, 69, 849-860.

Marshall, A. R., Lovett, J. C., & White, P. C. L. (2008). Selection of line-transect methods

for estimating the density of group-living animals: lessons from primates. American Journal

of Primatology, 70, 452–462.

Márquez, R., Villanueva, A. and Peñaflores, C. 1976. Sinopsis de datos biologicos sobre la

tortuga golfina, Lepidochelys olivacea (Eschscholtz, 1829). Instituto Nacional De Pesca,

México, INP/52 Sinopsis sobre la Pesca.

CRF151


42

Marquez, R., Peñaflores C., & Vasconcelos, J. (1996). Olive Ridley Turtles (Lepidochelys

olivacea) show signs of recovery at La Escobilla. Oaxaca Marine Turtle Newsletter, 73, 5-

7. Available at: www.seaturtle.org [Accessed: 21st September 2014]

Melquist, W. E. & Hornocker, M. G. (1983). Ecology of river otters in west central Idaho.

Wildlife Monographs, 83, 3-60.

Miller, S. G., Knight, R. L. & Miller, C. K. (1998). Influence of recreational trails on

breeding bird communities. Ecological Applications, 8, 162-169.

Mittermeier, R. A. (1987). Effects of hunting on rain forest primates. Primate Conservation

in the Tropical Rain Forest. American Journal of Physical Anthropology, 74(4), 542-544.

Minca, C. & Linda, M. (2002). Ecotourism on the Edge: the case of Corcovado National

Park, Costa Rica. In: Font, X. & Tribe, J. editors. Forest tourism and recreation: case

studies in environmental management. Oxon: CABI Publishing, UK. 103-127

Norvell, R.E., F.P. Howe, & J.R. Parrish. (2003). A seven-year comparison of relative-

abundance and distance-sampling methods. The Auk, 120, 1013-1028.

Noss, A. J., Cuéllar, R. L., Barrientos, J., Maffei, L., Cuéllar, E., Arispe, R., Rúmiz, D. &

Rivero, K. (2003). A Camera Trapping and Radio Telemetry Study of Lowland Tapir

(Tapirus terrestris) in Bolivian Dry Forests. Tapir Conservation, 12, 24-32.

Obbard, M. E., Howe, E. J. & CJ Kyle. (2010). Empirical comparison of density estimators

for large carnivores. Journal of Applied Ecology, 47, 76-84.

O'Brien, T. G. (2008). On the use of automated cameras to estimate species richness for

large- and medium-sized rainforest mammals. Animal Conservation, 11, 179-181.

Olifiers, N., Loretto, D., Rademake, V., & Cerqueira, R. (2011). Comparing the

effectiveness of tracking methods for medium to large-sized mammals of Pantanal.

Zoologia, 28(2), 207-213.

Oliveira-Santos, L. G. R., Zucco, C. A., Antunes, P. C. & Crawshaw, P. G. (2010). Is it

possible to individually identify mammals with no natural markings using camera-traps? A

controlled case study with lowland tapirs. Mammal Biology, 75, 375-378.

Paterson, J.D. (2001) Primate behaviour. 2nd

edition. Waveland Press Inc. 230 p.

Pejchar, L., Pringle, R.M., Ranganathan, J., Zook, J.R., Duran, G., Oviedo, F., Daily, G.C.

(2008) Birds as agents of seed dispersal in a human-dominated landscape in southern Costa

Rica. Biological Conservation 141, 536-544.

Peres CA. 1999. General guidelines for standardizing line

transect surveys of tropical forest primates. Neotropical

Primates 7:11–16.

Pettorelli, N., Lobora. A. L., Msuha, M. J., Foley, C. & Durant, S. M. (2009). Carnivore

biodiversity in Tanzania: revealing the distribution patterns of secretive mammals using

camera traps. Animal Conservation, 13, 131-139.

Plumptre AJ (2000) Monitoring mammal populations with line

transect techniques in African forests. J Appl Ecol 37:356–368

CRF151


43

Plumptre, A. J., & Cox, D. (2006). Counting primates for conservation: primate surveys in

Uganda. Primates, 47, 65–73.

Powell, G.V.N., Barborak, J., & Rodriguez, M.S. (2000). Assessing representativeness of

protected natural areas in Costa Rica for conserving biodiversity: a preliminary gap

analysis. Biological Conservation, (93), 35-41.

Prenda, J. & Granado-Lorencio, C. (1996). The relative influence of riparian habitat

structure and fish availability on otter Lutra lutra l. sprainting activity in a small

Mediterranean catchment. Biological Conservation, 76, 9-15.

Pruetz, J. D., & Leasor, H. C. (2002). Survey of three primate species in forest fragments at

La Suerte Biological Field Station, Costa Rica. Neotropical Primates, 10(1), 4-8.

Quadros, J. & Monteiro-Filho, E. L. A. (2002). Sprainting sites of the neotropical otter,

Lontra longicaudis, in an Atlantic forest area of southern Brazil. Journal of Neotropical

Mammalology, 9, 39-46.

Remonti, L., Balestrieri, A., Smiroldo G., & Prigioni, C. (2011). Scent marking of key food

sources in the Eurasian otter. Annales Zoologici Fennici, 48, 287-294.

Rose, L., Perry, S., Panger, M., Jack, K., Manson, J., Gros-Louis, J., and Mackinnin, K.

(2003). "Interspecific Interactions between Cebus capucinus and other Species: Data from

Three Costa Rican Sites". International Journal of Primatology 24 (4): 780–785.

Rostain, R. R., Ben-David, M., Groves, P. & Randall, J. A. (2004). Why do river otters

scent-mark? An experimental test of several hypotheses. Animal Behaviour, 68, 703-711.

Rowcliffe, J. M. & Carbone, C. (2008). Surveys using camera traps: are we looking to a

brighter future? Animal Conservation, 11, 185-186.

Rowcliffe, J. M., Field. J., Turvey, S. T. & Carbone, C. (2008). Estimating animal density

using camera traps without the need for individual recognition. Journal of Applied Ecology,

45, 1228-1236.

Sánchez-Azofeifa, G. A., Harriss, R. C. & Skole, D. L. (2001). Deforestation in Costa Rica:

A quantitative analysis using remote sensing imaging. Biotropica, 33, 378-384.

Sánchez-Azofeifa, G. A., Rilvard, B., Calvo, J. & Moorthy, I. (2002). Dynamics of tropical

deforestation around national parks: remote sensing of forest change on the Osa Peninsula

of Costa Rica. Mountain Research and Development, 22, 352-358.

Santos, L. B. & Dos Reis, N. R. (2012). Use of shelters and marking sites by Lontra

longicaudis (Olfers, 1818) in lotic and semilotic environments. Biota Neotropica, 12, 199-

205.

Sarmento, P., Cruz, J., Eira, C. & Fonseca, C. (2009). Evaluation of Camera Trapping for

Estimating Red Fox Abundance. Journal of Wildlife Management, 73, 1207-1212.

Seminoff, J.A. (Southwest Fisheries Science Center, U.S.). 2004. Chelonia mydas. The

IUCN Red List of Threatened Species 2004

CRF151


44

Smythe, N. (1978). The Natural History of the Central American Agouti (Dasyprocta

punctata). Smithsonian Institution Press, Washington, USA.

Solís, D.S., Orrego, C.M., Blanco-Segura, R.V., Harfush-Meléndez, M.R., Albavera-

Padilla, E.O. and Valverde, R.A. 2007. Estimating arribada size: going global. Presented at

the 27th Annual Symposium on Sea Turtle Conservation and Biology. Myrtle Beach, South

Carolina, 22-28 February, 2007.

Stevens, S. S. & Serfass, T. L. (2008). Visitation patterns and behaviour of nearctic river

otters (Lontra canadensis) at latrines. Northeastern Naturalist, 15, 1-12.

Stiles, F.G. and Skutch, A.F. 1989. A Guide to the Birds of Costa Rica. Cornell University

Press, Ithaca, NY.

Swimley, T. J., Serfass, T. L., Brooks, R. P. & Tzilkowski, W. M. (1998). Predicting river

otter latrine sites in Pennsylvannia. Wildlife Society Bulletin, 26, 836-845.

Thomas, L., Buckland, S. T., Rexstad, E. A., Laake, J. L., Strindberg, S., Hedley, S. L.,

Bishop, J. R. B., Marques, T. A. & Burnham, K. P. (2010). Distance software: design and

analysis sampling surveys for estimating population size. Journal of Applied Ecology, 47,

5-14.

Troëng S., & Rankin, E., (2004). Long-term conservation efforts contribute to positive

green turtle Chelonia mydas nesting trend at Tortuguero Park, Costa Rica. Biological

Conservation, 121, 111-116.

Trolle, M., Noss, A. J., Lima, E.S. & Dalponte, J. C. (2007). Camera-trap studies of maned

wolf density in the Cerrado and Pantanal of Brazil. Biodiversity and Conservation, 16,

1197-1204.

Trolle, M., Noss, A. J., Cordeiro, J. L. P. & Oliveira, L. F. B. (2008). Brazilian Tapir

Density in the Pantanal: A Comparison of Systematic Camera-Trapping and line-Transect

Surveys. Biotropica, 40, 211-217.

Turkozan, O., Yamamoto, C., & Yilmaz, C. (2011). Nest Site Preference and Hatching

Success of Green (Chelonia mydas) and Loggerhead (Caretta caretta) Sea Turtles at

Akyatan Beach, Turkey. Chelonian Conservation and Biology, 10 (2), 270-275.

Wainwright, M. & Arias, O. (2007). The mammals of Costa Rica: a natural history and

field guide. Cornell University Press, United States.

Waldemarin, H. F. & Alvarez, R. (2008). Lontra longicaudis. IUCN Red List of Threatened

Species. Version 2013.2. Available at: www.iucnredlist.org. [Accessed: 25th May, 2013].

Weghorst, J. A. (2007). High population density of black-handed spider monkeys (Ateles

geoffroyi) in Costa Rican lowland wet forest. Primates, 48, 108-116.

Zimmermann, A., Walpole, M. J., and Leader-Williams, N. (2005). Cattle ranchers’

attitudes to conflicts with Jaguar Panthera onca in the Pantanal of Brazil. Oryx 39, 406-

412.

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COSTA RICA FOREST RESEARCH PROGRAMME (CRF ......Frontier’s Costa Rica Forest Research (CRF) programme began in July 2009 in collaboration with the local non-governmental organisation