Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64706, mayo 2025 (Publicado May. 15, 2025)

Agricultural landscapes in Costa Rica: forest remnants account

for a rich mammal (Mammalia) community

Maria I. Runnebaum1; https://orcid.org/0000-0003-0908-723X

Manuel R. Spinola2; https://orcid.org/0000-0002-7839-1908

J. Edgardo Arévalo1; https://orcid.org/0000-0003-4160-8373

Bernal Rodríguez-Herrera1,3; https://orcid.org/0000-0001-8168-2442

1. Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica; mariaruj@gmail.com (*Correspondence), jose.

arevalohernandez@ucr.ac.cr, bernal.rodriguez@ucr.ac.cr

2. Instituto Internacional en Conservación y Manejo de Vida Silvestre, Universidad Nacional, ´ Heredia, Costa Rica;

mspinola10@gmail.com

3. Centro de Investigaciones en Biodiversidad y Ecología Tropical (CIBET), Universidad de Costa Rica, San José, Costa

Rica; bernal.rodriguez@ucr.ac.cr

Recibido 03-IX-2024. Corregido 25-III-2025. Aceptado 07-IV-2025.

ABSTRACT

Introduction: The effects of habitat loss and fragmentation on wildlife are complex processes mediated by fac-

tors other than habitat size and isolation alone. For example, the quality of the surrounding matrix, edge-induced

effects, and proximity to large forest tracks are of particular importance. These factors may allow or limit animal

movements and, thus, population persistence in human-modified landscapes. This is the case in some remaining

forest fragments in Costa Rican landscapes.

Objective: To investigate the influence of the landscape composition on medium (< 10 kg) and large-sized (>

10 kg) terrestrial mammals thriving in an agricultural landscape, we surveyed mammal species in 30 sites in the

Sarapiquí region, Costa Rica.

Methods: We used 45 camera traps to assess the richness and composition of mammal species in forest frag-

ments embedded in pineapple plantations and pastures from 2013 to 2014. Richness estimates were calculated

using capture-recapture models for closed populations. We adjusted the models for repeated count data analysis

to determine landscape cover types that best explained species richness.

Results: Twenty-two species of mammals in nine orders and 16 families were recorded. Despite the habitat loss,

fragmentation, and agricultural practice pressures over the years, the Sarapiquí region maintains a significant

portion of its native mammalian fauna compared to comprehensive historical inventories available for the area.

We found that forest cover best predicts the levels of species richness.

Conclusion: many forest-dependent species, such as the threatened Baird’s Tapir, can thrive in fragmented

habitats in agricultural landscapes, while other species seem to be heavily affected by habitat modification and

land use type. Forested areas and pastures with a high density of scattered trees and proximity to extensive

forests could enhance the conservation of mammal communities despite the intense human land use in these

agricultural landscapes.

Keywords: Biodiversity; conservation; forest cover; landscape composition; matrix quality.

https://doi.org/10.15517/rev.biol.trop..v73iS2.64706

SUPPLEMENT

SECTION: ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64706, mayo 2025 (Publicado May. 15, 2025)

INTRODUCTION

Studies on tropical forests show that cru-

cial ecological processes for wildlife thriving

in fragmented habitats are complex and are

highly influenced by the quality of the matrix

where the fragments are imbedded (Crome,

1997; Debinski, 2006; García, 2011; Laurance &

Bierregaard, 1997; Semper-Pascual et al., 2021).

Animal populations may be negatively affected

by the reduction of the original forests and the

increase in isolation between forest fragments

(Andrade-Núñez & Aide, 2010; Chetcuti et al.,

2021; Murcia, 1995; Renjifo, 2001; Saunders

et al., 1991). This is because the reduction

in area and isolation of the fragments can

modify the physical and biological conditions

of animals, leading to the loss of species and a

decline in population size (Andrade-Núñez &

Aide, 2010). In addition, species in forest frag-

ments may experience reduced immigration

rates, suffer increased predation and parasit-

ism, and may be affected by invasions of exotic

species (Goodman & Rakotondravony, 2000;

Lynam, 1997; Parsons, 1972; Ramos, 2004).

These alterations can be further exacerbated by

variable edge effect conditions (Bernard & Fen-

ton, 2007; García, 2011; Semper-Pascual et al.,

2021). The severity of the edge effects depends

on the quality and composition of the matrix,

which, in turn, may influence animal move-

ments between fragments. Thus, the composi-

tion of the matrix may function as a buffering

element or become additional habitats for some

animal species (Kattan, 2002; Laurance & Peres,

2006; Medellín & Equihua, 1998; Pardini, 2004;

Pardini et al., 2000; Prevedello & Vieira, 2010).

Many species of mammals are strongly

affected by land modifications such as the

ones described above (Chiarello, 2000; Da Silva

& Mendes-Pontes, 2008). Some species may

be sensitive to habitat loss and fragmentation

RESUMEN

Paisajes agrícolas en Costa Rica: remanentes de bosque albergan una rica comunidad de mamíferos

Introducción: Los efectos de la pérdida y fragmentación de hábitats en la vida silvestre son procesos complejos,

influenciados por factores más allá del tamaño y el aislamiento del hábitat. Por ejemplo, la calidad de la matriz

circundante, los efectos inducidos por los bordes y la proximidad a grandes áreas forestales son de particular

importancia. Estos factores pueden facilitar o limitar los movimientos de los animales, y, por lo tanto, la persis-

tencia de las poblaciones en paisajes modificados por humanos, como ocurre en los fragmentos de bosque que

aún existen en algunas regiones de Costa Rica.

Objetivo: Investigar cómo la composición del paisaje influye en los mamíferos terrestres de tamaño mediano (<

10 kg) y grande (> 10 kg) que viven en un paisaje agrícola. Para ello, realizamos un estudio de las especies de

mamíferos en 30 sitios de la región de Sarapiquí, Costa Rica.

Métodos: Utilizamos 45 cámaras trampa para evaluar la riqueza y la composición de las especies de mamíferos

en fragmentos de bosque situados entre plantaciones de piña y pastizales, desde 2013 hasta 2014. Calculamos

las estimaciones de riqueza utilizando modelos de captura-recaptura para poblaciones cerradas. Ajustamos estos

modelos para el análisis de datos de conteo repetido, con el fin de identificar los tipos de cobertura del paisaje que

mejor explican la riqueza de especies.

Resultados: Se registraron 22 especies de mamíferos, pertenecientes a nueve órdenes y 16 familias. A pesar de la

pérdida de hábitat, la fragmentación y las presiones de las prácticas agrícolas a lo largo de los años, la región de

Sarapiquí conserva una parte significativa de su fauna mamífera nativa, comparada con los inventarios históricos

disponibles para el área. Descubrimos que la cobertura forestal es el mejor predictor de los niveles de riqueza de

especies.

Conclusión: Muchas especies dependientes del bosque, como el amenazado tapir de Baird, pueden prosperar en

hábitats fragmentados dentro de paisajes agrícolas, mientras que otras parecen verse fuertemente afectadas por

la modificación del hábitat y el tipo de uso del suelo. Las áreas forestales y los pastizales con alta densidad de

árboles dispersos, así como la proximidad a grandes extensiones de bosque, podrían mejorar la conservación de

las comunidades de mamíferos, a pesar del intenso uso humano del suelo en estos paisajes agrícolas.

Palabras clave: Biodiversidad, cobertura boscosa, composición del paisaje, calidad de la matriz.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64706, mayo 2025 (Publicado May. 15, 2025)

(Chetcuti et al., 2021; Ewers & Didham, 2005;

Harvey et al., 2006), while others benefit from

agriculture or silviculture expansion (Lessa et

al., 2012; Lyra-Jorge et al., 2008). For instance,

large-sized species that have wide home ranges,

specific habitat requirements, and low popu-

lation densities may be particularly affected

by habitat alterations (Brashares et al., 2001;

García, 2011; Kinnaird et al., 2003; Michalski

& Peres, 2005; Silver et al., 2004). Moreover,

large-sized mammals might be more vulnerable

to local extinction than small mammal species

(Bennett, 1990; Daily et al., 2003; Elmhagen &

Angerbjörn, 2001; Robinson, 1996). This can

have ecological implications as it is known that

large-sized to medium-sized mammals play an

important role in tropical ecosystem function as

seed dispersers and energy cycle regulators (De

la Cruz, 2012; Howe & Smallwood, 1982; Silver

et al., 2004; Terborgh, 1992). These attributes

make some mammal species of special inter-

est for conservation (Ceballos & Ehrlich, 2002;

Chiarello, 2000; Da Silva & Mendes Pontes,

2008; Daily et al., 2003; Kerley et al., 2003; Lino

et al., 2019), such as the Baird’s Tapirs (Tapi-

rus bairdii) and Jaguars (Panthera onca), that

have been recognized as flagship species for

conservation programs because of their large

forest area dependency, along with many other

species that are listed under Appendix 1 of the

Convention on International Trade in Endan-

gered Species (CITES) (Caro & O’Doherty,

1999; Kinnaird et al., 2003).

In Costa Rica, the historical loss of for-

est cover has been attributed to agricultural

development practices (e.g., monocultures) and

cattle grazing, human population growth, and

the expansion and construction of roads (Bar-

rantes, 2000; Cove et al., 2013). Particularly

during the ’80s, Costa Rica had the highest rates

of deforestation in Central America with more

than 70% of primary forests lost by the end

of that decade (Sader & Joyce, 1998; Sánchez-

Azofeifa et al., 2001; Watson et al., 1998). This

deforestation process created landscape mosaics

of disturbed habitats, pastures, and single-spe-

cies crops. For example, the heavily deforested

northern region of the country that includes the

Sarapiquí region is now extensively covered by

pineapple and banana plantations, mixed agri-

culture, forest fragments as well as private and

state-owned protected areas (Butterfield, 1994;

Chiarello, 2000; De la Cruz, 2012; Lyra-Jorge et

al., 2008; Sánchez-Azofeifa et al., 2001; Semper-

Pascual et al., 2021). Since the late 90’s, private

initiatives in the area have augmented natural

reserves that may have reduced pressure from

agriculture and farming; however, the spread of

large-scale pineapple and banana plantations,

as well as cattle grazing are still posing pressure

on the remaining forest habitats (Araya, 2017;

Cove et al., 2012; Lino et al., 2019; Montagnini,

1994; Sánchez-Azofeifa et al., 2001).

Despite the increasing number of studies

highlighting the importance of the quality of

the matrix for the maintenance of biodiversity

in fragmented landscapes (Fahrig et al., 2011;

Perfecto & Vandermeer, 2010), there is still a

lack of information about the land use char-

acteristics that may favor or limit richness and

composition of terrestrial mammal species in

human-dominated landscapes (Cuarón, 2000;

Daily et al., 2003; Lino et al., 2019; Urquiza-

Haas et al., 2009). In tropical countries like

Costa Rica, the dynamic turnover of land use

types and its potential consequences for animal

communities needs further investigation (De la

Cruz, 2012; Gascon et al., 1999). The objective

of this study is to assess the species composition

of medium and large-sized mammals thriv-

ing in an agricultural landscape in the Carib-

bean slope of Costa Rica. We hypothesize that

the amount of forest cover and proximity to

large tracks of protected forest would increase

habitat availability, thus favoring mammal spe-

cies abundance. In addition, we expect that

structurally low-quality matrices such as pas-

ture and pineapple near or adjacent to forest

fragments would decrease the abundance of

mammal species.

METHODS

Study Area: We conducted the study in

Sarapiquí, near Puerto Viejo and La Virgen,

province of Heredia, from November 2013

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64706, mayo 2025 (Publicado May. 15, 2025)

to May 2014. The area experiences a short

dry season from March to May, followed by a

prolonged rainy season from May to Febru-

ary. The average annual temperature is 25.3º

C, and the mean annual precipitation is 3777

mm (Matlock & Hartshorn, 1999). The study

area covered 32,716 hectares comprising 54%

of forest fragments, 24 % pastures primarily

for cattle grazing, and the remaining 22 % with

pineapple and other scattered crop patches

(Appendix 1). The study area is divided by

the Sarapiquí River and the main road from

Horquetas to La Virgen, containing important

human settlements (Butterfield, 1994; Schelhas

& Sánchez-Azofeifa, 2006). Large and continu-

ous forest areas are found both in the northern

and southern areas, adjacent to the northern

limit of the Braulio Carrillo National Park

(BCNP). With 47,586 hectares of forest, this

park is the most extensive one in the region and

has an ample altitudinal range, varying from 32

to 2,906 meters above sea level. In addition, the

BCNP has a large proportion of primary for-

est that allows for suitable habitats for several

threatened, endemic, and narrow-limited spe-

cies in Sarapiquí (Butterfield, 1994; Schelhas

& Sánchez-Azofeifa, 2006). Several forest frag-

ments embedded in cattle pastures are found

in proximity to this protected area, including

Pozo Azul (161.8 ha), Selva Verde (202 ha), and

Tirimbina (345 ha), which are private reserves

for ecotourism and scientific research. The

northern side of the study area contains the

largest forest remnants within private reserves,

including EcoVida (650 ha), Alfa Industrias

(550 ha), and Santa Ines (526 ha) (Appen-

dix 2). Given their relatively large size, these

forest remnants may represent an important

habitat for many species. Nonetheless, there

is a significant amount of pressure from the

expansion of the agricultural frontier, mainly

pineapple. For example, Finca La Virgen, which

cultivates pineapple, has several remnants of

mostly riparian forests that are immersed both

in pastures and pineapple plantations. There

are also rivers, roads and small towns in the

surrounding area.

Sampling site selection: We laid out a grid

of hexagons of 1 km2 on a map of the study area

using ArcGIS 10. We selected 30 hexagons with

at least 10 % forest cover in a stratified manner

and deployed autonomous camera traps at each

of the 30 selected sampling sites. Each camera-

trap was at least 1 km apart from one another.

Landscape analysis: We conducted a land-

scape analysis using ArcGIS 10 to classify

the different landscape elements and land use

types in all sites. Since no prior categorization

was available, we performed the classification

based on direct visual assessment of the satel-

lite imagery (Hook et al., 2022). identifying

distinct land cover types according to their

composition and configuration. Specifically,

we categorized areas based on forest density,

the extent of pasturelands, and the presence

of plantations, which were distinguishable in

the images. When possible, we validated the

classification through on-site verification. In

addition, we measured the distances between

forest fragments that could serve as potential

suitable habitats for most mammals, which we

defined in this study as forest remnants larger

than 500 ha . This threshold was established

based on internal research criteria, consider-

ing the need for sufficiently large areas to

support viable populations of terrestrial mam-

mals. While specific references using this exact

threshold were not identified, previous studies

have highlighted the importance of fragment

size in biodiversity conservation. For instance,

Hending et al. (2023) demonstrated that for-

est fragmentation and associated edge effects

reduce tree species diversity and structural

diversity in Madagascar’s transitional forests.

Similarly, Ries et al. (2004) discussed how a

decrease in fragment size results in an increased

edge-to-core ratio, which can be disadvanta-

geous to habitat specialist species. Furthermore,

we assessed the distances between structural

landscape elements, such as live fences and

small forest patches, which can influence con-

nectivity between these fragments, either facili-

tating or limiting species movement.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64706, mayo 2025 (Publicado May. 15, 2025)

Camera-traps: We monitored medium (<

10 kg) and large terrestrial mammals (> 10 kg)

in the study area with the use of camera traps

(Bushnell Trophy Cam HD). This method is

based on identification of animal species using

photographs and videos taken by automatic

cameras. A total of 45 permanent cameras

remained active for a period of 6 months in

2013–2014. The number of camera-trapping

days is defined as the 24-hour period that a

camera operated from the moment the camera

was mounted until it was removed, or when the

last picture was taken. Each activation captured

a sequence of three consecutive photos fol-

lowed by a 10-second video, with a 30-second

interval between detections. Sampling points

were visited periodically to collect the recorded

data and change the cameras’ location within

the same site. This approach can maximize

detection of species whose home ranges are less

than 1 km2.

Cameras were strategically placed 50 cm

above the ground on sites with evidence of

animal presence (footprints, marks, or past

sightings), close to trails, rivers, or streams.

All cameras were geo-referenced with a por-

table GPS and placed under a forest canopy

(protected from direct sunlight since they are

activated by exposure to intense heat). Stations

were baited with a mammal attractant (Calvin

Klein Obsession®) on a cloth-impregnated shel-

tered stake, following a standardized protocol

to ensure consistency in scent dispersion and

avoid biases in detection differences between

stations. This method has been previously used

in similar studies to attract a variety of mammal

species in tropical habitats (Wildlife Conserva-

tion Society, 2013; Holinda et al., 2020; Wildlife

Conservation Society, 2010). Since people occa-

sionally walked through the sites, we placed

a warning sign explaining the purpose of the

ongoing Project.

We identified all recorded animals to a

species level, noting the time and date of the

record. All species of more than 1 kg were con-

sidered, and taxonomic nomenclature follows

Wilson and Reeder (2005) and Rodríguez-Her-

rera et al. (2014). We did not include species of

rodents in the families Muridae and Cricetidae,

nor the order Chiroptera, which were diffi-

cult to identify with this method. In addition,

we used a comprehensive long-term database

developed by the Panthera and TEAM (TEAM

Network, 2011) and other monitoring projects

in the area as a sound reference of the presence

and absence of mammal species.

Data Analysis: We developed a detection

history (1 = detected; 0 = undetected) for the

total time the cameras were active at each site.

For this study, a “detection” was defined as the

occurrence of a species within the camera’s field

of view, regardless of whether it was the same

individual observed at different times. There-

fore, repeated detections of the same species

during different periods or frames were treated

as separate events. This definition is important

for the application of the occurrence models

and the subsequent species richness estimation.

We then ran a Cluster Analysis using PAST v

1.0.0.0, applying hierarchical clustering with

complete linkage, using the detection history to

determine Euclidian’s distance for grouping the

sites according to their similarity.

The overall species richness of medium and

large terrestrial mammals was estimated using

both rarefaction analysis and capture-recapture

models for closed populations, implemented in

R v3.3.2 (R Development Core Team, 2016) for

species detection records (Boulinier et al., 1998;

Chao et al., 2014). In these models, a species

was considered detected at a site if recorded at

least once during the entire sampling period,

regardless of repeated detections of the same

or different individuals. This estimation meth-

od accounts for imperfect species detection,

assuming that observed species richness under-

estimates the true richness in the area. Since the

rarefaction curves were generated using cap-

ture-recapture models that incorporate detec-

tion probability and associated uncertainty, the

resulting estimates directly reflect the expected

species richness (Chao et al., 2014; Colwell et

al., 2012; Hwang et al., 2002)

To assess the influence of landscape vari-

ables on species richness (forest cover, land use

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64706, mayo 2025 (Publicado May. 15, 2025)

types such as pastures, pineapple plantations,

and distance to the nearest forest fragment), we

explored multiple occurrence models, combin-

ing the mentioned landscape variables. We used

the Akaike’s Information Criterion (AIC) to

maximize log-likelihood for the best approxi-

mating model and the true generating mecha-

nism, where the best model would be the one

with the lowest value of AIC (Anderson, 2008).

To determine which variable best-explained

species richness, we adjusted Repeated Count

Data Analysis (Royle, 2004), taking into

account detection probability for each species

at each site. Using the ranked models and the

determined variables, we constructed a species

richness interpolation map. We used R v 3.3.2

(R Development Core Team, 2016) package

ggplot 2 v. 0.8.9 (Wickham, 2016) to generate

the graphs.

RESULTS

We obtained 1 653 records of mammals

(5 984 days/camera), representing 22 terrestrial

native mammal species. This makes 86 % of

the species reported for the area in the last 60

years (Appendix 3). Of the recorded mammals,

16 were medium-sized and six large-sized spe-

cies distributed in nine orders and 16 families

(Appendix 3); placing the order Carnivora as

the most diverse group with 10 species. We

highlight that nine of the 22 species detected are

Table 1

Medium and large-sized species of mammals recorded in thirty different sites. Camera trap detections in Sarapiquí, Costa

Rica, 2013-2014.

Order Family Species Number of sites

detected

Number of detections

in different sites

A B C

Didelphimorphia Didelphidae Didelphis marsupialis 16 70 6 4

Didelphimorphia Didelphidae Philander melanurus 19 55 34 35

Pilosa Myrmecophagidae Tamandua mexicana 19 31 8 10

Cingulata Dasypodidae Dasypus novemcinctus 29 232 112 135

Rodentia Erethizontidae Coendou mexicanus 1 1 0 0

Rodentia Dasyproctidae Dasyprocta punctata 16 202 16 0

Rodentia Cuniculidae Cuniculus paca 8 31 1 0

Lagomorpha Leporidae Sylvilagus gabbii 3 3 0 0

Carnivora Canidae Canis latrans 5 9 1 3

Carnivora Felidae Leopardus pardalis 21 24 8 7

Carnivora Felidae Leopardus tigrinus 1 1 0 0

Carnivora Felidae Leopardus wiedii 5 7 0 0

Carnivora Felidae Herpailurus yagouaroundi 5 3 1 1

Carnivora Procyonidae Nasua narica 20 80 12 33

Carnivora Procyonidae Procyon lotor 13 13 25 32

Carnivora Mustelidae Eira barbara 15 30 8 8

Carnivora Mustelidae Galictis vittata 1 1 0 0

Carnivora Mephitidae Conepatus semistriatus 1 2 0 0

Perissodactyla Tapiridae Tapirus bairdii 4 14 0 0

Artiodactyla Tayassuidae Dicotyles tajacu 12 42 3 3

Artiodactyla Cervidae Mazama temama 4 15 1 0

Artiodactyla Cervidae Odocoileus virginianus 3 6 0 0

A. Forest fragments (18 Fragments) in high forest cover and in close proximity to extensive protected forests. / B. Forest

fragments (6 Fragments) surrounded by pastures and far from extensive protected forests. / C. Forest fragments (6

Fragments) immersed in pineapple plantations.

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officially listed as threatened and have reduced

populations in Costa Rica (Sistema Nacional

de Áreas de Conservación (SINAC), Ministerio

de Ambiente y Energía (MINAE), 2007). The

names of the updated species are (Ramírez-

Fernández et al., 2023): Baird’s Tapir, Ocelots

(Leopardus pardalis), Margays (Leopardus wie-

dii), Oncillas (Leopardus tigrinus) and Jag-

uarundis (Herpailurus yagouaroundi), Spotted

Pacas (Cuniculus paca), Central American

Red Brockets (Mazama temama), Collared

Peccary (Dicotyles tajacu) and Lesser Grison

(Galictis vittata).

The most common species in the area

were Nine-banded Armadillo (Dasypus novem-

cinctus), White-nosed Coati (Nasua narica),

Northern Tamandua (Tamandua mexicana),

Grey Four-eyed Opossum (Philander melan-

urus) and Ocelots. In contrast, rare species

such as Striped Hog-nosed Skunk (Conepatus

semiestriatus), Oncillas, Mexican Hary Dwarf

Porcupine (Coendou mexicanus) and Lesser

Grison were detected at one site; some recorded

only once (Table 1).

The cluster analysis grouped sites based on

species composition, indicating that fragments

surrounded by forest and near large protected

areas shared more similar species assemblages.

In contrast, fragments embedded in pastures

or pineapple plantations formed distinct clus-

ters, suggesting an influence of land-use type

on species composition (Fig. 1). In addition,

the number of species increases faster in frag-

ments surrounded by forest and in proxim-

ity to protected areas as compared with those

embedded in land with pastures and pineapple

plantations (Fig. 2).

The best model that estimated 22 species as

the overall richness in the area was Mh Darroch

as shown in Table 2 (Darroch et al., 1993). Two

Fig. 1. Site Cluster Analysis of mammal species using Euclidian’s index in relation to the land use cover and distance to

the nearest extensive protected forest. Sites with –indicate more than 75% of forest, sites with– indicate more than 30% of

pineapple, and sites with * indicate more than 30% pastures. The clusters are labeled as A. Forest fragments in high forest

cover and in close proximity to extensive protected forests, B. Forest fragments surrounded by pastures and far from extensive

protected forests, and C. Forest fragments immersed in pineapple plantations.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64706, mayo 2025 (Publicado May. 15, 2025)

different model types adequately describe the

dynamics of these species, including one with

an environmental covariate, assuming forest

cover as the determinant variable for species

richness and considering detectability within

this land cover (Table 3).

Our results show that the species richness

of mammals varied according to landscape

characteristics, where pineapple-dominated

areas had the fewest species; and many of the

sites with large forest cover had the largest

number of species (Fig. 3).

DISCUSSION

The amount of forest cover best explains

the species richness and detectability in this

area. Despite the level of habitat loss and frag-

mentation, most remnants of natural forests

surveyed in this study represent potential

habitats for many mammal species. Although

distance from protected areas was not a deter-

minant variable, mammal richness was greater

in sites with large forest cover compared to

fragments surrounded by less forest cover. For

example, EcoVida (EV1) was the forest that

provided a greater detection of medium and

large land mammals with 16 species, despite

being further away from the largest protected

forest: Braulio Carrillo National Park (BCNP).

This is probably because this site is connected

with other relatively large forest fragments,

supporting the idea that large forest areas sup-

port more species (Chiarello, 2000; Da Silva &

Fig. 2. Species rarefaction curves of the sites in clusters A. Forest fragments (18 Fragments) in high forest cover and in close

proximity to extensive protected forests, B. Forest fragments (6 Fragments) surrounded by pastures and far from extensive

protected forests, and C. Forest fragments (6 Fragments) immersed in pineapple plantations. Camera trap detections in

Sarapiquí, Costa Rica, 2013-2014.

Table 2

Capture and recapture models for closed populations to estimate overall species richness of medium and large terrestrial

mammals in the area of Sarapiquí, Costa Rica, 2013-2014.

Model Richness Standard deviation deviance AIC

Observed Estimate

Mh Darroch 22.0 22.3 0.6 34.144 72.347

Mh Chao (LB) 22.0 26.3 6.6 24.988 73.191

Mh Gamma3.5 22.0 80.7 37.7 48.810 87.013

Mh Poisson2 22.0 22.0 0.0 208.458 246.661

M0 22.0 22.0 0.0 230.984 267.187

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Mendes-Pontes, 2008; Fahrig, 2003; Gurd et al.,

2001; Michalski & Peres, 2007).

Mammal species composition in forest

sites, such as the ones surveyed in this study,

indicates that this type of heterogeneous land-

scape offers a variety of resources, favoring

the dispersal of animals between fragments

of forests. For instance, on the southern side

of BCNP, we found that the closest site (MG)

had high species detection, including several

detections of Baird’s Tapir. Moreover, although

a number of other sites close to BCNP had low

species detection (e.g., ZB, SF, FO, and TV),

many of the forests in this area are not discrete

patches, but forest remnants bigger than XX ha

that can provide greater habitat amount and

connectivity between different environments.

Habitat heterogeneity with highly permeable

matrices (greater proportion of trees, crops

and secondary forests) allow animal move-

ments through the landscape, maintaining eco-

logical dynamic processes that are essential for

the persistence of mammal populations and

diversity and thus are of great conservation

importance (Asensio et al., 2009; Fahrig, 2013;

Fahrig et al., 2011).

Table 3

Model selection for covariates affecting species richness in different types of landscapes in Sarapiquí, Heredia, Costa Rica,

2013-2014.

Model AIC delta AIC AIC wgt K R2

λ (Forest), r (Forest) 1766.58 0 0.480 4 0.160

λ (.), r (.) 1767.76 1.19 0.260 2 0.000

λ (.), r (Pineapple) 1769.40 2.82 0.120 3 0.012

λ (.), r (Forest) 1769.76 3.18 0.097 3 0.000

λ (Pineapple), r (Pineaple) 1771.19 4.61 0.048 4 0.019

λ (Distance), r (.) 1802.17 35.59 0.000 4 1.900

Fig. 3 Species richness interpolation map (Kriging) with 95% confidence of interval on varying forest covers. Camera trap

detections in Sarapiquí, Costa Rica, 2013-2014.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64706, mayo 2025 (Publicado May. 15, 2025)

Major changes in landscape configuration

like large pineapple plantations can negatively

affect mammals, reducing species survival and

population viability (Banks et al., 2005; Bélisle

et al., 2001; Carroll et al., 2004; Trombulak &

Frissell, 2000). For example, structural contrast

between forest remnants and the matrix can be

abrupt, increasing the edge effect for many spe-

cies. In addition, the degree of forest loss and

fragmentation in areas with pineapple planta-

tions reduces connectivity between patches,

exacerbating the negative effects that limit ani-

mal movements. Nonetheless, this type of cover

maintains some forest remnants and riparian

forests that act as corridors, while maintaining

a certain degree of physical connectivity with

other forest fragments. It has been reported

that several species of mammals use this type

of remnants to move, maintaining the connec-

tivity of their populations and thus their sur-

vival in altered landscapes (Hermes-Calderón,

2008); this could be the case for Ocelots in our

study. However, Ocelots or other species with

relatively large habitat requirements have lim-

ited ability to move, since elongated fragments

like the ones found in our study area have a

greater perimeter relative to area, so the edge

effect would be further exacerbated.

Conservation value of forest remnants:

We estimated 86 % of the species of terres-

trial native, medium and large sized mammals,

reported for the area in the last six decades

(Appendix 3). Species such as Common Opos-

sum (Didelphis marsupialis) and Grey Four-

eyed Opossum were documented regularly and

in a variety of habitats. A similar case happened

with Northern Tamandua and Nine-banded

Armadillo (Wilson & Mittermeier, 2009). The

latter was the most common species in our

study. Although the Nine-banded Armadil-

lo’s habits are poorly understood, it is known

that it moves and uses different environments

including secondary forests and agricultural

fields (Cuarón, 2000; González-Zamora, 2011;

Navarrete & Ortega, 2011; Nuñez-Perez et

al., 2011; Wainwright & Arias-Sánchez, 2007;

Wilson & Mittermeier, 2009), suggesting its

tolerance towards habitat alteration (De Villa

Meza et al., 2002).

The presence of other species, such as Cen-

tral American Agouti (Dasyprocta punctata),

are commonly reported in various types of

land cover, and are presumed to be tolerant to

deforestation (Reid, 2009; Wainwright & Arias-

Sánchez, 2007; Wilson & Mittermeier, 2009).

Although they were quite common in sev-

eral sites, it was not detected at all in sites with

pineapple coverage. Likewise, Spotted Paca was

found mainly in sites with forest and pasture

cover. Unlike the previously mentioned spe-

cies, many carnivores require large-scale forest

mosaics to meet their daily metabolic needs

(Michalski & Peres, 2005). Such is the case of

the Ocelots, which occur in both continuous

and fragmented forests. However, this species

was only detected once in pineapple plantations

(Table 1), suggesting a transitory occurrence

throughout the area. Ocelots are abundant

opportunistic predators and relatively easy to

study compared with the other wild cats (De

Villa Meza et al., 2002; Di Bitetti et al., 2006;

Wilson & Mittermeier, 2009). A similar find-

ing was obtained for other small cats such as

the Oncillas, Margays and Jaguarundis, whose

detection was low, but they were still present in

small fragments.

There is evidence that not all species are

negatively affected or declining due to habi-

tat fragmentation (Davies et al., 2000). For

instance, Canis latrans was commonly detected

in highly fragmented sites and pineapple plan-

tations, occupying a variety of habitats such

as open areas and forest edges (Bekoff, 1977;

Wilson & Mittermeier, 2009). This flexible

behavior allows them to venture into human-

altered landscapes, invading otherwise unsuit-

able habitats (Cove et al., 2012). Other species

like the Northern raccoon (Procyon lotor),

White-nosed Coati and Tayras (Eira Barbara

showed high tolerance to forest alterations.

These mammals are generalist species that

move across large areas of non-forest habitats

and may use resources from habitat edges and

the landscape matrices (Cassano et al., 2012;

Cuarón, 2000; González-Zamora, 2011; Lessa

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64706, mayo 2025 (Publicado May. 15, 2025)

et al., 2012; Lyra-Jorge et al., 2008; Massara et

al., 2016; Mendes-Pontes et al., 2016; Wilson

& Mittermeier, 2009) . Although we had few

records of Lesser Grison and Striped Hog-

nosed Skunks these species are reported to be

able to traverse open areas and even use hostile

matrices of actively managed grasslands and

cultivated areas (Kasper et al., 2009; Michalski

& Peres, 2007; Wilson & Mittermeier, 2009).

The Collared Peccary was mostly recorded

in sites with high forest cover, and some in

forest among pasture areas. However, both

individuals and groups of Collared Peccaries

were also detected in pineapple plantations,

contrary to other studies (e.g. Cove et al., 2012;

De la Cruz, 2012). This species uses resources

in open areas (Keuroghlian & Eaton, 2008;

Tejeda-Cruz et al., 2009), and it has been

associated with levels of forest fragmentation

(Garmendia et al., 2013; Wilson & Mittermeier,

2009). It seems that Collared Peccaries could

benefit by a moderate degree of forest loss and

fragmentation in the landscape (Tejeda-Cruz et

al., 2009; Thornton et al., 2011; Urquiza-Haas

et al., 2009). In contrast, White-tailed Deer

(Odocoileus virginianus) and Central American

Red Brocket (Mazama americana) were only

recorded in sites with high forest cover; how-

ever, both species have been reported to ben-

efit from open areas (Garmendia et al., 2013;

Keuroghlian & Eaton, 2008; Tejeda-Cruz et

al., 2009; Wilson & Mittermeier, 2009). Finally,

Baird’s Tapir was only recorded in sites with

high forest cover and close to water bodies; a

habitat known to be preferred by the species

(Bodmer et al., 1997; Wilson & Mittermeier,

2009). In addition, tapirs are usually sensitive to

habitat loss and human disturbance (Cove et al.,

2014; Garmendia et al., 2013), although at Selva

Verde (SV) site, some individuals were detected

not far from the lodge and main road.

We were unable to obtain records of some

species expected in the region, such as the

jaguar and puma, even in the sites closest to

BCNP. However, both jaguar and pumas have

been seen by locals in the study area (Mat-

tey, personal communication 2015). Although

these mammals tend to prefer trails where

cameras were located (Arroyo-Arce et al., 2014;

Chávez, 2010; Conde et al., 2010; Kelly, 2008;

Silver et al., 2004; Trolle & Kéry, 2005), the

lack of detections might have been the result

of our sampling design and the relatively short

period of time of the study. Another spe-

cies not detected in our study area was the

Northern Naked Tailed Armadillo (Cabassous

centralis) which resides mostly underground

(Wilson & Mittermeier, 2009), so it is a rare

species in camera trap studies. Similarly, the

Neotropical River otter (Lontra longicaudis)

prefers aquatic environments, and the Mexican

Hary Dwarf Porcupine is an arboreal mammal

(Wilson & Mittermeier, 2009), so they may

also go undetected by cameras. In contrast, the

Giant Anteater (Myrmecophaga tridactyla) is

believed to have been extirpated from the area

(Wainwright & Arias-Sánchez, 2007), while the

White-lipped peccary (Tayassu pecari), popula-

tion now occurs mostly in Corcovado National

Park (Carrillo et al., 2002). Although detec-

tion was reduced for other species like Central

American Red Brocket and Forest rabbit (Syl-

vilagus gabbii), they are not extirpated from the

area as some suggest (Cove et al., 2012). Their

low incidence may be due to differences in

habitat preferences or low population densitiesv

(Wilson & Mittermeier, 2009), It is important to

note that the lack of records of a given species

during our study does not mean that it is absent

or extinct. Indeed, the presence of domestic

dogs and the robbery of four cameras sug-

gest poaching pressure. It is likely that human

pressure is causing the reduction of some spe-

cies of mammals (e.g. Spotted Pacas, Central

American Agouti, Collared Peccary and Cen-

tral American Red Brocket), affecting forest

ecosystems processes and interactions within

mammal communities (Arias Le Claire, 2000;

Asquith et al., 1997; Bodmeret al., 1997; Forget

& Milleron, 1991; Guariguata et al., 2000). The

fact that most of the species detected in sites

near pineapple plantations are listed under the

least concern category (Appendix 3), suggests

that the persistence of generalist species such

as raccoons, coatis and Grey Four-eyed opos-

sums, are least affected by land modifications

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64706, mayo 2025 (Publicado May. 15, 2025)

(Parry et al., 2007; Tejeda-Cruz et al., 2009).

The absence of Central American Agouti in this

area is of great concern, since this species’ home

range is around 2 ha and they are territorial and

locally common (Wainwright & Arias-Sánchez,

2007). It is possible that habitat alteration and

poaching are heavily impacting this species.

The results of this study draw attention

to the biological importance and conserva-

tion value of forest fragments, as many mam-

mal species persist in fragmented landscapes

(Bruna et al., 2010; Lyra-Jorge et al., 2008).

Species-specific responses to habitat loss and

fragmentation are related to interspecific differ-

ences in the perception of landscape structure

and the scale of habitat alteration (Lima & Zoll-

ner, 1996; Lord & Norton, 1990; Vos et al., 2001;

Zollner & Lima, 1997). For example, larger

species with extensive home ranges are able to

perceive landscapes as more homogenous than

smaller and less vagile species (Elmhagen &

Angerbjörn, 2001; Gehring & Swihart, 2003;

Lyra-Jorge et al., 2008). In addition, some

animals may even adapt to modifications to

their original habitats (McDougall et al., 2006;

Morán-López et al., 2006; Tabeni & Ojeda,

2005). Our results suggest that many large and

medium sized mammals in fragmented land-

scapes explore the region as a whole, and are

not necessarily restricted to the native vegeta-

tion patches (Donadio et al., 2001; Franklin et

al., 1999; Lyra-Jorge et al., 2008), such as Coy-

otes and Tayras that adapt to human-modified

landscapes (Lyra-Jorge et al., 2008).

In conclusion, it is necessary to preserve

large as well as small forest fragments, includ-

ing riparian forests that serve as corridors

between otherwise isolated forest fragments.

Also, scattered trees and living fences within

the landscape enhance quality and increase

the permeability of the matrix (Umetsu & Par-

dini, 2007). Finally, the conservation of private

nature reserves can increase landscape con-

nectivity and habitat availability, thus favoring

inter-patch movements. Both forest cover and

matrix quality are key in determining the com-

plex ecological dynamics for the maintenance

of mammal species diversity in agricultural

landscapes (Fahrig, 2013; Kupfer et al., 2006).

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