668 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 668-687, e48444, enero-diciembre 2022 (Publicado Set. 27, 2022)

Patterns of vertebrate biodiversity in a tropical dry

and mangrove forest matrix

Adam Yaney-Keller1*; https://orcid.org/0000-0003-1538-664X

Pilar Santidrián Tomillo2,3; https://orcid.org/0000-0002-6895-7218

Mark A. Jordan4; https://orcid.org/0000-0003-0106-5781

Javier Francisco Lopez Navas3; https://orcid.org/0000-0001-6684-4538

Frank V. Paladino3,4; https://orcid.org/0000-0002-6452-0086

1. School of Biological Sciences, Monash University, Clayton, VIC, 3800, Australia; adam.yaney-keller@monash.edu

(*Correspondence)

2. Animal Demography and Ecology Unit, GEDA, Institut Mediterrani d’Estudis Avançats (CSIC-UIB), Miquèl Marques

21, 01790, Esporles, Spain; bibi@leatherback.org

3. The Leatherback Trust, Goldring-Gund Marine Biology Station, Playa Grande, Guanacaste, Costa Rica; javier@

leatherback.org; paladino@pfw.edu

4. Purdue University Fort Wayne, 2101 E. Coliseum Boulevard, Fort Wayne, Indiana, USA, 4680; jordanma@pfw.edu

Received 10-X-2021. Corrected 23-VI-2022. Accepted 20-IX-2022.

ABSTRACT

Introduction: Tropical dry forests and mangroves, two of the world’s most endangered ecosystems, each host a

different set of environmental conditions which may support unique assemblages of species. However, few stud-

ies have looked at the unique vertebrate biodiversity in regions where both habitats occur side-by-side.

Objective: To assess the vertebrate diversity and patterns of habitat usage in a mangrove and tropical dry forest

matrix in an unprotected region of Northwestern Costa Rica.

Methods: The study was conducted in a 7 km2 matrix of mangrove and tropical dry forests between Cabuyal

and Zapotillal bays in Northwestern Costa Rica, south of Santa Rosa National Park. From September 2017 to

March 2018, we used 13 automatic camera traps over 1 498 trap days to capture species utilizing the region and

assess their patterns of habitat usage both spatially and temporally.

Results: Seventy vertebrate species from 42 families in 27 orders were detected, including several globally

threatened species. Over half of all species were detected in only one habitat, particularly amongst avian (78 %)

and mammalian (42 %) species. Tropical dry forests hosted the greatest number of unique species and supported

a greater percentage of herbivores than mangrove or edge habitats, which were dominated by carnivorous and

omnivorous species. Mean detections per camera trap of all species increased significantly from the coldest and

wettest month (Oct) to the hottest and driest months (Jan & Feb) in tropical dry forests. Sample-based rarefaction

analysis revealed that survey length was sufficient to sample the tropical dry forest and edge habitats, though

mangroves require further sampling.

Conclusions: Taxa found to utilize different forest types may utilize each for different stages of their life cycle,

moving between areas as environmental conditions change throughout the year. General patterns of global bio-

diversity favoring carnivore and omnivore usage of mangrove forests was confirmed in our study.

Key words: camera traps; Costa Rica; endangered ecosystems; species richness; Guanacaste.

https://doi.org/10.15517/rev.biol.trop.2022.48444

TERRESTRIAL ECOLOGY

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INTRODUCTION

The North Pacific coast of Costa Rica

contains side-by-side two of the world’s most

endangered forest types; tropical dry forests

and mangrove estuaries (Cortés, 2014; Duke

et al., 2007; Janzen, 1988; Miles et al., 2006).

Outside of the protected areas of Santa Rosa

National Park (SRNP) (10° 50’ 35.2” N - 85°

42’ 13.0” W) and the Horizontes Experimental

Forestry Station (10° 42’ 56.2” N - 85° 34’ 0.7”

W), tracts of tropical dry forest in this region

are fragmented into small and isolated pockets,

often converted to land for cattle haciendas

or hotel development (Janzen, 1988; Jimé-

nez, 2004). Mangrove estuaries are afforded

protection against impacts and removal via

Costa Rica’s National Wetland Policy, how-

ever these habitats and their surrounding areas

remain at risk of degradation as human coastal

populations grow (Jiménez, 2004; Slobodian &

Badoz, 2019). In the North Pacific, as unpro-

tected tropical dry forest is removed around

mangrove estuaries, remaining forests of both

types become increasingly isolated. Patches

of intact forest may become ‘islands’ of biodi-

versity in which a surprisingly high number of

species may still persist, but may be exposed

to an increasing host of issues. This includes

decreased gene flow, edge effects, and low

population sizes, all of which can contribute

to the eventual decline of species richness and

ecosystem health (Andren, 1994; Saunders et

al., 1991; Turner & Corlett, 1996).

Globally, survey efforts for mangrove for-

est fauna are amongst the poorest for any

habitat, despite their potential to act as popu-

lation refuges in areas of high anthropogenic

disturbance and their importance to a variety of

charistmatic megafauna globally (Barlow et al.,

2011; Nagelkerken et al., 2008; Nowak, 2013;

Rog et al., 2017; Thompson & Rog, 2019).

Central America has one of the highest alpha-

diversities of terrestrial vertebrates utilizing

mangroves of any region globally (Rog et al.,

2017), however few if any studies have exam-

ined the terrestrial vertebrate communities of

Northern Pacific Costa Rican mangroves or

tropical dry forests oustide of protected areas

such as SNRP (Bonoff & Janzen, 1980; Esco-

bar-Lasso et al., 2017; Montalvo et al., 2015;

Montalvo et al., 2020).

Even fewer studies exist on the composi-

tion of vertebrate communities within the tropi-

cal dry forest and mangrove estuary habitat

matrix, and how they may utilize both habitats

over time, despite their established conserva-

tion value and unique characteristics (Jiménez,

2004; Luther & Greenberg, 2009; Nagelkerken

et al., 2008; Rog et al., 2017; Zamora-Trejos

& Cortés, 2009). Both mangrove estuaries and

tropical dry forests are dynamic environments,

changing seasonally (e.g. wet and dry sea-

sons) and in the case of mangroves, daily (e.g.

tidal fluctuations), and may contain unique

assemblages of vertebrate fauna adapted to

such challenging environments (Jiménez, 2004;

Zamora-Trejos & Cortés, 2009).

To address this gap in our knowledge of

the vertebrate community of the tropical dry-

mangrove forest matrix, we deployed a non-

fixed duration camera trapping grid within and

between these habitats in a remote, unprotected

area of North Pacific Costa Rica. We aimed to

sample across habitat types during the late wet

to early dry seasons in order to determine how

species detections may change spatially and

temporally in this environment. Our goal was to

create a species inventory for this unprotected

area which may be valuable for conservation

management as well as improve our under-

standing of how vertebrate species may persist

in this unique and threatened ecosystem.

MATERIALS AND METHODS

Study Site: The Cabuyal estuary (10°

40’ 21.6” N - 85° 39’ 06.9” W) in the Nacas-

colo District of Guanacaste, Costa Rica is an

approximately 60 ha intertidal estuary system

characterized by mangrove swamp surround-

ed by tropical dry forest (Cordero-Umaña &

Santidrián-Tomillo, 2020; Córdoba-Muñoz et

al., 1998; Yaney-Keller et al., 2019). The area

receives approximately 1 400 mm of rainfall

per year, virtually all during the rainy season

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(May–November), and is fed by a seasonal

tributary of the Tempisque river (Córdoba-

Muñoz et al., 1998). A much smaller (approxi-

mately 1.75 ha), intertidal estuary known as

“Zapotillal” (10°39’29.3” N - 85°40’10.9”

W) sits approximately one km to the South of

Cabuyal, on the Northern Peninsula Papagayo.

The surrounding area is a mixture of tropical

dry forest and agricultural land with few roads

and paths. While the mangrove swamps remain

fairly undisturbed, areas of tropical dry forest

have experienced clearing and development in

the past.

Camera Stations: A total of 13 different

automatic camera trap stations were placed in

a non-random location matrix with no fixed

time limits on trap duration within and around

the estuaries and forests of Cabuyal and Zapo-

tillal between September 2017 and February

2018 (Fig. 1). Camera traps photograph wild

animals via the use of a passive infrared sensor

which detects movement and differential heat

signatures from a subject and its surrounding

environment (Mohd-Azlan et al., 2016; Swann

et al., 2004). Trap locations were chosen to

maximize species detections based on presence

of animal signs (e.g. tracks and scat), proxim-

ity to trails and water features and distance

from other camera traps (minimum distance =

0.04 km, maximum distance = 1.5 km, average

distance between traps = 0.5 km). Traps were

checked approximately every ten to fourteen

days. If a camera did not yield photo captures

within the first sampling period, it was removed

from its location, and placed in a more suitable

location. Cameras were also moved if the cam-

era was likely to be tampered with.

All cameras were initially set to take a

series of three photographs at the default trig-

ger rate of the camera, if cameras began yield-

ing large (> 1 000) sets of images in a single

Fig. 1. Map of camera trap locations (n = 22) by habitat type in the Cabuyal and Zapotillal estuaries. Contour lines represent

elevation. Map data from ESRI imagery.

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sampling period, they were switched to take a

single photograph. If sampling yielded a spe-

cies or behavior of interest, cameras were set

to capture video. Cameras were mounted on

trees, logs, or fence posts at approximately 30

cm height when possible and 1.5 to 3 m from

the desired area to be sampled, following rec-

ommendation from TEAM Network (2011).

Camera photos were downloaded and checked

in the field to reduce the amount of time cam-

eras remained out of operation.

Photograph Analysis: The number of

trap days per camera per location, defined

as 24-hour periods over which camera traps

remained in operation, was calculated from the

number of days cameras were in operation at

each location, subtracting days of malfunction.

Camera trap locations were put into one of

three habitat types in post-hoc analysis; edge,

mangrove forest, and tropical dry forest. These

categories were based on two metrics: 1) the

abundance and species of mangrove vegetation

around the trap location and 2) the presence

of natural standing water visible within 10 m

of the camera trap location. Mangrove species

tend to form fairly monotypic stands in gener-

ally well-defined geographic zones (Ellison

2002; Snedaker, 1982). In dry, coastal zones

similar to the Cabuyal and Zapotillal estuaries,

Avicennia germinans is found in higher eleva-

tion sites that are drier and hypersaline, while

species of the genus Rhizophora spp. tend to

occur at lower elevation, near water channels

and in less saline soil (Castañeda-Moya et al.,

2006; Delgado et al., 2001; Samper-Villarreal

et al., 2012). Based on Yaney-Keller et al.,

(2019), Laguncularia racemosa distribution

in Cabuyal and Zapotillal estuaries forms an

intermediate zonation remaining generally

more abundant near fresh-water inputs, similar

to other regional mangrove forests (Delgado

et al., 2001; Samper-Villarreal et al., 2012).

Mangrove forest locations were thus defined

as those with a dominant vegetation type of R.

racemosa and/or L. racemosa and located with-

in 10 m of standing water that remained for the

majority of the study duration. Edge locations

were classified as those containing a mixture

of either L. racemosa and/or A. germinans and/

or tropical dry forest vegetation and did not

meet the standing water criterion. Tropical dry

forest contained only typical tropical dry forest

vegetation and no mangroves. Mangroves were

identified based on Tomlinson (1986). Camera

trap days were totaled and averaged across

camera locations per habitat type. The number

of traps in each habitat type was proportional

to its relative area in the region, accessibility,

and amount of animal sign seen, and all habitat

types were sampled simultaneously.

Two full analyses of the photos and videos

taken were performed to identify positive fau-

nal detection events (n = 2 648). For the pur-

poses of this analysis, a three-photo sequence

or a single photo were considered single events,

as were individual videos regardless of length.

Each photo and video taken was examined to

determine whether it represented an animal

detection or not. Positive detection events were

defined by 1) a photo or video containing an

individual or group of animals of a single spe-

cies and 2) an individual of a species that does

not re-occur within a single 60-min period,

based on methodology following O’Brien et al.,

(2003), Yasuda (2004), and Meek et al., (2014).

Species were identified and categorized into

herbivore, carnivore, and omnivore foraging

guilds using Stiles and Skutch (1989), Leen-

ders (2001), and Reid (2009). Species richness

and the number of unique species was calcu-

lated for all habitat types.

A rarefaction analysis was used to com-

pare species detections and trapping effort in

the entire study and the different habitat types

sampled. In sample-based rarefaction analysis,

rarefaction curves are created from the means

of species accumulation curves, which are cre-

ated by randomized and repeated re-sampling

of detections from a species occurrence data-

set (Gotelli & Colwell, 2001). This allows the

expected number of species in a given sampled

area to be extrapolated over increased sampling

and time. As rarefaction curves reach an asymp-

tote, they assess the adequacy of sampling effort

in estimating complete diversity (Colwell et al.

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2004; Colwell & Coddington, 1994; Gotelli &

Colwell, 2001; Si et al., 2014). Sample-based

rarefaction curves for each habitat type and

mean species accumulation curve for total

observed species were calculated in EstimateS

and plotted against the total number of camera

trap days (Colwell, 2005). One thousand runs

were used for all randomizations, following

Tobler et al., (2008).

Statistical analysis was used to determine

the influence of month on species detections

within each vertebrate class and habitat type.

We used one-way repeated measure ANOVA’s

with trap location as a random effect and Tukey

HSD post hoc tests to compare camera trap

detections between months within the edge,

mangrove and tropical dry forest habitats. We

tested for normality using Shapiro-Wilks and

sphericity using Mauchly’s test of spheric-

ity (Mauchly, 1940). All statistical tests were

conducted with an α = 0.05 in R version 4.0.3

using base (R Core Team, 2020) and ‘rstatix’

(Kassambra, 2020) packages.

RESULTS

A total of twenty-two camera trap loca-

tions were set in the Cabuyal and Zapotillal

areas between September 2017 and March

2018. There was a mean number of 55 trap

days per trap location, with a total of 1 498 trap

days for the duration of the project. The lowest

number of trap days in one location was seven

days, while the one with the greatest number of

trap days was 153 days (Table 1).

Throughout the total survey, 27 orders,

42 families and 70 species of vertebrate fauna

were detected, not including domestic species

(n = 4). Tropical dry forest, followed closely

by edge, had the greatest total richness (Fig. 2).

TABLE 1

Total number of camera trap locations, mean number of trap days per location and total number of trap days per habitat

type in the Cabuyal and Zapotillal regions from September 2017 to March 2018

Habitat Type Total Trap Locations Mean Trap Days per Location Total Trap Days

Mangrove Forest 4 38.9 272

Tropical Dry Forest 8 62.7 557

Edge 10 59.9 669

Total 22 55.5 1 498

Fig. 2. Avian (n = 47), mammalian (n = 19), and herpetofaunal (n = 4) species richness of the Cabuyal & Zapotillal regions

by habitat type (edge, mangrove forest and tropical dry forest).

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Avian richness was greatest in tropical dry

forest, followed closely by mangroves, while

edge habitat led in mammalian richness. Her-

petofauna richness was equal, but very low,

amongst all three habitats (Fig. 2). In total 36

species were found to uniquely occur in one

of the sampled habitat types, over half of all

species detected (Table 2). Tropical dry forest

had the highest number of total avifauna and

herpetofauna species not found in either of the

other habitat types, while edge habitat had the

greatest number of unique mammalian species

(Table 2).

Between all vertebrate species, carnivores

made up the greatest percentage of species

detected in the edge (49 %) and mangrove

forest (56 %), while herbivores were the low-

est in all forest types (23 %) (Fig. 3). Amongst

avifauna, carnivores made up the majority

of edge (68 %) and mangrove (69 %) and a

large percentage of tropical dry forest (41

%) richness (Fig. 3). Omnivores made up the

majority of mammalian species detected in all

habitat types (Fig. 3). Among herpetofauna

species, carnivore, omnivore, and herbivores

were equivalently detected in edge and man-

grove forest, while only carnivores (67 %) and

herbivores (33 %) were detected in tropical dry

forest (Fig. 3).

Rarefaction analysis showed that differ-

ences in sampling effort likely accounted for

some of the differences in richness between

TABLE 2

Number of unique species not detected in other habitat types within vertebrate groupings (avian, mammalian and

herpetofaunal) detected by camera traps in the Cabuyal and Zapotillal regions between September 2017 and March 2018

Habitat Type Avian Species Mammalian Species Herpetofaunal Species Total Unique Species

Edge 4 6 0 10

Mangrove Forest 11 0 0 11

Tropical Dry Forest 13 2 1 16

Fig. 3. Percentage of (A) total (n = 70), (B) avian (n = 47), (C) mammalian (n = 19) and (D) herpetofaunal species (n = 4)

detected in carnivore, herbivore and omnivore foraging guilds within edge, mangrove forest and tropical dry forest habitat

types of the Cabuyal and Zapotillal regions.

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the habitat types (Fig. 4). Tropical dry forest

habitat rarefaction curves and 95 % confi-

dence intervals (CI) indicate that the sampling

effort of 669 trap days was likely sufficient to

account for the majority of species within this

habitat type (Fig. 4). Edge habitat sampling was

somewhat less sufficient than tropical dry forest

sampling, although the 95 % CI of relative spe-

cies richness overlapped between these habitats

and accounted for 90 percent of the species in

the area (Fig. 4). Mangrove habitat was the least

sampled type both in duration and number of

locations, and rarefaction analysis revealed that

sampling was likely inadequate to determine

species richness in this habitat type (Fig. 4).

Shapiro-Wilks tests revealed that no mean

detections per camera trap for any species

grouping (all, avian, mammal or herpetofauna)

met assumptions of normality. Means were

then square root, log, or log (x + 0.5) trans-

formed depending on whether they contained

zero or non-zero count data (Berry, 1978), after

which normality was met for all data sets (W >

0.90, P > 0.05). Data was automatically tested

for assumptions of sphericity via Mauchly’s test

with the anova_test function within the R pack-

age “rstatix”, and Greenhouse-Geisser correc-

tions were automatically applied to F-values via

the get_anova_table function when sphericity

was not met (Bathke et al., 2009; Kassambra,

2020). Mixed-effects one-way repeated mea-

sure ANOVA’s revealed statistically significant

differences in mean detections per camera trap

across months for all species within the edge (F

(5.23) = 2.76, p = 0.043) and tropical dry forest

(F (5.21) = 3.34, p = 0.022), but not mangrove

forest (F (5.8) = 3.63, p = 0.052) (Fig. 5A). For

all species, Tukey HSD post-hoc comparisons

indicated significant increases in detections

within the tropical dry forest between October

and January (p = 0.045) and October and Feb-

ruary (p = 0.024), but not between September,

November and December. (Fig. 5A). No sig-

nificant differences in avian species detections

between months could be ascertained in any

habitat type (Fig. 5B). Statistically significant

differences were found in mammalian species

detections between months within the edge (F

(5.19) = 5.00, p = 0.004) and tropical dry forest

(F (5.17) = 4.17, p = 0.012), but not mangrove

forest (F (5.5) = 2.47, p = 0.172) (Fig. 5C).

Tukey HSD post-hoc comparisons indicated

significant increases in edge mammalian detec-

tions between September and December (p =

0.031), September and January (p = 0.02), and

October and January (p = 0.031). Mamma-

lian detections significantly increased in tropi-

cal dry forests between October and January

Fig. 4. Sample-based rarefaction curves for edge, mangrove forest, and tropical dry forest habitats extrapolated to 1 500

samples. Solid lines represent the rarefaction richness estimate, while dashed lines indicate 95 % confidence intervals.

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(p = 0.047) and October and February (p =

0.008), but not between September, November

and December. (Fig. 5C). Statistically sig-

nificant differences in herpetofauna detections

were found between months within the edge

habitat (F (5.13) = 3.77, p = 0.025), but not

within tropical dry (F (5.7) = 2.69, p = 0.115)

or mangrove forests (F (5.3) = 0.92, p = 0.564).

Over 1 498 trap days, a total of 2 648

positive detection events were registered. The

species with the highest number of positive

detection events for the entire camera trap-

ping season and positive detection events per

day was Nyctanassa violacea (yellow-crowned

night heron) (Appendix 1). The species with

the largest group size photographed together in

Fig. 5. Average A. total, B. avian, and C. mammal species detections per camera trap within edge, mangrove forest, and

tropical dry forest habitats between September 2017 and February 2018 in the Cabuyal and Zapotillal regions. Error bars

represent standard error from the mean.

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a single positive detection event (the minimum

number of individuals potentially photographed

in the detection area) was Nasua narica (white-

nosed coati) (Appendix 1). Ten species protect-

ed under the Costa Rican environmental law,

Decreto Número 32 633-MINAE, Artículos

26 y 29 (2005), which protects species with

decreasing populations (article 26) and those

that are endangered (article 29), were detected

in the study, as well as four classified as “vul-

nerable” or “near threatened” under the Inter-

national Union for the Conservation of Nature’s

Red List (see Appendix 2 and Appendix 3 for

lists of species).

DISCUSSION

Tropical dry forests and associated man-

grove estuaries are considered more species

poor than other forest types in the tropics, so

when combined with the historical deforesta-

tion and fragmentation in the area, the overall

diversity of species found in this region was

surprising (Jiménez, 2004). The unique assem-

blages of species which occur within each habi-

tat type as well as the high overall biodiversity

between them highlights the importance of

the tropical dry forest–mangrove forest matrix

towards maintenance of biodiversity in the area.

While true absence of species from this site

cannot be fully determined, the total sampling

effort was relatively high for a camera trapping

study of a site this size (Kelly, 2008; Kelly

& Holub, 2008; Tobler et al., 2008, Trolle &

Kéry, 2003). While edge habitat was sampled at

more locations and over a longer overall period

of time, rarefaction analysis points to a lower

species richness in the edge than tropical dry

forest, though increased sampling effort would

likely yield increased detections (Fig. 4). At

the maximum number of camera trap days for

mangrove habitats, rarefaction curves indicated

trapping effort was likely not sufficient in this

habitat type to register all species present (Fig.

4). Increased sampling effort to at least 1 000

camera trap days per habitat type would likely

capture a large majority of the species present in

all habitat types in this region (Ahumada et al.,

2011; Carbone et al., 2001; Tobler et al., 2008).

Birds are the most diverse vertebrate species

class, which may also explain the relatively

high richness we found within and between

habitat types in this group, though increased

sampling may yield more detections (Fig. 1)

(Rahbek & Graves, 2021). Further, increasing

the number of trap locations and/or sampling

techniques would likely also increase species

detections, especially for species groupings

not easily detected by camera traps, such as

arboreal species and small mammals, birds and

herpetofauna (Rog et al., 2020). To this point,

two species listed as “vulnerable” by the IUCN

(Allouta palliata, mantled howler monkey and

Eupsittula canicularis, orange-fronted para-

keet) and one listed as “endangered” (Amazo-

na auropalliata, yellow-naped Amazon) were

frequently encountered in the Cabuyal and

Zapotillal region during our study in all three

habitats, but were not detected by camera traps,

illustrating the need for a diversity of sampling

types to determine species presence/absence in

this area (IUCN, 2020).

Seasonal Changes in Mean Detections:

The increase in mean detections from the end

of the wet to the beginning of the dry season in

tropical dry and edge habitats we observed may

be explained by increased movements of wild-

life in the area or individuals entering it from

other regions (Fig. 5). In tropical dry forests,

seasonal shifts in behavior have been observed

in several vertebrate groups (Asensio et al.,

2012 Fuller et al., 2020; García et al., 2010;

Herrera et al., 2018; MacKinnon, 2006; Maffei

et al., 2005; Mosdossy et al., 2015; Nuñez-Per-

ez & Miller, 2019; Valenzuela & MacDonald,

2002). These shifts may be especially pro-

nounced in areas with high temporal and spatial

scarcity in water and food resources, such as

the tropical dry forests of Northwestern Costa

Rica (Montalvo et al., 2015). These patterns are

thought to be tied to a variety of biological fac-

tors, including foraging guild, energetic needs

and capacity for group formation, and can vary

greatly between species (Johnson et al., 2002;

Reiss, 1988). However, underlying ecological

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mechanisms may also govern seasonal changes

in vertebrate movements and density within

and between these environments. Each year,

food and water availability decreases dramati-

cally in tropical dry forests with the onset of

the dry season, as water availability is reduced

to small pools of collected water and flowering

plants bloom and shed their leaves to time fruit

production with the later onset of rains (Stan &

Sanchez-Azofeifa, 2019). This in turn will have

bottom-up influences on individuals, popula-

tions and communities of vertebrate species in

this environment (Boyle et al., 2020; Castro et

al., 2018). Tropical storm Nate, which arrived

in the Cabuyal-Zapotillal region in early Octo-

ber 2017, brought over 400 mm of rain in 48

hours (approximately 20% of 2017’s annual

rainfall), and flooded much of the study area.

Although camera trapping continued during

this time and no equipment was damaged, it is

likely that the event influenced animal move-

ment patterns during and after. Long-term

studies of species responses to both acute

and persistent environmental changes in this

region will be increasingly important as climate

change is predicted to raise temperatures and

alter the frequency and intensity of tropical

storms and El Niño Southern Oscillation in

Northwestern Costa Rica (Nakicenovic et al.,

2000; Santidrián-Tomillo et al., 2012).

While no significant differences were

found in the detection rates of species between

months in mangroves in our study, mean detec-

tions per trap did increase from September

through December and January for all, avian

and mammalian species before decreasing

in February (Fig. 5). Minimum and average

monthly tide height followed this same pattern,

peaking in January and declining in February

(Appendix 4). Increasing tide heights during

this period may change the availability of prey

items, such as arthropods, fish and crustaceans,

which may become prevalent throughout these

months as higher tides bring these resources

into areas of the mangrove forests more acces-

sible to terrestrial species.

The Tropical Dry Forest – Mangrove

Forest Matrix: Over half of all species detect-

ed in our study were found to occur within

only one habitat type and all habitat types

were found to host unique assemblages of spe-

cies (Table 2). On the Pacific coast of Central

America, mangrove forests may play a special

role in harboring unique species, due to the

contrast of the wet mangrove forest with the

neighboring arid tropical dry forest (Luther

& Greenberg, 2009; Woodcock & Woodcock,

2007). Woodcock y Woodcock (2007) found

a greater diversity of bird species in North

Pacific Costa Rican mangroves than neighbor-

ing tropical dry forests and similar to this study,

different assemblages of species as well. This

is thought to be due to different prey commu-

nities found between the mangrove and other

habitat types (Lefebvre & Poulin, 1997; Luther

& Greenberg, 2009; Woodcock & Woodcock,

2007). Our results appear to support this, as

tropical dry forests supported a greater number

of herbivorous and omnivorous bird species

than neighboring edge and mangrove forests,

which were dominated by carnivorous species

(Fig. 3). While mangroves support a variety

of prey for piscivores and other wetland birds,

tropical dry forests host a greater variety of

flowering plants, providing fruit, nectar, and

insects for forest birds. On a regional scale,

differences in species communities can be seen

even between the same habitat types due to

differences in physical factors between sites

(e.g., rainfall, phenology, salinity) (Lefebvre &

Poulin, 1997). Rog et al., (2020) found similar

findings of unique terrestrial vertebrate assem-

blages within Australian mangrove forests. This

emphasizes the need for increased research on

faunal communities of all mangrove estuaries,

regardless of size or abiotic characteristics, as

well as the habitats around them to maintain

biodiversity in the region.

The high amount of mammalian richness

found in the edge habitat in our study could be

due to the preferential use of human-created

paths within these habitats or the transient use

of mangroves as foraging grounds, but not as

permanent residence (Luther & Greenberg,

678 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 668-687, e48444, enero-diciembre 2022 (Publicado Set. 27, 2022)

2009). In the Cabuyal-Zapotillal region, man-

groves are especially important considering

the limited availability of neighboring intact

forest, as mangroves may be refuges of habitat

and resources, especially during the seasonal

declines in neighboring dry forest productivity

(Jiménez, 2004). Global reviews on facultative

mammalian usage of wetlands suggest that

very few mammalian species are restricted to

mangroves for their entire life history (Hogarth,

2015; Luther & Greenberg, 2009; Rog et al.,

2017). To truly asses mammal communities

in mangroves, other survey techniques such

as nocturnal transects and live or hair traps

may be more optimal than camera traps (Rog

et al., 2020). However, camera traps appear to

have some utility across longer sampling peri-

ods in locations where they can be protected

from inundation and where exposed banks or

upland areas used for travel or foraging may

be present.

Our results conform to the general global

pattern reported by Rog et al., (2017) of high

proportions of carnivorous and omnivorous

terrestrial vertebrate usage of mangrove forests

(Fig. 3). Herbivores may not find these envi-

ronments ideal compared to neighboring tropi-

cal dry forests due to the high salt content of

mangrove leaves, though they may opportunis-

tically utilize these environments for nesting,

roosting, or refuge while foraging in adjacent

habitats (Kathiresan & Bingham, 2001; Luther

& Greenberg, 2009). The high proportion of

mammalian omnivores found between all habi-

tat types is likely reflective of the adaptive

nature of this foraging guild towards survival

in this climatically and ecologically diverse

region (Reid, 2009). It is important to note that

the Cabuyal-Zapotilall region has also experi-

enced significant deforestation and remaining

forests are surrounded by and interspersed with

small human habitations and pasture lands.

These environments are known to influence

community compositions, favoring generalist

over specialist species, a pattern reflected in the

relative abundance of species detected in our

study (Appendix 1) (Prist et al., 2012). Release

of meso-predator populations via decreases of

larger predator (ie. jaguars and pumas) popula-

tions in the region also explains the high pro-

portion of small carnivores and omnivores seen

in this area, though large predator populations

are rebounding in nearby SRNP (Crooks &

Soulé, 1999; Montalvo et al., 2015).

Conservation Implications: Our findings

highlight the need for further research into the

vertebrate community of this region. While

rich in biodiversity, the region is largely unpro-

tected and faces imminent threat from devel-

opment (Appendix 5). Though current legal

frameworks protect mangroves and bordering

habitats within a 150-meter buffer, surrounding

tropical dry forests that support a high level of

both unique and co-occurring biodiversity are

left outside of these current protections (Slo-

bodian & Badoz, 2019). Wide ranging species

which may utilize mangrove and edge habitats

during the wet and transitionary months most

certainly leave the protective boundaries of

these habitats in search of resources during the

dry season. The single jaguar detected in this

study was found to match a previously identi-

fied approximately three-year old female, last

seen in SRNP two years prior and known to

range within the park, indicating that wildlife

dispersal between the park and this region does

take place (Luis G. Fonseca, pers. comm.)

(Appendix 6). Further studies integrating tech-

niques from spatial ecology on vertebrates

in the region will be useful for exploring the

importance of the tropical dry forest-mangrove

forest matrix for species in the region.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

679

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ACKNOWLEDGMENTS

We would like to thank all the field assis-

tants and volunteers at Playa Cabuyal who

assisted in this study, with special thanks to

Keilor Enrique Cordero, Kelcy Tolliver, and

Verónica Valverde. We especially thank the

Guanacaste Conservation Area for providing

scientific permits and in particular Roger Blan-

co for facilitating the process.

RESUMEN

Patrones de biodiversidad de vertebrados en una

matriz de bosque seco tropical y manglar

Introducción: Los bosques secos tropicales y los mangla-

res, dos de los ecosistemas más amenazados del mundo,

albergan cada uno un grupo de condiciones ambientales

que pueden albergar conjuntos únicos de especies. Sin

embargo, pocos estudios han analizado la biodiversidad

única de vertebrados en regiones donde ambos hábitats se

encuentran uno al lado del otro.

Objetivo: Evaluar la diversidad de vertebrados y los patro-

nes de uso del hábitat en una matriz de manglar y bosque

seco tropical en una región no protegida del noroeste de

Costa Rica.

Métodos: El estudio se realizó en una matriz de 7 km2

de manglares y bosques secos tropicales en las bahías de

Cabuyal y Zapotillal en el noroeste de Costa Rica, al sur del

Parque Nacional Santa Rosa. De septiembre 2017 a marzo

2018, utilizamos 13 cámaras trampa automáticas durante

1 498 días trampa para capturar especies que utilizan la

región y evaluar sus patrones de uso espacial y temporal

del hábitat.

Resultados: Se detectaron 70 especies de vertebrados de

42 familias y 27 órdenes, incluidas varias especies amena-

zadas a nivel mundial. Más de la mitad de todas las espe-

cies se encontraron en un solo hábitat, particularmente aves

(78 %) y mamíferos (42 %). Los bosques secos tropicales

albergan el mayor número de especies únicas y sustentan

un mayor porcentaje de herbívoros que los hábitats de

borde de manglares, que estaban dominados u hospedados

por especies carnívoras y omnívoras. Las detecciones

promedio por cámara trampa de todas las especies aumen-

taron significativamente desde el mes más frío y húmedo

(octubre) hasta los meses más cálidos y secos (enero y

febrero) en los bosques secos tropicales. El análisis de

rarefacción basado en muestras reveló que la duración del

estudio fue suficiente para muestrear los hábitats de bosque

seco tropical y de borde, aunque los manglares requieren

más muestreo.

Conclusiones: Se encontró que los taxones pueden usar

varios tipos de bosque en las diferentes etapas de su ciclo

de vida, moviéndose entre áreas a medida que las condi-

ciones ambientales cambian a lo largo del año. En nuestro

estudio se confirmaron patrones generales de la biodiversi-

dad global que favorecen el uso de los bosques de manglar

por parte de carnívoros y omnívoros.

Palabras clave: cámaras trampa; Costa Rica; ecosistemas

en peligro; riqueza de especies; Guanacaste.

APPENDIX 1

Minimum number of unique individuals (a single group photographed together) identified, total

number of positive detection events, and number of positive detections events per camera trapping

day for each species detected between September 2017 and March 2018 in the Cabuyal and Zapo-

tillal region

Species Name (by class) Common name

Minimum

Number of

Individuals

Total Number of

Positive Detection

Events

Positive Detection

Events per Day

Aves

Acitis macularius Spotted sandpiper 1 29 0.019

Amazilia sp. Hummingbird 1 1 0.001

Aramides axillaris Rufous-necked wood rail 1 1 0.001

Aramus guarauna Limpkin 1 3 0.002

Ardea alba Great egret 3 43 0.034

Ardea herodias Great blue heron 1 41 0.027

Buteo plagiatus Gray hawk 1 2 0.001

Buteogallus anthracinus subtilis Common black hawk 2 97 0.065

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Species Name (by class) Common name

Minimum

Number of

Individuals

Total Number of

Positive Detection

Events

Positive Detection

Events per Day

Butorides virescens Green heron 1 10 0.007

Calocitta formosa White-throated magpie jay 2 2 0.002

Campylorhynchus rufinucha Rufous-naped wren 1 1 0.001

Caracara cheriway Crested caracara 2 13 0.009

Cathartes aura Turkey vulture 4 2 0.003

Columbina inca Inca dove 4 127 0.119

Coragyps atratus Black vulture 4 13 0.011

Crax rubra Great currasow 2 23 0.017

Crotophaga sulcirostris Groove-billed ani 11 26 0.054

Crypturellus cinnamomeus Thicket tinamou 1 1 0.001

Dryocopus lineatus Lineated woodpecker 1 3 0.002

Egretta caerulea Little blue heron 1 14 0.009

Egretta thula Snowy egret 7 45 0.059

Egretta tricolor Tri-colored heron 3 8 0.007

Eudocimus albus White ibis 4 34 0.040

Eumomota superciliosa Turquoise-browed motmot 1 1 0.001

Himantopus mexicanus Black-necked stilt 6 61 0.078

Icterus galbula Baltimore oriole 1 1 0.001

Icterus pustulatus Streak-backed oriole 2 12 0.010

Leptotila plumbeiceps Gray-headed dove 2 30 0.021

Leptotila verrauzi White-tipped dove 2 24 0.017

Megascops cooperi Pacific screech owl 1 1 0.001

Melanerpes hoffmanni Hoffman’s woodpecker 1 5 0.003

Mycteria americana Wood stork 2 7 0.005

Myiozetetes similis Social flycatcher 1 2 0.001

Numenius phaeopus Whimbrel 2 2 0.002

Nyctanassa violacea Yellow-crowned night heron 2 307 0.208

Parkesia noveboracensis Northern waterthrush 1 8 0.005

Passerina ciris Painted bunting 1 3 0.002

Patagioenas flavirostris Red-billed pigeon 1 1 0.001

Penelope purpurascens Crested guan 1 1 0.001

Piaya cayana Squirrel cuckoo 1 10 0.007

Pitangus sulphuratus Great kiskadee 2 69 0.049

Platalea ajaja Roseate spoonbill 1 2 0.001

Plegadis falcinellus Glossy ibis 1 2 0.001

Tigrisoma mexicanum Bare-throated tiger heron 1 34 0.023

Tringa semipalmata Willet 1 1 0.001

Turdus grayi Clay-colored thrush 1 1 0.001

Tyrannus melancholicus Tropical kingbird 1 13 0.009

Zenaida asiatica White-winged dove 5 82 0.070

Mammalia

Cebus capucinus White-faced capucin 11 60 0.066

Conepatus semistriatus Striped hog-nosed skunk 1 5 0.003

Dasyprocta punctata Central American agouti 1 2 0.001

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Species Name (by class) Common name

Minimum

Number of

Individuals

Total Number of

Positive Detection

Events

Positive Detection

Events per Day

Didelphis marsupialis Common opossum 2 240 0.162

Eira barbara Tayra 2 1 0.001

Herpailurus yagouaroundi Jaguarundi 1 3 0.002

Leopardus pardalis Ocelot 1 15 0.010

Nasua narica White-nosed coati 13 24 0.046

Odocoilius virgianus Virginia opossum 2 8 0.006

Panthera onca Jaguar 1 1 0.001

Pecari tajacu Collared peccari 1 5 0.003

Procyon lotor Northern raccoon 5 177 0.147

Puma concolor Puma 1 5 0.003

Sciurus variegatoides Variegated squirrel 1 7 0.005

Spilogale angustifrons Southern spotted skunk 1 33 0.022

Sylvilagus floridanus Eastern cottontail 1 1 0.001

Tamandua mexicana Northern tamandua 1 1 0.001

Urocyon cineroargenteus Gray fox 2 119 0.083

Reptilia

Crocodylus acutus American crocodile 1 16 0.011

Ctenosaura similis Black ctenosaur 3 252 0.176

Iguana iguana Green igauna 1 8 0.005

Amphibia

Bufo marinus Cane toad 1 1 0.001

APPENDIX 2

Species detected in the Cabuyal region between September 2017 and March 2018 that are mentio-

ned in Article 26 or 29 of Decreto Numero 32633-MINAE, ‘Reglamento A Ley De Conservacion

De La Vida Silvestre’, 2005

Species Common Name, English Common Name, Spanish Article #

Crax rubra Great Curassow Pavón Grande 26

Penelope purpurascens Crested Guan Pava Crestada 26

Aramides axillaris Rufous-necked Wood Rail Rascón Cuellirrufo 26

Cebus capucinus White-faced Capuchin Monkey Mono Capucino 26

Crocodylus acutus American Crocodile Cocodrilo Americano 29

Leopardus pardalis Ocelot Ocelote 29

Puma concolor Puma Puma 29

Herpailurus yagouaroundi Jaguarundi León Breñero 29

Panthera onca Jaguar Jaguar 29

682 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 668-687, e48444, enero-diciembre 2022 (Publicado Set. 27, 2022)

APPENDIX 3

Four species detected in the Cabuyal region between September 2017 and March 2018 listed under

vulnerable or near threatened criterion by the IUCN Red-List (accessed 2018)

Species Common Name,

English Habitat Type Present IUCN Status Assessment

Crax rubra Great Curassow Edge, Mangrove Forest,

Tropical Dry Forest

Vulnerable (BirdLife Intl., 2016a)

Crocodylus acutus American Crocodile Edge, Mangrove Forest Vulnerable (Ponce-Campos et al., 2012)

Panthera onca Jaguar Tropical Dry Forest Near Threatened (Quigley et al., 2017)

Passerina ciris Painted Bunting Tropical Dry Forest Near Threatened (BirdLife Intl., 2016b)

APPENDIX 4

A. Average temperature (C°), B. rainfall accumulated (mm), C, minimum monthly tide height (cm)

and D. average daily tide height (cm) between September 2017 and February 2018 in the Cabuyal

region. Air temperature and precipitation data came from the Daniel Oduber International Airport

in Liberia (~50 km from site). Data were obtained from the National Meteorological Institute of

Costa Rica (IMN)

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APPENDIX 5

Camera trap images taken in the same exact location of an a) Leopardus pardalis, Ocelot in Nov-

ember 2017 and b) heavy construction equipment and road clearing activities in February 2018,

indicating the speed of development in the Cabuyal-Zapotillal region

APPENDIX 6

Camera trap images of A. Panthera onca, Jaguar, B. Puma concolor, Puma, C. Crax rubra, Great

Curassow, D. Procyon lotor, Northern raccoon eating a mangrove crab, E. Avian assemblage in

Cabuyal mangrove forest, and F. Crocodylus acutus, American crocodile.

684 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 668-687, e48444, enero-diciembre 2022 (Publicado Set. 27, 2022)

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