Universidad de Costa Rica - Sede de Occidente

Revista Pensamiento Actual - Vol 19 - No. 33 2019

ISSN Impreso: 1409-0112 ISSN Electrónico 2215-3586

Ciencias Naturales

Período Diciembre 2019 - Mayo 2020

190.

- 204.

DOI 10.15517/pa.v19I33.39637

Brayan H. Morera-Chacón - Víctor J. Acosta-Chaves

190

Amphibians from the cloud forest of El Silencio de Los Ángeles, San Ramón de

Alajuela, Costa Rica

Anfibios del bosque nuboso de El Silencio de Los Ángeles, San Ramón de Alajuela, Costa Rica

Brayan H. Morera-Chacón¹

Víctor J. Acosta-Chaves²

Fecha de recepción: 4-1-2019

Fecha de aprobación: 14-10-2019

Abstract

We present the list of amphibians for the El Silencio de Los Ángeles Cloud Forest (Villa Blanca Hotel and Reserve) in San Ra-

món de Alajuela, Costa Rica, Central America. We performed nocturnal visual and acoustic surveys in the trail system, mainly

from 2013 to 2014. We also received data from the local guides up to 2019. We compared the similarity of amphibian richness

of our site against other premontane reserves in Costa Rica with a cluster analysis (Jaccard index, single linkage). We recorded

27 species distributed in 17 genera, nine families and three orders. Notrotiton gamezi was the only threatened species detected.

The El Silencio de los Ángeles Cloud Forest site is around 80 % similar to the San Lorencito River Station and 55% to Nectandra

Reserve. Containing 12% of the Costa Rica’s amphibian richness, this premontane woodland should be considered among the

most important clouded forest in Central Costa Rica for amphibian conservation.

Key Words: Biological inventory, Central American Herpetofauna, citizen science, herping, Neotropical region, Nototriton gamezi.

Resumen

Presentamos la lista de anfibios para el Bosque Nuboso de El Silencio de Los Ángeles (Hotel y Reserva Villa Blanca) en San Ramón

de Alajuela, Costa Rica, Centro América. Realizamos estudios nocturnos visuales y acústicos en el sistema de senderos, principal-

mente de 2013 a 2014. También recibimos datos de los guías locales hasta 2019. Comparamos la similitud de la riqueza de anfibios

de nuestro sitio contra otros sitios premontanos en Costa Rica con un Análisis Clúster (índice de Jaccard, enlace único). Regis-

tramos 27 especies distribuidas en 17 géneros, nueve familias y tres órdenes. Notrotiton gamezi fue la única especie amenazada

detectada. El sitio del Bosque Nuboso de El Silencio de los Ángeles presenta una similitud de alrededor del 80% a la Estación del

Río San Lorencito y 55% a la Reserva Nectandra. Con un 12% de la riqueza de anfibios de Costa Rica, este bosque premontano

debe considerarse entre los bosques nublados más importantes del centro de Costa Rica para la conservación de los anfibios.

Palabras Clave: ciencia ciudadana, inventario biológico, herpetofauna centroamericana, Nototriton gamezi, observación de

anfibios, región Neotropical.

Bachiller en Gestión de los Recursos Naturales, Sede de Occidente, Universidad de Costa Rica. Estudiante de Maestría en Conservación

y Manejo de Vida Silvestre, Universidad Nacional, Heredia, Costa Rica. Correo electrónico: morera.b91@gmail.com

Máster en Biología, Universidad de Costa Rica. Profesor en la carrera de Turismo Ecológico, Recinto de Paraíso, Sede Atlántico Universidad

de Costa Rica y el Centro de Programas Internacionales de Universidad Veritas. Miembro de la Red Mesoamericana y del Caribe para la

Conservación de Anfibios y Reptiles. Correo electrónico: victor.acosta@ucr.ac.cr / victor.acosta@veritas.cr

Ciencias Naturales

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I. Introduction

Additionally, we compared the richness for ESLA

Cloud Forest against other reserves located within the

Costa Rica contains nearly 215 species of amphibians

foothills of central Costa Rica in order to understand

in a relative small area (51100 km2) (Zumbado-Ulate et

the similarities and differences between compositions.

al., 2019). The diversity and distribution of amphibians

Based on similar elevation and life zones, we predicted

in Costa Rica is considered among the best known in

that ESLA Cloud Forest amphibian diversity will be

comparison with other Neotropical countries (Savage,

comparable to the richness of the Nectandra Reserve and

2002), but despite this, there is an absence of amphibian

San Lorencito River Station of AMBBR. In the future this

and reptile checklists from the Western region of Central

research will be useful to compare with other checklists

Valley in comparison with areas such as Sarapiquí,

to determine which species are currently colonizing and/

Monteverde, San Vito or Fila Costeña (Rovito et al., 2015).

or disappearing from the middle elevations in Costa Rica

Bolaños and Ehmcke (1996) inventoried the herpetofauna

(Acosta-Chaves and Cossel, 2016; Acosta-Chaves et al.,

of “Alberto Manuel Brenes” Biological Reserve (hereafter

2019).

AMBBR) in Northwest San Ramón from 1986 to 1996,

and later that effort was updated by Morera-Chacón and

II. Material and methods

Sánchez-Porras (2015), Morera-Chacón and Jiménez (2017),

and Acosta-Chaves et al., (2019) to obtain

41 species of

II.1. Study area

amphibians; unfortunately, some were enigmatically

extirpated from the reserve. More recently the Nectandra

The ESLA Cloud Forest is within the Caribbean basin,

Reserve was inventoried with 17 species of amphibians

close to the continental divide, and located approximately

recorded (Rovito et al., 2015). Other recent central Costa

16 km north the town of San Ramón, San Ramón

Rica checklists between 500 to 1800 meters above sea

canton, province of Alajuela. Our study site is about nine

level (m asl) by Arias and Bolaños (2014) in San Isidro

kilometers east from the highway to La Fortuna (Route

de Dota from the Pacific slope of San José where 30

702), that also dissects the Nectandra Reserve and later

species were documented, and later by Acosta-Chaves

travels adjacent to the entrance of the AMBBR (Rovito

et al., (2015) and Acosta-Chaves et al., (2016) in Río Macho

et al., 2015). This type of forest is a wet premontane

Biological Station of the Orosi Valley with 12 amphibians

belt according to the Holdridge life zones classification

species reported. Recently, with data obtained by citizen

(Holdridge, 1987). Our work was carried out in the private

science Gómez-Hoyos et al., (2018) generated a checklist

reserve of the Villa Blanca Hotel and Cloud Forest Reserve

of 14 amphibian species for the surrounded premontane

(1127803,742m N; 446907,055m W, datum WGS84; 1100

areas of La Amistad International Park in Costa Rica.

m. ASL Figure 1). Annual precipitation varies between

Currently, other survey efforts to understand the diversity

2000 to 4000 mm (Morera and Granados, 2013), and the

of herpetofauna from middle elevation forests in Costa

average temperture is of approximately 19° C. The reserve

Rica are limited to museum specimens collected (Acosta-

encompasses 70 hectares, it is mostly vegetated with

Chaves, obs.pers.).

secondary forest with at least 20 years of regeneration

that are surrounded by fragments of primary forest,

By means of multiple surveys and citizen science

and it has several bodies of standing water and streams

submissions a checklist of amphibians observed in the

(Appendix 1).

premontane woodland in the El Silencio de Los Angeles

Cloud Forest (hereafter ESLA Cloud Forest) of San Ramón,

Costa Rica has been produced and is presented here.

The purpose of this checklist is to draw attention to the

ESLA Cloud Forest amphibian diversity and to enhance

conservation efforts through further research.

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Figure 1. Map of Costa Rica showing the location of El Silencio de Los Ángeles Cloud Forest (Villa Blanca Hotel), Nectandra Reserve, San

Lorencito River Station of Alberto Manuel Brenes Biological Reserve, San Isidro de Dota and Río Macho Biological Station. Additionally, there

is a close up of the trail system in Villa Blanca Hotel and Cloud Forest Reserve.

Source: Own elaboration.

II.2. Data collection and analysis

produced following Amphibian Species of the World

(Frost, 2018). We identified endangered species following

From August 2013 to March 2014, July 2018 and September-

the IUCN Red List of Threatened species (IUCN 2018) and

november 2019, we conducted visual and acoustic

the Conservation Priority levels of endemic amphibian

encounter surveys (Heyer et al., 1994). We sampled the

and reptiles of Central America (Mata-Silva et al. 2019).

trails (Quebrada Trail, Self-guided Trail, Ficus Trail and

Ferns Trail) and the gardens in Villa Blanca Hotel and

To understand what the level of similarity in amphibian

Cloud Forest Reserve (Figure 1, Appendix 1), searching for

richness between, the ESLA Cloud Forest and other recent

amphibians in areas with primary and secondary forest,

checklists from premontane localities is, we compared our

streams, and ponds. The sampling effort consisted of

results against those reported for the Nectandra Reserve

two-hour survey once a month. We additionally utilized

(1000-1200 m ASL), the San Lorencito River Station of

the reports of species with photographic records made

AMBBR (500-1000 m ASL), the San Isidro de Dota (680-

by the local tour guides and random observations. No

800 m ASL) and the Río Macho Station (1500-1800 m

individuals were collected during surveys. All animals

ASL). A cluster analysis (single linkage, Jaccard index)

were identified based on preview experience (e.g. Acosta-

using the software PAST 3.2 (Hammer et al., 2001) was

Chaves et al. 2015, 2016, 2019), and field guides such as

calculated to obtain the level of similarity between sites.

Savage (2002) and Leenders (2016). Our checklist was

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III. Results

The total species richness for the ESLA Cloud Forest

the highest number of species in the ESLA Cloud Forest,

consisted of 27 species distributed in three orders, nine

each with six species (Table 1). However, if Strabomantidae

families, and 17 genera (Table 1, Appendix 2). Currently, the

is a valid family (Heinicke et al., 2018) then Craugastoridae,

ESLA Cloud Forest contains about 12% of the amphibians

Strabomantidae, Bufonidae, Ranidae, and Centrolenidae

registered for Costa Rica. Following the classification of

contained a similar number of species (Table 1).

Frost (2018), both Hylidae and Craugastoridae families had

Table 1. List of amphibians found in the El Silencio de Los Ángeles cloud forest, Costa Rica, Central America. Sampled

areas and trails: QT = Quebrada Trail, SgT = Self-guided Trail, FT = Ficus Trail, FeT = Ferns Trail, G = Gardens.

SgT

FeT

Taxon

Order Gymnophiona

Family Dermophiidae

Gymnopis multiplicata Peters, 1874

Order Caudata

Family Plethodontidae Gray, 1850

Oedipina uniformis (Keferstein, 1868)

Nototriton gamezi (García-París & Wake, 2000)

Order Anura

Family Bufonidae J. E Gray 1825

Incilius coniferus (Cope, 1862)

Incilius melanochlorus (Cope, 1877)

Rhinella horribilis (Wiegmann, 1833)

Family Centrolenidae Taylor, 1951

Cochranella granulosa (Taylor, 1949)

Espadarana prosoblepon (Boettger, 1892)

Teratohyla pulverata (Peters, 1873)

Family Craugastoridae Hedges, Duellman & Heinicke, 2008

Craugastor crassidigitus (Taylor, 1952)

Craugastor fitzingeri (Schmidt, 1857)

Craugastor underwoodi (Boulenger, 1896)

Pristimantis cerasinus (Cope, 1875)

Pristimantis cruentus (Peters, 1873)

Pristimantis ridens (Cope, 1866)

Family Eleutherodactylidae Lutz, 1954

Diasporus diastema (Cope, 1875)

Family Hylidae Rafinesque, 1815

Dendropsophus ebraccatus (Cope, 1874)

Duellmanohyla rufioculis (Taylor, 1952)

Scinax elaeochrous (Cope, 1875)

Smilisca manirosum (Taylor, 1954)

Smilisca phaeota (Cope, 1862)

Smilisca sordida (Peters, 1863)

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Familia Leptodactylidae Werner, 1896 (1838)

Leptodactylus savagei Heyer, 2005

Family Phyllomedusidae Gunther, 1858

Agalychnis callidryas (Cope, 1862)

Family Ranidae Rafinisque, 1814

Lithobates taylori ( Smith, 1959)

Lithobates vaillanti (Brocchi, 1877)

Lithobates warszewitschii (Schmidt, 1857)

Total number of species

Source: Own elaboration.

The species richness was different between trails: the

compared with localities outside San Ramón the contrast

Ferns Trail contained the highest number of species, while

was higher; for the San Isidro de Dota and the Río Macho

the Ficus Trail contained the lowest (Table 1). Some species

Station, the relationship was lower than 35% and 30 %

such as Craugastor underwoodi, Diasporus diastema,

respectively (Figure 2).

and Lithobates warszewitschii were found everywhere,

while others including Gymnopis multiplicata Oedipina

uniformis, Nototriton gamezi, Rhinella horribilis,

Cochranella granulosa, Teratohyla pulverata, Scinax

elaeochrous and Smilisca sordida, Leptodactylus savagei,

and Lithobates vaillanti were captured only at one location

(Table 1).

Most of the species detected in the ESLA Cloud Forest

are considered as Least Concerned according to the

IUCN Red List of Threatened Species (UICN 2018); only

the salamander N. gamezi is classified as Vulnerable.

However, the 42% of the amphibians of ESLA Cloud

Forest are endemic to Central America, especially from

the Isthmian Central American highlands and Caribbean

lowlands from Nicaragua to Panama (Mata-Silva et al.,

2019). According with the Conservation Priority levels

established recently by Mata-Silva et al. (2019) the species

N. gamezi, O. uniformis, C. underwoodi, D. rufioculis, S.

manisorum are in priority one, P. cerasinus is in priority

three, D. diastema is in priority four, G. multiplicata C.

granulosa is in priority five, I. melanochlorus and L.

Figure 2. Cluster analysis (Jaccard index, single linkage) showing the

percent of similarity between amphibian richness of recent checklists

taylori are in priority seven, and L. warszewitschii is in

from different premontane and lower montane locations in central

priority ten.

Costa Rica (San Isidro de Dota, Nectandra Biological Reserve, San

Lorencito River Station of Alberto Manuel Brenes Biological Reserve,

After comparing the amphibian richness of the ESLA

El Silencio de Los Ángeles Cloud Forest and Río Macho Biological

Station).

Cloud Forest against other localities from San Ramón,

we found that it was roughly 80% similar with the San

Source: Own elaboration.

Lorencito River Station and less than 55% similar with

the Nectandra Reserve. When the ESLA Cloud Forest was

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IV. Discussion

by Bolaños and Ehmcke (1996), Acosta-Chaves et al.

2019). According to the literature (Bolaños and Ehmcke,

There is a strong association between environment

1996; Savage, 2002; Leenders, 2016, Acosta-Chaves et

variation and amphibian diversity at the ESLA Cloud

al. 2019), we expect that other rare amphibians with

Forest. Microhabitats (primary and secondary forest,

secretive arboreal and/or fossorial habits could occur

streams and ponds) along the Fern Trail correlated to

in the ESLA Cloud Forest. Some examples of expected

greater amphibian richness. In contrast, fewer species

species are Bolitoglossa alvaradoi, Craugastor andi,

were observed in the primary forest of the Ficus Trail.

Craugastor fleischmanni, Pristimantis caryophyllaceus,

Common species such as C. underwoodi, D. diastema and

Anotheca spinosa and Ecnomiohyla spp. Other species

L. warszewitschii were detected in all the sites due to their

such as Craugastor ranoides, Atelopus varius and

wide habitat parameters: C. underwoodi utilizes suitable

Agalychnis lemur should have occurred in the past within

secondary and primary forest (Acosta-Chaves et al., 2015;

the ESLA Cloud Forest, but to date those species have

2016), D. diastema inhabits the understory and canopy

been extirpated from that region (Morera-Chacón and

layers of forest and borders, using bromeliads as breeding

Sánchez-Porras, 2015, Acosta-Chaves et al.,2019.).

sites (Savage, 2002; Acosta-Chaves et al., 2015); while L.

warszewitschii breeds in streams and ponds, and can

Although the similarity with the San Lorencito River

forage on the interior forest floor (Savage, 2002). The least

Station was predicted after the conclusions of Rovito et

common species were microhabitat specialist occupying:

al. (2015) for the Nectandra Reserve and our own surveys

salamanders (N. gamezi and O. uniformis) were observed

in AMBBR (Acosta-Chaves et al., 2019.), originally we

on streambanks with accompanying mosses R. horribilis

expected a higher similarity between the ESLA Cloud

inhabits open and disturbed sites and D. rufiocollis, C.

Forest and the Nectandra Reserve. Nectandra and

granulosa, T. pulverata and S. sordida were restricted

ESLA are similar in elevation and proximity between

to streams and rivers (Savage, 2002; Leenders, 2016). In

reserves than with the San Lorencito River Station. Other

general, the trail system in the ESLA Cloud Forest provides

similarities include the resemblance in the form of the

abundant natural and artificial ponds that are used by frogs

forest patch, size of the patch and matrix structure can

and toads from the families Hylidae, Phyllomedusidae,

determine the structure and composition of species in

Bufonidae and Ranidae for reproductive activities.

a site (Herrera, 2011). Additional surveys are needed for

detection of species absent from their list; we believe

Additionally, several species that are common at lower

that the amphibian richness of the Nectandra Reserve

elevations have been gradually appearing in the ESLA

should be greater than the reported by Rovito et al. (2015).

Cloud Forest. An example of potential successful

Due to the confluence of the widespread species of the

colonization involves Agalychnis callidryas, because it was

premontane elevation and the herpetofauna from the

recorded until 2014 in the ponds next to the “José Miguel

Pacific slope, the premontane forest of San Isidro de Dota

Alfaro” Biological Station; since then a well-established

(Arias and Bolaños, 2014) has richer species diversity

population has been observed in succeeding years. Two

than the ESLA Cloud Forest. Finally, the lower montane

other species, L.savagei and L. vaillanti, were also recorded

forest of Río Macho is in a different and higher life zone

until 2019, then we cannot discard a current colonization

that naturally limits the distribution of some species

process occurring in the ESLA Cloud Forest, as it have

common in the other analyzed localities, but additionally

been documented for other middle elevations (Acosta-

Río Macho also lost a greater part of its amphibian species

Chaves and Cossel, 2016; Acosta-Chaves et al. 2019).

richness because the enigmatic decline of populations

(Acosta-Chaves et al., 2015).

The Costa Rican endemic and endangered salamander

N. gamezi observed along the Ferns Trail was previously

Our surveys of the ESLA Cloud Forest complements

only registered for the Monteverde region (Pounds et al.,

the inventories of the Nectandra Reserve and the San

2008) and San Ramón (previously named N. abscodens

Lorencito River Station, helping to provide a better

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understanding of the amphibian richness in the western

VII. Bibliography

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