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.
1
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
2
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
191
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.
192
Revista Pensamiento Actual - Vol 19 - No. 33 2019 - Universidad de Costa Rica - Sede de Occidente
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
Ciencias Naturales
193
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.
QT
SgT
FT
FeT
G
Taxon
Order Gymnophiona
Family Dermophiidae
x
Gymnopis multiplicata Peters, 1874
Order Caudata
Family Plethodontidae Gray, 1850
Oedipina uniformis (Keferstein, 1868)
x
Nototriton gamezi (García-París & Wake, 2000)
x
Order Anura
Family Bufonidae J. E Gray 1825
Incilius coniferus (Cope, 1862)
x
x
x
Incilius melanochlorus (Cope, 1877)
x
x
x
x
Rhinella horribilis (Wiegmann, 1833)
x
Family Centrolenidae Taylor, 1951
Cochranella granulosa (Taylor, 1949)
x
Espadarana prosoblepon (Boettger, 1892)
x
x
x
x
Teratohyla pulverata (Peters, 1873)
x
Family Craugastoridae Hedges, Duellman & Heinicke, 2008
Craugastor crassidigitus (Taylor, 1952)
x
x
x
x
Craugastor fitzingeri (Schmidt, 1857)
x
x
x
x
Craugastor underwoodi (Boulenger, 1896)
x
x
x
Pristimantis cerasinus (Cope, 1875)
x
x
x
Pristimantis cruentus (Peters, 1873)
x
x
x
x
Pristimantis ridens (Cope, 1866)
x
x
x
x
Family Eleutherodactylidae Lutz, 1954
Diasporus diastema (Cope, 1875)
x
x
x
x
x
Family Hylidae Rafinesque, 1815
Dendropsophus ebraccatus (Cope, 1874)
x
x
x
Duellmanohyla rufioculis (Taylor, 1952)
x
x
Scinax elaeochrous (Cope, 1875)
x
Smilisca manirosum (Taylor, 1954)
x
Smilisca phaeota (Cope, 1862)
x
x
x
Smilisca sordida (Peters, 1863)
x
194
Revista Pensamiento Actual - Vol 19 - No. 33 2019 - Universidad de Costa Rica - Sede de Occidente
Familia Leptodactylidae Werner, 1896 (1838)
Leptodactylus savagei Heyer, 2005
x
Family Phyllomedusidae Gunther, 1858
Agalychnis callidryas (Cope, 1862)
x
x
Family Ranidae Rafinisque, 1814
Lithobates taylori ( Smith, 1959)
x
Lithobates vaillanti (Brocchi, 1877)
x
Lithobates warszewitschii (Schmidt, 1857)
x
x
x
x
x
Total number of species
14
10
7
20
11
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
Ciencias Naturales
195
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
196
Revista Pensamiento Actual - Vol 19 - No. 33 2019 - Universidad de Costa Rica - Sede de Occidente
understanding of the amphibian richness in the western
VII. Bibliography
Central Valley. The ESLA Cloud Forest can be considered
the second richest cloud forest in the San Ramón area
Acosta-Chaves, V.J., Bolaños, F., Spínola, R.M., Chaves,
for conservation and amphibian watching, and among
G. 2016. “Density, biomass, and phenology of
the better clouded forests in central Costa Rica. However,
Craugastor underwoodi (Boulenger, 1896) from
the significance of the ESLA Cloud Forest as reservoir
mid-elevation forests in the Valle de Orosi, Costa
of herpetofauna is currently underestimated and the
Rica”. Mesoamerican Herpetology, 3(4): 900-908.
likelihood for exploitation is high. Species such as A.
callidryas, D. ruficollis, L. warszewitschii and the three
Acosta-Chaves, V.J., Chaves, G., Abarca, J.G., García-
glass frogs (Centrolenidae) are attractive animals, an
Rodríguez, A., Bolaños, F. 2015. “A checklist of the
eye-catching commodity for photographers. The other
amphibians and reptiles of Río Macho Biological
species, which is restricted to premontane and montane
Station, Provincia de Cartago, Costa Rica”. Check
belts, may also be focal point for specialized herpetological
List, 11(6): 1784.
tours. In order to reduce perturbation and disturbance of
all species and ecosystems in the ESLA Cloud Forest, we
Acosta-Chaves, V.J., Cossel, J.O. 2016. “Smilisca phaeota
recommend that ethical field caution should occur during
(Cope, 1862). Colonization”. Mesoamerican
human interaction with the herpetofauna.
Herpetology, 3(3): 713-715.
Finally, we strongly suggest continuing the amphibian
Acosta-Chaves, V.J., Madrigal-Elizondo, V., Chaves,
surveys in unexplored areas of the ESLA Cloud Forest,
G., Morera-Chacón, B., García-Rodríguez, A.,
for example the recently open sector “Pittier Trail” that
Bolaños, F. 2019. “Shifts in the diversity of an
encompass pristine forest in a better conservation status
amphibian community from a premontane forest
that the others we surveyed for this manuscript. Continued
of San Ramón, Costa Rica”. Revista de Biología
surveys and research is still needed at premontane and
Tropical, 67(2): 259-273.
middle elevations throughout Costa Rica in order to
monitor amphibian population dynamics and community
Arias, E., Bolaños, F. 2014. “A checklist of the amphibians
structure in relationship to habitat fragmentation, climate
and reptiles of San Isidro de Dota, Reserva Forestal
change, intra- and interspecific competition, colonization
Los Santos, Costa Rica”. Check List, 10(4): 870-877.
and/or extinction of Costa Rican clouded forest species.
Bolaños, F., Ehmcke, J. 1996. “Anfibios y reptiles de la
VI. Acknowledgements
Reserva Biológica San Ramón, Costa Rica”.
Pensamiento Actual, 2(1): 107-112.
The Villa Blanca Hotel and Cloud Forest provided us
the facilities. We are especially grateful to Roy Valverde
Frost, D. (2018). Amphibian Species of the World: an
and Esteban Hernández from the “José Miguel Alfaro”
Online Reference. Version 6.0. New York:
Biological Station, and other staff members, for sharing
American Museum of Natural History. Available
their observations and resources. Finally, we thank
Robert Goodman, and two anonymous reviewers, for
amphibia/ (18 July 2018).
their valuable comments improving the manuscript.
Gómez-Hoyos, D., Méndez-Arrieta, R., Méndez-Arrieta, A.,
Seisdedos-de-Vergara, R., Abarca, J., Barrio-Amorós,
C., González-Maya, J. 2018. “Anuran inventory in a
locality of the buffer area of La Amistad International
Park, Costa Rica: pilot study for Citizen Science
application”. Anales de Biología, 40(1): 57-64.
Ciencias Naturales
197
Hammer, Ø., Harper, D.A.T., Ryan, P.D. 2001. “PAST:
Morera, B., Granados, A. 2013. “Distribución y abundancia
Paleontological statistics software package for
de Musa velutina en un bosque nuboso, Ángeles
education and data analysis”. Palaeontologia
de San Ramón, Alajuela, Costa Rica”. Red
Electron, 4(1): 1-9.
Latinoamericana para el Estudio de Especies
Invasoras, 3(1): 16-22.
Heinicke, M.P., Lemmon, A.R., Lemmon, E.M., McGrath,
K., Hedges, S.B. 2018. “Phylogenomic support for
Morera-Chacón, B.H., Jiménez-Castro, J.E. 2017. “Primer
evolutionary relationships of New World direct-
reporte de Agalychnis callidryas (Hylidae) en
developing frogs (Anura: Terraranae)”. Molecular
la Reserva Biológica Alberto Manuel Brenes”.
phylogenetics and evolution, 118(1): 145-155.
Pensamiento Actual, 17: 59-60.
Herrera, J.M. 2011. “El papel de la matriz en el
Morera-Chacón, B.H., Sánchez-Porras, R. 2015. “Anfibios
mantenimiento de la biodiversidad en hábitats
y reptiles de la Reserva Biológica Alberto Manuel
fragmentados. De la teoría ecológica al desarrollo
Brenes”. Pensamiento Actual, 15(25): 39-59.
de estrategias
de conservación”. Ecosistemas,
20(2): 21-34.
Pounds, J., Bolaños, F., Wake, D., Savage, J. (2008).
Nototriton gamezi. The IUCN Red List of
Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Hayek, L.C.,
Threatened Species. International Union for
Foster, M.S. (1994). Measuring and monitoring
Conservation of Nature and Natural Resources.
biological diversity: Standard methods for
amphibians. Washington, DC: Smithsonian
details/59294/0 (18 July 2018).
Institution Press, 323 p.
Rovito, S.M., Devitt, T.J., Devitt, S.C. 2015. “First survey
Holdridge, LR (1987). Ecología: basada en zonas de vida.
of the amphibians and reptiles of theNectandra
San José, Costa Rica: Instituto Interamericano de
Cloud Forest Reserve, Alajuela, Costa Rica”. Check
Cooperacion para la Agricultura, 206 p.
List, 11(2): 1570.
IUCN (2018). The IUCN Red list of Threatened Species.
Savage, J.M. (2002). The amphibians and reptiles of Costa
International Union for Conservation of Nature
Rica: a herpetofauna between two continents,
between two seas. Chicago: University of Chicago
iucnredlist.org/ (18 July 2018).
press, 934p.
Leenders, T. (2016). Amphibians of Costa Rica: A
Zumbado-Ulate, H., Nelson, K. N., García-Rodríguez,
field guide. Ithaca, New York: Zona Tropical
A., Chaves, G., Arias, E., Bolaños, F., Whitfield,
Publications,544 p.
S. M., Searle, C. L. 2019. “Endemic Infection of
Batrachochytrium dendrobatidis in Costa Rica:
Mata-Silva, V., DeSantis, D. L., García-Padilla, E.,
Implications for Amphibian Conservation at
Jhonson, J. D., Wilson, L. D. 2019. “The endemic
Regional and Species Level”. Diversity, 11(8): 1-20.
herpetofauna of Central America: a casualty
of anthropocentrism”. Amphibian & Reptile
Conservation, 13(1): 1-64.
198
Revista Pensamiento Actual - Vol 19 - No. 33 2019 - Universidad de Costa Rica - Sede de Occidente
Annexes
Appendix 1. Types of microhabitats in Villa Blanca Hotel. Gardens and open areas (A) & (B). Secondary forest (Ferns
trail) (C). Artificial pond (Ferns trail) (D). Primary forest (Ficus trail) (E). Brayan Morera sampling in primary forest
(Ficus trail) (F). Photos by Víctor Acosta.
Ciencias Naturales
199
Appendix 2. Amphibian species found in the ESLA cloud forest. Oedipina uniformis (01). Nototriton gamezi (02). Incilius
coniferus (adult) (03). Incilius coniferus (juvenile) (04). Incilius melanochlorus (05). Rhinella horribilis (06). Photos
01, 03, 05 and 06 by Brayan Morera, Villa Blanca; 02 by Esteban Hernández, Villa Blanca; 04 by Víctor Acosta, Villa
Blanca (Figure continued in following page).
200
Revista Pensamiento Actual - Vol 19 - No. 33 2019 - Universidad de Costa Rica - Sede de Occidente
Appendix 2, continued. Amphibian species found in the ESLA cloud forest. (7) Espadarana prosoblepon. (8) Cochranella
granulosa. (9) Teratohyla pulvarata. (10) Craugastor crassidigitus (morph1) (11) Craugastor crassidigitus (morph2).
(12) Craugastor fitzingeri. Photos 7,10 and 11 by Víctor Acosta, Villa Blanca; 9 by Víctor Acosta, Peñas Blancas de San
Ramón; 8 and 12 by Brayan Morera, Villa Blanca. (Figure continued in following page).
Ciencias Naturales
201
Appendix 2, continued. Amphibian species found in the ESLA cloud forest. Craugastor underwoodi (morph1) (13).
Craugastor underwoodi (morph2) (14). Pristimantis cerasinus (morph1) (15). Pristimantis cruentus (morph1) (16).
Pristimantis cruentus (morph1) (17). Diasporus diastema (18). Photos 13, 16 and 18 by Víctor Acosta, Villa Blanca; 14,
15 and17 by Brayan Morera, Villa Blanca (Figure continued in following page).
202
Revista Pensamiento Actual - Vol 19 - No. 33 2019 - Universidad de Costa Rica - Sede de Occidente
Appendix 2, continued. Amphibian species found in the ESLA cloud forest. Pristimantis ridens (19). Dendropsophus
ebraccatus (20). Duellmanohyla rufiocollis (21). Scinax elaeochrous (22). Smilisca manisorum (23). Smilisca phaeota
(24). Photos 19, 22 and 23 by Brayan Morera, Villa Blanca; 20, 21 and 24 by Víctor Acosta, Villa Blanca (Figure continued
in following page).
Ciencias Naturales
203
Appendix 2, continued. Amphibian species found in the ESLA cloud forest. Smilisca sordida (25). Agalychnis callidryas
(26). Lithobates taylori (27). Lithobates warszewitschii (28). Lithobates vaillanti (29). Leptodactylus savagei (30). Photos
25, 26, 28 and 30 (Villa Blanca), 27 (Río Macho) and 29 (Soltis Center) by Víctor Acosta.
204
Revista Pensamiento Actual - Vol 19 - No. 33 2019 - Universidad de Costa Rica - Sede de Occidente
Appendix 2, continued. Amphibian species found in the ESLA cloud forest. Gymnopis multiplicata from Villa Blanca,
from Víctor Acosta.
31