Amphibian diversity in Serranía de Majé, an isolated mountain range in eastern Panamá

Abstract

Eastern Panamá is within the Mesoamerican biodiversity hotspot and supports an understudied amphibian fauna. Here we characterize the amphibian diversity across an elevational gradient in one of the least studied mountain ranges in eastern Panamá, Serranía de Majé. A total of 38 species were found, which represent 17% of all species reported for Panamá. Based on expected richness function and individual-based rarefaction curves, it is estimated that this is an underestimate and that at least 44 amphibian species occur in this area. Members of all three amphibian orders were encountered, represented by ten families and 22 genera, including five species endemic to Central America. Estimated species richness decreased with elevation, and the mid-elevation site supported both lowland and highland species. Our study provides a baseline for understanding the distribution pattern of amphibians in Panamá, for conservation efforts, and for determining disease-induced changes in amphibian communities.

Full text

Amphibian diversity in Serranía de Majé, Panamá 117
Amphibian diversity in Serranía de Majé, an isolated
mountain range in eastern Panamá
Daniel Medina1,2, Roberto Ibáñez2,3,4,5, Karen R. Lips2,6, Andrew J. Crawford2,3,7
1 Laboratório de História Natural de Anfíbios Brasileiros (LaHNAB), Departamento de Biologia Animal,
Universidade Estadual de Campinas, Campinas, SP 13083-862, Brazil 2 Smithsonian Tropical Research
Institute, Apartado Postal 0843-03092, Panamá, República de Panamá 3 Círculo Herpetológico de Panamá,
Estafeta Universitaria, Apartado Postal 10762, Panamá, República de Panamá 4 Departamento de Zoo-
logía, Universidad de Panamá, Panamá, República de Panamá 5 Sistema Nacional de Investigación, Panamá,
República de Panamá 6 Department of Biology, University of Maryland, College Park, MD 20742, USA
7Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, 111711, Colombia
Corresponding author: Roberto Ibáñez (ibanezr@si.edu)
Academic editor: Anthony Herrel|Received 4 January 2019|Accepted 29 March 2019|Published 2 July 2019
http://zoobank.org/57338B9B-D249-47EE-B152-9828A8B446AA
Citation: Medina D, Ibáñez R, Lips KR, Crawford AJ (2019) Amphibian diversity in Serranía de Majé, an isolated
mountain range in eastern Panamá. ZooKeys 859: 117–130. https://doi.org/10.3897/zookeys.859.32869
Abstract
Eastern Panamá is within the Mesoamerican biodiversity hotspot and supports an understudied amphib-
ian fauna. Here we characterize the amphibian diversity across an elevational gradient in one of the least
studied mountain ranges in eastern Panamá, Serranía de Majé. A total of 38 species were found, which
represent 17% of all species reported for Panamá. Based on expected richness function and individual-
based rarefaction curves, it is estimated that this is an underestimate and that at least 44 amphibian species
occur in this area. Members of all three amphibian orders were encountered, represented by ten families
and 22 genera, including ve species endemic to Central America. Estimated species richness decreased
with elevation, and the mid-elevation site supported both lowland and highland species. Our study pro-
vides a baseline for understanding the distribution pattern of amphibians in Panamá, for conservation
eorts, and for determining disease-induced changes in amphibian communities.
Keywords
Altitudinal diversity, amphibian species inventory, Panamá
ZooKeys 859: 117–130 (2019)
doi: 10.3897/zookeys.859.32869
http://zookeys.pensoft.net
Copyright Daniel Medina et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Daniel Medina et al. / ZooKeys 859: 117–130 (2019)
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Introduction
Mesoamerica is a global biodiversity hotspot (Johnson et al. 2015). Within this region,
Panamá has the second greatest number of reptile and amphibian species, containing
26% of all amphibian species reported for Mesoamerica (Jaramillo et al. 2010). How-
ever, a substantial portion of eastern Panamá has been understudied. Geographically,
eastern Panamá comprises the northernmost part of the Chocó biogeographical region
(Duque-Caro 1990), and it is part of the Tumbes-Chocó-Magdalena global biodiver-
sity hotspot (Mittermeier et al. 1999). is region includes a number of relatively low
mountain ranges, including the Serranía de San Blas + Serranía del Darién on Carib-
bean side, the inland Serranía de Pirre + Altura de Nique + Altos de Quía, Serranía de
Majé, and the Serranía de Sapo + Serranía de Jingurudó + Altos de Aspavé + Cordillera
de Juradó along the Pacic Ocean (Duque-Caro 1990; Batista et al. 2016).
Whiteld et al. (2016) analyzed regional trends and reported that eastern Panamá
has a very small number of recognized species in relation to its geographic area, which
reects the limited number of eld surveys in the area. A sharp increase in the number
of eld surveys during the last decade has led to the discovery of several new amphibian
species with restricted distribution ranges (e.g., Ibáñez and Crawford 2004; Crawford
et al. 20104a; Batista et al. 2014a, 2014b, 2016) supporting the hypothesis that east-
ern Panamá is a region with a high endemic amphibian diversity. is is in contrast to
the claim that it was mainly a dispersal route during the Great American Biotic Inter-
change (Webb 2006), and was colonized by species groups from the north and South
America (Vanzolini and Heyer 1985; Pinto-Sánchez et al. 2012).
One reason to establish baseline estimates of amphibians is to assess changes fol-
lowing loss caused by disease epidemics. e pathogenic fungus Batrachochytrium den-
drobatidis (Bd) causes population declines and extinctions of many amphibian spe-
cies worldwide, particularly in the Neotropics (James et al. 2015, Lips 2016). Bd has
caused dramatic declines of amphibian communities in the highlands of western and
central Panamá (Lips 1999; Lips et al. 2006; Crawford et al. 2010b). Importantly, to
our knowledge, at the time of sampling there were no published data reporting the
presence of Bd in the region – though the amphibian species present at this region can
either represent the original community or a subset as a consequence of an undetected
Bd epidemic. Here, we describe the results from eld surveys to characterize α and β di-
versity along an altitudinal gradient in the isolated Serranía de Majé of eastern Panamá.
Materials and methods
Study sites
During the wet season, from June 23 to July 2 2007, we conducted eld surveys at
three study sites located at a low, middle, and high elevations in the Serranía de Majé.
is mountain range is located on the Pacic coast, previously known as Serranía de
Cañazas (Myers 1969), and is isolated from others mountainous areas by the Chepo

Amphibian diversity in Serranía de Majé, Panamá 119
and Chucunaque Rivers (Figure 1; Angehr and Christian 2000). Its highest point,
Cerro Chucantí (1,489 m), stands on the eastern end of the mountain range, at the
boundary of the Panamá and Darién provinces (Angher and Christian 2000).
e three study sites were located in Lowland Wet/Moist Forest (LWM) below 600
m, and Premontane Rain Forest/Wet Forest (PRW) above 600 m (Holdridge 1967).
e sites were: a low elevation site, Centro Cristo Misionero (8.96N, 78.457W) at
120–150 m elevation; a mid-elevation site, located within the Reserva Natural Privada
Cerro Chucantí (8.79N, 78.451W) at 797 m elevation; and, the high elevation site,
also located in the Cerro Chucantí private natural reserve (8.80N, 78.462W), near
the top of the Cerro Chucantí, at 1,240–1,365 m elevation. e approximate airline
distances between the study sites were 19, 18, and 2 km for lowland-mid-elevation,
lowland-highland and mid-elevation-highland sites, respectively.
Data collection
e surveys were conducted using the sampling technique “free and unrestricted search”,
which is considered to be one of the most ecient methods to record a high number of
species in a relatively short amount of time (Rueda et al. 2006). Dierent types of habitat
such as forest, streams, ponds, and open areas with grass were surveyed during the day and
night. Species identication and individual counts were performed using the techniques
‘visual encounter survey’ (VES) and ‘acoustic encounter survey’ (AES). In addition, the
search eort invested (in person-hours) at each sampling site was calculated by multiply-
ing the search time by the number of observers, and the catch per unit of search eort
for each site was calculated by dividing the number of post-metamorphic amphibians
encountered by the search eort at the respective site as estimated by Kilburn et al. (2011).
A few specimens of each species were collected as voucher specimens (Suppl. mate-
rial 1: Table S1), photographed, and deposited in the reference Collection of Herpetol-
ogy (specimen tags CH and AJC) at the Smithsonian Tropical Research Institute, and
in the Museo de Vertebrados de la Universidad de Panamá (tags MVUP). Amphib-
ians to be preserved were rst euthanized using Orajel (benzocaine 20%) or occasion-
ally 10% ethanol. Before xation, liver samples were taken from each specimen and
preserved for future phylogenetic and phylogeographic analyses (Seutin et al. 1991).
Vouchers were then xed in 10% formalin in a position that facilitates examination.
To verify the identication of specimens we used all relevant literature available on the
amphibians of Panamá (e.g., Ibáñez et al. 1999a), and compared specimens with those
in the CH reference collection. e identication of anuran advertisement calls was
facilitated by audio recordings of Panamanian frogs (Ibáñezetal. 1999b).
Data analyses
We calculated α diversity based on all post-metamorphic amphibians captured at each
site (Hortal et al. 2006), using the software EstimateS 8.0.0 (Colwell 2006). We calcu-

Daniel Medina et al. / ZooKeys 859: 117–130 (2019)
120
Figure 1. Map showing the location of the study sites in the Serranía de Majé and the Serranía de
Piedras-Pacora across the valley of the Chepo River.
lated Mao Tau (Colwell et al. 2004) and plotted sample-based rarefaction curves with
95% condence intervals.
To determine β diversity for assessing the variation in species composition across
sites, we also used all post-metamorphic amphibians captured at each site, and con-
ducted a cluster analysis based on Jaccard dissimilarity measures estimated with the R
function vegdist from the vegan package (Oksanen et al. 2017). In order to identify
clusters, we built a dendrogram using the unweighted pair-group method based on
arithmetic averages (UPGMA), using function hclust from the default R package stats.
is analysis was completed in the R version 3.3.3 (R Core Team, 2017).
Results
Our team conducted 280 person-hours of surveys (lowland site: 125; mid-elevation
site: 96; highland site: 59) and identied 38 amphibian species from all three amphib-
ian orders, ten families, and 22 genera (Table 1). e total number of species for the
surveyed area within the Serranía de Majé was estimated as 44 species based on the
upper 95% condence interval of the Mao Tau function (Table 2).

Amphibian diversity in Serranía de Majé, Panamá 121
Table 1. List of species and number of post-metamorphic individuals found at the three surveyed sites
across the elevational gradient in the Serranía de Majé. e letter ‘L’ refers to a species that was recorded
by its larvae and ‘V’ by its vocalizations. e IUCN conservation status is based on the IUCN (2018). ‘E’
represents a species that is endemic to Central America (CA) based on Johnson et al. (2015).
Order Family Genus Species Lowland Mid-
elevation
Highland IUCN
status
Endemic
to CA
Anura Aromobatidae Allobates talamancae 2 1 LC
Bufonidae Rhaebo haematiticus 9 11 LC
Rhinella alata 13 1 1 LC
Rhinella horribilis 2 1 LC
Centrolenidae Espadarana prosoblepon L 8 V LC
Cochranella euknemos 3LC
Hyalinobatrachium colymbiphyllum 1LC
Hyalinobatrachium eischmanni 3LC
Hyalinobatrachium vireovittatum 1 DD E
Craugastoridae Craugastor crassidigitus 1 9 1 LC
Craugastor tzingeri 5 3 LC
Craugastor raniformis 15 3 LC
Pristimantis a. latidiscus 4 – –
Pristimantis caryophyllaceus 57 NT E
Pristimantis cruentus 1 71 LC
Pristimantis gaigei 1LC
Pristimantis moro 10 LC
Pristimantis pardalis 1 NT E
Pristimantis ridens 1LC
Pristimantis taeniatus VLC
Strabomantis bufoniformis 2LC
Dendrobatidae Colostethus a. pratti 11 9 4 – –
Dendrobates auratus 8 19 LC
Silverstoneia a. nubicola 3 12 4 – –
Eleutherodactylidae Diasporus a. diastema* 21 – –
Diasporus majeensis** 1 – E
Hylidae Agalychnis callidryas L 4 LC
Dendropsophus microcephalus 10 LC
Boana rosenbergi 4LC
Scinax rostratus 2LC
Scinax ruber 3LC
Smilisca phaeota 6LC
Smilisca sila 12 LC
Leptodactylidae Engystomops pustulosus 13 1 LC
Leptodactylus fragilis 3LC
Leptodactylus savagei 1 V LC
Caudata Plethodontidae Oedipina complex 1LC
Gymnophiona Caeciliidae Caecilia isthmica 1 DD E
3 10 22 38 130 99 166
* is species refers to the Diasporus a. diastema from the Serranía de Majé as suggested by Batista et al. (2016).
** Described by Batista et al. (2016), only known from Panamá; therefore, considered endemic to CA.

Daniel Medina et al. / ZooKeys 859: 117–130 (2019)
122
e greatest number of species was found at the lowland site (24 spp., Table 2;
individuals catch per unit of search eort: 1.04), where the search eort was the
highest, and where multiple aquatic habitats were available (i.e. ponds and forest
streams). e most abundant species at this site were Diasporus a. diastema (sensu
Batista et al. 2016), Craugastor raniformis and Engystomops pustulosus (Table 1). Es-
padarana prosoblepon and Agalychnis callidryas were detected at this site with larval
surveys. e mid-elevation site had fewer species than the lowland site (22 spp.,
Table 2; individuals catch per unit of search eort: 1.03); however, despite lower
search eort at this site, the upper 95% condence intervals of the Mao Tau func-
tion estimated very similar species number (i.e., 25 spp. at the lowland site and 26
spp. at the mid-elevation site). e most abundant species at the mid-elevation site
were Dendrobates auratus, Silverstoneia a. nubicola and Smilisca sila (Table 1). In
addition, at this site two species were detected only by their vocalizations: Pristi-
mantis taeniatus and Leptodactylus savagei. e lowest richness was observed at the
highland site (13 spp., Table 2; frog catch per unit of search eort: 2.81), because of
limited searching eort, fewer habitats, and the lower diversity of the upland area.
e estimated number of species for this site based on the upper 95% condence
intervals of the Mao Tau function was 17 spp., and the most abundant species at this
site were Rhaebo haematiticus, Pristimantis caryophyllaceus, P. cruentus, and P. moro
(Table 1). Moreover, the glassfrog, Espadarana prosoblepon, was detected at this site
only by its vocalization.
e individual-based rarefaction curves for the total area surveyed (Figure 2A) and
at the site level (Figure 2B) showed a substantial decrease in the slope as the number
of individuals increased with search eort. us, while the upper 95% condence
interval of the Mao Tau function suggests that not all species present in the area were
observed, the amphibian community determined in these surveys might be representa-
tive of the extant community in Serranía de Majé.
Based on the Jaccard dissimilarity coecients calculated, the community compo-
sition was more similar between the low and mid-elevation sites relative to the high
elevation site (Table 3, Figure 3). As expected, the sites that most diered were the
low versus high elevation sites. However, six species were consistently present across
all three elevation sites: Rhinella alata, Espadarana prosoblepon, Craugastor crassidigitus,
Colostethus a. pratti, and Silverstoneia a. nubicola.
Table 2. Total number of post-metamorphic individuals and species per site, and the site-level estimated
richness as a function of the 95% condence intervals (CI) calculated by the function Mao Tao.
Site Number of Individuals Number of species observed (Sobs) Expected 95% CI upper limit
Lowland 130 22 24.64
Mid-elevation 99 19 25.58
Highland 166 12 16.57
All sites 395 37 44.08

Amphibian diversity in Serranía de Majé, Panamá 123
Table 3. Number of species shared between pairs of sites along an elevational transect of the Serranía de
Majé (below the diagonal); total number of species per site including the species registered by post-meta-
morphic stages, vocalization, or larval stage (diagonal); and Jaccard similarity coecients (1 - dissimilarity
estimate) for each pair of sites (above the diagonal).
Lowland Mid-elevation Highland
Lowland 24 0.32 0.13
Mid-elevation 13 22 0.24
Highland 5 7 13
Figure 2. Individual-based rarefaction curves showing the estimated richness as a function of the upper
95% condence interval (CI) calculated by the function Mao Tao. A Rarefaction curve combining all
data obtained for the Serranía de Majé transect B rarefaction curves for low (120 – 150 m), intermediate
(797m), and high elevation (1,240–1,365 m) survey sites.

Daniel Medina et al. / ZooKeys 859: 117–130 (2019)
124
Discussion
e present study represents the rst attempt to characterize the composition and al-
titudinal diversity pattern of the amphibian community from the isolated Serranía de
Majé of eastern Panamá. We determined that the composition of the species commu-
nity across the altitudinal gradient was comprised by species from both Mesoamerican
and South American groups, and that taxonomic genera from South America domi-
nated the composition of the community (South American genera: 82%; Mesoameri-
can genera: 18%). In addition, the observed proportion in the composition of genera is
consistent with the diversity pattern determined by Savage (2002) for eastern Panamá,
where genera from South American groups represented over 50% of the genera com-
prising the amphibian assemblage.
e species found during this study represent 17% of the native amphibian spe-
cies of Panamá (AmphibiaWeb 2018). However, the estimated total number of species
based on the rarefaction analysis suggests that the richness of the study area is slightly
higher than what we observed. In addition, the recent discovery of two new amphib-
ian species from the Serranía de Majé, Bolitoglossa chucantiensis and Diasporus majeensis
(see Batista et al. 2014b, 2016), suggest that this region might be high in endemism, as
previously suggested for eastern Panamá (Crawford et al. 2010a).
Amphibians, occurring in Central America, have their highest species richness at
intermediate elevations (Savage 2002, Wiens et al. 2006, Whiteld et al. 2016). is
general altitudinal diversity pattern might also apply to the Serranía de Majé consider-
ing that, despite the relatively lower search eort and lower number of individuals en-
countered at the mid-elevation site, we observed and estimated a species richness simi-
Figure 3. Site-level dendrogram based on Jaccard dissimilarities and built with the unweighted pair-
group method based on arithmetic averages (UPGMA). is analysis was based on all post-metamorphic
amphibians captured at each site.

Amphibian diversity in Serranía de Majé, Panamá 125
lar to that of the lowland site (i.e., site with the highest observed richness). In addition,
we determined similar estimates of individuals catch per unit of search eort (lowland
site: 1.04 vs. mid-elevation site:1.03) between the lowland and mid-elevation sites.
Hence, these results suggest that an increase in sampling eort at the mid-elevation site
will potentially increase the number of species detected. Lastly, the observed altitudinal
pattern of species richness could have been inuenced by the variation across sites in
the area covered during the surveys and the habitat types present at the sampling sites.
In particular, the number of observed species at the highland site was potentially aect-
ed by the absence of streams and ponds, and the reduced patch size of the cloud forest.
In terms of β diversity, the higher similarity in the community composition be-
tween the mid-elevation and highland sites compared to that between the lowland and
highland sites, suggests that the composition at intermediate elevations in Serranía de
Majé might result, in part, by an overlap in the altitudinal distribution of the species
associated with higher and lower altitudes; a pattern previously observed for the anuran
communities from the Panamá Canal watershed (Ibáñez et al. 2002). In addition, de-
spite the mid-elevation and highland sites being closer to each other (i.e., ~2 km apart)
than to the lowland site, the community composition between the mid-elevation and
highland sites was less similar than the composition between the mid-elevation and
lowland sites. e higher similarity in the community composition between the mid-
elevation and lowland sites compared to that with the highland site suggests that the
highland site might be comprised by species with restricted altitudinal distributions.
For instance, the dissimilarity associated with the highland site in our study was poten-
tially inuenced by the observation of species with restricted altitudinal ranges, such as:
Pristimantis a. latidiscus, P. caryophyllaceus, P. moro, P. pardalis and Diasporus majeensis.
e Serranía de Majé is isolated from the other mountain ranges in the region by
the valleys of the Chepo and Chucunaque Rivers (Figure 1), which could have rep-
resented physical barriers leading to genetic isolation of populations that could have
resulted in allopatric speciation (Cadena et al. 2011). Preliminary results from a com-
parison between the amphibian communities from the Serranía de Majé and Serranía
de Piedras-Pacora (Ibáñez et al. 1994, Sosa and Guerrel 2013), located across the valley
of the Chepo River (Figure 1), showed a lower species diversity at the Serranía de Majé
and a decrease in the similarity of species composition as elevation increases (Figure 4).
In addition, the highest elevations studied at these two mountain ranges are about 106
km apart (airline distance), and their dissimilarity is largely due to the disproportionate
number of species that are present in Serranía de Piedras-Pacora but potentially absent in
Serranía de Majé. Hence, thus far, seems that dispersal limitation has potentially played
a major role in shaping the amphibian community at Serranía de Majé; nonetheless,
more studies would be necessary to address this. Lastly, the decrease in similarity in spe-
cies composition as elevation increases is consistent with the general pattern of amphib-
ians endemism observed in Central America, that shows that a substantial portion of
endemic species in the region are associated with upland regions (Whiteld et al. 2016).
Central America, while being a hotspot for amphibian diversity, is a region with
a high proportion of threatened amphibian species. For instance, 41% of the regional

Daniel Medina et al. / ZooKeys 859: 117–130 (2019)
126
pool of species that have been assessed by the IUCN (International Union for Conser-
vation of Nature) are under one of the following categories of the Red List of reat-
ened Species: critically endangered, endangered or vulnerable (reviewed in Whiteld
et al. 2016). Within this context, the amphibian community of the Serranía de Majé
does not seem, at rst, to be comprised of species of high conservation concern given
that 76% of the species registered in this study are under the category ‘least concern’
of the IUCN Red List of reatened Species (IUCN 2018). However, the Serranía de
Majé harbors amphibian species that could be regarded as threatened species, as well as
poorly known species lacking an evaluation of their conservation status. For example,
based on the IUCN criteria, two of the recorded species are considered near threatened
(i.e., Pristimantis caryophyllaceus and P. pardalis), and two others are data decient (i.e.,
Caecilia isthmica, and Hyalinobatrachium vireovittatum). Importantly, these two spe-
cies that are considered near threatened and the two data decient ones are endemic
to Central America (Johnson et al. 2015). Notably, in this study we also found four
species, which include one species from the genus Pristimantis (P. a. latidiscus), two
dendrobatids (Colostethus a. pratti and Silerstoneia a. nubicola) and one species from
the Diasporus diastema species group (i.e., Diasporus a. diastema suggested by Batista
et al. 2016), that are potential new species and, together with the recently described
Diasporus majeensis, lack an assessment by the IUCN.
Our survey provides baseline information for exploration and conservation eorts
by identifying species in the area requiring immediate assessment and conservation ac-
tion (Table 1). Importantly, this study might also inform the delimitation of protected
areas based on species with restricted distribution ranges. is is particularly relevant
given the absence of biological reserves within this mountain range that are recognized
by the national system of protected areas (Jaramillo et al. 2010), and the increasing
deforestation pressure in the region (Parker et al. 2004). Lastly, considering the ar-
rival of Bd to the Serranía de Majé some years after this study (Küng et al. 2014), the
Figure 4. Diagram showing a decrease with elevation in the similarities of amphibian species assemblages
associated with sites from the Serranía de Piedras-Pacora mountain range and the isolated Serranía de
Majé mountain range. e numbers represent the shared species between sites (N), Jaccard similarity coef-
cients (N) and total number of species at the site level (N). Each color represents an elevation category,
where the lowlands (< 400 m) are represented in yellow, mid-elevation sites (400–800 m) in green, and
highlands (> 800 m) in blue. NA = no data available.

Amphibian diversity in Serranía de Majé, Panamá 127
baseline information provided by this inventory could potentially serve to determine
Bd-induced changes in the amphibian community. In particular, at mid and high el-
evations, where disease-induced losses of amphibian diversity have been substantial in
Central America, including Panamá (Lips 2016).
Acknowledgements
anks to Arquimedes Batista, Roberto Brenes, Jhoana De Alba, Edgardo J Grith,
Susanne Lanckowsky, Kirsten Nicholson, and Daedre Craig for their eld assistance.
To Guido C Berguido for his support with the logistics to work at the Reserva Natural
Privada Cerro Chucantí, and to Fr Wally Kasuboski for providing housing at the Cen-
tro Cristo Misionero. is survey was possible thanks to the Committee for Research
and Exploration of the National Geographic Society (grant number 8133-06). Also,
thanks to the Autoridad Nacional del Ambiente (now, Ministerio de Ambiente) for the
collecting/research permit No. SE/A-37-07. RI was supported by the Sistema Nacional
de Investigación of Panamá, the Panamá Amphibian Rescue and Conservation Project,
and Minera Panamá, during the preparation of the manuscript. e reviewers Raoni
Rebouças Santos and Jiri Moravec helped to improve the manuscript.
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Supplementary material 1
Table S1. List of voucher specimens collected at the three surveyed sites along the
altitudinal gradient in the Serranía de Majé
Authors: Daniel Medina, Roberto Ibáñez, Karen R. Lips, Andrew J. Crawford
Data type: specimen list.
Explanation note: e list includes taxonomy of voucher specimens and collection num-
ber, date and locality data. CH = Collection of Herpetology, AJC = Andrew J. Craw-
ford eld tag, and MVUP = Museo de Vertebrados de la Universidad de Panamá.
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/zookeys.859.32869.suppl1