ArticlePDF Available

Abstract and Figures

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.
Content may be subject to copyright.
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 (
Academic editor: Anthony Herrel|Received 4 January 2019|Accepted 29 March 2019|Published 2 July 2019
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.
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.
Altitudinal diversity, amphibian species inventory, Panamá
ZooKeys 859: 117–130 (2019)
doi: 10.3897/zookeys.859.32869
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.
Launched to accelerate biodiversity research
A peer-reviewed open-access journal
Daniel Medina et al. / ZooKeys 859: 117–130 (2019)
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)
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).
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-
Highland IUCN
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)
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)
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)
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).
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.
AmphibiaWeb (2018) AmphibiaWeb. University of California, Berkeley. http://amphibiaweb.
org [Accessed 17 September 2018]
Angher GR, Christian DG (2000) Distributional records from the highlands of the Serranía
de Majé, an isolated mountain range in eastern Panamá. Bulletin-British Ornithologists
Club 120: 173–178.
Batista A, Hertz A, Mebert K, Köhler G, Lotzkat S, Ponce M, Vesely M (2014a) Two new
fringe-limbed frogs of the genus Ecnomiohyla (Anura: Hylidae) from Panamá. Zootaxa
3826: 449–25.
Batista A, Köhler G, Mebert K, Vesely M (2014b) A new species of Bolitoglossa (Amphibia:
Plethodontidae) from eastern Panamá, with comments on other species of the adspersa
species group from eastern Panamá. Mesoamerican Herpetology 1: 97–121. https://doi.
Batista A, Köhler G, Mebert K, Hertz A, Vesely M (2016) An integrative approach to reveal
speciation and species richness in the genus Diasporus (Amphibia: Anura: Eleutherodactyli-
dae) in eastern Panamá. Zoological Journal of the Linnean Society 178: 267–311. https://
Cadena CD, Kozak KH, Gomez JP, Parra JL, McCain CM, Bowie RCK, Carnaval AC, Moritz
C, Rahbek C, Roberts TE, Sanders NJ, Schneider ChJ, VanDerWal J, Zamudio KR, Gra-
ham CH (2011) Latitude, elevational climatic zonation and speciation in New World
vertebrates. Proceedings of the Royal Society B: Biological Sciences 279: 194–201. https://
Daniel Medina et al. / ZooKeys 859: 117–130 (2019)
Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing inci-
dence-based species accumulation curves. Ecology 85(10): 2717–2727. https://doi.
Colwell RK (2006) EstimateS: Statistical Estimation of Species Richness and Shared Species from
Samples (Software and User´s Guide), Version 8.0.
Crawford AJ, Ryan MJ, Jaramillo CA (2010a) A new species of Pristimantis (Anura: Strabomanti-
dae) from the Pacic Coast of the Darien Province, Panamá, with a molecular analysis of its
phylogenetic position. Herpetologica 66: 192–206.
Crawford AJ, Lips KR, Bermingham E (2010b) Epidemic disease decimates amphibian abun-
dance, species diversity, and evolutionary history in the highlands of Central Panamá.
Proceedings of the National Academy of Sciences USA 107: 13777–13782. https://doi.
Duque-Caro H (1990) e Choco Block in the northwestern corner of South America: struc-
tural, tectonostratigraphic, and paleogeographic implications. Journal of South American
Earth Sciences 3: 71–84.
Holdridge LR (1967) Life Zone Ecology. Tropical Science Center, San Jose, 206 pp.
Hortal J, Borges PAV, Gaspar C (2006) Evaluating the performance of species richness estima-
tors: sensitivity to simple grain size. Journal of Animal Ecology 75: 274–287. https://doi.
Ibáñez R, Arosemena FA, Solís FA, Jaramillo CA (1994) Anbios y reptiles de la Serranía
Piedras-Pacora, Parque Nacional Chagres. Scientia 9: 17–31.
Ibáñez R, Rand AS, Jaramillo CA (1999a) Los Anbios del Monumento Natural Barro Colo-
rado, Parque Nacional Soberanía y Areas Adyacentes / e Amphibians of Barro Colorado
Nature Monument, Soberanía National Park and Adjacent Areas. Editorial Mizrachi &
Pujol, Panamá, 187 pp.[0628:br];2
Ibáñez R, Rand AS, Ryan MJ, Jaramillo CA (1999b) Vocalizaciones de Ranas y Sapos del Mon-
umento Natural Barro Colorado, Parque Nacional Soberanía y Areas Aledañas / Vocaliza-
tions of Frogs and Toads from Barro Colorado Nature Monument, Soberanía National
Park and Adjacent Areas. Compact Disc. Sony Music Entertainment, Costa Rica. https://[0628:br];2
Ibáñez R, Condit R, Angehr G, Aguilar S, García T, Martínez R, Sanjur A, Stallard R, Wright
SJ, Rand AS, Heckadon S (2002) An ecosystem report on the Panama Canal: monitoring
the status of the forest communities and the watershed. Environmental Monitoring and
Assessment 80: 65–95.
Ibáñez R, Crawford AJ (2004) A new species of Eleutherodactylus (Anura: Leptodactylidae)
from the Darién Province, Panamá. Journal of Herpetology 38: 240–243. https://doi.
IGNTG (Instituto Geográco Nacional “Tommy Guardia”) (2007) Atlas Nacional de la
República de Panamá. Novo Art, Panamá, 290 pp.
James TY, Toledo LF, Rödder D, Leite DS, Belasen AM, Betancourt-Román CM, Jenkinson
TS, Lambertini C, Longo AV, Ruggeri J, Collins JP, Burrowes PA, Lips KR, Zamudio KR,
Longcore JE (2015) Disentangling host, pathogen, and environmental determinants of a
recently emerged wildlife disease: lessons from the rst 15 years of amphibian chytridiomy-
cosis research. Ecology and Evolution 5: 4079–4097.
Amphibian diversity in Serranía de Majé, Panamá 129
Jaramillo CA, Wilson LD, Ibáñez R, Jaramillo F (2010) e herpetofauna of Panamá: Distribution
and conservation status. In: Wilson LD, Twonsend JH, Johnson JD (Eds) Conservation of Mes-
oamerican Amphibians and Reptiles. Eagle Mountain Press, Eagle Mountain, Utah, 604–671.
Johnson JD, Mata-Silva V, Wilson LD (2015) A conservation reassessment of the Central
American based on the EVS measure. Amphibian & Reptile Conservation 9: 1–94.
Kilburn VL, Ibáñez R, Sanjur O, Bermingham E, Suraci JP, Green DM (2011) Ubiquity of
the pathogenic chytrid fungus, Batrachochytrium dendrobatidis, in anuran communities in
Panamá. EcoHealth 7: 537–548.
Kozak KH, Wiens JJ (2010) Niche conservatism drives elevational diversity patterns in Appala-
chian salamanders. e American Naturalist 176: 40–54.
Küng D, Bigler L, Davis LR, Gratwicke B, Grith E, Woodhams DC (2014) Stability of micro-
biota facilitated by host immune regulation: informing probiotic strategies to manage am-
phibian disease. PloS One 9(1): e87101–11.
Lips KR (1999) Mass mortality and population declines of anurans at an upland site in western Pan-
amá. Conservation Biology 13: 117–125.
Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Carey C, Livo L, Pessier AP, Collins
JP (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical am-
phibian community. Proceedings of the National Academy of Sciences 103: 3165–3170.
Lips KR (2016) Overview of chytrid emergence and impacts on amphibians. Philosophical Trans-
actions of the Royal Society B 317: 20150465.
Mittermeier RA, Myers N, Gil PR, Mittermeier CG (1999) Hotspots. CEMEX, Mexico City.
Myers CW (1969) e ecological geography of cloud forest in Panamá. American Museum
Novitates 2396: 1–52.
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara
RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) vegan: Communi-
ty Ecology Package. R package version 2.4–3.
Parker T, Carrion J, Samudio R (2004) Environment, biodiversity, water, and tropical for-
est conservation, protection, and management in Panamá: assessment and recommenda-
tions (biodiversity and tropical forestry assessment of the USAID/PANAMÁ Program).
Washington, PA: Chemonics International Inc. Task Order# 824, BIOFOR IQC No.
Pinto-Sánchez NR, Ibáñez R, Madriñán S, Sanjur OI, Bermingham E, Crawford AJ (2012)
e Great American Biotic Interchange in frogs: multiple and early colonization of Central
America by the South American genus Pristimantis (Anura: Craugastoridae). Molecular
Phylogenetics and Evolution 62: 954–972.
R Core Team (2017) R: A language and environment for statistical computing. R Foundation
for Statistical Computing, Vienna, Austria. URL
Rebollar EA, Hughey MC, Harris RN, Domangue RJ, Medina D, Ibáñez R, Belden LK (2014)
e lethal fungus Batrachochytrium dendrobatidis is present in lowland tropical forests of far
eastern Panamá. PLoS ONE 9: e95484–8.
Rodríguez-Brenes S, Rodríguez D, Ibáñez R, Ryan MJ (2016) Spread of amphibian chytrid fun-
gus across lowland populations of Túngara frogs in Panamá. PLoS ONE 11: e0155745–8.
Daniel Medina et al. / ZooKeys 859: 117–130 (2019)
Rueda JV, Castro F, Cortez C (2006) Técnicas para el inventario y muestreo de anbios: Una
compilación. In: Angulo A, Rueda-Almonacid JV, Rodríguez-Mahecha JV, La Marca E
(Eds) Técnicas de Inventario y Monitoreo para los Anbios de la Región Tropical Andina.
Conservación Internacional. Serie Manuales de Campo N°2. Panamericana Formas e Im-
presos SA, Bogotá, 135–171.
Savage JM (2002) e Amphibians and Reptiles of Costa Rica: a Herpetofauna between Two
Continents, between Two Seas. University of Chicago Press, Chicago, 934 pp. https://doi.
Seutin G, White WN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA
analyses. Canadian Journal of Zoology 69: 82–90.
Sosa A, Guerrel J (2013) Riqueza, diversidad, y abundancia de anbios en el bosque nuboso de
Cerro Azul, sector Alto Chagres, Parque Nacional Chagres, Panamá. Tecnociencia 15: 57–75.
e IUCN Red List of reatened Species (2018) Version 2018-1. [Down-
loaded on 23 September 2018]
Vanzolini PE, Heyer WR (1985) e american herpetofauna and the interchange. In: Stehli
FG, Webb SD (Eds) e Great American Biotic Interchange. Plenum Press, New York,
Webb DS (2006) e Great American Biotic Interchange: patterns and processes. Annals of
the Missouri Botanical Garden 93: 245–257.
Whiteld SM, Lips KR, Donnelly MA (2016) Amphibian decline and conservation in Central
America. Copeia 104: 351–379.
Wiens JJ, Graham CH, Moen DS, Smith SA, Reeder TW (2006) Evolutionary and ecologi-
cal causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the
roots of high tropical diversity. e American Naturalist 168: 579–596. https://doi.
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
( 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.
... Furthermore, there is an urgent need to evaluate the exact species composition and status of the amphibians and reptiles of the Cerro Chucantí sky island, because high altitude ectothermic animals are particularly vulnerable to climate change due to their low dispersal ability, a high level of habitat specialization, and fragmented distributions (Davies et al. 2004;Sinervo et al. 2010). A few herpetological studies have been conducted in the Majé Mountains; including the first amphibian diversity study in 2007 by Medina et al. (2019), and some effort focusing on the entire herpetofauna of the Cerro Chucantí by the current authors since 2012 (e.g., Batista et al. 2014b), resulting in one new species of salamander and a snake described for this peak area (Batista et al. 2014a(Batista et al. , 2016b. This article presents the first check list on the herpetofauna of CPNR, including the recently described species and those in anticipation of a formal description. ...
... This confirms the general rule of diversity patterns in the American tropics (Wilson et al. 2010), with decreasing diversity from intermediate elevations where diversity is highest (Whitfield et al. 2016), to higher altitudes where cooler temperatures physiologically restrict ectothermic animals. Medina et al. (2019) suggested that the reduced number of observed species at the highland site on Cerro Chucanti may reflect the absence of streams and ponds, and the reduced patch size of the cloud forest. However, the altitude range at the CPNR was too small to experience large climatic differences, and the area available for the cloud forest (PWF) is very limited, roughly estimated at only 1.8 km 2 above 1,200 m asl (Batista et al. 2016;Medina et al. 2019). ...
... Medina et al. (2019) suggested that the reduced number of observed species at the highland site on Cerro Chucanti may reflect the absence of streams and ponds, and the reduced patch size of the cloud forest. However, the altitude range at the CPNR was too small to experience large climatic differences, and the area available for the cloud forest (PWF) is very limited, roughly estimated at only 1.8 km 2 above 1,200 m asl (Batista et al. 2016;Medina et al. 2019). These factors may possibly dampen the effect of altitudinal zonation due to overlap between the two forest types. ...
Full-text available
Cerro Chucantí in the Darién province is the highest peak in the Majé Mountains, an isolated massif in Eastern Panama. In addition to common herpetological species such as the Terraranas, Pristimantis cruentus, and P. caryophyllaceus, rare species such as Pristimantis moro and Strabomantis bufoniformis occur as well. Recent expeditions to Cerro Chucantí revealed a remarkably rich diversity of 41 amphibian (19% of the total in Panama) and 35 reptile (13% of the total in Panama) species, including new and endemic species such as a salamander, Bolitoglossa chucantiensis, a frog Diasporus majeensis, and a snake, Tantilla berguidoi. Here, an up-to-date summary is presented on the herpetological species observed on this sky island (an isolated mountain habitat with endemic species), including several species without definitive taxonomic allocation, new elevation records, and an analysis of species diversity.
Full-text available
We present the results of herpetological surveys in two adjacent mountains where the EcoMinga Foundation protects the cloud forest in the Upper Rio Pastaza watershed, in the Llanganates Sangay Ecological Corridor in Ecuador. A rapid assessment of the amphibian communities of the study sites reveals a diverse and heterogeneous composition, dominated by terrestrial frogs from the genus Pristimantis . We also identify a cryptic diversity with a significant number of candidate new species. We describe two new species of terrestrial frogs of the genus Pristimantis . Pristimantis maryanneae sp. nov. is characterised by not having tympanum externally visible and having 2–3 subconical tubercles in the upper eyelid; and Pristimantis burtoniorum sp. nov. is characterised by the presence of red colouration in hidden surfaces of the hind-limbs, tubercles on the upper eyelid, interorbital tubercle and a row of rounded tubercles along the snout to the tip and a pale red venter with dark brown mottled pattern. Our samples from the two Reserves do not share species between them, so the proportion of shared species seems to be relatively low. In addition, we highlight the importance of updating the knowledge of amphibians that are restricted to this important conservation region and comment about the threats and composition of the amphibian communities on the eastern slopes of the Upper Rio Pastaza watershed.
Full-text available
Mesoamerica, the area composed of Mexico and Central America, is the third largest of the world’s biodiversity hotspots. The Central American herpetofauna currently consists of 493 species of amphibians and 559 species of crocodylians, squamates, and turtles. In this paper, we use a revised EVS measure to reexamine the conservation status of the native herpetofauna of this region, utilize the General Lineage Concept of Species to recognize species-level taxa, and employ phylogenetic concepts to determine evolutionary relationships among the taxa. Since the publication of Conservation of Mesoamerican Amphibians and Reptiles, in 2010, 92 species of amphibians and squamates have been described, resurrected, or elevated from subspecies to species level, and one species of anuran has been synonymized. The herpetofaunal diversity of Central America is comparable to that of Mexico, an especially significant finding because the land area of Mexico is 3.75 times larger. The number of amphibian species is 1.3 times greater in Central America, whereas the number of species of turtles, crocodylians, and squamates is 1.5 times greater in Mexico. Endemicity also is significant in Central America (65.6% among amphibians, 46.5% among turtles, crocodylians, and squamates), with a combined average of 55.6%. We regard the IUCN system as expensive, time-consuming, tending to fall behind systematic advances, and over-dependent on the Data Deficient and Least Concern categories. Conversely, the EVS measure is economical, can be applied when species are described, is predictive, simple to calculate, and does not “penalize” poorly known species. Our EVS analysis of amphibians demonstrates that on average salamanders are more susceptible to environmental deterioration, followed by caecilians, and anurans. Among the remainder of the herpetofauna, crocodylians are the most susceptible and snakes the least, with turtles and lizards in between. We compared the EVS results for the Central American herpetofauna with those reported for Mexico; the results from those regions show an increase in numbers and percentages from low through medium to high. Arguably, attempting to conserve biodiversity is one of the most important and intransigent issues facing humanity, a situation partially due to humanity’s lack of appreciation for its most serious concerns, and brought about by its anthropocentric focus.
Full-text available
Como ha sido ampliamente divulgado en las revistas científicas y medios de comunicación del orbe, los anfibios enfrentan, en la actualidad, una grave amenaza para su conservación. Esta crisis mundial es el resultado de una sinergia de muchas amenazas que están conspirando contra la supervivencia de uno de los grupos de vertebrados de una forma nunca observada en tiempos modernos. Con este conjunto de situaciones negativas como la creciente pérdida de hábitat, el inclemente uso de pesticidas, el aumento de la radiación ultravioleta, y la peligrosa expansión y patogenicidad de la chitridomicosis, los anfibios en general y muy seguramente otros grupos de especies de nuestra rica biodiversidad tendrán que enfrentar un futuro sombrío. La buena noticia, si hay alguna, es que aún podemos hacer algo, pero requerimos dedicar esfuerzos a adquirir información reciente sobre la situación de conservación de las poblaciones, hacerles seguimiento y obtener de esta manera elementos de juicio para adelantar acciones novedosas y creativas que contrarresten esta crisis de conservación. Igualmente es importante resaltar que la investigación in situ y el trabajo mancomunado de muchos actores debe ser un componente central y clave para desarrollar este nuevo conocimiento. El reto es enorme, máxime si reconocemos y comprendemos que el estar en el epicentro de la biodiversidad convierte a los cinco países andinos en un escenario de máxima vulnerabilidad, pues los impactos de esa aún incomprendida sinergia de amenazas creciente, pueden ser desastrosos sobre nuestros recursos dado que siempre tendremos mucho que perder, pero también mucho que ganar en la medida que establezcamos un frente común para contenerlos. Al igual que el estatus de conservación de las especies de anfibios en los Andes tropicales, nuestro conocimiento sobre la historia natural, niveles poblacionales y usos benéficos está en peligro. Y aunque los científicos lleven muchos años trabajando para incrementar el conocimiento sobre la diversidad de especies y se hayan adelantado los pasos necesarios para identificar algunas de las causas más importantes de la disminución de sus poblaciones, la realidad es que hay aún un enorme desconocimiento sobre aspectos relevantes de la historia natural en general y sobre la identidad de muchas de las especies que habitan en diversas regiones inexploradas o exploradas parcialmente. Todo ello conduce a pensar que el gran número de especies deficientes de datos (DD), casi amenazadas (NT) listadas en la última evaluación global de anfibios de 2004 según los criterios de UICN, pueden modificar sustancialmente e incrementar el número de especies en los niveles de amenaza(CR, EN, VU) que surjan de próximas evaluaciones a nivel nacional o global y probablemente, en la medida que conozcamos más sobre la situación real, se incrementen también tristemente en la categoría de extinta (EX). Esta situación nos señala que las exploraciones de campo deben ser una prioridad para la investigación en el futuro y dentro de ellas las que contribuyan a implementar actividades de monitoreo de las especies identificadas como amenazadas y los inventarios de sitios inexplorados. Con esta gran preocupación en mente este manual recoge la experiencia de varios investigadores quienes han dedicado buena parte de su vida profesional al desarrollo de técnicas de seguimiento y a la ardua tarea de ponerlas en prueba por largos periodos para ver sus bondades en los resultados generados. De la misma manera estas experiencias se han puesto en práctica en los tres cursos de campo sobre inventario y monitoreo de anfibios desarrollados por la Iniciativa Atelopus de Conservación Internacional y la Iniciativa Darwin en Perú, Venezuela y Bolivia. El resultado final de este proceso de depuración es el producto que hoy se presenta a la comunidad académica y en general a todos aquellos interesados en los anfibios. Igualmente este manual representa una pequeña pero estratégica parte del esfuerzo global para enfrentar las disminuciones y extinciones como se menciona en el Plan para la Conservación de los Anfibios (ACAP), documento desarrollado durante la Cumbre de la Conservación de los Anfibios que se reunió en Washington, D.C. en septiembre de 2005, y que es la guía para las acciones de conservación de los anfibios que se implementen, a nivel global, durante los próximos años. Esperamos que al promover la investigación con iniciativas como ésta, podamos incrementar nuestro conocimiento
Full-text available
Chytridiomycosis is an emerging infectious disease of amphibians that affects over 700 species on all continents where amphibians occur. The amphibian–chytridiomycosis system is complex, and the response of any amphibian species to chytrid depends on many aspects of the ecology and evolutionary history of the amphibian, the genotype and phenotype of the fungus, and how the biological and physical environment can mediate that interaction. Impacts of chytridiomycosis on amphibians are varied; some species have been driven extinct, populations of others have declined severely, whereas still others have not obviously declined. Understanding patterns and mechanisms of amphibian responses to chytrids is critical for conservation and management. Robust estimates of population numbers are needed to identify species at risk, prioritize taxa for conservation actions, design management strategies for managing populations and species, and to develop effective measures to reduce impacts of chytrids on amphibians. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.
Full-text available
Central America hosts a diverse, unique, and imperiled amphibian fauna, and for decades Central America been a major epicenter of research into amphibian decline and conservation. In this critical and quantitative review, we synthesize current knowledge regarding amphibian decline and conservation in the seven countries that constitute Central America. There are 495 currently recognized amphibian species known from the region, distributed among the three extant orders, 16 families, and 69 genera—though description of new species continues to occur at a rapid pace. Central America's amphibian fauna is unique: 251 species are restricted to the region, and amphibian diversity varies among the major biogeographic provinces and climatic zones found in Central America. We use data generated by the International Union for the Conservation of Nature (IUCN) to evaluate trends in extinction risk among Central American amphibians. As of 2014, there are 207 amphibian species considered threatened by the IUCN, and threat status varies according to taxonomic groupings, biogeographical association, elevation, and life history variables. Major threats to Central American amphibians include both conventional threats (habitat modification, habitat fragmentation, overharvesting, and invasive species) as well as emerging threats that operate on large spatial scales (pollution, emerging infectious diseases, UV-B radiation, and climate change). We conducted a quantitative literature review to document conservation research and to show trends in research activity. While the number of published studies on amphibian conservation increases each year, there are pronounced biogeographic biases in the distribution of published research, and most research is conducted by scientists at institutions outside of Central America with limited involvement of host-nation biologists in amphibian research. We synthesize empirical studies of conservation impacts to amphibians in Central America from habitat modification and fragmentation, overharvesting, invasive species, pollution, UV-B radiation, chytridiomycosis and other amphibian pathogens, climate change, and synergistic interactions among these threats. Much research in the past decade has focused on chytridiomycosis and the amphibian chytrid fungus (Batrachochytrium dendrobatidis), with far fewer studies on habitat modification, other amphibian pathogens, or climate change impacts to amphibians. We describe ongoing conservation actions for amphibians in the region, including monitoring, protected areas, captive assurance programs, protection of relict populations, reintroductions, and development of in-country capacity for research and conservation programs. We conclude with a list of priorities in research and conservation action for amphibians in the region.
Full-text available
Chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), is an emergent infectious disease partially responsible for worldwide amphibian population declines. The spread of Bd along highland habitats (> 500 meters above sea level, m a.s.l.) of Costa Rica and Panamá is well documented and has been linked to amphibian population collapses. In contrast, data are scarce on the prevalence and dispersal of Bd in lowland habitats where amphibians may be infected but asymptomatic. Here we describe the spread (2009 to 2014) of Bd across lowland habitats east of the Panamá Canal (< 500 m a.s.l.) with a focus on the Túngara frog (Physalaemus [Engystomops] pustulosus), one of the most common and abundant frog species in this region. Highland populations in western Panamá were already infected with Bd at the start of the study, which was consistent with previous studies indicating that Bd is enzootic in this region. In central Panamá, we collected the first positive samples in 2010, and by 2014, we detected Bd from remote sites in eastern Panamá (Darién National Park). We discuss the importance of studying Bd in lowland species, which may serve as potential reservoirs and agents of dispersal of Bd to highland species that are more susceptible to chytridiomycosis.
Why are there more species in the tropics than in temperate regions? In recent years, this long‐standing question has been addressed primarily by seeking environmental correlates of diversity. But to understand the ultimate causes of diversity patterns, we must also examine the evolutionary and biogeographic processes that directly change species numbers (i.e., speciation, extinction, and dispersal). With this perspective, we dissect the latitudinal diversity gradient in hylid frogs. We reconstruct a phylogeny for 124 hylid species, estimate divergence times and diversification rates for major clades, reconstruct biogeographic changes, and use ecological niche modeling to identify climatic variables that potentially limit dispersal. We find that hylids originated in tropical South America and spread to temperate regions only recently (leaving limited time for speciation). There is a strong relationship between the species richness of each region and when that region was colonized but not between the latitudinal positions of clades and their rates of diversification. Temperature seasonality seemingly limits dispersal of many tropical clades into temperate regions and shows significant phylogenetic conservatism. Overall, our study illustrates how two general principles (niche conservatism and the time‐for‐speciation effect) may help explain the latitudinal diversity gradient as well as many other diversity patterns across taxa and regions.
We have applied an integrative taxonomic approach, including bioacoustics, ecology, morphology, and molecular genetics (barcoding and phylogeography), to explore species richness in the genus Diasporus in eastern Panama, from where only Diasporus quidditus (Lynch, 2001) was previously known. During fieldwork in eastern Panama in 2011 and 2012 we found six additional species, four of which we are describing here as new to science, plus two species that are new for this region. We have evaluated the presence of Diasporus diastema (Cope, 1875) in eastern Panama by comparing morphological, genetic, and bioacoustic characters of specimens from near the type locality in central Panama with specimens from eastern Panama. We further describe and compare male advertisement calls of most Diasporus species. The phylogeographic analysis suggests the allopatric speciation of Diasporus species in eastern Panama following the completion of the Panamanian isthmus in the middle Miocene. Subsequent geological events concur with the vicariant evolution of different lineages in situ, suggesting eastern Panama to be a centre of endemism for this group of frogs. We present an integrative analysis of the species from eastern Panama and include an identification key for all species of the genus.