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On the distribution and conservation of two “Lost World” tepui summit endemic frogs, Stefania ginesi Rivero, 1968 and S. satelles Señaris, Ayarzagüena, and Gorzula, 1997


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It has been suggested that the inability to migrate in response to climate change is a key threat to tepui summit biota. Tepui summit organisms might thus seriously be threatened by global warming, and there is an urgent need to accurately evaluate their taxonomic status and distributions. We investigated phylogenetic relationships among several populations of Stefania ginesi and S. satelles, two endemic species reported from some isolated tepui summits, and we examined their IUCN conservation status. Molecular phylogenetic analysis and preliminary morphological assessment indicate that both species are actually restricted to single tepui summits and that five candidate species are involved under these names. We advocate upgrading the conservation status of S. ginesi from Least Concern to Endangered, and that of S. satelles from Near Threatened to Endangered.
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Amphib. Reptile Conserv. April 2016 | Volume 10 | Number 1 | e115
Amphibian & Reptile Conservation
10(1) [Special Section]: 5–12 (e115).
On the distribution and conservation of two “Lost World”
tepui summit endemic frogs, Stefania ginesi Rivero, 1968 and
S. satelles Señaris, Ayarzagüena, and Gorzula, 1997
1,3Philippe J. R. Kok, 1,4Valerio G. Russo, 1,5Sebastian Ratz, and 2,6Fabien Aubret
1Amphibian Evolution Lab, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, BELGIUM 2Station d’Ecologie Expérimentale du CNRS à
Moulis, USR 2936, 09200 Moulis, FRANCE
Abstract.—It has been suggested that the inability to migrate in response to climate change is a key
threat to tepui summit biota. Tepui summit organisms might thus seriously be threatened by global
warming, and there is an urgent need to accurately evaluate their taxonomic status and distributions.
We investigated phylogenetic relationships among several populations of Stefania ginesi and
S. satelles, two endemic species reported from some isolated tepui summits, and we examined
their IUCN conservation status. Molecular phylogenetic analysis and preliminary morphological
assessment indicate that both species are actually restricted to single tepui summits and that ve
candidate species are involved under these names. We advocate upgrading the conservation status
of S. ginesi from Least Concern to Endangered, and that of S. satelles from Near Threatened to
Key words. Endangered species, Hemiphractidae, IUCN, molecular phylogenetics, molecular taxonomy, Venezuela
Citation: Kok PJR, Russo VG, Ratz S, Aubret F. 2016. On the distribution and conservation of two “Lost World” tepui summit endemic frogs, Stefania
ginesi Rivero, 1968 and S. satelles Señaris, Ayarzagüena, and Gorzula, 1997. Amphibian & Reptile Conservation 10(1): 5–12 (e115).
Copyright: © 2016 Kok et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-
NoDerivatives 4.0 International License, which permits unrestricted use for non-commercial and education purposes only, in any medium, provided
the original author and the o󰀩cial and authorized publication sources are recognized and properly credited. The o󰀩cial and authorized publication
credit sources, which will be duly enforced, are as follows: o󰀩cial journal title Amphibian & Reptile Conservation; o󰀩cial journal website <amphibian->.
Received: 08 March 2016; Accepted: 29 March 2016; Published: 12 April 2016
Correspondence. Email: (Corresponding author);;;
O󰀩cial journal website:
The frog genus Stefania (Hemiphractidae) is endemic
to an iconic South American biogeographical region
named “Pantepui” (Mayr and Phelps 1967; McDiarmid
and Donnelly 2005) (Fig. 1). Pantepui, often referred to
as the “Lost World” because of Arthur Conan Doyle’s
famous novel (1912), lies in the western Guiana Shield.
The region harbors numerous isolated Precambrian
sandstone tabletop mountains more formally known as
“tepuis” (Fig. 2). Although Pantepui was initially re-
stricted to tepui slopes and summits above 1,500 m el-
evation (Mayr and Phelps 1967; Rull and Nogué 2007),
Steyermark (1982), followed by Kok et al. (2012) and
Kok (2013a), expanded the original denition of Pan-
tepui to include the intervening Pantepui lowlands (200-
400 m asl) and uplands (400-ca. 1,200 m asl) in order
to better reect the biogeography and biotic interactions
in the area (Kok 2013a). The genus Stefania currently
includes 19 species, 15 of which are restricted to tepui
slopes or summits (Duellman 2015; Frost 2015). Stefa-
nia species are direct-developers (eggs and juveniles car-
ried on the back of the mother) and occupy various types
of habitats from lowland rainforest to tepui bogs (Kok
2013a; Schmid et al. 2013; Duellman 2015). The genus
Stefania was erected by Rivero (1968) to accommodate
Cryptobatrachus evansi and a few related new species all
morphologically divergent from other Cryptobatrachus.
Shortly later, Rivero (1970) recognized two species-
groups within Stefania: the evansi group including spe-
cies having the head longer than broad and found in the
lowlands and uplands of Pantepui, and the goini group
including species having the head broader than long and
found in the highlands of Pantepui. Kok et al. (2012),
followed by Castroviejo et al. (2015), showed that, based
on molecular data, these groups are actually not recip-
rocally monophyletic. A complete molecular phyloge-
netic analysis of the genus Stefania is still lacking, and
6Amphib. Reptile Conserv. April 2016 | Volume 10 | Number 1 | e115
Kok et al.
relationships between many species or populations are
unknown. Likewise, the exact distribution of some tepui
summit species is uncertain (e.g., Gorzula and Señaris
1999). Among these, two tepui summit endemic Stefania
species are known from several isolated tepui summits:
Stefania ginesi Rivero, 1968, which is reported from six
tepuis in the Chimantá massif (Chimantá-tepui, Amurí-
tepui, Abakapá-tepui, Churí-tepui, Akopán-tepui, and
Murei-tepui; Señaris et al. 1997; Gorzula and Señaris
1999; Barrio-Amorós and Fuentes 2012; Fig. 1), and Ste-
fania satelles Señaris, Ayarzagüena, and Gorzula, 1997,
which has a highly disjunct distribution, being reported
from Aprada-tepui (in the Aprada Massif), Angasima-
tepui, and Upuigma-tepui (two southern outliers of the
Chimantá massif), and from Murisipán-tepui and Ka-
markawarai-tepui (in the Los Testigos Massif, north of
the Chimantá massif) (Señaris et al. 1997; Gorzula and
Señaris 1999; Fig. 1). Stefania ginesi is listed as Least
Concern (LC) by the International Union for Conserva-
tion of Nature (IUCN) (Stuart et al. 2008) and S. satelles
is listed as Near Threatened (NT) (Stuart et al. 2008).
However, preliminary data suggest that their respec-
tive distributions could be more restricted than initially
thought because more than two species could be involved
under these names (the authors, unpublished; see also Se-
ñaris et al. 2014 regarding the distribution of S. ginesi).
Herein we used molecular phylogenetics to investigate
the relationships among three populations of S. ginesi and
four populations of S. satelles. We also aim at providing
a more precise distribution of these two taxa in order to
rene their conservation status. Indeed, tepui ecosystems
are reported as particularly sensitive to global warming
(Nogué et al. 2009), and tepui summit organisms might
be seriously threatened by habitat loss due to upward
displacement (Rull and Vegas-Vilarrúbia 2006; see also
below). Likewise, climate envelope distribution models
of tepui ecosystems based on future scenarios show that
potential distributions become drastically smaller under
global warming (Rödder et al. 2010). Species restricted
to tepui summits are thus clearly at risk of extinction, and
there is an urgent need to evaluate their exact taxonomic
status and precise distribution.
Materials and Methods
Tissue sampling and molecular data
We combined available GenBank sequences of Stefania
ginesi and S. satelles for fragments of the mitochondrial
16SrRNA gene (16S) and the protein-coding mitochon-
drial gene NADH hydrogenase subunit 1 (ND1) with 40
novel DNA sequences of Stefania ginesi and S. satelles:
nine of fragments of 16S, ve of ND1, 13 of the nuclear
recombination activating gene 1 (RAG1), and 13 of the
nuclear CXC chemokine receptor type 4 gene (CXCR4).
We combined this dataset with DNA sequences of four
additional members of the genus Stefania from out-
side the studied area (three species from east of the Río
Caroní: S. scalae, an upland species, S. riveroi and S.
schuberti, two highland species; and one highland spe-
Fig. 1. Left: Map of Pantepui and its location within South America (inset); the thick blue line indicates the Río Caroní. Right: Map
of the area under study showing localities mentioned in the text (yellow dots represent known localities of occurrence of Stefania
satelles, white dots represent known localities of occurrence of Stefania ginesi). Numbers indicate sampled localities and Roman
numerals indicate unsampled localities, as follows: (1) Aprada-tepui, Venezuela; (2) Murisipán-tepui, Venezuela; (3) Upuigma-
tepui, Venezuela; (4) Angasima-tepui, Venezuela; (5) Abakapá-tepui, Venezuela; (6) Chimantá-tepui, Venezuela; (7) Amurí-tepui,
Venezuela; (i) Kamarkawarai-tepui, Venezuela; (ii) Murei-tepui, Venezuela; (iii) Churí-tepui, Venezuela; (iv) Akopán-tepui, Ven-
7Amphib. Reptile Conserv. April 2016 | Volume 10 | Number 1 | e115
“Lost World” tepui summit endemic frogs, Stefania ginesi and S. satelles
cies from west of the Río Caroní: S. riae; in total 16 novel
sequences), and with Fritziana ohausi, member of the
clade sister to Stefania (Castroviejo et al. 2015), which
was selected as outgroup (see Table 1). Novel sequences
have been catalogued in GenBank under the accession
numbers KU958582-958637.
Total genomic DNA was extracted and puried using
the Qiagen DNeasy® Tissue Kit following manufactur-
er’s instructions. Fragments of 16S (ca. 550 base pairs
[bp]), of ND1 (ca. 650 bp), and of RAG1 (ca. 550 bp)
and CXCR4 (ca. 625 bp) were amplied and sequenced
using the primers listed in Kok et al. (2012) and Biju and
Bossuyt (2003) under previously described PCR condi-
tions (Biju and Bossuyt 2003; Roelants et al. 2007; Van
Bocxlaer et al. 2010). PCR products were checked on
a 1% agarose gel and were sent to BaseClear (Leiden,
The Netherlands) for purication and sequencing. Chro-
matograms were read using CodonCode Aligner 5.0.2
Fig. 2. Typical Pantepui landscape. Photograph taken on 8th June 2012 from the summit of Upuigma-tepui, showing Angasima-tepui
on the left and Akopán-tepui and Amurí-tepui on the right. Note stretches of savannah mainly caused by anthropogenic res. Photo
Voucher 16S ND1 RAG1 CXCR4 Genus Species Locality Country Coordinates Elevation (m)
IRSNB16724 JQ742191 JQ742362 KU958600 KU958619 Stefania scalae Salto El Danto Venezuela N 5°57’52” W 61°23’31” 1208
Uncatalogued JQ742172 JQ742343 KU958601 KU958620 Stefania riae Sarisariñama-tepui Venezuela N 4°41’ W 64°13’ ca. 1100
IRSNB15703 JQ742177 JQ742348 KU958602 KU958621 Stefania riveroi Yuruaní-tepui Venezuela N 5°18’50” W 60°51’50” 2303
IRSNB15716 JQ742178 JQ742349 KU958603 KU958622 Stefania riveroi Yuruaní-tepui Venezuela N 5°18’50” W 60°51’50” 2303
IRSNB16725 JQ742173 JQ742344 KU958604 KU958623 Stefania “ginesi” Abakapá-tepui Venezuela N 5°11’23” W 62°17’52” 2137
IRSNB16726 JQ742174 JQ742345 KU958605 KU958624 “ginesi” “ginesi” Abakapá-tepui Venezuela N 5°11’07” W 62°17’21” 2209
IRSNB15839 JQ742175 JQ742346 KU958606 KU958625 Stefania “satelles” Angasima-tepui Venezuela N 5°02’36” W 62°04’51” 2122
IRSNB15844 JQ742176 JQ742347 KU958607 KU958626 Stefania “satelles” Angasima-tepui Venezuela N 5°02’36” W 62°04’51” 2122
IRSNB16727 KU958582 KU958593 KU958608 KU958627 Stefania “satelles” Upuigma-tepui Venezuela N 5°05’10” W 61°57’32” 2134
IRSNB16728 KU958583 KU958609 KU958628 Stefania satelles Aprada-tepui Venezuela N 5°24’39” W 62°27’00” 2551
IRSNB16729 KU958584 KU958610 KU958629 Stefania satelles Aprada-tepui Venezuela N 5°24’43” W 62°27’03” 2576
IRSNB16730 KU958585 KU958594 KU958611 KU958630 Stefania “ginesi” Amurí-tepui Venezuela N 5°08’34” W 62°07’08” 2215
IRSNB16731 KU958586 KU958595 KU958612 KU958631 Stefania “ginesi” Amurí-tepui Venezuela N 5°08’35” W 62°07’08” 2213
IRSNB16732 KU958587 KU958596 KU958613 KU958632 Stefania schuberti Auyán-tepui Venezuela N 5°45’56” W 62°32’25” 2279
IRSNB16733 KU958588 KU958597 KU958614 KU958633 Stefania schuberti Auyán-tepui Venezuela N 5°45’56” W 62°32’25” 2279
IRSNB16734 KU958589 KU958598 KU958615 KU958634 Stefania “satelles” Murisipán-tepui Venezuela N 5°52’03” W 62°04’30” 2419
IRSNB16735 KU958590 KU958599 KU958616 KU958635 Stefania “satelles” Murisipán-tepui Venezuela N 5°52’03” W 62°04’30” 2419
IRSNB16736 KU958591 KU958617 KU958636 Stefania ginesi Chimantá-tepui Venezuela N 5°19’12” W 62°12’07” 2180
IRSNB16737 KU958592 KU958618 KU958637 Stefania ginesi Chimantá-tepui Venezuela N 5°19’12” W 62°12’07” 2180
MZUSP139225 JN157635 KC844945 KC844991 Fritziana ohausi n/a Brazil n/a n/a
Table 1. List of Stefania taxa and outgroup used in this study, with localities and GenBank accession numbers. Sequences newly
generated are in boldface. IRSNB = Institut Royal des Sciences Naturelles de Belgique, Belgium; MZUSP = Museu de Zoologia,
Universidade de São Paulo, Brazil.
8Amphib. Reptile Conserv. April 2016 | Volume 10 | Number 1 | e115
Kok et al.
( and a consensus
sequence was assembled from the forward and reverse
primer sequences. MAFFT version 7 (http://mat.cbrc.
jp/alignment/server/) was used to perform preliminary
alignment using G-INS-i and default parameters. Mi-
nor alignment corrections were made using MacClade
4.08 (Maddison and Maddison 2005). Protein-coding
sequences were translated into amino-acid sequences to
check for unexpected stop codons. Alignment-ambiguous
regions of 16S were excluded from subsequent analyses.
Molecular phylogenetic analyses
The combined 16S + ND1 + RAG1 + CXCR4 dataset
(totalling 2,359 bp after exclusion) was subjected to phy-
logenetic inference using Bayesian analyses. Optimal
partitioning schemes were estimated with PartitionFinder
v1.1.1 (Lanfear et al. 2012) using the “greedy” algorithm,
the “mrbayes” set of models, and the Bayesian Informa-
tion Criterion (BIC) to compare the t of dierent mod-
els. Bayesian posterior probabilities (PP) were used to
estimate clade credibility in MrBayes 3.2.2 (Ronquist et
al. 2012) on the CIPRES Science Gateway V 3.3 (https://, Miller et al. 2010). The Bayesian analy-
ses implemented the best substitution models inferred by
PartitionFinder v1.1.1 partitioned over the dierent gene
fragments, at Dirichlet priors for base frequencies and
substitution rate matrices and uniform priors for among-
site rate parameters. Four parallel Markov chain Monte
Carlo (MCMC) runs of four incrementally heated (tem-
perature parameter = 0.2) chains were performed, with a
length of 20,000,000 generations, a sampling frequency
of 1 per 1,000 generations, and a burn-in correspond-
ing to the rst 1,000,000 generations. Convergence of
the parallel runs was conrmed by split frequency SDs
(<0.01) and potential scale reduction factors (~1.0) for
all model parameters, as reported by MrBayes. All analy-
ses were checked for convergence by plotting the log-
likelihood values against generation time for each run,
using Tracer 1.5 (Rambaut and Drummond 2009). Eec-
tive sample sizes (ESS) largely over 200 were obtained
for every parameter. Results were visualized and edited
in FigTree 1.4.1 (Rambaut 2014).
Stefania ginesi and S. satelles as currently recognized
are recovered non-reciprocally monophyletic (Fig. 3).
Our molecular phylogeny also reveals the occurrence of
ve candidate species (sensu Padial et al. 2010) that have
been misidentied for more than a decade as S. ginesi
(two candidate species) or S. satelles (three candidate
species) (e.g., Señaris et al. 1997; Gorzula and Señaris
1999). Preliminary morphological analyses (in progress)
indicate a few, sometimes subtle, morphological charac-
ters allowing discrimination among these candidate spe-
Fig. 3. Phylogenetic relationships as recovered in the MrBayes analysis (concatenated dataset, 2359 bp), outgroup not shown.
Values at each node represent Bayesian posterior probabilities; asterisks indicate values > 95%. Stefania ginesi sensu stricto, and
S. satelles sensu stricto are highlighted in red. Relation between eye color and tepui summit surface is indicated on the right side of
the gure. Photos PJRK.
9Amphib. Reptile Conserv. April 2016 | Volume 10 | Number 1 | e115
“Lost World” tepui summit endemic frogs, Stefania ginesi and S. satelles
cies and S. ginesi and S. satelles. Our combined results
indicate that S. ginesi sensu stricto is likely restricted to
its type locality, Chimantá-tepui, as we suspect that pop-
ulations from other tepuis in the Chimantá Massif that
were not sampled in this study will prove to be distinct as
well. As for Stefania satelles, the species is restricted to
its type locality, Aprada-tepui.
Discussion and conservation recommendations
We assumed that misidentications were likely due
to a rather conserved external morphology (e.g., head
broader than long, skin strongly granular, absence of
prominent cranial crests) of all tepui summit species pre-
viously identied as Stefania ginesi or S. satelles. This
conserved morphology appears to be symplesiomorphic,
and probably the result of an allopatric non-adaptive ra-
diation (lineage diversication with minimal ecological
diversication, see Rundell and Price 2009). It is, how-
ever, intriguing that two slightly divergent phenotypes (a
satelles phenotype” with brown eyes and a “ginesi phe-
notype” with blue eyes) evolved independently in each
subclade (see Fig. 3). Interestingly, selection towards one
of these two phenotypes seems closely associated with
the size of the summit surface on which the species occur
(see Fig. 3). The “ginesi phenotype” is found on large
tepui summits (surface > 25 km2) in the central Chimantá
Massif, whereas the “satelles phenotype” is found on
much smaller tepui summits (surface < 5 km2) in the pe-
riphery of the core Chimantá Massif. Disentangling this
phenomenon and the nature of the ecological constraints
possibly involved and their inuence on phenotypic tra-
jectories is beyond the scope of this paper and will be
treated in a separate study.
Most importantly, our results have direct implica-
tions on the conservation status of the populations un-
der study. A complete taxonomic revision of the genus
is in progress, but meanwhile we wish to emphasize the
restricted distributions of all the populations previously
known as Stefania ginesi or S. satelles. Our results argue
for the upgrading of the conservation status of S. gine-
si from LC to Endangered (EN), and that of S. satelles
from NT to EN, based on the same argument recently
developed for other species restricted to the summit of
one or two tepuis, e.g., Pristimantis imthurni and P. jam-
escameroni (Kok 2013b), or P. aureoventris (IUCN SSC
Amphibian Specialist Group 2014), thus in accordance
with criteria B1 a-b (iii) and B2 a-b (iii) of the IUCN
Red List of Threatened Species (IUCN 2014). We indeed
argue that (1) extents of occurrence of S. ginesi and S.
satelles are much less than 5,000 km2 (less than 100 km2
and ve km2, respectively); (2) areas of occupancy of S.
ginesi and S. satelles are much less than 500 km2 (less
than 100 km2 and ve km2, respectively); (3) there is an
inferred and projected decline in the quality of habitat
due to the eects of global warming upon tepui ecosys-
tems, with an expected 2–4 °C increase in temperature
in the region through the next century (IPCC 2007). As
stressed by Nogué et al. (2009) and Rödder et al. (2010),
this rise in temperature will likely cause a decrease in
habitat suitability for tepui biota. In addition, numerous
anthropogenic res in the region (Means 1995; Rull et al.
2013, 2016), coupled with a global rise of temperature,
may cause an up to 10% decrease in precipitation (IPCC
2007) instigating an increase in re range and intensity
(Rull et al. 2013, 2016); and (4) the altitudinal range of
Stefania ginesi and S. satelles allows no vertical migra-
tion in order to avoid these threats. As mentioned by Rull
and Vegas-Vilarrúbia (2006), the inability to migrate to
compensate for the climate change is a key threat to tepui
summit biota.
There is an urgent need to gain a greater understand-
ing of species boundaries and distributions in Pantepui,
especially in Venezuela where the threats are the highest
due to ongoing uncontrolled anthropogenic res (Rull
et al. 2013, 2016). However, it is assumed that an even
greater threat to Pantepui biota is global climate change.
Local actions (such as stopping res), even if necessary,
might only have a limited impact on the long-term sur-
vival of Pantepui organisms. Conservation awareness is
critically important in the area, notably due to the inac-
cessibility of tepui ecosystems where an out of sight, out
of mind eect may have taken place.
This study adds to the many studies now available
demonstrating that estimates of amphibian diversity
based on morphology alone are often misleading. Molec-
ular data have indeed been shown to be of great help in
detecting cryptic species (e.g., Hebert et al. 2004; Vences
et al. 2005; Fouquet et al. 2007; Burns et al. 2008; Fou-
quet et al. 2016). Unfortunately, while everyone seems to
agree that gaining a greater understanding of the world
biodiversity is needed in order to prioritize biodiversity
conservation (e.g., Wilson 2016), the task turns more and
more often into a bureaucratic obstacle course, if not an
impossible mission for scientists working with molecular
Acknowledgments.—PJRK’s work is supported by
a postdoctoral fellowship from the Fonds voor Weten-
schappelijk Onderzoek Vlaanderen (FWO12A7614N).
Many thanks are due to C.L. Barrio-Amorós (Doc Frog
Expeditions, Costa Rica) and C. Brewer-Carías (Caracas,
Venezuela) for the loan of tissue samples. C. Brewer-
Carías also provided invaluable advice and help with lo-
gistics in Venezuela.
Literature Cited
Barrio-Amorós CL, Fuentes O. 2012. The herpetofauna
of the Lost World. Pp 140–151 In: Venezuelan Tepuis,
Their Caves and Biota. Editors, Aubrecht R, Barrio-
Amorós CL, Breure ASH, Brewer-Carías C, Derka T,
Fuentes-Ramos OA, Gregor M, Kodada J, Kováčik Ľ,
Lánczos T, Lee NM, Liščák P, Schlögl J, Šmída B,
10Amphib. Reptile Conserv. April 2016 | Volume 10 | Number 1 | e115
Kok et al.
Vlček L. Comenius University, Bratislava, Slovakia.
168 p.
Biju SD, Bossuyt F. 2003. New frog family from India
reveals an ancient biogeographical link with the Sey-
chelles. Nature 425: 711–714.
Burns JM, Janzen DH, Hajibabaei M, Hallwachs W, He-
bert PDN. 2008. DNA barcodes and cryptic species of
skipper butteries in the genus Perichares in Area de
Conservación Guanacaste, Costa Rica. Proceedings
of the National Academy of Sciences of the United
States of America 105: 6,350–6,355.
Castroviejo-Fisher S, Padial JM, De la Riva I, Pombal Jr
JP, da Silva HR, Rojas-Runjaic FJM, Medina-Méndez
E, Frost DR. 2015. Phylogenetic systematics of egg-
brooding frogs (Anura: Hemiphractidae) and the evo-
lution of direct development. Zootaxa 4004: 1–75.
Doyle AC. 1912. The Lost World. Hodder & Stoughton,
London, United Kingdom. 309 p.
Duellman WE. 2015. Marsupial Frogs. Gastrotheca &
Allied Genera. Johns Hopkins University Press, Balti-
more, Maryland, USA. 432 p.
Fouquet A, Gilles A, Vences M, Marty C, Blanc M, Gem-
mell NJ. 2007. Underestimation of species richness
in Neotropical frogs revealed by mtDNA analyses.
PLOS One 2: e1109.
Fouquet A, Martinez Q, Zeidler L, Courtois EA, Gaucher
P, Blanc M, Lima JD, Marques Souza S, Rodrigues
MT, Kok PJR. 2016. Cryptic diversity in the Hypsi-
boas semilineatus species group (Amphibia, Anura)
with the description of a new species from the eastern
Guiana Shield. Zootaxa 4084: 79–104
Frost DR. 2015. Amphibian Species of the World: An on-
line reference. Version 6.0. Available: http://research. [Ac-
cessed 01 October 2015].
Gorzula S, Señaris JC. 1999 “1998.” Contribution to the
herpetofauna of the Venezuelan Guayana. I. A data
base. Scientia Guaianae 8: 1–269.
Hebert PDN, Penton EH, Burns JM, Janzen DH, Hall-
wachs W. 2004. Ten species in one: DNA barcoding
reveals cryptic species in the neotropical skipper but-
tery Astraptes fulgerator. Proceedings of the Na-
tional Academy of Sciences of the United States of
America 101: 14,812–14,817.
IPCC. 2007. Climate Change 2007: Synthesis Report.
Contribution of Working Groups I, II and III to the
Fourth Assessment Report of the Intergovernmen-
tal Panel on Climate Change. Core Writing Team,
Pachauri RK and Reisinger A (Editors). IPCC, Ge-
neva, Switzerland. 104 p.
IUCN. 2014. Guidelines for using the IUCN Red List
Categories and Criteria. Version 11. Available: http://
pdf [Accessed 01 October 2015].
IUCN SSC Amphibian Specialist Group. 2014. Pristi-
mantis aureoventris. The IUCN Red List of Threat-
ened Species 2014: e.T46086220A46086224. Avail-
RLTS.T46086220A46086224.en. [Accessed 01 Oc-
tober 2015].
Kok PJR. 2013a. Islands in the Sky: Species Diversity,
Evolutionary History, and Patterns of Endemism
of the Pantepui Herpetofauna. Ph.D. Dissertation,
Leiden University, The Netherlands. 305 p.
Kok PJR. 2013b. Two new charismatic Pristimantis spe-
cies (Anura: Craugastoridae) from the tepuis of “The
Lost World” (Pantepui region, South America). Euro-
pean Journal of Taxonomy 60: 1–24.
Kok PJR, MacCulloch RD, Means DB, Roelants K, Van
Bocxlaer I, Bossuyt F. 2012. Low genetic diversity in
tepui summit vertebrates. Current Biology 22: R589–
Lanfear R, Calcott B, Ho SY, Guindon S. 2012. Partition-
Finder: Combined selection of partitioning schemes
and substitution models for phylogenetic analyses.
Molecular Biology 29: 1,695–1,701.
Maddison DR, Maddison WP. 2005. MacClade 4 v. 4.08
for OSX. Sinauer Associates, Sunderland, Massachu-
setts, USA.
Mayr E, Phelps WH. 1967. The origin of the bird fauna
of the south Venezuelan highlands. Bulletin of the
American Museum of Natural History 136: 269–328.
McDiarmid RW, Donnelly MA. 2005. The herpetofauna
of the Guayana highlands: amphibians and reptiles of
the Lost World. Pp. 461–560 In: Ecology and Evo-
lution in the Tropics: A Herpetological Perspective.
Editors, Donnelly MA, Crother BI, Guyer C, Wake
MH, White ME. University of Chicago Press, Chi-
cago, USA. 584 p.
Means DB. 1995. Fire ecology of the Guayana Region,
Northeastern South America. Pp. 61–77 In: Fire in
Wetlands: A Management Perspective. Proceedings
of the Tall Timbers Fire Ecology Conference 19. Tall
Timbers Research Station. Tallahassee, Florida, USA.
175 p.
Miller MA, Pfeier W, Schwartz T. 2010. Creating the
CIPRES Science Gateway for inference of large phy-
logenetic trees. Proceedings of the Gateway Comput-
ing Environments Workshop (GCE): 1–8. New Or-
leans, Louisiana, USA. 115 p.
Nogué S, Rull V, Vegas-Vilarrúbia T. 2009. Modeling
biodiversity loss by global warming on Pantepui,
northern South America: Projected upward migration
and potential habitat loss. Climatic Change 94: 77–85.
Padial JM, Miralles A, De la Riva I, Vences M. 2010. The
integrative future of taxonomy. Frontiers in Zoology
7: 16.
Rambaut A. 2014. Figtree, a graphical viewer of phylo-
genetic trees. Available:
Rambaut A, Drummond AJ. 2009. Tracer v1.5. Avail-
Rivero JA. 1968 “1966”. Notes on the genus Cryptoba-
trachus (Amphibia, Salientia) with the description of
11Amphib. Reptile Conserv. April 2016 | Volume 10 | Number 1 | e115
“Lost World” tepui summit endemic frogs, Stefania ginesi and S. satelles
a new race and four new species of a new genus of hy-
lid frogs. Caribbean Journal of Science 6: 137–149.
Rivero JA. 1970. On the origin, endemism and distribu-
tion of the genus Stefania Rivero (Amphibia, Salien-
tia) with a description of a new species from south-
eastern Venezuela. Boletín de la Societa Venezolana
de Ciencias Naturales 28: 456–481.
Rödder D, Schlüter A, Lötters S. 2010. Is the “Lost
World” Lost? High Endemism of Aphibians (sic) and
Reptiles on South American Tepuís in a Changing
Climate. Pp. 401–416 In: Relict Species: Phylogeog-
raphy and Conservation Biology. Editors, Habel JC,
Assmann T. Springer Berlin Heidelberg, Germany.
451 p.
Roelants K, Gower DJ, Wilkinson M, Loader SP, Biju
SD, Guillaume K, Moriau L, Bossuyt F. 2007. Global
patterns of diversication in the history of modern
amphibians. Proceedings of the National Academy of
Sciences of the United States of America 104: 887–
Ronquist F, Teslenko M, van der Mark P, Ayres DL,
Darling A, Höhna S, Larget B, Liu L, Suchard MA,
Huelsenbeck JP. 2012. MrBayes 3.2: ecient Bayes-
ian phylogenetic inference and model choice across a
large model space. Systematic Biology 61: 539–542.
Rull V, Vegas-Vilarrúbia T. 2006. Unexpected biodi-
versity loss under global warming in the neotropical
Guayana Highlands. Global Change Biology 12: 1–9.
Rull V, Vegas-Vilarrúbia T, Montoya E. 2016. The neo-
tropical Gran Sabana region: Palaeoecology and con-
servation. The Holocene, In Press.
Rull V, Montoya E, Nogué S, Vegas-Vilarrúbia T, Safont
E. 2013. Ecological palaeoecology in the neotropical
Gran Sabana region: Long-term records of vegetation
dynamics as a basis for ecological hypothesis testing.
Perspectives in Plant Ecology, Evolution and System-
atics 15(2013): 338–359.
Rundell RJ, Price TD. 2009. Adaptive radiation, non-
adaptive radiation, ecological speciation and noneco-
logical speciation. Trends in Ecology and Evolution
24: 394–399.
Schmid M, Steinlein C, Bogart JP, Feichtinger W, Haaf
T, Nanda I, del Pino EM, Duellman WE, Hedges SB.
2013 “2012.” The hemiphractid frogs. Phylogeny,
embryology, life history, and cytogenetics. Cytoge-
netic and Genome Research 13: 69–384.
Señaris JC, Ayarzagüena J, Gorzula S. 1997 “1996.” Re-
visión taxonómica del género Stefania (Anura: Hyli-
dae) en Venezuela con la descripción de cinco nuevas
especies. Publicaciones de la Asociación Amigos de
Doñana 7: 1–57.
Señaris JC, Lampo M, Rojas-Runjaic FJM, Barrio-
Amorós CL. 2014. Guía ilustrada de los anbios del
Parque Nacional Canaima, Venezuela. Altos de Pipe,
Venezuela. 261 p.
Steyermark JA. 1982. Relationships of some Venezu-
elan forest refuges with lowland tropical oras. Pp.
182–220 In: Biological Diversication in the Tropics.
Editor, Prance GT. Columbia University Press, New
York, USA. 714 p.
Stuart SN, Homann M, Chanson JS, Cox NA, Berridge
RJ, Ramani P, Young BE (Editors). 2008. Threatened
Amphibians of the World. Lynx Edicions, Barcelona,
Spain; IUCN, Gland, Switzerland; and Conservation
International, Arlington, Virginia, USA. 758 p.
Van Bocxlaer I, Loader SP, Roelants K, Biju SD, Mene-
gon M, Bossuyt F. 2010. Gradual adaptation toward a
range-expansion phenotype initiated the global radia-
tion of toads. Science 327: 679–682.
Vences M, Thomas M, Bonett RM, Vieites DR. 2005.
Deciphering amphibian diversity through DNA bar-
coding: chances and challenges. Philosophical Trans-
actions of the Royal Society London B 360: 1,859–
Wilson EO. 2016. Half-Earth, Our Planet’s Fight for
Life. Livelight Publishing Corporation, New York,
New York, USA. 272 p.
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Sebastian Ratz has a Bachelor’s degree in biology from the University of Tübingen, Germany. He currently
works on his Master thesis (phylogeography of the genus Oreophrynella) at the Vrije Universiteit Brussel, Bel-
gium. His main interests focus on the diversity and evolution of Neotropical amphibians.
Philippe J.R. Kok is a Belgian evolutionary biologist and herpetologist. He obtained his Ph.D. in biology at the
Leiden University (The Netherlands) in 2013. He is currently postdoctoral researcher at the Vrije Universiteit
Brussel, Belgium, where he teaches Field Herpetology to the second year Master students. His interests are
eclectic, the main ones being the evolution, systematics, taxonomy, biogeography, and conservation of amphib-
ians and reptiles in the Neotropics, more specically from the Guiana Shield. His work now primarily focuses
on vertebrate evolution in the Pantepui region.
Valerio G. Russo is an Italian herpetologist and naturalist mainly interested in Neotropical and Mediterranean
biodiversity. He obtained his Master’s degree in biology in 2015 at the Vrije Universiteit Brussel (VUB), Bel-
gium, with a thesis on the systematics of the frog genus Stefania. He is now collaborating as an independent
researcher with the Biology Department of the VUB.
Fabien Aubret is a French evolutionary biologist and herpetologist. He completed his Doctoral and Post-
doctoral studies between 2001 and 2008 in Australia (University of Western Australia and University of Syd-
ney). Since 2009, he has been working as a full time researcher for the CNRS (National Centre for Scientic
Research) at the Station of Theoretical and Experimental Ecology (SETE, Moulis, France). Fabien’s research
is mostly empirical, with an experimental backbone, and involves a variety of snake and lizard models. His
research is pluri-disciplinary and involves eco-physiology, phenotypic plasticity, climate change, thermoregula-
tion, and reproductive biology.
Kok et al.
... Murisipán-tepui is a small, poorly surveyed sandstone table-top mountain (tepui) located in the Los Testigos Massif in the Bolívar State of Venezuela, ca. 43 km north of the Chimantá Massif Locality data are based on specimens examined (see Appendix S1) and literature records (Señaris et al. 1997, Kok et al. 2016, 2017. Photos Philippe J.R. Kok. , covers a total area of ca. ...
... Previous authors had raised concerns about the identity of the Stefania populations from the Los Testigos Massif, noting a difference in tympanum size compared to S. satelles from the type locality (Señaris et al. 1997, Gorzula & Señaris 1999. Kok et al. (2016Kok et al. ( , 2017 demonstrated that four distinct species are likely confused under that name, all of them seemingly distributed on different tepui summits, with S. satelles being restricted to its type locality (Aprada-tepui, Bolívar State, Venezuela). The population from Murisipántepui was recovered as sister to three undescribed species in a clade that is sister to the clade containing S. ginesi and S. satelles from the type localities (Kok et al. 2016, 2017). ...
... Kok et al. (2016Kok et al. ( , 2017 demonstrated that four distinct species are likely confused under that name, all of them seemingly distributed on different tepui summits, with S. satelles being restricted to its type locality (Aprada-tepui, Bolívar State, Venezuela). The population from Murisipántepui was recovered as sister to three undescribed species in a clade that is sister to the clade containing S. ginesi and S. satelles from the type localities (Kok et al. 2016, 2017). Kok et al. (2017) referred to this undescribed taxon as Stefania sp. 2. Both S. satelles and the morphologically cryptic S. sp. 2 are members of what Kok et al. (2017) named the S. ginesi clade, which also comprises S. ginesi and four additional undescribed species. ...
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Previous molecular analyses of the frog genus Stefania have shown that species boundaries in that group are often difficult to delineate when solely based on morphology. As a consequence, “taxonomically cryptic” species are not uncommon in the genus. Several highland Stefania species remain to be described, some potentially critically endangered due to their highly restricted geographic ranges. One case is the microendemic Stefania population from the summit of Murisipán-tepui, a poorly explored table-top mountain in the Los Testigos Massif, a small tepui mountain range located north to the much larger Chimantá Massif in southern Venezuela. That population, mistaken as S. satelles for two decades, was later reported as Stefania sp. 2 and belongs to the S. ginesi clade. The new species is phylogenetically distinct but phenotypically similar to S. satelles, a taxon restricted to its type-locality, i.e. the summit of Aprada-tepui in Venezuela. The new species is described based on morphology and cranial osteology. Molecular divergences with S. satelles are high (> 8%) in the barcoding fragment of 16S rRNA. Amended definitions for the two other described species in the S. ginesi clade (S. ginesi and S. satelles) are also provided. The new species should be listed as critically endangered according to IUCN criteria
... An ancient clade of Microhylidae frogs in the genera Adelastes, Otophryne, and Synapturanus is distributed mostly across the Guiana Shield, likely originating from Pantepui (Fouquet et al. 2021). At least 21 species of carrying frogs of the family Hemiphractidae in the genus Stefania are exclusively confined to Pantepui and primarily endemic on individual tepuis (Duellman 2015, Kok et al. 2016. In fact, MacCulloch & Lathrop (2002) described "exceptional diversity of Stefanias" on Mt. ...
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We describe three new species of landfrogs, genus Pristimantis, from near the summit of Mt. Kopinang, one of the several high points of the Wokomung Massif, a large horseshoe-shaped tepui (= mesa) in west-central Guyana. Pristimantis koki n. sp. is known from 1,067 to 1,525 m elevation. It is characterized by small-sized adults averaging 12.4 mm SVL (snout-vent length) in males and 18.4 mm in females; a pointed, depressed, elongated snout; lack of an obvious tympanum, vocal slit, or sac; and diagnostically black pigment prominently arranged around the anus fringed by light pigment. When handled, P. koki seems to emit volatile organic compounds and leaves a slightly numbing taste at the base of the human tongue. Pristimantis kopinangae n. sp. is known from three specimens collected at approx. 1,385 m elevation on the Wokomung Massif and two specimens from slightly higher in elevation on Mt. Ayanganna. About the size of most Pristimantis inhabiting the Guyana uplands and highlands (20-30 mm SVL), it is characterized by 2-3 light yellow inguinal flash-mark blotches, short broadly round snout, large eye with a blue iris, white skin of chin and areolate belly with dark brown vermiculations; and absence of a tympanum. Pristimantis kalamandeenae n. sp. is known from three specimens collected on the Wokomung Massif including an amplexing pair at approx. 1,550 m elevation. Similar in size to P. kopinangae, it is characterized by an acuminate snout, black iris, obvious tympanum, and uniform tan pigmentation dorsally after dark that becomes uniformly dark brown in daytime. Phylogenetic results show that P. koki and P. kopinangae are sister species and are members of a larger assemblage of related species endemic to the Pantepui Region within the P. unistrigatus species group. Pristimantis kalamandeenae is not closely related to these species, instead forming a clade with the P. lacrimosus species group. The three new species occur in sympatry with at least five other Pristimantis species on the Wokomung Massif, the greatest known Pristimantis species richness on a single tepui of the Guiana Shield.
... In many cases, the initial recognition of diversity is based on genetic data (commonly based on a single or very few genes), but after closer examination most of the genetic lineages also present conspicuous phenotypic A. Fouquet, K. Leblanc, A.-C. Fabre et al. Zoologischer Anzeiger 293 (2021) 46e73 diagnostic characters (Peloso et al., 2014;Fouquet et al., 2013;Kok et al., 2016;Carvalho et al., 2021). Therefore, it is likely that many new taxa will continue to be discovered through the integrative use of DNA sequences and detailed phenotypic analyses, progressively unveiling the unknown diversity of Amazonian amphibians. ...
The genus Synapturanus includes three nominal species of fossorial Amazonian frogs. A previous study combining molecular, morphological and acoustic data suggested that there may be six times more species than currently recognized. Herein we describe and name three of these new species and compare their osteology. Synapturanus zombie sp. nov. occurs in French Guiana and Amapá (Brazil), S. mesomorphus sp. nov. in Guyana and adjacent Venezuela, and S. ajuricaba sp. nov. in the northern part of the Brazilian states of Amazonas and Pará. These species are readily differentiated from congeners by a combination of external morphological characters such as body size, development of fringes on fingers and coloration, by advertisement call variables, and by osteological traits. Along with osteological reinforcement of the skull, atlas and scapular region, the reduction of the size of phalanges, more developed fringes on fingers, smaller eyes and larger body size, altogether suggest an overall increase of the fossorial habits in the easternmost species. In contrast, the relatively conserved morphology of the posterior part of the body across the genus suggests that fossoriality mostly involves the anterior part. Furthermore, the fusion of tarsal bones in the species of the western clade may indicate locomotory adaptation to more epigean habits.
... ej. Jungfer et al. 2013, Gehara et al. 2014, Kok et al. 2016, Jablonski et al. 2017, que junto a las revisiones de ejemplares en museos y colecciones, y las futuras prospecciones, podrían elevar y probablemente sobrepasar la riqueza anfibia de la región a más de 250 especies. ...
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Resumen: La fauna de anfibios del escudo Guayanés en Venezuela reúne 195 especies de anfibios —189 anuros y seis cecilias—, cifra que representa el 54% de la riqueza total del país, alrededor del 6,6% de la megadiversa fauna anfibia de Suramérica. Un tercio de esta enorme diversidad es endémica de la región, con tres géneros y unas 65 especies exclusivas. Debido a los grandes vacíos de información, se considera que esta diversidad está subestimada, esperándose un incremento sostenido como resultado de nuevas exploraciones a la región y el estudio de las muestras de colecciones nacionales e internacionales. Las formaciones boscosas de la Guayana albergan la mayor riqueza de anfibios; la riqueza disminuye con la elevación pero, en contraste, el grado de endemismo se eleva, de allí que el Pantepui —tierras ≥1500 m s.n.m.— alberguen algo más de la mitad de los taxones exclusivos. La mayoría de las especies características de la región son microendemismos, condición que las categoriza en riesgo de extinción. Actualmente la minería ilegal, y sus consecuencias, es la principal amenaza a las comunidades de anfibios guayaneses; sin embargo, se prevé que el cambio climático pueda ser la mayor amenaza futura. Abstract: The amphibian fauna of the Guiana Shield in Venezuela includes 195 species —189 anurans and six caecilians— representing 54% of the total of the country, and 6.6% of the megadiverse amphibian fauna of South America. One third of this enormous diversity is endemic to the region, with three exclusive genera and 65 species. Due to large gaps in information, this diversity is considered underestimated; an important increase is expected as result of new explorations to the region and the study of samples from national and international collections. The forest formations harbor the greatest richness of amphibians; the diversity diminishes with an increase in elevation, but in contrast, endemism increases, and the Pantepui —lands above 1500 masl— house more than half of the endemic taxa. Most of the species characteristic of the region are microendemics, a condition that automatically categorizes them as threatened because of their small range. Currently deforestation and mining (legal and illegal) and their consequences, are the main threats to Guianan amphibian communities; however, it is anticipated that climate change may be the greatest threat in future, especially in the highlands.
... Remarkably, Oreophrynella is absent from the Chimant a Massif although Chimant a is geographically much closer to the Auy an Massif than to the eastern tepui chain (Figure 1). In strong contrast to Oreophrynella, there is a radiation of at least seven microendemic species of Stefania (i.e. the "ginesi-clade") occurring in the Chimant a Massif and peripheral tepuis (Kok, Russo, Ratz, & Aubret, 2016;Kok et al., 2017). Oreophrynella might have gone extinct in the Chimant a Massif, due to factors that are better tolerated by Stefania. ...
Aim Using the Pantepui palaeoendemic toad genus Oreophrynella , we explored (1) the origin of Pantepui endemism and the hypothesis of Pantepui being a source of diversity for the surrounding areas, including the geologically younger Andes; (2) whether early diversification of Oreophrynella conforms with that of Stefania (Hemiphractidae), another Pantepui endemic amphibian, which was recently shown to have vicariantly diverged from Pantepui highlands widespread Oligocene ancestors. Location The fractured island‐like topography of the Pantepui biogeographical region in north‐eastern South America. Methods We inferred the molecular phylogeny of Oreophrynella and other “basal” Bufonidae genera using three mitochondrial and two nuclear DNA sequences under Bayesian and maximum likelihood methods. We estimated divergence times using a relaxed‐clock model and reconstructed ancestral areas through multiple models in a common likelihood framework. Results Phylogenetic analyses recovered a monophyletic Oreophrynella sister to Atelopus . Biogeographical analyses strongly suggested colonization of Pantepui via a pre‐Miocene (Eocene/Oligocene) long‐distance dispersal of a proto‐Andean ancestor, followed by pre‐Quaternary (lower Miocene) vicariant divergences of main lineages, and endemism of these main lineages to distinct biogeographical subunits. Main conclusions Our results suggest that at least part of the Pantepui diversity stemmed from dispersals from the proto‐Andes. Three hypotheses emerge for the origin and evolution of Pantepui endemism, the Distance Dispersal theory, the Plateau theory and the Disturbance–Vicariance theory. Our results indicate that the early diversification of Oreophrynella conforms to that of Stefania , but hint at different factors responsible for the survival or extinction of different tepui summit amphibians.
... Pristiman tis has a complex taxonomy and biogeographical history (Padial et al. 2014), and since most tepui summits and slopes have been inadequately sampled (Kok 2013b) any additional information about tepuian Pristimantis populations is crucial. Furthermore, any data about the distribution of tepuian species are important in terms of conservation because tepui summit organisms might seriously be threatened by global warming (e.g., Rödder et al. 2010, Kok et al. 2016a. ...
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Pantepui s.l. is a remote, biodiverse region of ~400 000 km2 containing at least five endemic reptile genera and a number of ancient vertebrate lineages. Here, we describe an additional endemic snake genus and species, Paikwaophis kruki gen. nov., sp. nov. (Dipsadidae: Xenodontinae), recently collected in the Pantepui cloud forest that sits at the base of the steep cliffs of Roraima-tepui and Wei-Assipu-tepui (table mountains of the Eastern Tepui Chain) in Guyana, South America. Multilocus molecular data strongly support Paikwaophis gen. nov. to be most closely related to Xenopholis Peters, 1869, although both genera are strikingly different morphologically. Osteological and other phenotypic data suggest that Paikwaophis is semi-fossorial; its diet includes minute lizards. Paikwaophis is currently the only known Pantepui endemic snake genus. The immature female holotype is the only known specimen.
Venezuelan Guayana covers a fifth of the Precambrian Guiana Shield in South America, one of the largest wilderness areas on the planet. Scientific knowledge of its herpetofauna has increased in a remarkable and sustained way in recent decades, but is still incomplete, with enormous geographical sampling gaps and almost total ignorance about species ecology. Currently, records exist of 195 species of amphibians (189 anurans and six caecilians) and 221 of reptiles (202 lizards and snakes, 15 turtles, and four crocodilians). Together, they represent nearly the 14% of the megadiverse South America herpetofauna. Such diversity and taxonomic composition of amphibians and reptiles are unevenly distributed in the Guayanan region: richness decreases with elevation, while endemism increases. Thirty-four percent of the amphibians and 22% of the reptiles are exclusive to the uplands and the highlands of Central Guayana province, including four genera. In the peripheral lowlands, herpetofaunal communities are dominated by taxa that are widespread or that have an Amazonian-Guianan distribution. Presently, Venezuelan Guayana biodiversity is seriously threatened by increasing deforestation, uncontrolled illegal mining, and uncontrolled mega-developments. Few highlands are affected by uncontrolled tourism, but climate change has emerged recently as a significant threat for the endemic Pantepui diversity. It is imperative and urgent to increase national and international efforts to study and monitor the most vulnerable populations of amphibians and reptiles in Venezuelan Guayana, before many of them disappear.
Pantepui is an archipelago of sky islands formed by the flat summits of the Neotropical Guiana table mountains (tepuis) situated between the Orinoco and Amazon basins. Pantepui is a virtually pristine land and a natural laboratory to study the origin and evolution of Neotropical biodiversity. This review aims to synthesize the existing biological knowledge of Pantepui, with an emphasis on the latest developments in biogeographical, ecological and evolutionary studies. Biogeographically, Pantepui is a province of the Guiana region, within the Neotropical realm, but the precise definition of this province varies according to the taxonomic group studied. Here we adopt a definition based on elevation, with a diffuse lower boundary at 1200–1500 m and an upper boundary at the uppermost elevations of the Guiana Highlands (ca. 3000 m). The biodiversity and endemism patterns of Pantepui are outstanding. With almost 2600 known species (>5000 species/10,000 km²), plants are the most diverse organisms and situate Pantepui among the most diverse regions of the world. Endemism usually ranges from 30 to 40% but may reach 55% in amphibians. Ecology is poorly known. Autecological studies are lacking, and community studies are available only for vegetation and solely in descriptive terms. Paleoecological studies have shown that plant communities have changed through time under the action of Holocene climatic changes and fire. Glacial-interglacial alternation has deeply modified the Pantepui biota and this biogeographical unit has been recurrently disassembled during glaciations and reassembled during interglacials. The origin and evolution of the Pantepui biota has been explained by diverse evolutionary processes involving a variety of environmental drivers and diversification mechanisms. Most of these hypotheses emerged from the study of extant biogeographical patterns and geological-paleoecological reconstructions. The inception of molecular phylogenetics, albeit still incipient in Pantepui, has provided evidence useful for testing these proposals. Taken individually, none of the proposed hypotheses can explain the evolution of the whole Pantepui biota, whose proper understanding requires complex thinking and the consideration of multiple drivers and a diversity of ecological and evolutionary processes and mechanisms acting together across spatiotemporal scales. Pantepui pristinity could be threatened by direct human disturbance and global warming. Preliminary estimates suggest that, under the worst warming scenario, >80% (including >50% of endemics) of the unique vascular flora could lose their habitat by the end of this century. In situ conservation actions are difficult to implement, and ex situ strategies (germplasm banks, botanical gardens, managed relocation) should thus be considered. More systematic and target-focused, rather than exploratory, approaches are needed for future research on Pantepui. International cooperation and the improvement of bureaucratic facilities are required to preserve the still-pristine Pantepui biota and ecosystems.
Full-text available The Brazilian mountain ranges from the Guiana Shield highlands are largely unexplored, with an under-studied herpetofauna. Here the amphibian and reptile species diversity of the remote Serra da Mocidade mountain range, located in extreme northern Brazil, is reported upon, and biogeographical affinities and taxonomic highlights are discussed. A 22-days expedition to this mountain range was undertaken during which specimens were sampled at four distinct altitudinal levels (600, 960, 1,060 and 1,365 m above sea level) using six complementary methods. Specimens were identified through an integrated approach that considered morphological, bioacoustical, and molecular analyses. Fifty-one species (23 amphibians and 28 reptiles) were found, a comparable richness to other mountain ranges in the region. The recorded assemblage showed a mixed compositional influence from assemblages typical of other mountain ranges and lowland forest habitats in the region. Most of the taxa occupying the Serra da Mocidade mountain range are typical of the Guiana Shield or widely distributed in the Amazon. Extensions of known distribution ranges and candidate undescribed taxa are also recorded. This is the first herpetofaunal expedition that accessed the higher altitudinal levels of this mountain range, contributing to the basic knowledge of these groups in remote areas.
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We used molecular and morphological data to investigate the hidden diversity within the Hypsiboas semilineatus species group, and more specifically within H. geographicus, an allegedly widespread species in northern South America. As a result, the identity of H. geographicus was clarified, several candidate species were detected and one of them, from the eastern Guiana Shield, is described herein as a preliminary step to resolve the taxonomy of the group. Hypsiboas diaboli-cus sp. nov. is mainly distinguished from closely-related species by an acuminate snout in lateral view, well-developed webbing between fingers and toes, and unspotted carmine/crimson colouration on the concealed surfaces of legs, feet and hands in life. The tadpole of the new species is described and is characterized by a large A-2 gap, a mostly single row of large marginal papillae, and a dark brown to black colouration. We also describe the advertisement call of the new species, which is defined as a soft call consisting of short clusters of 2-3 chuckles with a dominant frequency ranging between 1.11-1.19 kHz. Hypsiboas diabolicus sp. nov. is currently known only from the eastern Guiana Shield, and is probably endemic to that region. The new species' range overlaps broadly with another candidate species referred to as H. aff. semi-lineatus 1. Our preliminary results stress out a high cryptic diversity in that species group and the need for a formal rede-scription of Hypsiboas geographicus based on more topotypic material than what is currently available to properly sort out the taxonomic status of several lineages in that clade.
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Egg-brooding frogs (Hemiphractidae) are a group of 105 currently recognized Neotropical species, with a remarkable diversity of developmental modes, from direct development to free-living and exotrophic tadpoles. Females carry their eggs on the back and embryos have unique bell-shaped gills. We inferred the evolutionary relationships of these frogs and used the resulting phylogeny to review their taxonomy and test hypotheses on the evolution of developmental modes and bellshaped gills. Our inferences relied on a total evidence parsimony analysis of DNA sequences of up to 20 mitochondrial and nuclear genes (analyzed under tree-alignment), and 51 phenotypic characters sampled for 83% of currently valid hemiphractid species. Our analyses rendered a well-resolved phylogeny, with both Hemiphractidae (sister of Athesphatanura) and its six recognized genera being monophyletic. We also inferred novel intergeneric relationships [((Cryptobatrachus, Flectonotus), (Stefania, (Fritziana, (Hemiphractus, Gastrotheca))))], the non-monophyly of all species groups previously proposed within Gastrotheca and Stefania, and the existence of several putative new species within Fritziana and Hemiphractus. Contrary to previous hypotheses, our results support the most recent common ancestor of hemiphractids as a direct-developer. Free-living aquatic tadpoles apparently evolved from direct-developing ancestors three to eight times. Embryos of the sister taxa Cryptobatrachus and Flectonotus share a pair of single gills derived from branchial arch I, while embryos of the clade including the other four genera have two pairs of gills derived from branchial arches I and II respectively. Furthermore, in Gastrotheca the fusion of the two pairs of gills is a putative synapomorphy. We propose a revised taxonomy concordant with our optimal topologies.
The Gran Sabana (GS) is a key region for understanding the origin of neotropical savannas and is an ideal location to test ecological hypotheses on long-term vegetation dynamics under the action of natural and anthropogenic drivers. The conservation of the GS is a controversial issue because of the confluence of disparate cultural and socio-economic interests, with a strong debate surrounding fire practices by indigenous people. Late glacial to Holocene pollen and charcoal records obtained thus far in this region have documented the main palaeoecological trends along with the climatic and anthropogenic (mostly fire) drivers involved. Here we discuss how these records can be used to inform conservation and restoration practices in the GS. The main points of the discussion are the local vs. regional character of palaeoecological evidence, the support provided by this evidence for the existing fire management proposals and the role of spatiotemporal environmental and ecological heterogeneity in the definition and evaluation of realistic restoration targets. A general conclusion is that past ecological reconstructions do not fully support either of the current options for fire management, i.e., either total fire suppression or the continuity of indigenous fire practices. It is recommended to replace this dual and rigid conservation framework with a more diverse and flexible approach that considers the complex spatiotemporal heterogeneity documented in palaeoecological records.
This scientific masterpiece reveals many aspects of the lives of marsupial frogs and closely allied genera. Native to Central and South America, these amphibians differ from other frogs in that they protect their eggs after oviposition by either adhering them to the female’s back or placing them in a specialized dorsal pouch (thus the common name, marsupial frog). During mating, the male typically collects the eggs from the female with his feet—often one at a time and always out of water—fertilizes them, and then tucks them into the female’s pouch or attaches them to her back. In some species these eggs hatch as tadpoles, but most emerge as miniatures of the adults. Even among the tadpoles there is remarkable divergence, with some behaving in the typical manner (feeding and metamorphosing), whereas others forego all feeding until they metamorphose. In Marsupial Frogs, William E. Duellman’s synthesis of all that is known about the unique family Hemiphractidae is largely based on decades of his own careful laboratory and field study. He reveals the diversity of exotic color patterns and the frog’s geographic distribution by providing more than 200 photographs, illustrations, and maps. This exceptional tome should find its way into the libraries of serious herpetologists, tropical biologists, and developmental biologists. Included in this book are: A molecular phylogeny of the family Hemiphractidae A thorough osteological analysis • A review of external morphological features An overview of the evolution of reproductive modes A biogeographic synthesis Keys to genera and species Diagnosis and thorough description of each species of marsupial frog Colored physiographic maps depicting species distributions.