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Published: 2016-02-24

Cryptic diversity in the Hypsiboas semilineatus species group (Amphibia, Anura) with the description of a new species from the eastern Guiana Shield

CNRS Guyane USR3456, Immeuble Le Relais, 2 Avenue Gustave Charlery, 97300, Cayenne, French Guiana
CNRS Guyane USR3456, Immeuble Le Relais, 2 Avenue Gustave Charlery, 97300, Cayenne, French Guiana
Museum of Vertebrate Zoology, University of California, Berkeley, CA, USA
CNRS Guyane USR3456, Immeuble Le Relais, 2 Avenue Gustave Charlery, 97300, Cayenne, French Guiana
CNRS Guyane USR3456, Immeuble Le Relais, 2 Avenue Gustave Charlery, 97300, Cayenne, French Guiana
Pointe Maripa, RN2/PK35, 97311, Roura, French Guiana
Centro de Pesquisas Zoobotânicas e Geologicas (CPZG), Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá (IEPA), Macapá, AP, Brazil
Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461, CEP 05508-090, São Paulo, SP, Brazil
Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461, CEP 05508-090, São Paulo, SP, Brazil
Centro de Pesquisas Zoobotânicas e Geologicas (CPZG), Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá (IEPA), Macapá, AP, Brazil
Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461, CEP 05508-090, São Paulo, SP, Brazil
Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461, CEP 05508-090, São Paulo, SP, Brazil
Amphibian Evolution Lab, Biology Department, Vrije Universiteit Brussel, 2 Pleinlaan, B-1050 Brussels, Belgium
Amphibia Anura conservation endemism Guiana Shield taxonomy


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 diabolicus 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. semilineatus 1. Our preliminary results stress out a high cryptic diversity in that species group and the need for a formal redescription 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.



  1. Angulo, A. & Icochea, J. (2010) Cryptic species complexes, widespread species and conservation: lessons from Amazonian frogs of the Leptodactylus marmoratus group (Anura: Leptodactylidae). Systematics and Biodiversity, 8, 357–370.

    Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution, 22, 148–155.

    Blaustein, A.R. & Dobson, A. (2006) Extinctions: a message from the frogs. Nature, 439, 143–144.

    Bokermann, W.C. (1963) Girinos de anfíbios brasileiros I (Amphibia, Salientia). Anais da Academia Brasileira de Ciências, 35, 465–474.

    Boulenger, G. (1882) Catalogue of the Batrachia Salientia s. Ecaudata in the Collection of the British Museum. 2nd Edition. Printed by order of the Trustees, London, 600 pp.

    Caldwell, J.P. (1989) Structure and behavior of Hyla geographica tadpole schools, with comments on classification of group behavior in tadpoles. Copeia, 1989 (4), 938–948.

    Caramaschi, U., Feio, R.N. & Pimenta, B.V.S. (2004) Nova espécie do grupo Hyla geographica Spix, 1824 da Floresta Atlântica, Brasil (Amphibia, Anura, Hylidae). Boletim do Museu Nacional. Nova Serie, Zoologia, 518, 1–14.

    da Silva, J.M., Rylands, A.B. & da Fonseca, G.A. (2005) The fate of the amazonian areas of endemism. Conservation Biology, 19, 689–694.

    Dewynter, M., Marty, C., Blanc, M., Gaucher, P., Vidal, N., Frétey, T., de Massary, J.-C. & Fouquet, A. (2008) Liste des Amphibiens et des Reptiles de Guyane. Available online: (accessed 16 August 2013)

    Duellman, W.E. (1970) The Hylid Frogs of Middle America. 2 Vols. Monographs of the Museum of Natural History, University of Kansas, Lawrence, 753 pp.

    Duellman, W.E. (1973) Frogs of the Hyla geographica group. Copeia, 1973 (3), 515–533.

    Duellman, W.E. (2005) Cusco Amazónico: the lives of amphibians and reptiles in an Amazonian rainforest. Comstock Pub, Cornell University Press, Ithaca & London, 433 pp.

    Duellman, W.E. & Lescure, J. (1973) Life history and ecology of the hylid frog Osteocephalus taurinus, with observations on larval behavior. Occasional Papers of the Museum of Natural History, University of Kansas, 13, 1–12.

    Faivovich, J., Haddad, C.F., Garcia, P.C., Frost, D.R., Campbell, J.A. & Wheeler, W.C. (2005) Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bulletin of the American Museum of Natural History, 294, 1–240.[0001:SROTFF]2.0.CO;2

    Fouquet, A., Cassini, C., Haddad, C.F.B., Pech, N. & Rodrigues, M.T. (2014) Species delimitation, patterns of diversification and historical biogeography of a Neotropical frog genus; Adenomera (Anura, Leptodactylidae). Journal of Biogeography, 41 (5), 855–870.

    Fouquet, A., Gilles, A., Vences, M., Marty, C., Blanc, M. & Gemmell, N.J. (2007a) Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS one, 2, e1109.

    Fouquet, A., Noonan, B.P., Rodrigues, M.T., Pech, N., Gilles, A. & Gemmell, N.J. (2012) Multiple quaternary refugia in the Eastern Guiana Shield revealed by comparative phylogeography of 12 frog species. Systematic Biology, 61, 461–489.

    Fouquet, A., Vences, M., Salducci, M.D., Meyer, A., Marty, C., Blanc, M. & Gilles, A. (2007b) Revealing cryptic diversity using molecular phylogenetics and phylogeography in frogs of the Scinax ruber and Rhinella margaritifera species groups. Molecular Phylogenetics and Evolution, 43 (2), 567–582.

    Frost, D.R. (2015) Amphibian Species of the World: an Online Reference. Version 6.0. Electronic Database. American Museum of Natural History, New York, USA. Available from: (accessed 1 June 15)

    Funk, W.C., Caminer, M. & Ron, S.R. (2012) High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society B: Biological Sciences, 279, 1806–1814.

    Gans, C. (1960) Notes on a herpetological collecting trip through the southeastern lowlands of Bolivia. Annals Carnegie Museum, 283–314.

    Gosner, K.L. (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183–190.

    Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.

    d’Heursel, A. & de Sá, R.O. (1999) Comparing the tadpoles of Hyla geographica and Hyla semilineata. Journal of Herpetology, 33, 353–361.

    Hillis, D.M., Moritz, C. & Mable, B.K. (1996) Molecular Systematics. Second edition. Sinauer Associates, Sunderland, MA, 636 pp.

    Hoogmoed, M.S. & Gruber, U. (1983) Spix and Wagler type specimens of reptiles and amphibians in the Natural History Musea in Munich (Germany) and Leiden (The Netherlands). Spixiana Supplement, 9, 319–415.

    Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.

    Jansen, M., Bloch, R., Schulze, A. & Pfenninger, M. (2011) Integrative inventory of Bolivia’s lowland anurans reveals hidden diversity. Zoologica Scripta, 40, 567–583.

    Junca, F.A., Camurugi, F. & Merces, E.D.A. (2012) The tadpole of Hypsiboas pombali (Caramaschi, Pimenta & Feio, 2004) (Anura, Hylidae). Zootaxa, 3184, 64–66.

    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780.

    Kenny, J.S. (1969) The Amphibia of Trinidad. Studies of the Fauna of Curaçao and other Caribbean Islands, 108, 1–78.

    Köhler, G. (2012) Color catalogue for field biologists. Herpeton, Offenbach, 49 pp.

    Kok, P.J.R. & Kalamandeen, M. (2008) Introduction to the taxonomy of the amphibians of Kaieteur National Park, Guyana. Belgian Development Cooperation, 278 pp.

    Laurance, W.F., Albernaz, A.K., Schroth, G., Fearnside, P.M., Bergen, S., Venticinque, E.M. & Da Costa, C. (2002) Predictors of deforestation in the Brazilian Amazon. Journal of biogeography, 29, 737–748.

    Lavilla, E.O., Caramaschi, U., Langone, J.A., Pombal, J.P. Jr. & De Sa, R.O. (2013) The identity of Rana margaritifera Laurenti, 1768 (Anura, Bufonidae). Zootaxa, 3646 (3), 251–264.

    Lima, A.P., Magnusson, W.E., Menin, M., Erdtmann, L.K., Rodrigue, D.J., Keller, C. & Hödl, W. (2006) Guia de sapos da Reserva Adolpho Ducke – Amazônia Central / Guide to the frogs of Reserva Adolpho Ducke – Central Amazonia. Áttema, Manaus, 176 pp.

    Linneaus, C. von (1758) 1 Systema naturae: per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Impensis Direct. Laurentii Salvii, Holmiae, 847 pp.

    Márquez, R., De la Riva, I., Bosch, J. & Matheu, E. (2002) Sounds of frogs and toads of Bolivia. [CD audio]

    Myers, C.W. & Duellman, W.E. (1982) A new species of Hyla from Cerro Colorado, and other tree frog records and geographical notes from western Panama. American Museum Novitates, 2752, 1–32.

    Nunes, P.M., Fouquet, A., Curcio, F.F., Kok, P.J. & Rodrigues, M.T. (2012) Cryptic species in Iphisa elegans Gray, 1851 (Squamata: Gymnophthalmidae) revealed by hemipenial morphology and molecular data. Zoological Journal of the Linnean Society, 166, 361–376.

    Orton, G.L. (1953) The systematics of vertebrate larvae. Systematic Biology, 2, 63–75.

    Parker, H. (1936) A collection of reptiles and amphibians from the Upper Orinoco. Bulletin du Musée Royal d'Histoire Naturelle de Belgique, 12, 1–4.

    Parker, H.W. (1933) A list of the frogs and toads of Trinidad. US Government Printing Office.

    Peloso, P.L.V. (2010) A safe place for amphibians? A cautionary tale on the taxonomy and conservation of frogs, caecilians, and salamanders in the Brazilian Amazonia. Zoologia, 27 (5), 667–673.

    Peloso, P.L.V., Sturaro, M.J., Forlani, M.C., Gaucher, P., Motta, A.P. & Wheeler, W.C. (2014) Phylogeny, taxonomic revision, and character evolution of the genera Chiasmocleis and Syncope (Anura, Microhylidae) in Amazonia, with descriptions of three new species. Bulletin of the American Museum of Natural History, 386, 1–112.

    Posada, D. (2008) JModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Pyburn, W.F. & Hall, D.H. (1984) A new stream-inhabiting treefrog (Anura: Hylidae) from southeastern Colombia. Herpetologica, 40, 366–372.

    Pyron, A.R. & Wiens, J.J. (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61, 543–583.

    Rambaut, A. & Drummond, A.J. (2007) Tracer Version 1.5.Available from: (accessed 20 May 15)

    Savage, J.M. & Heyer, W.R. (1967) Variation and distribution in the tree-frog genus Phyllomedusa in Costa Rica, central America. Studies on Neotropical Fauna and Environment, 5, 111–131.

    Schulze, A., Jansen, M. & Koehler, G. (2015) Tadpole diversity of Bolivia's lowland anuran communities: molecular identification, morphological characterisation, and ecological assignment. Zootaxa, 4016 (1), 1–111.

    Silveira, S.R. & Caramaschi, U. (1989) Revalidação de Hyla semilineata Spix, 1824 (Anura, Hylidae). Resumos XVI Congresso Brasileiro de Zoologia, Universidade Federal da Paraiba, João Pessoa, Paraiba. [unkown pagination]

    Spix, J.B. (1824) Animalia Nova sive species novae testudinum et ranarum, quas in itinere per Brasiliam, annis 1817-1820 jussu et auspiciés Maximiliani Josephi 1. typ. Franc. Seraph. Hübschmanni, 53 pp.

    Sturaro, M.J. & Peloso, P.L.V. (2014) A new species of Scinax Wagler, 1830 (Anura: Hylidae) from the Middle Amazon River Basin, Brazil. Papéis Avulsos de Zoologia São Paulo, 54, 9–23.

    Sueur, J., Aubin, T. & Simonis, C. (2008) Equipment review: seewave, a free modular tool for sound analysis and synthesis. Bioacoustics, 18, 213–226.

    Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

    Wagler, J.G. (1830) Natürliches System der Amphibien: mit vorangehender Classification der Säugethiere und Vögel. In der J.G. Cotta'scchen Buchhandlung, München, Stuttgart, Tübingen, 382 pp.

    Wiens, J.J., Kuczynski, C.A., Hua, X. & Moen, D.S. (2010) An expanded phylogeny of treefrogs (Hylidae) based on nuclear and mitochondrial sequence data. Molecular Phylogenetics and Evolution, 55, 871–882.