Five new species of Pristimantis (Anura: Strabomantidae) from the coastal cloud forest of the Península de Paria, Venezuela

Main Article Content

Hinrich Kaiser
César L. Barrio-Amorós
Gilson A. Rivas
Claus Steinlein
Michael Schmid

Abstract

Fieldwork in the cloud forest of Venezuela’s remote Península de Paria in 2001 resulted in the collection of several specimens that could unquestionably be classified as members of the genus Pristimantis.  Subsequent analysis of comparative material in museum collections brought the total number of specimens to 44, and these collectively represent five new species. Two of these species, P. geminus sp. nov. and P. nubisilva sp. nov., have phenotypes remarkably similar to the Trinidadian P. urichi, supporting a prediction that Pristimantis from easternmost Venezuela may have given rise to Trinidadian forms. Pristimantis hoogmoedi sp. nov. is easily identified by its large size and red eyes. Two of the species, P. longicorpus sp. nov. and P. pariagnomus sp. nov., are very distinct morphologically but are known only from the holotypes. The former is characterized by an elongate body form supported by relatively short limbs, whereas the latter has very distinctive hand morphology and is likely the smallest Venezuelan frog. Chromosome banding studies of P. nubisilva sp. nov. and P. hoogmoedi sp. nov. revealed chromosome numbers of 2n = 36 and 2n = 26, respectively, with an unusual submetacentric fusion chromosome 11;18 in some males of the former and a unique meiotic pairing of chromosomes in males of the latter.  All five species can be readily distinguished by their osteology, such as by the extent of the sphenethmoid and features on the roof of the mouth, as well as by the shape and rearrangement of mesopodial elements.  The unexpectedly high diversity of Pristimantis in this region, along with high endemism of amphibians and reptiles in general, underscores the position of the Península de Paria as a center for frog biodiversity in Venezuela.  The similarity of these Paria species to Pristimantis from Trinidad, Tobago and the central Cordillera de la Costa represents a tangible piece of evidence for the close biogeographic link of the anuran fauna of these landmasses.

Article Details

How to Cite
[1]
Kaiser, H., Barrio-Amorós, C.L., Rivas, G.A., Steinlein, C. and Schmid, M. 2015. Five new species of Pristimantis (Anura: Strabomantidae) from the coastal cloud forest of the Península de Paria, Venezuela. Journal of Threatened Taxa. 7, 4 (Apr. 2015), 7047–7088. DOI:https://doi.org/10.11609/JoTT.o4197.7047-88.
Section
Monograph
Author Biographies

Hinrich Kaiser, Department of Biology, Victor Valley College, 18422 Bear Valley Road, Victorville, California 92395, USA; and Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20013, USA

Dr. Hinrich Kaiser is a Professor in the Department of Biology at Victor Valley College in Victorville, California, USA and a Research Collaborator of the United States National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA. He currently serves as an Associate Editor with both Journal of Herpetology and Herpetology Notes, and as a member of the International Advisory Board of the Foundation for Post-Conflict Development, New York. Hinrich’s most recent publications have focused on the herpetofauna of Timor-Leste and nearby areas of Wallacea, as well as on the defense of herpetological taxonomy against taxonomic vandalism.

César L. Barrio-Amorós, Doc Frog Expeditions, Apartado Postal 220-8000, San José, Perez Zeledon, San Isidro del General 11901, Costa Rica

César L. Barrio Amorós is a freelance researcher and photographer and the owner of Doc Frog Expeditions and Photography. His research focus is on the taxonomy of Venezuelan amphibians and reptiles, especially Terrarana and Dendrobatoidea. He has published or coauthored more than 200 articles, including the description of 50 mainly Venezuelan new species. César currently resides in Costa Rica, where he teaches herpetology courses and leads nature tours with a herpetological emphasis.

Gilson A. Rivas, Museo de Biologia, Facultad Experimental de Ciencias, La Universidad del Zulia, Apartado Postal 526, Maracaibo 4011, Maracaibo, Venezuela

Gilson A. Rivas earned a BSc in Animal Science from Fundación La Salle de Ciencias Naturales and currently serves as co-editor of the journal Anartia in the Museo de Biología, Facultad Experimental de Ciencias, Universidad del Zulia, Maracaibo, Venezuela. He has been involved in research on the systematics and conservation of the Venezuelan herpetofauna for two decades, having co-authored more than 100 scientific contributions, including descriptions of over 20 new species of amphibians and reptiles. Gilson’s research focus is the herpetofauna of the Península de Paria and surrounding areas, particularly with respect to systematics and conservation,as well as the influence of invasive species and human development and their impact on the native fauna. 

Claus Steinlein, Institut für Humangenetik, Universität Würzburg, Biozentrum Am Hubland, 97074 Würzburg, Germany

Claus Steinlein holds an engineering degree from the University of Applied Sciences, Hamburg, Germany. His unrivaled expertise in the development of cytogenetics techniques and protocols has enabled him to produce exceptional chromosome data sets over the past three decades, leading to his co-authorship of numerous research articles in the highest ranked scientific journals. He currently serves as Editorial Administrator of the journals Cytogenetic and Genome Research, Sexual Development, and Molecular Syndromology.

Michael Schmid, Institut für Humangenetik, Universität Würzburg, Biozentrum Am Hubland, 97074 Würzburg, Germany

Dr. Michael Schmid obtained his doctorate in human biology from the University of Ulm, Germany. He directs the cytogenetics group in the Department of Human Genetics, University of Würzburg, Germany, where he has been a professor since 1995. Aside from his main line of research in human genetics, Michael has broad interest in vertebrate cytogenetics, and his series of papers on chromosome banding in Amphibia remains a standard setting contribution. He is Editor-in-Chief of the journals Cytogenetic and Genome Research, Sexual Development, and Molecular Syndromology. He was one of the founding editors of the journal Chromosome Research. He currently serves as Editor of the revived book series Monographs in Human Genetics and as Executive Editor of the new book series Genome Dynamics.

References

ASIH (American Society of Ichthyologists and Herpetologists) (2004). Guidelines for Use of Live Amphibians and Reptiles in Field and Laboratory Research, 2nd Edition. ASIH, Lawrence, Kansas, USA.

Ayarzagüena, J. & C. Señaris (1996). Dos nuevas especies de Cochranella (Anura; Centrolenidae) para Venezuela. Publicaciones de la

Asociación de Amigos de Doñana 8: 1–16.

Barrio-Amorós, C.L. (1998). Sistemática y biogeografía de los anfibios (Amphibia) de Venezuela. Acta Biologica Venezuelica 18(2): 1–93.

Barrio-Amorós, C.L. & H. Kaiser (2008). Distribution of Strabomantis biporcatus (Terrarana: Strabomantidae) in northern Venezuela, with comments on its phenotypic variation. Salamandra 44: 248–254.

Barrio-Amorós, C.L., G. Rivas & H. Kaiser (2006). New species of Colostethus (Anura, Dendrobatidae) from the Península de Paria, Venezuela. Journal of Herpetology 40: 371–377; http://dx.doi.org/10.1670/0022-1511(2006)40[371:NSOCAD]2.0.CO;2

Barrio-Amorós, C.L., G.A. Rivas, C. Molina, J.C. Santos & H. Kaiser (2010a). Intraspecific variation in the endangered frog Mannophryne riveroi (Anura, Dendrobatidae, Aromobatinae), with comments on coloration and natural history. Herpetology Notes 3: 151–160.

Barrio-Amorós, C.L., F.J.M. Rojas-Runjaic & T.R. Barros (2010b). Two new Pristimantis (Anura: Terrarana: Strabomantidae) from the Sierra de Perijá, Venezuela. Zootaxa 2329: 1–21.

Barrio-Amorós, C.L., J.M. Guayasamin & S.B. Hedges (2012). A new minute Andean Pristimantis (Anura: Strabomantidae) from Venezuela. Phyllomedusa 11: 83–93.

Barrio-Amorós, C.L., M.P. Heinicke & S.B. Hedges (2013). A new tuberculated Pristimantis (Anura, Terrarana, Strabomantidae) from the Venezuelan Andes, redescription of Pristimantis pleurostriatus, and variation within Pristimantis vanadisae. Zootaxa 3647(1): 43–62.

Donoso-Barros, R. (1965a). Nuevos reptiles y anfibios de Venezuela. Noticiario Mensual, Museo Nacional de Historia Natural, Santiago, Chile 102: 2–3.

Donoso-Barros, R. (1965b). A new dendrobatidae [sic] frog, Prostherapis riveroi from Venezuela. Caribbean Journal of Science 4: 485–489.

Donoso-Barros, R. (1966). Dos nuevos Gonatodes de Venezuela. Publicación Ocasional del Museo Nacional de Historia Natural, Santiago de Chile 11: 1–32.

Edwards, S.R. (1974). Taxonomic notes on South American dendrobatid frogs of the genus Colostethus. Occasional Papers of the Museum of Natural History, University of Kansas 30: 1–14.

Evenhuis, N.L. (2008). A compendium of zoological type nomenclature: a reference source. Bishop Museum Technical Report 41: 1–25.

Frost, C.D. & A.W. Snoke (1989). Tobago, West Indies, a fragment of a Mesozoic oceanic island arc: petrochemical evidence. Journal of the Geological Society, London 146: 953–964; http://dx.doi.org/10.1144/gsjgs.146.6.0953

Hanken, J. (1982). Appendicular skeletal morphology in minute salamanders, genus Thorius (Amphibia: Plethodontidae): growth regulation, adult size determination, and natural variation. Journal of Morphology 174: 57–77.

Hanken, J. & D.B. Wake (1993). Miniaturization of body size: organismal consequences and evolutionary significance. Annual Review of Ecology, Evolution, and Systematics 24: 501–519.

Hanken, J. & D.B. Wake (1994). Five new species of minute salamanders, genus Thorius (Caudata: Plethodontidae), from northern Oaxaca, Mexico. Copeia 1994(3): 573–590.

Hardy, J.D., Jr. (2001). A new frog of the genus Eleutherodactylus from the Island of Tobago, West Indies. Bulletin of the Maryland Herpetological Society 37: 25–31.

Hedges, S.B., W.E. Duellman & M.P. Heinicke (2008). New World direct-developing frogs (Anura: Terrarana): molecular phylogeny, classification, biogeography, and conservation. Zootaxa 1737: 1–182.

Heyer, W.R., M.A. Donnelly, R.W. McDiarmid, L.C. Hayek & M.S. Foster (Eds.) (1994). Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithsonian Institution Press, Washington, USA, 364pp.

Hoyos, J.M., C. Mantilla, D. Galindo & L. Salgar (2014). Phylogenetic analysis whithin [sic] the Pristimantis unistrigatus (Anura, Craugastoridae) group based on morphological characters. Caldasia 36(1): 107–124.

IUCN (2001). IUCN Red List Categories and Criteria: Version 3.1. IUCN Species Survival Commission. IUCN, Gland, Switzerland and Cambridge, United Kingdom.

Jowers, M.J., R.M. Lehtinen, R.J. Downie, A.P. Georgiadis & J.C. Murphy (2014). Molecular phylogenetics of the glass frog Hyalinobatrachium orientale (Anura: Centrolenidae): evidence for Pliocene connections between mainland Venezuela and the island of Tobago. Mitochondrial DNA, Early Online 1–6; http://dx.doi.org/10.3109/19401736.2014.880888

Kaiser, H. (1993). Systematics and Biogeography of Eastern Caribbean Frogs. Unpubl. PhD Thesis, McGill University, Montréal, Québec, Canada.

Kaiser, H. (1994). Two origins for Eastern Caribbean Eleutherodactylus (Anura: Leptodactylidae): molecular evidence and its biogeographic consequences. Abstract, 74th Annual Meeting of the American Society of Ichthyologists and Herpetologists, Los Angeles, California, USA.

Kaiser, H. (1996). Systematics and biogeography of Eastern Caribbean Eleutherodactylus (Anura: Leptodactylidae): consensus from a multidisciplinary approach, pp. 129–140. In: Powell, R. & R.W. Henderson (eds.). Contributions to West Indian Herpetology: a Tribute to Albert Schwartz. Society for the Study of Amphibians and Reptiles, Ithaca, New York, USA.

Kaiser, H. (1997). Origins and introductions of the Caribbean frog, Eleutherodactylus johnstonei (Leptodactylidae): management and conservation concerns. Biodiversity and Conservation 6: 1391–1407.

Kaiser, H., D.M. Green & M. Schmid (1994a). Systematics and

biogeography of Eastern Caribbean frogs (Leptodactylidae: Eleutherodactylus), with the description of a new species from Dominica. Canadian Journal of Zoology 72(2): 2217–2237; http://dx.doi.org/10.1139/z94-297

Kaiser, H., J.D. Hardy, Jr. & D.M. Green (1994b). Taxonomic status of Caribbean and South American frogs currently ascribed to Eleutherodactylus urichi (Anura: Leptodactylidae). Copeia 1994(3): 780–796.

Kaiser, H., C.M. Dwyer, W. Feichtinger & M. Schmid (1995). A new species of Eleutherodactylus (Anura: Leptodactylidae) from Tobago, West Indies and its morphometric and cytogenetic characterization. Herpetological Natural History 3: 151–163.

Lehr, E. & L.A. Coloma (2008). A minute new Ecuadorian Andean frog (Anura: Strabomantidae, Pristimantis). Herpetologica 64(3): 354–367; http://dx.doi.org/10.1655/07-089.1

Lynch, J.D. & W.E. Duellman (1997). Frogs of the genus Eleutherodactylus (Leptodactylidae) in Western Ecuador: systematics, ecology, and biogoegraphy. Special Publication of the Museum of Natural History, University of Kansas 23: 1–236.

Lynch, J.D. & E. La Marca (1993). Synonymy and variation in Eleutherodactylus bicumulus (Peters) from northern Venezuela, with a description of a new species (Amphibia: Leptodactylidae). Caribbean Journal of Science 29: 133–146.

Maggenti, M.A.B., A.R. Maggenti & S.L. Gardner (Eds.) (2005). Online Dictionary of Invertebrate Zoology. http://digitalcommons.unl.edu/onlinedictinvertzoology/2/. Accessed on 17 March 2015.

Manzanilla, J., M.J. Jowers, E. La Marca & M. García-París (2007). Taxonomic reassessment of Mannophryne trinitatis (Anura: Dendrobatidae) with a description of a new species from Venezuela. Herpetological Journal 17(1): 13–42.

MacArthur, R.H. & E.O. Wilson (1967). The Theory of Island Biogeography. Princeton University Press, Princeton, New Jersey, USA, 203pp.

Mijares-Urrutia, A., J.C. Señaris & A. Arends (2000). Taxonomía de algunos microtéidos (Squamata) de Venezuela, I: Variación y distribución geográfica de Euspondylus del nordeste de Venezuela. Revista de Biología Tropical 48: 671–680.

Pérez, M.H.S. (2014). Standard Symbolic Codes for Institutional Resource Collections in Herpetology and Ichthyology: an Online Reference. Version 5.0 (22 September 2014). American Society of Ichthyologists and Herpetologists, Washington, D.C., USA.

Rivas F.G., E. La Marca & O. Oliveros (1999). Una nueva especie de Anadia (Reptilia: Sauria: Gymnophthalmidae) del noreste de Venezuela. Acta Biologica Venezuelica 19(4): 27–32.

Rivas, G., W.E. Schargel & J.M. Meik (2005). A new species of Riama (Squamata: Gymnophthalmidae), endemic to the Península de Paria, Venezuela. Herpetologica 61(4): 461–468; http://dx.doi.org/10.1655/04-96.1

Rivas, G.A., P.M. Sales Nunes, J.R. Dixon, W.E. Schargel, J.R. Caicedo, T.R. Barros, E.G. Camargo & C.L. Barrio-Amorós (2012). Taxonomy, hemipenial morphology, and natural history of two poorly known species of Anadia (Gymnophthalmidae) from northern South America. Journal of Herpetology 46(1): 33–40; http://dx.doi.org/10.1670/10-139

Rivero, J.A. (1961). Salientia of Venezuela. Bulletin of the Museum of Comparative Zoology 126: 1–207.

Rivero, J.A. (1964). The distribution of Venezuelan frogs. Caribbean Journal of Science 4: 307–318.

Schargel, W.E., G. Rivas Fuenmayor & C.W. Myers (2005). An enigmatic new snake from cloud forest of the Península de Paria, Venezuela (Colubridae: Genus Taeniophallus ?). American Museum Novitates 3484: 1–24; http://dx.doi.org/10.1206/0003-0082(2005)484[0001:AENSFC]2.0.CO;2

Schmid, M., C. Steinlein & W. Feichtinger (1992). Chromosome banding in Amphibia. XVII. First demonstration of multiple sex chromosomes in amphibians: Eleutherodactylus maussi (Anura, Leptodactylidae). Chromosoma 101(5–6): 284–292;

http://dx.doi.org/10.1007/BF00346007

Schmid, M., W. Feichtinger, C. Steinlein, T. Haaf, M. Schartl, R. Visbal García, J. Manzanilla Pupo & A. Fernández Badillo (2002). Chromosome banding in Amphibia. XXVI. Coexistence of homomorphic XY sex chromosomes and a derived Y-autosome translocation in

Eleutherodactylus maussi (Anura, Leptodactylidae). Cytogenetics and Genome Research 99(1–4): 330–343; http://dx.doi.org/10.1159/000071612

Schmid, M., W. Feichtinger, C. Steinlein, R. Visbal García & A. Fernández Badillo (2003). Chromosome banding in Amphibia. XXVIII. Homomorphic XY sex chromosomes and a derived Y-autosome translocation in Eleutherodactylus riveroi (Anura, Leptodactylidae). Cytogenetics and Genome Research 101(1): 62–73; http://dx.doi.org/10.1159/000073420

Schmid, M., C. Steinlein, J.P. Bogart, W. Feichtinger, P. León, E. La Marca, L.M. Diaz, A. Sanz, S.-H. Chen & S.B. Hedges (2010). The chromosomes of terraranan frogs: insights into vertebrate cytogenetics. Cytogenetics and Genome Research 130–131: 1–568.

Terán-Valdez, A. & J.M. Guayasamin (2010). The smallest terrestrial vertebrate of Ecuador: a new frog of the genus  Pristimantis (Amphibia: Strabomantidae) from the Cordillera del Cóndor. Zootaxa 2447: 53–68.

Walker, C.F. & F.H. Test (1955). New Venezuelan frogs of the genus Eleutherodactylus. Occasional Papers of the Museum of Zoology, University of Michigan 561: 1–12.

Yeh, J. (2002). The effect of miniaturized body size on skeletal morphology in frogs. Evolution 56(3): 628–641; http://dx.doi.org/10.1111/j.0014-3820.2002.tb01372.x