Amended diagnosis and redescription of Pristimantis marmoratus (Boulenger, 1900) (Amphibia: Craugastoridae), with a description of its advertisement call and notes on its breeding ecology and phylogenetic relationships

  • Philippe J.R. Kok Amphibian Evolution Lab, Biology Department, Vrije Universiteit Brussel, 2 Pleinlaan, B-1050 Brussels
  • Raheleh Dezfoulian Amphibian Evolution Lab, Biology Department, Vrije Universiteit Brussel, 2 Pleinlaan, B-1050 Brussels
  • D. Bruce Means Coastal Plains Institute and Land Conservancy, 1313 Milton Street, Tallahassee, Florida 32303
  • Antoine Fouquet Laboratoire Écologie, Évolution, Interactions des Systèmes Amazoniens (USR 3456 LEEISA), Université de Guyane, CNRS Guyane, Cayenne
  • César L. Barrio-Amorós Doc Frogs Expeditions, Apartado Postal 220-8000, San José, Pérez Zeledón, San Isidro del General, 11901
DOI: https://doi.org/10.5852/ejt.2018.397
Keywords: Anura, Guiana Shield, Pantepui, systematics, Terrarana

Abstract

The frog Pristimantis marmoratus was originally described as Hylodes marmoratus by George A. Boulenger in 1900 based on a single specimen reported to have been collected at the foot of Mount Roraima in Guyana in 1898. We herein discuss the exact location of the type locality of P. marmoratus and provide a redescription of the species based on new material from Kaieteur National Park and from the slopes of Maringma-tepui in Guyana. We also describe the previously unknown vocalization and breeding ecology of the species, and conducted an exploratory molecular analysis of the phylogenetic relationships within the genus Pristimantis represented by the members of the “unistrigatus species group” in the Guiana Shield. Pristimantis marmoratus is a small-sized species mainly distinguished from its known Guiana Shield congeners by the combination of F I < II, SVL ≤ 20.4 in males, presence of vocal slits in males, granular/pustulate dorsal skin with well-developed scapular ridges, basal webbing between fingers, fringes on fingers and toes, crossed iris, diffuse yellow or pale green wash on groin, and absence of flashy colour on axillary/pre-axillary region. The advertisement call consists of a single note repeated at a rate of ca 11 calls/min with a dominant frequency ranging from 2756 to 3101 Hz. Pristimantis marmoratus is primarily arboreal, exclusively active at dusk, and probably restricted to the pristine rainforests of the Pantepui uplands and highlands, east of the Gran Sabana between ca 600 and 1800 m above sea level. Preliminary molecular analyses recovered Pristimantis marmoratus as sister to an unnamed species from the Eastern Guiana Shield. On grounds of the newly established distributional extent we suggest maintaining the IUCN conservation status as Least Concern.

References

Avila-Pires T.C.S., Hoogmoed M.S. & Rocha W.A. 2010. Notes on the vertebrates of northern Pará, Brazil: a forgotten part of the Guianan Region, I. Herpetofauna. Boletim do Museu Paraense Emílio Goeldi. Ciências Naturais 5 (1): 13–112.

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

Bossuyt F. & Milinkovitch M.C. 2000. Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proceedings of the National Academy of Sciences 97: 6585–6590. https://doi.org/10.1073/pnas.97.12.6585

Boulenger G.A. 1900. Batrachians. In: Lankester E.R. (ed.) Report on a collection made by Messrs. McConnell, F.V. & Quelch J.J. at Mount Roraima in British Guiana. Transactions of the Linnean Society of London, Series 2, Zoology 8: 55–56. https://doi.org/10.1111/j.1096-3642.1900.tb00308.x

Brown N.E. and others (sic). 1901. Report on two botanical collections made by Messrs. F.V. McConnell and J.J. Quelch at Mount Roraima in British Guiana. Transactions of the Linnean Society of London, Series 2, Botany 6: 1–107. https://doi.org/10.1111/j.1095-8339.1901.tb00001.x

Canedo C. & Haddad C.F.B. 2012. Phylogenetic relationships within anuran clade Terrarana, with emphasis on the placement of Brazilian Atlantic rainforest frogs genus Ischnocnema (Anura: Brachycephalidae). Molecular Phylogenetics and Evolution 65: 610–620. https://doi.org/10.1016/j.ympev.2012.07.016

Charif R.A., Waack A.M. & Strickman L.M. 2010. Raven Pro 1.4 User’s Manual. Cornell Laboratory of Ornithology, Ithaca, NY.

Chubb C. 1921. The Birds of British Guiana. Volume 2. Bernard Quaritch, London.

Cole C.J., Townsend C.R., Reynolds R.P., MacCulloch R.D. & Lathrop A. 2013. Amphibians and reptiles of Guyana, South America: illustrated keys, annotated species accounts, and a biogeographic synopsis. Proceedings of the Biological Society of Washington 125 (4): 317–620. https://doi.org/10.2988/0006-324X-125.4.317

Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: More models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2019

Dias Lima J. 2008. A herpetofauna do Parque Nacional do Montanhas do Tumucumaque, Amapá, Brasil, Expedições I a V. In: Bernard E. (ed.) Inventários Biológicos Rápidos no Parque Nacional Montanhas do Tumucumaque, Amapá, Brasil. RAP Bulletin of Biological Assessment 48: 38–50.

Duellman W.E. 1997. Amphibians of La Escalera Region, southeastern Venezuela: taxonomy, ecology, and biogeography. Scientific Papers of the Natural History Museum of the University of Kansas 2: 1–52.

Duellman W.E. & Lehr E. 2009. Terrestrial-breeding frogs (Strabomantidae) in Peru. NTV Science, Münster, Germany.

Ernst R., Rödel M. & Arjoon D. 2005. On the cutting edge – The anuran fauna of the Mabura Hill Forest Reserve, Central Guyana. Salamandra 41(4): 179–194.

Fouquet A., Gilles A., Vences M., Marty C., Blanc M. & Gemmell N.J. 2007. Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS ONE 2 (10): e1109. https://doi.org/10.1371/journal.pone.0001109

Fouquet A., Martinez Q., Courtois E.A., Dewynter M., Pineau K., Gaucher P., Blanc M., Marty C. & Kok P.J.R. 2013. A new species of the genus Pristimantis (Amphibia, Craugastoridae) associated with the moderately elevated massifs of French Guiana. Zootaxa 3750: 569–586. https://doi.org/10.11646/zootaxa.3750.5.8

Fouquet A., Martinez Q., Zeidler L., Courtois E.A., Gaucher P., Blanc M., Dias Lima J., Marques Souza S., Rordrigues M.T. & Kok P.J.R. 2016. Cryptic diversity in the Hypsiboas semilineatus species group (Amphibia, Anura) with the description of a new species from the eastern Guiana Shield. Zootaxa 4084: 79–104. https://doi.org/10.11646/zootaxa.4084.1.3

Frost D.R. (1985) Amphibian Species of the World. A Taxonomic and Geographical Reference. Allen Press, Lawrence, Kansas, U.S.A.

Frost D.R. (2016) Amphibian Species of the World: an Online Reference. Version 6.0, American Museum of Natural History, New York, USA. Available from http://research.amnh.org/herpetology/amphibia/index.html [accessed 1 Aug. 2016].

Guayasamin J.M., Krynak T., Krynak K., Culebras J. & Hutter C.R. 2015. Phenotypic plasticity raises questions for taxonomically important traits: a remarkable new Andean rainfrog (Pristimantis) with the ability to change skin texture. Zoological Journal of the Linnean Society 173: 913–928.

https://doi.org/10.1111/zoj.12222

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

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

IUCN Standards and Petitions Subcommittee. 2016. Guidelines for Using the IUCN Red List Categories and Criteria. Version 12. Prepared by the Standards and Petitions Subcommittee. Available from http://www.iucnredlist.org/documents/RedListGuidelines.pdf [accessed 27 Oct. 2017]

Katoh K. & Standley D.M. 2013. MAFFT Multiple Sequence Alignment Software Version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.

https://doi.org/10.1093/molbev/mst010

Köhler J., Jansen M., Rodríguez A., Kok P.J.R., Toledo L.F., Emmrich M., Glaw F., Haddad C.F.B., Rödel M.-O. & Vences M. 2017. The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa 4251: 1–124. https://doi.org/10.11646/zootaxa.4251.1.1

Kok P.J.R. 2013. Two new charismatic Pristimantis species (Anura: Craugastoridae) from the tepuis of the “Lost World” (Pantepui region, South America). European Journal of Taxonomy 60: 1–24. https://doi.org/10.5852/ejt.2013.60

Kok P.J.R. & Barrio-Amorós C.L. 2013. On the taxonomic validity of Pristimantis tepuiensis (Schlüter & Rödder, 2007) and P. stegolepis (Schlüter & Rödder, 2007), with remarks on the type series of P. guaiquinimensis (Schlüter & Rödder, 2007). Zootaxa 3694: 75–80. https://doi.org/10.11646/zootaxa.3694.1.6

Kok P.J.R. & Kalamandeen M. 2008. Introduction to the Taxonomy of the Amphibians of Kaieteur National Park, Guyana. Abc Taxa 5, Royal Belgian Institute of Natural Sciences, Brussels.

Kok P.J.R., Means D.B. & Bossuyt F. 2011. A new highland species of Pristimantis Jiménez de la Espada, 1871 (Anura: Strabomantidae) from the Pantepui region, northern South America. Zootaxa 2934: 1–19.

Kok P.J.R., MacCulloch R.D., Gaucher P., Poelman E.H., Bourne G.R., Lathrop A. & Lenglet G.L. 2006. A new species of Colostethus (Anura, Dendrobatidae) from French Guiana with a redescription of Colostethus beebei (Noble, 1923) from its type locality. Phyllomedusa 5: 43–66.

Kok P.J.R., MacCulloch R.D., Means D.B., Roelants K., Van Bocxlaer I. & Bossuyt F. 2012. Low genetic diversity in tepui summit vertebrates. Current Biology 22: R589–R590.

https://doi.org/10.1016/j.cub.2012.06.034

Kok P.J.R., Willaert B. & Means D.B. 2013. A new diagnosis and description of Anomaloglossus roraima (La Marca, 1998) (Anura: Aromobatidae: Anomaloglossinae), with description of its tadpole and call. South American Journal of Herpetology 8(1): 29–45. https://doi.org/10.2994/SAJH-D-12-00021.1

Lescure J. 1976. Contribution à l’étude des amphibiens de Guyane Française. VI. Liste préliminaire des anoures. Bulletin du Museum National d’Histoire Naturelle, Série 3, Zoologie 377: 475–524.

Lescure J. 1981. Contribution à l’étude des amphibiens de Guyane Française. VII. Les Eleutherodactylus (Anura, Leptodactylidae). Revue française d’Aquariologie 8: 25–32.

Lescure J. & Marty C. 2001. Atlas des Amphibiens de Guyane. Patrimoines Naturels, Muséum national d’Histoire naturelle, Paris.

MacCulloch R.D. & Lathrop A. 2009. Herpetofauna of Mount Ayanganna, Guyana. Results of the Royal Ontario Museum Ayanganna Expedition 2000. Royal Ontario Museum Science Contributions 4: 1–36.

MacCulloch R., Reynolds R., Rodrigues M.T. & Mijares A. 2010. Pristimantis marmoratus. The IUCN Red List of Threatened Species 2010: e.T56743A11529534. https://doi.org/10.2305/IUCN.UK.2010-2.RLTS.T56743A11529534.en

Marty C. & Gaucher P. 1999. Guide sonore des Amphibiens Anoures de Guyane. CD audio. CEBA, Mens, France.

McDiarmid R.W. & Donnelly M.A. 2005. The herpetofauna of the Guayana Highlands: amphibians and reptiles of the Lost World. In: Donnelly M.A., Crother B.I., Guyer C., Wake M.H. & White M.E. (eds) Ecology and Evolution in the Tropics: A Herpetological Perspective: 461–560. University of Chicago Press, Chicago.

Mendoza Á.M, Ospina O.E., Cárdenas-Henao H. & García-R.J.C. 2015. A likelihood inference of historical biogeography in the world’s most diverse terrestrial vertebrate genus: Diversification of direct-developing frogs (Craugastoridae: Pristimantis) across the Neotropics. Molecular Phylogenetics and Evolution 85: 50–58. https://doi.org/10.1016/j.ympev.2015.02.001

Myers C.W. & Donnelly M.A. 2001. Herpetofauna of the Yutajé–Corocoro massif, Venezuela: second report from the Robert G. Goelet American Museum–Terramar expedition to the Northwestern tepuis. Bulletin of the American Museum of Natural History 261: 1–85.

Ouboter P.E. & Jairam R. 2012. Amphibians of Suriname. Brill Academic Publishers, Leiden.

Padial J.M., Grant T. & Frost D.R. 2014. Molecular systematics of terraranas (Anura: Brachycephaloidea) with an assessment of the effects of alignment and optimality criteria. Zootaxa 3825: 1–132. https://doi.org/10.11646/zootaxa.3825.1.1

Phelps W.H. 1938. The geographical status of the birds collected at Mount Roraima. Boletín de la Sociedad Venezolana de Ciencias Naturales 36: 83–95.

Pyron R.A. & 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. https://doi.org/10.1016/j.ympev.2011.06.012

Rambaut A. 2014. Figtree, a graphical viewer of phylogenetic trees. Available from http://tree.bio.ed.ac.uk/software/gtree [accessed 6 Sep. 2016].

Rambaut A. & Drummond A.J. 2007. Tracer version 1.5.

Available from http://tree.bio.ed.ac.uk/software/tracer [accessed 6 Sep. 2016].

R Development Core Team. 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from http://www.R-project.org [accessed 25 Jul. 2016].

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

Rivero J.A. 1968. A new species of Eleutherodactylus (Amphibia, Salientia) from the Guayana Region, Edo. Bolívar, Venezuela. Breviora 306: 1–10.

Roelants K., Gower D.J., Wilkinson M., Loader S.P., Biju S.D., Guillaume K., Moriau L. & Bossuyt F. 2007. Global patterns of diversification in the history of modern amphibians. Proceedings of the National Academy of Sciences 104: 887–892. https://doi.org/10.1073/pnas.0608378104

Simon C., Frati F., Beckenbach A., Crespi B., Liu H. & Flook P. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87: 651–702.

Sueur J., Aubin T. & Simonis C. 2008. Equipment review: Seewave, a free modular tool for sound analysis and synthesis. Bioacoustics 18 (2): 213–226. https://doi.org/10.1080/09524622.2008.9753600

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. https://doi.org/10.1093/molbev/msr121

Tate G.H. 1930. Notes on Mount Roraima region. Geographical Review 20: 312–52.

Vences M., Thomas M., van der Meijden A., Chiari Y. & Vieites D.R. 2005. Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Frontiers in Zoology 2: 5.

https://doi.org/10.1186/1742-9994-2-5

Published
2018-01-23
How to Cite
Kok, P. J., Dezfoulian, R., Means, D. B., Fouquet, A., & Barrio-Amorós, C. L. (2018). Amended diagnosis and redescription of Pristimantis marmoratus (Boulenger, 1900) (Amphibia: Craugastoridae), with a description of its advertisement call and notes on its breeding ecology and phylogenetic relationships. European Journal of Taxonomy, (397). https://doi.org/10.5852/ejt.2018.397
Issue
No. 397 (2018): Amended diagnosis and redescription of Pristimantis marmoratus (Boulenger, 1900) (Amphibia: Craugastoridae), with a description of its advertisement call and notes on its breeding ecology and phylogenetic relationships
Section
Zoology
Copyright (c) 2018 Philippe J.R. Kok, Raheleh Dezfoulian, D. Bruce Means, Antoine Fouquet, César L. Barrio-Amorós

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