Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2017-05-22
Page range: 245–264
Abstract views: 244
PDF downloaded: 2

A new morphologically cryptic species of Phyllomedusa (Anura: Phyllomedusidae) from Amazonian forests of northern Peru revealed by DNA sequences

Lab. de Sistemática de Vertebrados, Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Av. Ipiranga, 6681, Prédio 40, sala 110, 90619-900, Porto Alegre, Brazil. Department of Herpetology, American Museum of Natural History, Central Park West & 79th St., New York, NY 10024, USA.
Hessisches Landesmuseum Darmstadt, Friedensplatz 1, 64283 Darmstadt, Germany.
Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales-CSIC, C/ José Gutiérrez Abascal 2, 28006 Madrid, Spain.
Department of Herpetology, American Museum of Natural History, Central Park West & 79th St., New York, NY 10024, USA.
Amphibia Phyllomedusinae leaf frogs monkey frogs Phyllomedusa camba Phyllomedusa tarsius phylogeny sibling species species group

Abstract

We describe and name Phyllomedusa chaparroi sp. nov., a medium-sized species (snout–vent length in adult males 67.9–77.5 mm) of monkey frog from Amazonian rainforests of northern Peru. Although morphologically most similar to P. boliviana and P. camba (indistinguishable from the latter in external qualitative and quantitative traits), phylogenetic analysis of combined mitochondrial and nuclear markers place the new species sister to a clade containing P. neildi, P. tarsius, and P. trinitatis. Phyllomedusa chaparroi can be readily differentiated from these species by having a dark reddish-brown iris with indistinct tiny orange spots versus an orange iris with marked dark reticulation found in P. neildi, P. tarsius, and P. trinitatis. Furthermore, genetic distances for a 532 bp sequence of the 16S gene between the new species and its sister species are 2.8–4.1 %, whereas distances are 4.5–5.5 % to the morphologically cryptic P. camba. We briefly discuss the importance of DNA sequences in revealing morphologically cryptic species and modify the content of the P. tarsius species group based on phylogenetic analyses and observations on iris coloration.

References

  1. Bazinet, A.L., Zwickl, D.J. & Cummings, M.P. (2014) A gateway for phylogenetic analysis powered by grid computing featuring GARLI 2.0. Systematic Biology, 63, 812–818.
    https://doi.org/10.1093/sysbio/syu031

    Barrio-Amorós, C.L. (2006) A new species of Phyllomedusa (Anura: Hylidae: Phyllomedusinae) from northwestern Venezuela. Zootaxa, 1309, 55–68.

    Barrio-Amorós, C.L. (2009) Distribución y aspectos de la historia natural de las ranas lémur (Hylidae: Phyllomedusinae) en Venezuela. Memoria de la Fundación La Salle de Ciencias Naturales Caracas, 171, 19–46.

    Bremer, K. (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution, 42, 795–803.
    https://doi.org/10.2307/2408870

    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 & Evolution, 22, 148–155.
    https://doi.org/10.1016/j.tree.2006.11.004

    Bruschi, D.P., Lucas, E.M., Garcia, P.C.A. & Recco-Pimentel, S.M. (2014) Molecular and morphological evidence reveals a new species in the Phyllomedusa hypochondrialis group (Hylidae, Phyllomedusinae) from the Atlantic Forest of the highlands of southern Brazil. PLoS ONE, 9 (8), e105608.
    https://doi.org/10.1371/journal.pone.0105608

    Cannatella, D.C. (1982) Leaf-frogs of the Phyllomedusa perinesos group (Anura, Hylidae). Copeia, 1982, 501–513.
    https://doi.org/10.2307/1444649

    Cannatella, D.C. (1983) Synonymy and distribution of Phyllomedusa boliviana Boulenger (Anura: Hylidae). Proceedings of the Biological Society Washington, 96, 59–66.

    Caramaschi, U. (2006) Redefinição do grupo de Phyllomedusa hypochondrialis, com redescrição de P. megacephala (Miranda-Ribeiro, 1926), revalidação de P. azurea Cope, 1862 e descrição de uma nova espécie (Amphibia, Anura, Hylidae). Arquivos do Museu Nacional. Rio de Janeiro, 64, 159–179.

    Carstens, B.C., Pelletier, T.A., Reid, N.M. & Satler, J.D. (2013) How to fail at species delimitation. Molecular Ecology, 22, 4369–4383.
    https://doi.org/10.1111/mec.12413

    Cope, E.D. (1868) An examination of the Reptilia and Batrachia obtained by the Orton Expedition to Equador and the Upper Amazon, with notes on other species. Proceedings of the Academy of Natural Sciences of Philadelphia, 20, 96–140.

    De la Riva, I. (1999) A new Phyllomedusa from southwestern Amazonia (Amphibia: Anura: Hylidae). Revista Española de Herpetología, 13, 123–131.

    Duellman, W.E. (1974) Taxonomic notes on Phyllomedusa (Anura: Hylidae) from the upper Amazon basin. Herpetologica, 30, 105–112.

    Duellman, W.E. (1978) The biology of an equatorial herpetofauna in Amazonian Ecuador. University of Kansas Museum of Natural History Miscellaneous Publication, 65, 1–352.

    Duellman, W.E., Cadle, J.E. & Cannatella, D.C. (1988) A new species of terrestrial Phyllomedusa (Anura: Hylidae) from southern Peru. Herpetologica, 44, 91–95.

    Duellman, W. E (2005). Cusco Amazónico: The lives of amphibians and reptiles in an Amazonian rainforest. Comstock Publishing Associates, Ithaca and London, 433 pp.

    Duellman, W.E., Marion, A.B. & Hedges, S.B. (2016) Phylogenetics, classification, and biogeography of the treefrogs (Amphibia: Anura: Arboranae). Zootaxa, 4104, 1–109.
    https://doi.org/10.11646/zootaxa.4104.1.1

    Egge, J.J. & Simons, A.M. (2006) The challenge of truly cryptic diversity: diagnosis and description of a new madtom catfish (Ictaluridae: Noturus). Zoologica Scripta, 35, 581–595.
    https://doi.org/10.1111/j.1463-6409.2006.00247.x

    Faivovich, J., Haddad, C.F.B., Garcia, P., 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.
    https://doi.org/10.1206/0003-0090(2005)294[0001:SROTFF]2.0.CO;2

    Faivovich, J., Haddad, C.F.B., Baêta, D., Jungfer, K.-H., Álvares, G.F.R., Brandao, R. A., Sheil, C., Barrientos, L.S., Barrio-Amorós, C.L., Cruz, C.A.G. & Wheeler, W.C. (2010) The phylogenetic relationships of the charismatic poster frogs, Phyllomedusinae (Anura, Hylidae). Cladistics, 26, 227–261.
    https://doi.org/10.1111/j.1096-0031.2009.00287.x

    Farris, J.S., Albert, V.A., Källersjö, M., Lipscomb, D. & Kluge, A.G. (1996) Parsimony jackknifing outperforms neighbor-joining. Cladistics, 12, 99–124.
    https://doi.org/10.1111/j.1096-0031.1996.tb00196.x

    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, e1109.
    https://doi.org/10.1371/journal.pone.0001109

    Frost, D.R. (2017) Amphibian Species of the World: an online reference. Version 6.0 (29/01/2017). American Museum of Natural History, New York, USA. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 13 March 2017)

    Frost, D.R. & Kluge, A.G. (1994) A consideration of epistemology in systematic biology, with special reference to species. Cladistics, 10, 259–294.
    https://doi.org/10.1111/j.1096-0031.1994.tb00178.x

    Funk, W.C., Caminer, M. & Ron, S.R. (2012) High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society of London B, 279, 1806–1814.
    https://doi.org/10.1098/rspb.2011.1653

    Funkhouser, A. (1957) A review of the Neotropical tree-frogs of the genus Phyllomedusa. Occasional Papers of the Natural History Museum of Stanford University, 5, 1–90.

    Gehara, M., Crawford, A.J., Orrico, V.G.D., Rodríguez, A., Lötters, S., Fouquet, A., Barrientos, L.S., Brusquetti, F., De la Riva, I., Ernst, R., Gagliardi Urrutia, G., Glaw, F., Guayasamin, J.M., Hölting, M., Jansen, M., Kok, P.J.R., Kwet, A., Lingnau, R., Lyra, M., Moravec, J., Pombal Jr., J.P., Rojas-Runjaic, F.J.M., Schulze, A., Señaris, J.C., Solé, M., Trefaut Rodriguez, M., Twomey, E., Haddad, C.F.B., Vences, M. & Köhler, J. (2014) High levels of diversity uncovered in a widespread nominal taxon: continental phylogeography of the Neotropical tree frog Dendropsophus minutus. PLoS ONE, 9, e103958.
    https://doi.org/10.1371/journal.pone.0103958

    Ghiselin, M.T. (1974) A radical solution to the species problem. Systematic Biology, 23, 536–544.
    https://doi.org/10.1093/sysbio/23.4.536

    Goloboff, P.A., Farris, J.S. & Nixon, K.C. (2008) TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786.
    https://doi.org/10.1111/j.1096-0031.2008.00217.x

    Goodman, M., Olson, C.B., Beeber, J.E. & Czelusniak, J. (1982) New perspectives in the molecular biological analysis of mammalian phylogeny. Acta Zoologica Fennica, 169, 19–35.

    Grant, T. & Kluge, A.G. (2008a) Credit where credit is due: the Goodman-Bremer support metric. Molecular Phylogenetics and Evolution, 49, 405–406.
    https://doi.org/10.1016/j.ympev.2008.04.023

    Guayasamin, J.M., Castroviejo-Fisher, S., Ayarzagüena, J., Trueb, L. & Vilà, C. (2008) Phylogenetic relationships of glassfrogs (Centrolenidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 48, 574–595.
    https://doi.org/10.1016/j.ympev.2008.04.012

    Günther, A.C.L.G. (1858) On the systematic arrangement of the tailless batrachians and the structure of Rhinophrynus dorsalis. Proceedings of the Zoological Society of London, 1858, 339–352.
    https://doi.org/10.1111/j.1469-7998.1858.tb06387.x

    Hammer, Ø., Harper, D.A.T., Ryan, P.D. (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4 (1), 9 pp.
    http://palaeo-electronica.org/2001_1/past/issue1_01.htm

    Heyer, R., Donnelly, M. A., Foster, M. & Mcdiarmid, R. (Eds.) (1994) Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Institution Press, Washington & London, 364 pp.

    Hull, D.L. (1976) Are species really individuals? Systematic Biology, 25, 174–191.
    https://doi.org/10.2307/2412744

    Jungfer, K.-H., Faivovich, J., Padial, J.M., Castroviejo-Fisher, S., Lyra, M.L., Berneck, B.V.M., Iglesias, P.P., Kok, P.J.R., MacCulloch, R.D., Rodrigues, M.T., Verdade, V.K., Torres Gastello, C.P., Chaparro, J.C., Valdujo, P.H., Reichle, S., Moravec, J., Gvoždík, V., Gagliardi-Urrutia, G., Ernst, R., De la Riva, I., Means, D.B., Lima, A.P., Señaris, J.C., Wheeler, W.C. & Haddad, C.F.B. (2013) Systematics of spiny-backed treefrogs (Hylidae: Osteocephalus): an Amazonian puzzle. Zoologica Scripta, 42, 351–380.
    https://doi.org/10.1111/zsc.12015

    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

    Lanfear, R., Calcott, B., Ho S.Y. & Guindon S. (2012) PartitionFinder combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
    https://doi.org/10.1093/molbev/mss020

    Leaché, A.D. & Fujita, M.K. (2010) Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society of London B: Biological Sciences.
    https://doi.org/10.1098/rspb.2010.0662

    Mayr, E. (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press, Massachusetts, 372 pp.

    Padial, J.M., Miralles, A., De la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, 1–14.
    https://doi.org/10.1186/1742-9994-7-16

    Pante, E., Schoelinck, C. & Puillandre, N. (2014) From integrative taxonomy to species description: one step beyond. Systematic Biology, 64, 152–160.
    https://doi.org/10.1093/sysbio/syu083

    Pérez-Ponce de León, G. & Poulin, R. (2016) Taxonomic distribution of cryptic diversity among metazoans: not so homogeneous after all. Biology Letters, 12 (8), 1–5.
    https://doi.org/10.1098/rsbl.2016.0371

    Pombal, J.P. & Haddad, C.F.B. (1992) Espécies de Phyllomedusa do grupo burmeisteri do Brasil Oriental, com descrição de uma espécie nova (Amphibia, Hylidae). Revista Brasilera de Biologia, 52, 217–229.

    Ron, S.R., Almendáriz, A. & Cannatella, D.C. (2013) The Phyllomedusa perinesos group (Anura: Hylidae) is derived from a Miocene Amazonian Lineage. Zootaxa, 3741 (2), 289–294.
    https://doi.org/10.11646/zootaxa.3741.2.7

    Ron, S.R., Guayasamin, J.M., Yanez-Muñoz, M.H., Merino-Viteri, A. Ortiz, D.A. & Nicolalde, D.A. (2016) AmphibiaWebEcuador. Version 2016.0 (04/07/2016). Museo de Zoología, Pontificia Universidad Católica del Ecuador. Available from: http://zoologia.puce.edu.ec/Vertebrados/anfibios (accessed 13 March 2017)

    Shreve, B. (1959) A new species of Phyllomedusa from Bolivia (Salientia, Hylidae). Breviora, 113, 1–4.

    Simpson, G.G. (1951) The species concept. Evolution, 5, 285–298.
    https://doi.org/10.2307/2405675

    VerNet (2016) Version 2016-02-02T08:59-03:00. Available from: http://www.vertnet.org/index.html (accessed 13 March 2017)

    Wiens, J.J., Fetzner, J.W., Parkinson, C.L. & Reeder, T.W. (2005) Hylid frog phylogeny and sampling strategies for speciose clades. Systematic Biology, 54, 778–807.
    https://doi.org/10.1080/10635150500234625

    Wiens, J.J., Graham, C.H., Moen, D.S., Smith, S.A. & Reeder, T.W. (2006) Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity. The American Naturalist, 168, 579–596.
    https://doi.org/10.1086/507882

    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.
    https://doi.org/10.1016/j.ympev.2010.03.013

    Wiley, E.O. (1978) The evolutionary species concept reconsidered. Systematic Biology, 27, 17–26.
    https://doi.org/10.2307/2412809

    Wiley, E.O. (1981) Phylogenetics: theory and practice of phylogenetic systematics. Wiley Interscience, New York, 439 pp.

    Zwickl, D.J. (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. Dissertation, The University of Texas, Austin, 115 pp.