Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2018-07-19
Page range: 501–524
Abstract views: 119
PDF downloaded: 4

A new species of Phrynopus from the northeastern Andes of Peru, its phylogenetic position, and notes on the relationships of Holoadeninae (Anura: Craugastoridae)

División de Herpetología-Centro de Ornitología y Biodiversidad (CORBIDI), Urb. Huertos de San Antonio, Surco, Lima-Perú
División de Herpetología-Centro de Ornitología y Biodiversidad (CORBIDI), Urb. Huertos de San Antonio, Surco, Lima-Perú
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. Biological Sciences Department Bronx Community College City university of New York (CUNY) 2155 University Avenue, Bronx, New York 10453, USA
Amphibia Alto Mayo Amazon Basin Cordillera Central dynamic homology Terrarana tree-alignment Yungas

Abstract

We report the discovery of a geographically disjunct and morphologically distinctive species of direct-developing frog of the genus Phrynopus (Phrynopus mariellaleo sp. nov.) that changes considerably our understanding of the distribution of species in this Andean genus. The type locality lies on a subcordillera (Cerro de Campanario area) of the extreme northeastern portion of the Cordillera Central of Peru, on the headwaters of the Mayo River, Amazonas department, at 2575 m asl (6°6’42.9’’S, 77°26’24’’W). This area is situated 170 km to the NE from the northernmost record of Phrynopus known so far. Molecular phylogenetic analyses of a supermatrix (13269 aligned positions of gene sequences of four mitochondrial and ten nuclear genes) of 105 terminals (representing 93 named and 9 unnamed species of Holoadeninae) recover this new species as the sister to Phrynopus auriculatus, a species occurring more than 500 km south of the type locality of the new species. Both Phrynopus auriculatus and the new species occur at moderate elevations on the easternmost stretches of the Andean subcordilleras; their sister relationship point to a potentially broader distribution of species of Phrynopus along the poorly sampled intervening areas of the eastern hills of the Andes. The new species has a conspicuous and visibly large tympanic membrane (a trait rare in the clade), outlined by a marked bold black supratympanic fold and a black facial mask, and exhibits conspicuous dorsolateral, scapular, and middorsal Y-shaped folds. Specimens were found on the forest floor—a rocky substrate covered by a thick layer of leaf litter, moss and roots—of a primary humid montane forest (Yungas ecoregion) with scattered patches of bamboo (Chusquea spp.). Our phylogenetic analyses corroborate the monophyly of all Holoadeninae genera, including Euparkerella and Psychrophrynella, genera for which tests of monophyly were pending, and corroborates Hypodactylus nigrovittatus as part of Hypodactylus and sister to a clade that includes H. brunneus, H. elassodiscus and H. peraccai.

 

References

  1. Brack, A. (1986) Las Ecorregiones del Perú. Boletín de Lima, 44, 57–70.

    Canedo, C. & Haddad, C.F. (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

    Catenazzi, A. & Ttito, A. (2016) A new species of Psychrophrynella (Amphibia, Anura, Craugastoridae) from the humid montane forests of Cusco, eastern slopes of the Peruvian Andes. Peerj, 4 (e1807), 1–22.
    https://doi.org/10.7717/peerj.1807

    Chaparro, J.C., Padial, J.M. & De la Riva, I. (2008) Two sympatric new species of Phrynopus (Anura: Strabomantidae) from Yanachaga Chemillén National Park (central Peruvian Andes). Zootaxa, 1761, 49–58.

    Chávez, G., Santa Cruz, R., Rodríguez, D. & Lehr, E. (2015) Two new species of frogs of the genus Phrynopus (Anura: Terrarana: Craugastoridae) from the Peruvian Andes. Amphibian and Reptile Conservation, 9 (e105), 15–25.

    De la Riva, I., Chaparro, J.C., Castroviejo-Fisher, S. & Padial, J.M. (2017) Underestimated anuran radiations in the high Andes: five new species and a new genus of Holoadeninae, and their phylogenetic relationships (Anura: Craugastoridae). Zoological Journal of the Linnaean Society, 182, 129–172.
    https://doi.org/10.1093/zoolinnean/zlx020

    Duellman, W.E. & Pramuk, J.B. (1999) Frogs of the genus Eleutherodactylus (Anura: Leptodactylidae) in the Andes of northern Peru. Scientific Papers of the Natural History Museum, University of Kansas, 13, 1–78.

    Duellman, W.E. (2000) Leptodactylid frogs of the genus Phrynopus in northern Peru with descriptions of three new species. Herpetologica, 56, 273–285.

    Duellman, W.E. & Hedges, S.B. (2008) Two minute species of Phrynopus (Lissamphibia: Anura) from the Cordillera Oriental in Peru. Zootaxa, 1675, 59–66.

    Duellman, W.E. & Lehr, E. (2009) Terrestrial-breeding frogs (Strabomantidae) in Peru. Natur und Tier-Verlag, Naturwissenschaft, Münster, 382 pp.

    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

    Frost, D.R. (2018) Amphibian Species of the World: an Online Reference. Version 6.0. Electronic Database accessible. American Museum of Natural History New York, USA. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 15 March 2018)

    Fusinatto, L.A., Alexandrino, J., Haddad, C.F.B., Brunes, T.O., Rocha, C.F.D. & Sequeira, F. (2013) Cryptic genetic diversity is paramount in small-bodied amphibians of the genus Euparkerella (Anura: Craugastoridae) endemic to the Brazilian Atlantic forest. PLoS ONE, 8 (e79504), 1–12.
    https://doi.org/10.1371/journal.pone.0079504

    Goloboff, P.A. (1996) Methods for faster parsimony analysis. Cladistics, 12, 199–220.
    https://doi.org/10.1111/j.1096-0031.1996.tb00009.x

    Goloboff, P.A. (1999) Analyzing large data sets in reasonable times, solutions for composite optima. Cladistics, 15, 415–428.
    https://doi.org/10.1111/j.1096-0031.1999.tb00278.x

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

    Grant, T. & Kluge, A.G. (2008) Clade support measures and their adequacy. Cladistics, 24, 1051–1064.
    https://doi.org/10.1111/j.1096-0031.2008.00231.x

    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.

    Heinicke, M.P., Duellman, W.E. & Hedges, S.B. (2007) Major Caribbean and Central American frog faunas originated by ancient oceanic dispersal. Proceedings of the National Academy of Sciences of the United Stated of America, 24, 10092–10097.
    https://doi.org/10.1073/pnas.0611051104

    Heinicke, M.P., Duellman, W.E., Trueb, L., Means, D.B., MacCulloch, R.D. & Hedges, S.B. (2009) A new frog family (Anura: Terrarana) from South America and an expanded direct-developing clade revealed by molecular phylogeny. Zootaxa, 2211, 1–35.

    Heinicke, M.P., Lemmon, A.R., Lemmon, E.M., McGrathc, K. & Hedges, S.B. (2018) Phylogenomic support for evolutionary relationships of New World direct-developing frogs (Anura: Terraranae). Molecular Phylogenetics and Evolution, 118, 145–155.
    https://doi.org/10.1016/j.ympev.2017.09.021

    Heyer, W.R. (1975) A preliminary analysis of the intergeneric relationships of the frog family Leptodactylidae. Smithsonian Contributions to Zoology, 199, 1–55.
    https://doi.org/10.5479/si.00810282.199

    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. & Padial, J.M. (2016) Description and phylogenetic position of a new (singleton) species of Oreobates Jiménez de la Espada, 1872 (Anura: Craugastoridae) from the Yungas of Cochabamba, Bolivia. Annals of Carnegie Museum, 84, 23–38.
    https://doi.org/10.2992/007.084.0104

    Lehr, E. & Oróz. A. (2012) Two new species of Phrynopus (Anura: Strabomantidae) from the Cordillera de Carpish in central Peru (Departamento de Huánuco). Zootaxa, 3512, 53–63.

    Lehr, E., Moravec, J. & Cusi, J.C. (2012) Two new species of Phrynopus (Anura, Strabomantidae) from high elevations in the Yanachaga-Chemillén National park in Peru (Departamento de Pasco). ZooKeys, 235, 51–71.
    https://doi.org/10.3897/zookeys.235.3885

    Lehr, E. & Rodríguez, D. (2017) Two new species of Andes frogs (Craugastoridae: Phrynopus) from the Cordillera de Carpish in Central Peru. Salamandra, 53, 327–338.

    Lehr, E., von May, R., Moravec, J. & Cusi, J.C. (2017) Three new species of Pristimantis (Amphibia, Anura, Craugastoridae) from upper montane forests and high Andean grasslands of the Pui Pui Protected Forest in central Peru. Zootaxa, 4299 (3), 301–336.
    https://doi.org/10.11646/zootaxa.4299.3.1

    Lehr, E., von May, R., Moravec, J. & Cusi, J.C. (2017) A new species of Phrynopus (Amphibia, Anura, Craugastoridae) from upper montane forests and high Andean grasslands of the Pui Pui Protected Forest in central Peru. ZooKeys, 713, 131–157.
    https://doi.org/10.3897/zookeys.713.20776

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

    Mamani, L. & Malqui, S. (2014) A new species of Phrynopus (Anura: Craugastoridae) from the central Peruvian Andes. Zootaxa, 3838 (2), 207–214.
    https://doi.org/10.11646/zootaxa.3838.2.5

    Motta, A.P., Chaparro, J.C., Pombal, J.P., Junior Guayasamin, J.M., De la Riva, I. & Padial, J.M. (2016) Molecular phylogenetics and taxonomy of the Andean genus Lynchius Hedges, Duellman, and Heinicke 2008 (Anura: Craugastoridae). Herpetological Monographs, 30, 119–142.
    https://doi.org/10.1655/HERPMONOGRAPHS-D-16-00002

    Nixon, K.C. (1999) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics, 15, 407–414.
    https://doi.org/10.1111/j.1096-0031.1999.tb00277.x

    Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D’amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P. & Kassem, K.R. (2001) Terrestrial ecoregions of the world: a new map of life on earth. BioScience, 51, 933−938.
    https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2

    Padial, J.M., Chaparro, J.C., Castroviejo-Fisher, S., Guayasamín, J.M., Lehr, E., Delgado, A.J., Vaira, M., Teixeira, M., Aguayo, R. & De la Riva, I. (2012) A revision of species diversity in the Neotropical genus Oreobates (Anura: Strabomantidae) with the description of three new species from the Amazonian slopes of the Andes and the proposal of candidate species. American Museum Novitates, 3752, 1–55.
    https://doi.org/10.1206/3752.2

    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 (10), 1–132.
    https://doi.org/10.11646/zootaxa.3825.1.1

    Peloso, P.L.V., Frost, D.R., Richards, S.J., Rodrigues, M.T., Donnellan, S.C., Matsui, M., Raxworthy, C.J., Biju, S.D., Lemmon, E.M., Lemmon, A.R. & Wheeler, W.C. (2016) The impact of anchored phylogenomics and taxon sampling on phylogenetic inference in narrow-mouthed frogs (Anura, Microhylidae). Cladistics, 32, 113–140.
    https://doi.org/10.1111/cla.12118

    Peñaherrera del Águila, C. (1989) Atlas del Perú. Instituto Geográfico Nacional, Lima, 400 pp.

    Pyron, R.A. & Wiens, J.J. (2011) A large-scale phylogeny of Amphibia including over 2,800 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

    Rodríguez, L.O. & Catenazzi, A. (2017) Four new species of terrestrial-breeding frogs of the genus Phrynopus (Anura: Terrarana: Craugastoridae) from Río Abiseo National Park, Peru. Zootaxa, 4273 (3), 381–406.
    https://doi.org/10.11646/zootaxa.4273.3.4

    Roelants, K. & Bossuyt, F. (2005) Archaeobatrachian paraphyly and Pangaean diversification of crown-group frogs. Systematic Biology, 54, 111–126.
    https://doi.org/10.1080/10635150590905894

    Varón, A., Vinh, L.S. & Wheeler, W.C. (2010) POY version 4, phylogenetic analysis using dynamic homologies. Cladistics, 26, 72–85.
    https://doi.org/10.1111/j.1096-0031.2009.00282.x

    Von May, R., Lehr, E. & Rabosky, D.L. (2018) Evolutionary radiation of earless frogs in the Andes: molecular phylogenetics and habitat shifts in high-elevation terrestrial breeding frogs. PeerJ, 6, e4313.
    https://doi.org/10.7717/peerj.4313

    Wheeler, W.C. (1996) Optimization alignment, the end of multiple sequence alignment in phylogenetics? Cladistics, 12, 1–10.
    https://doi.org/10.1111/j.1096-0031.1996.tb00189.x

    Wheeler, W.C. (2003) Implied alignment, a synapomorphy-based multiple sequence alignment method and its use in cladogram search. Cladistics, 19, 261–268.
    https://doi.org/10.1111/j.1096-0031.2003.tb00369.x

    Wheeler, W.C., Arango, C.P., Grant, T., Janies, D., Varón, A., Aagesen, L., Faivovich, J., D'Haese, C., Smith, W.L. & Giribet, G. (2006) Dynamic Homology and Phylogenetic Systematics, A Unified Approach Using POY. American Museum of Natural History, New York, 365 pp.

    Wheeler, W.C., Lucaroni, N., Hong, L., Crowley, L.M. & Varón, A. (2015) POY version 5: phylogenetic analysis using dynamic homologies under multiple optimality criteria. Cladistics, 31, 189–196.
    https://doi.org/10.1111/cla.12083

    Zwickl, D.J. & Hillis, D.M. (2002) Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology, 51, 588–598.
    https://doi.org/10.1080/10635150290102339