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Type: Article
Published: 2018-08-23
Page range: 451–476
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Unveiling species diversity in collared frogs through morphological and bioacoustic evidence: a new Mannophryne (Amphibia, Aromobatidae) from Sierra de Aroa, northwestern Venezuela, and an amended definition and call description of M. herminae (Boettger, 1893)

Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Laboratório de Sistemática de Vertebrados. Av. Ipiranga 6681, Porto Alegre, RS 90619-900, Brazil. Fundación La Salle de Ciencias Naturales, Museo de Historia Natural La Salle. Apartado Postal 1930, Caracas 1010-A, Venezuela.
Asociación Civil Grupo Guardaparques Universitarios, Barquisimeto, Lara state, Venezuela. Universidad Central de Venezuela, Facultad de Ciencias, Escuela de Biología. Caracas, Venezuela
Universidad de Los Andes, Laboratorio de Biogeografía, Colección de Anfibios y Reptiles, Mérida 5101, Venezuela.
Amphibia Anura Aromobatinae Coastal Range Cordillera de la Costa Dendrobatoidea Integrative taxonomy

Abstract

Species diversity in collared frogs of the genus Mannophryne is presumed to be underestimated due to the paucity of external morphology characters, but combining morphology with bioacoustics and other lines of evidence has shown to be useful in delimiting species of this group. Herein we describe a new species of Mannophryne from Sierra de Aroa in northwestern Venezuela. The new species is morphologically similar to M. herminae but is readily recognized by its strikingly different advertisement call. It also can be distinguished from all its congeners by the unique combination of its small body size, general color pattern, basal toe webbing, and advertisement call consisting of long trills of single tonal notes emitted at a rate of 2–3 notes/s. Additionally, to facilitate future diagnosis of undescribed species related to M. herminae, we amend the definition of the latter, describe in detail its advertisement call, and redefine its known distribution range. The new species increases the number of described species of Mannophryne to 20.

 

References

  1. Angulo, A. & Reichle, S. (2008) Acoustic signals, species diagnosis, and species concepts: the case of a new cryptic species of Leptodactylus (Amphibia, Anura, Leptodactylidae) from the Chapare region, Bolivia. Zoological Journal of the Linnean Society, 152, 59–77.
    https://doi.org/10.1111/j.1096-3642.2007.00338.x

    Barbour, T. & Noble, G.K. (1920) Some amphibians from northwestern Peru, with a revision of the genera Phyllobates and Telmatobius. Bulletin of the Museum of Comparative Zoology, 63, 395–427.
    http://biodiversitylibrary.org/page/2817193

    Barrio-Amorós, C.L. (1999 “1998”) Sistemática y biogeografía de los anfibios (Amphibia) de Venezuela. Acta Biologica Venezuelica, 18, 1–93.

    Barrio-Amorós, C.L. & Santos, J.C. (2012) A phylogeny for Aromobates (Anura: Dendrobatidae) with description of three new species from the Andes of Venezuela, taxonomic comments on Aromobates saltuensis, A. inflexus, and notes on the conservation status of the genus. Zootaxa, 3422, 1–31.

    Barrio-Amorós, C.L., Rivas, G., Molina, C. & Kaiser, H. (2006) Mannophryne trinitatis (Anura: Dendrobatidae) is a Trinidadian single-island endemic. Herpetological Review, 37, 298–299.

    Barrio-Amorós, C.L., Santos, J.C. & Molina, C.R. (2010a) An addition to the diversity of dendrobatid frogs in Venezuela: description of three new collared frogs (Anura: Dendrobatidae: Mannophryne). Phyllomedusa, 9, 3–35.
    https://doi.org/10.11606/issn.2316-9079.v9i1p03-35

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

    Boettger, O. (1893) Reptilien und Batrachier aus Venezuela. Bericht der Senckenbergischen Naturforschenden Gesellschaft in Frankfurt am Main, 1893, 35–42.

    Brauer, A. (1899) Ein neuer Fall von Brutpflege bei Fröschen. Zoologische Jahrbücher. Abteilung für Systematik, Geographie und Biologie der Tiere, 12, 89–94.
    http://direct.biostor.org/reference/181238

    Dixon, J.R. & Rivero-Blanco, C. (1985) A new dendrobatid frog (Colostethus) from Venezuela with notes on its natural history and that of related species. Journal of Herpetology, 19, 177–184.
    https://doi.org/10.2307/1564170

    Dole, J.W. & Durant, P. (1974) Courtship behavior in Colostethus collaris (Dendrobatidae). Copeia, 1974, 988–990.
    https://doi.org/10.2307/1442607

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

    Duellman, W.E. (1966) Aggressive behavior in dendrobatid frogs. Herpetologica, 22, 217–221. Available from: http://www.jstor.org/stable/3890687 (Accessed 22 Aug. 2018)

    Duellman, W.E. (1970) The hylid frogs of Middle America. Vol. 1. Monograph of the Museum of Natural History, University of Kansas, 1, 1–427.
    https://doi.org/10.5962/bhl.title.2835

    Durant, P. & Dole, J.W. (1975) Aggressive behavior in Colostethus (=Prostherapis) collaris (Anura: Dendrobatidae). Herpetologica, 31, 23–26. Available from: http://www.jstor.org/stable/3891981 (Accessed 22 Aug. 2018)

    Edwards, S.R. (1971) Taxonomic notes on South American Colostethus with descriptions of two new species (Amphibia, Dendrobatidae). Proceedings of the Biological Society of Washington, 84, 147–162. Available from: http://direct.biostor.org/reference/65699 (Accessed 22 Aug. 2018)

    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.
    https://doi.org/10.5962/bhl.part.22165

    Ewel, J.J., Madriz, A. & Tosi, J.A. (1976) Zonas de vida de Venezuela. Memoria explicativa sobre el mapa ecológico. M.A.C. and FONAIAP, Caracas, 270 pp.

    Frost, D.R. (2017) Amphibian Species of the World: an Online Reference. Version 6.0. Electronic Database. American Museum of Natural History, New York, USA. Accessible from: http://research.amnh.org/herpetology/amphibia/index.html. (accessed 28 December 2017)

    García, F., Aular, L., Camargo, E. & Mújica, Y. (2012a “2010”) Murciélagos de la sierra de Aroa, estado Yaracuy, Venezuela. Memoria de la Fundación La Salle de Ciencias Naturales, 173–174, 135–154.

    García, F.J., Delgado-Jaramillo, M.I., Machado, M. & Aular, L. (2012b) Preliminary inventory of mammals from Yurubí National Park, Yaracuy, Venezuela with some comments on their natural history. Revista de Biología Tropical, 60, 459–472.
    https://doi.org/10.15517/rbt.v60i1.2781

    Ginés, H. (1959) Familias y géneros de anfibios -Amphibia- de Venezuela. Memoria de la Sociedad de Ciencias Naturales La Salle, 19, 84–146.

    Grant, T., Frost, D.R., Caldwell, J.P., Gagliardo, R., Haddad, C.F.B., Kok, P.J.R., Means, B.D., Noonan, B.P., Schargel, W.E. & Wheeler, W.C. (2006) Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of American Museum of Natural History, 299, 1–262.
    https://doi.org/10.1206/0003-0090(2006)299[1:PSODFA]2.0.CO;2

    Grant, T., Rada, M., Anganoy-Criollo, M., Batista, A., Dias, P.H., Jeckel, A.M., Machado, D.J. & Rueda-Almonacid, J.V. (2017) Phylogenetic systematics of dart-poison frogs and their relatives revisited (Anura: Dendrobatoidea). South American Journal of Herpetology, 12 (Special Issue 1), 1–90.
    https://doi.org/10.2994/SAJH-D-17-00017.1

    Harding, K.A. (1983) Catalogue of New World Amphibians. Pergamon Press, Oxford and New York, 406 pp.

    Hellmich, W. (1940) Beiträge zur Kenntnis der Gattung Hyloxalus (Brachycephalidae, Amphibia). Zoologischer Anzeiger, 131, 113–128.

    Hernández, O. (2015) In Memoriam: César Ramón Molina Rodriguez. FrogLog, 23, 26–28.

    Huber, O. & Alarcón, C. (1988) Mapa de vegetación de Venezuela. 1:2.000.000. (map).

    Huber, O. & Oliveira-Miranda, M.A. (2010). Ambientes terrestres. In: Rodríguez, J.P., Rojas-Suárez, F. & Giraldo H., D. (Eds.), Libro Rojo de los Ecosistemas Terrestres de Venezuela. Provita, Shell Venezuela, Lenovo, Caracas, pp. 29–89.

    IUCN (2012) IUCN Red List Categories and Criteria. Version 3.1. 2nd Edition. Gland and Cambridge, 32 pp.

    Kaplan, M. (1997) A new species of Colostethus from the Sierra Nevada de Santa Marta (Colombia) with comments on intergeneric relationships within the Dendrobatidae. Journal of Herpetology, 31, 369–375.
    https://doi.org/10.2307/1565665

    Kok, P.J.R. & Kalamandeen, M. (2008) Introduction to the taxonomy of the amphibians of Kaieteur National Park, Guyana. Abc Taxa, 5, 1–278.

    La Marca, E. (1989) A new species of collared frog (Anura: Dendrobatidae: Colostethus) from Serrania de Portuguesa, Andes of Estado Lara, Venezuela. Amphibia-Reptilia, 10, 175–183.
    https://doi.org/10.1163/156853889X00197

    La Marca E. (1992) Catálogo taxonómico, biogeográfico y bibliográfico de las ranas de Venezuela. Cuadernos Geográficos, 9, 1–297.

    La Marca, E. (1994) Taxonomy of the frogs of the genus Mannophryne (Amphibia: Anura: Dendrobatidae). Publicaciones de la Asociación Amigos de Doñana, 4, 1–75.

    La Marca, E., Vences, M. & Lötters, S. (2002) Rediscovery and mitochondrial relationships of the dendrobatid frog Colostethus humilis suggest parallel colonization of the Venezuelan Andes by poison frogs. Studies of Neotropical Fauna and Environment, 37, 233–240.
    https://doi.org/10.1076/snfe.37.3.233.8566

    Lentino, M. & Bruni, A.R. (1994) Humedales costeros de Venezuela: situación ambiental. Sociedad Conservacionista Audubon de Venezuela, Caracas, 188 pp.

    Lutz, A. (1927) Notas sobre batrachios da Venezuela e da ihla de Trinidad. Memórias do Instituto Oswaldo Cruz, 20, 35–65.

    https://doi.org/10.1590/S0074-02761927000100003

    Lynch, J.D. (1979) The amphibians of the lowland tropical forests. In: Duellman, W.E. (Ed), The South American Herpetofauna: its origin, evolution, and dispersal. Monograph 7. Museum of Natural History, University of Kansas, Lawrence, Kansas, pp. 189–215.

    Manzanilla, J., Jowers, M.J., La Marca, E. & García-París, M. (2007a) Taxonomic reassessment of Mannophryne trinitatis (Anura: Dendrobatidae) with a description of a new species from Venezuela. Herpetological Journal, 17, 31–42.

    Manzanilla, J., La Marca, E. Jowers, M., Sánchez, D. & García-París, M. (2007b “2005”) Un nuevo Mannophryne (Amphibia: Anura: Dendrobatidae) del macizo del Turimiquire, noreste de Venezuela. Herpetotropicos, 2, 105–113.

    Manzanilla, J., La Marca, E. & García-París, M. (2009) Phylogenetic patterns of diversification in a clade of Neotropical frogs (Anura: Aromobatidae: Mannophryne). Biological Journal of the Linnean Society, 97, 185–199.
    https://doi.org/10.1111/j.1095-8312.2009.01074.x

    MARNR (Ministerio del Ambiente y los Recursos Naturales Renovables) (1992) Áreas naturales protegidas de Venezuela. Serie Aspectos Conceptuales y Metodológicos. DGPOA/ACM/01. Ministerio del Ambiente y de los Recursos Naturales Renovables, Caracas, 150 pp.

    Mertens, R. (1957) Zoologische Beobachtungen im Nebelwalde von Rancho Grande, Venezuela. Natur und Volk, 87, 337–344.

    Mijares-Urrutia, A. & Arends R., A. (1999a) Un nuevo Mannophryne (Anura: Dendrobatidae) del Estado Falcón, con comentarios sobre la conservación del género en el noroeste de Venezuela. Caribbean Journal of Science, 35, 231–327.

    Mijares-Urrutia, A. & Arends R., A. (1999b) A new Mannophryne (Anura: Dendrobatidae) from western Venezuela, with comments on the generic allocation of Colostethus larandinus. Herpetologica, 55, 106–114.
    http://www.jstor.org/stable/3893069

    Mijares-Urrutia, A.M. & Rivero, R.A. (2000) A new treefrog from the Sierra de Aroa, northern Venezuela. Journal of Herpetology, 34, 80–84.
    https://doi.org/10.2307/1565242

    Oliveira-Miranda, M.A., Huber, O., Rodríguez, J.P., Rojas-Suárez, F., De Oliveira-Miranda, R., Hernández-Montilla, M. & Zambrano-Martínez, S. (2010) Riesgo de eliminación de los ecosistemas terrestres de Venezuela. In: Rodríguez, J.P., Rojas-Suárez, F. & Giraldo, H.D. (Eds.), Libro Rojo de los Ecosistemas Terrestres de Venezuela. Provita, Shell Venezuela, Lenovo, Caracas, pp. 29–89.

    Padial, J.M, Köhler, J., Muñoz, A. & De La Riva, I. (2008) Assessing the taxonomic status of tropical frogs through bioacoustics: geographical variation in the advertisement calls in the Eleutherodactylus discoidalis species group (Anura). Zoological Journal of the Linnean Society, 152, 353–365.
    https://doi.org/10.1111/j.1096-3642.2007.00341.x

    Quiroga-Carmona, M. & Molinari, J. (2012) Description of a new shrew of the genus Cryptotis (Mammalia: Soricomorpha: Soricidae) from the Sierra de Aroa, an isolated mountain range in northwestern Venezuela, with remarks on biogeography and conservation. Zootaxa, 3441, 1–20.

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

    https://biodiversitylibrary.org/page/2811325

    Rivero, J.A. (1963) The distribution of Venezuelan frogs. II. The Venezuelan Andes. Caribbean Journal of Science, 3, 87–102.

    Rivero, J.A. (1964) The distribution of Venezuelan frogs. IV. The Coastal Range. Caribbean Journal of Science, 4, 307–319.

    Rivero, J.A. (1976) Notas sobre los anfibios de Venezuela II. Sobre los Colostethus de los Andes venezolanos. Memoria de la Sociedad de Ciencias Naturales La Salle, 35, 327–344.

    Rivero, J.A. (1979) Sobre el origen de la fauna paramera de anfibios venezolanos. In: Salgado-Labouriau, M.L. (Ed.), El Medio Ambiente Páramo. Ediciones Centro de Estudios Avanzados, Mérida, pp. 165–179.

    Rivero, J.A. (1984a) Una nueva especie de Colostethus (Amphibia, Dendrobatidae) de la Cordillera de la Costa, con anotaciones sobre otros Colostethus, de Venezuela. Brenesia, 22, 51–56.

    Rivero, J.A. (1984b “1982”) Sobre el Colostethus mandelorum (Schmidt) y el Colostethus inflexus Rivero (Amphibia, Dendrobatidae). Memoria de la Sociedad de Ciencias Naturales La Salle, 188, 9–16.

    Rivero, J.A. (1990 “1988”) Sobre las relaciones de las especies del género Colostethus (Amphibia: Dendrobatidae). Memoria de la Sociedad de Ciencias Naturales La Salle, 48, 3–32.

    Rodríguez-Olarte, D., Amaro, A., Coronel, J. & Taphorn, D. (2006 “2005”) Los peces del río Aroa, cuenca del Caribe, Venezuela. Memoria de la Fundación La Salle de Ciencias Naturales, 164, 101–127.

    Rojas-Runjaic, F.J.M., Infante-Rivero, E.E. & Barrio-Amorós, C.L. (2011) A new frog of the genus Aromobates (Anura, Dendrobatidae) from Sierra de Perijá, Venezuela. Zootaxa, 2919, 37–50.

    Roze, J.A. & Solano, H. (1963) Resumen de la familia Caeciliidae (Amphibia: Gymnophiona) de Venezuela. Acta Biologica Venezuelica, 3, 287–300.

    Sexton, O.J. (1960) Some aspects of the behavior and of the territory of a Dendrobatid frog, Prostherapis trinitatis. Ecology, 41, 107–115.
    https://doi.org/10.2307/1931944

    Shreve, B. (1947) On Venezuelan reptiles and amphibians collected by Dr. H. G. Kugler. Bulletin of the Museum of Comparative Zoology, 99, 517–537.
    https://biodiversitylibrary.org/page/4322504

    Stebbins, R.C. & Hendrickson, J.R. (1959) Field studies of amphibians in Colombia, South America. University of California Publications in Zoology, 56, 497–540.

    Stejneger, L. (1901) An annotated list of batrachians and reptiles collected in the vicinity of La Guaira, Venezuela, with descriptions of two new species of snakes. Proceedings United States National Museum, 24, 179–192.
    https://doi.org/10.5479/si.00963801.24-1248.179

    Test, F.H. (1954) Social aggressiveness in an amphibian. Science, 120, 140–141.
    https://doi.org/10.1126/science.120.3108.140

    Test, F.H. (1956) Two new dendrobatid frogs from northern Venezuela. Occasional Papers of the Museum of Zoology, University of Michigan, 577, 1–9.

    Test, F.H. (1963) A protective behavior pattern in a Venezuelan frog of mountain streams. Caribbean Journal of Science, 3, 125–128.

    Test, F.H., Sexton, O.J. & Heatwole, H. (1966) Reptiles of Rancho Grande and vicinity, Estado Aragua, Venezuela. Miscellaneous Publications of the Museum of Zoology, University of Michigan, 128, 1–63.
    http://hdl.handle.net/2027.42/56372

    Vargas, J.Y.G. & La Marca, E. (2007 “2006”) A new species of collared frog (Amphibia: Anura: Aromobatidae: Mannophryne) from the Andes of Trujillo state, Venezuela. Herpetotropicos, 3, 51–57.

    Vences, M., Kosuch, J., Boistel, R., Haddad, C.F.B., La Marca, E., Lötters, S. & Veith, M. (2003) Convergent evolution of aposematic coloration in Neotropical poison frogs: a molecular phylogenetic perspective. Organisms Diversity and Evolution, 3, 215–226.
    https://doi.org/10.1078/1439-6092-00076

    Vivas, L. (2012) GeotemasVenezuela 2012. Fondo Editorial Simón Rodríguez de la Lotería del Táchira, Gráficas El Portatítulo, Mérida, 278 pp.

    Wells, K.D. (1977) The courtship of frogs. In: Taylor, D.H. & Guttman, S.I. (Eds.), The Reproductive Biology of the Amphibians. Plenum Publishing Corp, New York, pp. 233–262.
    https://doi.org/10.1007/978-1-4757-6781-0_7

    Wells, K.D. (1980) Social behavior and communication of a Dendrobatid frog (Colostethus trinitatis). Herpetologica, 36, 189–199.

    http://www.jstor.org/stable/3891485

    Wells, K.D. (2007) The Ecology and Behavior of Amphibians. The University of Chicago Press, Chicago, 1148 pp.
    https://doi.org/10.7208/chicago/9780226893334.001.0001

    Yústiz, E. (1991) Un nuevo Colostethus (Amphibia: Dendrobatidae) de la Sierra de Barbacoas, estado Lara, Venezuela. Bioagro, 3, 145–150.