Abstract
We studied the external and oral cavity morphology of the tadpoles of eight species of Hypsiboas in the H. albopunctatus, H. faber, H. punctatus and H. pulchellus species groups. After a review of the available information about larval external and oral cavity morphology, no character state seems to be synapomorphic for Hypsiboas. The presence of a fleshy projection in the inner margin of the nostrils and rounded vacuities of the anteromedial surface of the choanae (pending the confirmation of the latter in Hyloscirtus and Myersiohyla) seems to be synapomorphic for the tribe Cophomantini, as previously noticed by other authors. Some putative synapomorphies are suggested for some species groups of Hypsiboas, but a denser sampling is needed to study the taxonomic distribution of these character states, in order to determine which clades they may support. The presence of lateral flaps with labial teeth in the oral disc is a variable feature of many species in the H. faber and H. pulchellus groups. A spiracular tube free from the body wall is present in some species, mostly in the H. albopunctatus group, but also in the H. rufitelus, H. faber and H. pulchellus groups. Unique ventrolateral cumules of neuromasts are present in H. faber, and also in some species of other groups of Hypsiboas and of the sister genus Aplastodiscus. Our results highlight the importance of studying the taxonomic distribution of many character states that were sometimes overlooked in tadpole descriptions but seem relevant to test phylogenetic hypothesis.References
Aguilar, C., Siu-Ting, K. & Venegas, P. (2007) The rheophilous tadpole of Telmatobius atahualpai Wiens, 1993 (Anura: Ceratophryidae). South American Journal of Herpetology, 2, 165–174.
Alcalde, L. & Blotto, B. (2006) Chondrocranium, cranial muscles and buccopharyngeal morphology on tadpoles of the controversial leptodactylid frog Limnomedusa macroglossa (Anura: Leptodactylidae). Amphibia Reptilia, 27, 241–253.
Altig, R. & Johnston, G.F. (1989) Guilds of anuran larvae: Relationships among developmental modes, morphologies, and habitats. Herpetological Monographs, 3, 81–109.
Altig, R. & McDiarmid, R.W. (1999a) Body Plan. Development and Morphology. In: McDiarmid, R.W. & Altig, R. (Eds.), Tadpoles: The Biology of Anuran Larvae. Univ. of Chicago Press, Chicago, pp. 24–51.
Altig, R. & McDiarmid, R.W. (1999b) Diversity. Familial and Generic Characterizations. In: McDiarmid, R.W. & Altig, R. (Eds.), Tadpoles: The Biology of Anuran Larvae. Univ. of Chicago Press, Chicago, pp. 295–337.
Antunes, A.P., Faivovich, J. & Haddad, C. (2008) A new species of Hypsiboas from the Atlantic Forest of Southeastern Brazil (Amphibia: Anura: Hylidae). Copeia, 2008, 179–190.
Bokermann, W.C.A. (1963) Girinos de anfíbios Brasileiros I (Amphibia, Salientia). Anais da Academia Brasileira de Ciências, 35, 465–474.
Bokermann, W.C.A. (1968) Observações sobre Hyla pardalis Spix (Anura, Hylidae). Revista Brasileira de Biologia, 28, 1–6.
Bokermann, W.C.A. & Sazima, I. (1973) Anfíbios da Serra do Cipó, Minas Gerais, Brasil. 1–Espécies novas de “Hyla” (Anura, Hylidae). Revista Brasileira de Biologia, 33, 329–336.
Both, C., Kwet, A. & Solé, M. (2007) The tadpole of Hypsiboas leptolineatus (Braun & Braun, 1977), a species in the Hypsiboas polytaenius clade (Anura; Hylidae). Brazilian Journal of Biology, 67, 309–312.
Breder, C.M. Jr. (1946) Amphibians and reptiles of the Rio Chucunaque drainage, Darien, Panama, with notes on their life histories and habits. Bulletin of the American Museum of Natural History, 86, 375–436.
Caldwell, J.P. (1989) Structure and behavior of Hyla geographica tadpole schools, with comments on classification of group behavior in tadpoles. Copeia, 1989, 938–950.
Caramaschi, U., Jim, J. & de Carvalho, C.M. (1980) Observações sobre Aplastodiscus perviridis A. Lutz (Amphibia, Anura, Hylidae). Revista Brasileira de Biologia, 40, 405–408.
Carnaval, A.C.O.Q. & Peixoto, O.L. (2004) A new species of Hyla from northeastern Brazil (Amphibia, Anura, Hylidae). Herpetologica, 60, 387–395.
Carvalho-e-Silva, A.M.T.P. & Carvalho-e-Silva, S.P. (2005) New Species of the Hyla albofrenata Group, from the States of Rio de Janeiro and São Paulo, Brazil (Anura, Hylidae). Journal of Herpetology, 39, 73–81.
Cei, J.M. (1980) Amphibians of Argentina. Monitore Zoologico Italiano, (N.S.) Monogr. 2, Firenze, 609 pp.
Cei, J.M. (1987) Additional notes to “Amphibians of Argentina”: an update, 1980-1986. Monitore Zoologico Italiano, (N.S.), 21, 209–272.
Chacon-Ortiz, A., Diaz De Pascual, A. & Godoy, F. (2004) Aspectos reproductivos y desarrollo larval de Hyla pugnax (Anura: Hylidae) en el piedemonte andino de Venezuela. Revista de la Academia Colombiana de Ciencias, 28, 391–402.
Conte, C.E., Nomura, F., Rossa-Feres, D.C., d’Heursel, A. & Haddad, C.F.B. (2007) The tadpole of Scinax catharinae (Anura: Hylidae) with description of the internal oral morphology, and a review of the tadpoles from the Scinax catharinae group. Amphibia-Reptilia, 28, 177–192.
de Sá, R.O. (1995) Hyla albopunctata. Catalogue of American Amphibians and Reptiles, 602, 1–5.
de Sá, R.O. (1996) Hyla multifasciata. Catalogue of American Amphibians and Reptiles, 624, 1–4.
de Sá, R.O. & Lavilla, E.O. (1997) The tadpole of Pseudis minuta (Anura: Pseudidae), an apparent case of heterochrony. Amphibia-Reptilia, 18, 229–240.
d’Heursel, A. & de Sá, R.O. (1999) Comparing the tadpoles of Hyla geographica and Hyla semilineata. Journal of Herpetology, 33, 353–361.
d’Heursel, A. & Haddad, C.F.B. (2002) Schooling and swimming behaviors of Hyla semilineata tadpoles (Anura, Hylidae). Iheringia, Sér. Zool., 92, 99–104.
d’Heursel, A. & Haddad, C.F.B. (2007) Anatomy of the oral cavity of Hylid larvae from the genera Aplastodiscus, Bokermannohyla, and Hypsiboas (Amphibia, Anura): description and systematic implications. Journal of Herpetology, 41, 458–468.
Donoso-Barros, R. & León, J. (1972) Desarrollo y evolución larval de Hyla crepitans (Amphibia: Salientia). Boletín de la Sociedad de Biología de Concepción, 44, 117–127.
Duellman, W.E. (1970) Hylid frogs of Middle America. Monographs of the Museum of Natural History, University of Kansas, Kansas, 1–2, 753 pp.
Duellman, W.E. (1974) A reassessment of the taxonomic status of some neotropical hylid frogs. Occasional Papers of the Museum of Natural History, University of Kansas, 27, 1–27.
Duellman, W.E. (1978) The biology of an Ecuatorial herpetofauna in Amazonian Ecuador. Miscellaneous Publications of the Museum of Natural History of the University of Kansas, 65, 1–352.
Duellman, W. E. (1997). Amphibians of La Escalera region, Southeastern Venezuela: taxonomy, ecology and biogeography. Scientific Papers of the Natural History Museum, University of Kansas 2, 1–52.
Duellman, W.E. (2005) Cusco Amazónico: the lives of amphibians and reptiles in an Amazonian rainforest. Cornell University Press, New York, 433 pp.
Duellman, W.E. & de Sá, R.O. (1988) A new genus and species of South American hylid frog with a highly modified tadpole. Tropical Zoology, 1, 117–136.
Duellman, W.E. & Lescure, J. (1973) Life history and ecology of the hylid frog Osteocephalus taurinus with observations on larval behavior. Occasional Papers of the Museum of Natural History, University of Kansas, 13, 1–12.
Duellman, W.E., De La Riva, I. & Wild, E.R. (1997) Frogs of the Hyla armata and Hyla pulchella groups in the Andes of South America, with definitions and analyses of phylogenetic relationships of Andean groups of Hyla. Scientific Papers, Natural History Museum, University of Kansas, 3, 1–41.
Echeverría, D.D. (1992) Microscopía electrónica de barrido del aparato bucal de la larva de Hyla pulchella pulchella (Anura, Hylidae). Cuadernos de Herpetología, 7, 24–28.
Echeverría, D.D. (1997) Microanatomy of the buccal apparatus and oral cavity of Hyla minuta Peters, 1982 larvae (Anura, Hylidae), with data on feeding habits. Alytes, 15, 26–36.
Echeverría, D.D. & Montanelli, S.B. (1992) Esteromorfología del aparato bucal y cavidad oral de las larvas de Ololygon fuscovaria (Lutz, 1925) (Anura, Hylidae). Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia (Zool.), 16, 3–13.
Eterovick, P.C., Barros, I.S. & Sazima, I. (2002) Tadpoles of two species in the Hyla polytaenia species group and comparison with other tadpoles of Hyla polytaenia and Hyla pulchella groups (Anura, Hylidae). Journal of Herpetology, 36, 512–515.
Fabrezi, M. & Vera, R. (1997) Caracterización morfológica de larvas de anuros del noroeste argentino. Cuadernos de Herpetología, 11, 37–49.
Faivovich, J. (1996) La larva de Hyla semiguttata A. Lutz, 1925 (Anura, Hylidae). Cuadernos de Herpetología, 9, 61–67.
Faivovich, J., Garcia, P.C.A., Ananias, F., Lanari, L., Basso, N.G. & Wheeler, W.C. (2004) A molecular perspective on the phylogeny of the Hyla pulchella species group (Anura, Hylidae). Molecular Phylogenetics and Evolution, 32, 938–950.
Faivovich, J., Haddad, C.F.B., Garcia, P.C.A., Frost, D., 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.
Fernández, K. (1927) Sobre la biología y reproducción de batracios argentinos (Segunda Parte). Boletín de la Academia Nacional de Ciencias de la República Argentina, 29, 271–320.
Frost, D.R. (2007) Amphibian Species of the World: an Online Reference Version 5, American Museum of Natural History, New York, USA. Available from: http://research.amnh.org/herpetology/amphibia/index.php (accessed April 2007)
Gallardo, J.M. (1961) Observaciones biológicas sobre Hyla raddiana Fitz., en la Provincia de Buenos Aires. Ciencia e Investigación, 17, 63–69.
Gallardo, J.M. (1987) Anfibios Argentinos. Guía para su identificación. Librería Agropecuaria, Buenos Aires, 98 pp.
Garcia, P.C.A., Vinciprova, G. & Haddad, C.F.B. (2001a) Vocalização, girino, distribuição geográfica e novos comentários sobre Hyla marginata Boulenger (1887) (Anura, Hylidae, Hylinae). Boletim do Museu Nacional do Rio de Janeiro, 460, 19.
Garcia, P.C.A., Caramaschi, U. & Kwet, A. (2001b) O status taxonômico de Hyla cochranae Mertens e recaracterização de Aplastodiscus A. Lutz (Anura, Hylidae). Revista Brasileira de Zoologia, 18, 1197-1218.
Garcia, P.C.A., Vinciprova, G. & Haddad, C.F.B. (2003) The taxonomic status of Hyla pulchella joaquini B. Lutz, 1968 (Anura: Hylidae). Herpetologica, 59, 350–363.
Garcia, P.C.A., Faivovich, J. & Haddad, C.F.B. (2007) Redescription of Hypsiboas semiguttatus, with the description of a new species of the Hypsiboas pulchellus group. Copeia, 2007, 933–951.
Garcia, P.C.A., Peixoto, O.L. & Haddad, C.F.B. (2008) A new species of Hypsiboas (Anura: Hylidae) from the Atlantic Forest of Santa Catarina, southern Brazil, with comments on its conservation status. South American Journal of Herpetology, 3, 27–35.
Gomes, M.R. & Peixoto, O.L. (2002) O girino de Hyla leucopygia Cruz and Peixoto, 1984 (Amphibia, Anura, Hylidae). Boletim do Museo de Biologia Mello Leitão, Nova Serie, 13, 17–25.
Gosner, K.L. (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183–190.
Hero, J.M. (1990) An illustrated key to tadpoles occurring in the Central
Amazon rainforest, Manaus, Amazonas, Brazil. Amazoniana, 11, 201–262.Heyer, W.R., Rand, A. S., Gonçalves da Cruz, C. A., Peixoto, O. L. & Nelson, C. E. (1990) Frogs of Boracéia. Arquivos de Zoologia, 31, 237–410.
Hoffmann, H. (2005) The Tadpoles of Hyla rufitela (Anura: Hylidae). Revista de Biologia Tropical, 53, 561–568.
Hoogmoed, M.S. (1979) Resurrection of Hyla ornatissima Noble (Amphibia, Hylidae) and remarks on related species of green tree frogs from the Guiana area. Notes on the herpetofauna of Surinam VI. Zoologische Verhandelingen, 172, 1–46
Kenny, J.S. (1969) The Amphibia of Trinidad. Studies of the Fauna of Curaçao and other Caribbean Islands, 108, 1–78.
Kwet, A. & Di-Bernardo, M. (1999) Pró-Mata–Anfíbios. Amphibien. Amphibians. EDIPUCRS, Porto Alegre, Brasil, 107pp.
Lannoo, M.J. (1987) Neuromast topography in anuran amphibians. Journal of Morphology, 191, 115–129.
Lannoo, M.J., Towsend, D.S. & Wassersug, R.J. (1986) Larval life in leaves: Arboreal tadpoles types, with special attention to the morphology, ecology and behaviour of the oophagous Osteopilus brunneus (Hylidae) larvae. Fieldiana Zoology, new series, 38, 1–31.
Lavilla, E.O. (1984) Redescripción de larvas de Hyla pulchella andina (Anura: Hylidae) con un análisis de la variabilidad interpoblacional. Neotropica, 30, 19–30.
Lavilla, E.O. & Fabrezi, M. (1987) Anatomía de larvas de Hyla pulchella andina. (Anura: Hylidae). Physis, 45, 77–82.
Lavilla, E.O. & Scrocchi, G.J. (1986) Morfometría larval de los géneros de Telmatobiinae (Anura: Leptodactylidae) de Argentina y Chile. Physis, 44, 39–43.
Lavilla, E.O. & Cei, J.M. (2001) Amphibians of Argentina: a second update, 1987–2000. Museo Regionale di Scienze Naturali Torino, Monografie 28, Torino, 177 pp.
Limbaugh, B.A. & Volpe, E.P. (1957) Early development of the Gulf Coast toad, Bufo valliceps Wiegmann. American Museum Novitates, 1842, 1–32.
Lötters, S., Köhler, J. & Reichle, S. (1999) Description of the tadpole of the Andean treefrog Hyla marianitae (Amphibia: Anura: Hylidae). Folia Zoologica, 48, 49–53.
Lutz, B. (1951) Anfíbios anuros da Coleção Adolpho Lutz do Instituto Oswaldo Cruz. IV. Formas aliadas as Hylas verdes da região leste-meridional. Memórias Instituto Oswaldo Cruz, 47, 303–335.
Lutz, B. (1973) Brazilian Species of Hyla. University of Texas Press, Austin, Texas, 260 pp.
Martins, M. & Moreira, G. (1991) The nest and the tadpole of Hyla wavrini, Parker (Amphibia, Anura). Memorias do Instituto Butantan, 53, 197–204.
McDiarmid, R.W. & Altig, R. (1999) Research. Materials and Techniques. In Tadpoles: The Biology of Anuran Larvae, pp. 7–23. McDiarmid, R.W., Altig R., Eds., Chicago, Univ. of Chicago Press.
Mijares-Urrutia, A. (1992) Sobre el renacuajo de Hyla alemani Rivero (Anura: Hylidae). Acta Biologica Venezuelica, 13, 35–39.
Mijares-Urrutia, A. (1993) The tadpole of Hyla granosa (Anura: Hylidae) from southeastern Venezuela. Revista Chilena de Historia Natural, 66, 143–147.
Myers, C.W. & Donnelly, M.A. (1997) A Tepui herpetofauna on a granitic mountain (Tamacuari) in the borderland between Venezuela and Brazil: report from the Phipps Tapirapecó Expedition. American Museum Novitates, 3213, 1–71.
Myers, C.W. & Donnelly, M.A. (2008) The summit herpetofauna of Auyantepui, Venezuela: report from the Robert G. Goelet American Museum–Terramar Expedition. Bulletin of the American Museum of Natural History, 308, 1–147.
Napoli, M.F. & Cruz, I.C.S. (2005) The advertisement call of Hyla atlantica Caramaschi & Velosa, 1996, with considerations on its taxonomic status (Amphibia, Anura, Hylidae). Arquivos do Museu Nacional, Rio de Janeiro, 63, 283–288.
Noble, G.K. (1927) The value of life history data in the study of evolution of the Amphibia. Annals of the New York Academy of Sciences, 30, 31–128.
Orrico, V.G.D., Mongin, M.M. & de-Carvalho-e-Silva, A.M.P.T. (2007) The tadpole of Hypsiboas latistriatus (Caramaschi & Cruz, 2004), a species of the Hypsiboas polytaenius (Cope, 1870) clade (Amphibia, Anura, Hylidae). Zootaxa, 1531: 25–37.
Orton, G.L. (1953) The systematics of vertebrate larvae. Systematic Zoology, 2, 63–75.
Peixoto, O.L. & Cruz, C.A.G. (1983) Girinos de espécies de Hyla do grupo ‘‘albomarginata’’ do Sudeste brasileiro (Amphibia, Anura, Hylidae). Arquivos da Universidade Federal Rural do Rio de Janeiro, 6, 155–163.
Pyburn, W.F. & Hall, D.H. (1984) A new stream-inhabiting treefrog (Anura: Hylidae) from southeastern Colombia. Herpetologica, 40, 366–372.
Rada, D. (1981) Renacuajos de algunos anfibios de Clarines (Edo. Anzoátegui, Venezuela). Memorias de la Sociedad de Ciencias Naturales La Salle, 41, 57–76.
Rada de Martínez, D. (1990–1991) Contribución al conocimiento de las larvas de anfibios de Venezuela. Memorias de la Sociedad de Ciencias Naturales La Salle, 49–50, 391–403.
Rossa-Feres, D. de C. & Nomura, F. (2006) Characterization and taxonomic key for tadpoles (Amphibia: Anura) from the northwestern region of São Paulo State, Brazil. Biota Neotropica, 6. Available from http://www.biotaneotropica.org.br/v6n1/pt/abstract?identification-key+bn00706012006 (accessed 10 September 2006).
Sandoval, M.T. (2000) Microanatomía del disco oral y cavidad bucofaríngea de la larva de Scinax acuminatus (Anura: Hylidae). Facena, 16, 93–102.
Savage, J.M. (2002) The amphibians and reptiles of Costa Rica. A herpetofauna between two continents, between two seas. University of Chicago Press, Chicago, 954 pp.
Schiesari, L.C., Grillitsch, B. & Vogl, C. (1996) Comparative morphology of phytotelmonous and pond-dwelling larvae of four Neotropical treefrog species (Anura, Hylidae, Osteocephalus oophagus, Osteocephalus taurinus, Phrynohyas resinifictrix, Phrynohyas venulosa). Alytes, 13, 109–139.
Spirandeli Cruz, E.F. (1991) Estudo comparativo da morfologıa oral interna de larvas de anfíbios anuros que ocorrem na região de Botucatu, (Amphibia, Anura). Doctoral Thesis Dissertation, Instituto de Biociências, Universidade de São Paulo, 237 pp.
Vera Candioti, M.F. (2004) Morphology of premetamorphic larvae of Lysapsus limellus (Anura: Pseudinae). Amphibia-Reptilia, 25, 41–54.
Vera Candioti, M.F. (2007) Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits. Zootaxa, 1600, 1–175.
Vera Candioti, M.F., Lavilla, E.O. & Echeverría, D.D. (2004) Feeding mechanism in two three frogs, Hyla nana and Scinax nasicus (Anura: Hylidae). Journal of Morphology, 261, 206–224.
Viertel, B. (1982) The oral cavities of central European Anuran larvae (Amphibia). Morphology, ontogenesis and generic diagnosis. Amphibia-Reptilia, 4, 327–360.
Vizotto, L.D. (1967) Desenvolvimento de anuros da região norte-occidental do estado de São Paulo. Doctoral Thesis Dissertation, Faculdade de Filosofia, Ciências e Letras, Departamento de Zoologia, Universidade de São Paulo, 161 pp.
Wassersug, R.J. (1976). Internal oral features in Hyla regilla (Anura: Hylidae) larvae: an ontogenetic study. Occasional Papers of the Museum of Natural History, University of Kansas, 49, 1–24.
Wassersug, R.J. (1980) Internal oral features of larvae from eight families: functional, systematic, evolutionary and ecological considerations. Miscellaneous Publications of the Museum of Natural History, University of Kansas, 68, 1–146.
Wiens, J.J., Fetzner Jr., J.W., Parkinson, C.L. & Reeder, T.W. (2005) Hylid frog phylogeny and sampling strategies for speciose clades. Systematic Biology, 54, 719–748.
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. American Naturalist, 168. Online appendix.
Wild, E.R. (1992) The tadpoles of Hyla fasciata and H. allenorum, with a key to the tadpoles of the Hyla parviceps group (Anura: Hylidae). Herpetologica, 48, 439–447.
Wogel, H., Weber, L.N. & Abrunhosa, P.A. (2006) The tadpole of the casqued-headed frog Aparasphenodon brunoi Miranda- Ribeiro (Anura: Hylidae). South American Journal of Herpetology, 1, 54–60.