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Issue: Vol. 4388 No. 1: 1 Mar. 2018
Type: Article
Published: 2018-02-28
DOI: 10.11646/zootaxa.4388.1.4
Page range: 61–75
Abstract views: 78
PDF downloaded: 5

Vocalizations, tadpole, and natural history of Crossodactylus werneri Pimenta, Cruz & Caramaschi, 2014 (Anura: Hylodidae), with comments on distribution and intraspecific variation

Laboratório de Taxonomia, Sistemática e Evolução de Anuros Neotropicais, Universidade Federal de Uberlândia (UFU), campus Ituiutaba, Ituiutaba, MG, Brazil. Programa de Pós-Graduação em Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (Unicamp), Campinas, SP, Brazil.
Laboratório de Herpetologia, Instituto de Biociências/I.B., Departamento de Zoologia, Universidade Estadual Paulista (UNESP), campus Rio Claro, SP, Brazil.
Programa de Pós-Graduação em Ecologia de Ecossistemas, Universidade de Vila Velha (UVV), Vila Velha, ES, Brazil. Present address: Department of Biology, Queen’s University, K7K4W8, Kingston, ON, Canada.
Laboratório de Taxonomia, Sistemática e Evolução de Anuros Neotropicais, Universidade Federal de Uberlândia (UFU), campus Ituiutaba, Ituiutaba, MG, Brazil.
Pisces Advertisement call Atlantic Forest geographical distribution territorial call

Abstract

Crossodactylus werneri was described based on specimens collected in the 1970’s at Parque Nacional do Itatiaia, being also reported for nearby localities. We collected specimens that we assigned to C. werneri, and recorded calls of the species during fieldworks at Serra das Cabras (Campinas, state of São Paulo). In this paper, we describe for the first time the vocalizations, tadpole, coloration in life, and comment on aspects of the natural history of C. werneri. Besides, the examination of specimens in zoological collections allowed us to extend the geographic range for this species. We also make remarks on morphological/chromatic variation and provide 16S rDNA sequences for the species. Adults were found along a slow-flowing streamlet with sandy/muddy bottom within a small fragment of secondary forest. Males called between sunset and first hours of the night. Advertisement call consisted of series of pulsed notes. Call duration lasted around 3 s, emitted at the highest rate of 17 calls per minute and six notes per second. Note duration lasted around 18 ms. Notes had poorly defined pulses (irregular and/or weak amplitude modulations along the note). The dominant frequency was about 3380 Hz. Territorial call had a long, well-defined pulsed portion followed by a higher-amplitude “squeak”. The dominant frequency was around 3400 Hz. Tadpoles were essentially similar to those of other Crossodactylus species, except by not having nostril ornamentation. Our record of C. werneri in Serra das Cabras might be regarded a rediscovery of this species since C. werneri had not been recorded for more than 30 years until our first record of C. werneri in the field from 2011 and subsequent years. Our record is approximately 100 km west, and Mococa 200 km northwest, from Santo Antônio do Pinhal, the westernmost previous record for C. werneri up to date. Gene sequences (16S rRNA) give insights into the genetic divergence between C. werneri and some congeners.

 

References

  1. Aljanabi, S.M. & Martinez, I. (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25 (22), 4692–4693.
    https://doi.org/10.1093/nar/25.22.4692

    Altig, R. & McDiarmid, R.W. (1999) Body plan—Development and morphology. In: McDiarmid, R.W. & Altig, R. (Eds.), Tadpoles: The Biology of Anura Larvae. The University of Chicago Press, Chicago and London, pp. 24–51

    Bastos, R.P. & Pombal, J.P. (1995) New species of Crossodactylus (Anura: Leptodactylidae) from the Atlantic Rain Forest of southeastern Brazil. Copeia, 1995 (2), 436–439.
    https://doi.org/10.2307/1446907

    Bioacoustics Research Program (2012) Raven Pro: Interactive Sound Analysis Software. Version 1.5. Ithaca, New York: The Cornell Lab of Ornithology. Available from: http://www.birds.cornell.edu/raven (accessed 4 August 2014)

    Bokermann, W.C.A. (1963) Girinos de Anfíbios brasileiros 2 (Amphibia, Salientia). Revista Brasileira de Biologia, 23 (4), 349–353.

    Breiman, L. (2001) Random Forests. Machine Learning, 45 (1), 5–32.
    https://doi.org/10.1023/A:1010933404324

    Caldart, V.M., Iop, S. & Cechin, S.Z. (2011) Vocalizations of Crossodactylus schmidti Gallardo, 1961 (Anura, Hylodidae): advertisement call and aggressive call. North-Western Journal of Zoology, 7 (1), 118–124.

    Caldart, V.M., Iop, S., de Sá, F.P., Rocha, M.C., Arruda, J.L.S., Santos, T.G. & Cechin, S.Z. (2013) New records of Crossodactylus schmidti Gallardo, 1961 (Anura: Hylodidae) for the state of Rio Grande do Sul, Brazil with data on morphometry and an updated geografic distribution map. Check List, 9 (6), 1552–1555.
    https://doi.org/10.15560/9.6.1552

    Caldart, V.M., Iop, S., Lingnau, R. & Cechin, S.Z. (2016) Communication in a noisy environment: short-term acoustic adjustments and the underlying acoustic niche of a Neotropical stream-breeding frog. Acta Ethologica, 19 (3), 151–162. https://doi.org/10.1007/s10211-016-0235-2

    Caramaschi, U. & Sazima, I. (1985) Uma nova espécie de Crossodactylus da Serra do Cipó, Minas Gerais, Brasil (Amphibia, Leptodactylidae). Revista Brasileira de Zoologia, 3 (1), 43–49.
    https://doi.org/10.1590/S0101-81751985000100005

    Caramaschi, U. & Kisteumacher, G. (1989) O girino de Crossodactylustrachystomus (Reinhardt & Luetken, 1862) (Anura, Leptodactylidae). Revista Brasileira de Biologia, 49 (1), 237–239.

    Cochran, D.M. (1955 “1954”) Frogs of Southeastern Brazil. Bulletinn of the United States National Museum, 206 (1), 1–423.

    Cocroft, R.B. & Ryan, M.J. (1995) Patterns of advertisement call evolution in toads and chorus frogs. Animal Behavior, 49 (2), 283–303.
    https://doi.org/10.1006/anbe.1995.0043

    Cruz, C.A.G. & Peixoto, O.L. (1985) Espécies verdes de Hyla: o complexo “Albosignata” (Amphibia, Anura, Hylidae). Arquivos da Universidade Federal Rural do Rio de Janeiro, 7 (1), 31–47.

    Duellman, W.E. (1970) The hylid frogs of Middle America. Monographs of the Museum of Natural History of the University of Kansas, Lawrence, Kansas, 753 pp.
    https://doi.org/10.5962/bhl.title.2835

    Duellman, W.E. & Trueb, L. (1994) Biology of Amphibians. Johns Hopkins University Press, Baltimore and London, 670 pp.

    Faivovich, J. (1998) Comments on the larvae of the Argentine species of the genus Crossodactylus (Leptodactylidae, Hylodinae). Alytes, 16 (1), 61–67.

    Francioni, E. & Carcerelli, L.C. (1993) Descrição do girino de Crossodactylus gaudichaudii Duméril & Bibron, 1841 (Anura, Leptodactylidae). Memórias do Instituto Butantan, 55 (1), 63–67.

    Frost, D.R. (2016) Amphibian Species of the World: an Online Reference. Version 6.0 (21/04/2015). American Museum of Natural History, New York, USA. Electronic Database. Available from: http://research.amnh.org/vz/herpetology/amphibia/index.html (accessed 11 October 2016)

    Gallardo, J.M. (1961) Anfíbios anuros de Misiones con la descripción de una nueva espécie de Crossodactylus. Neotropica, 7 (23), 33-38.

    Giaretta, A.A. & Facure, K.G. (2008) Reproduction and habitat of ten Brazilian frogs (Anura). Contemporary Herpetology, 2008 (3), 1-4.

    Goebel, A.M., Donnelly, J.M. & Atz, M.E. (1999) PCR primers and amplification methods for 12S ribosomal DNA, the control region, cytochrome oxidase I, and cytochrome b in bufonids and other frogs, and an overview of PCR primers which have amplified DNA in amphibians successfully. Molecular Phylogenetics and Evolution, 11 (1), 163–199.
    https://doi.org/10.1006/mpev.1998.0538

    Gosner, K.L. (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16 (3), 183–196.

    Haddad, C.F.B. & Pombal Jr., J.P. (1987) Hyla hiemalis, nova espécie do grupo rizibilis do Estado de São Paulo (Amphibia, Anura, Hylidae). Revista Brasileira de Biologia, 47 (1), 127–132.

    Haddad, C.F.B. & Pombal Jr., J.P. (1995) A new species of Hylodes from southeastern Brazil (Amphibia: Leptodactylidae). Herpetologica, 51 (3), 279–286.

    Haddad, C.F.B., Garcia, P.C.A. & Pombal Jr., J.P. (2003) Redescrição de Hylodes perplicatus (Miranda-Ribeiro, 1926) (Amphibia, Anura, Leptodactylidae). Arquivos do Museu Nacional, 61 (4), 245–254.

    Hartmann, M.T., Hartmann, P.A. & Haddad, C.F.B. (2006) Repertório vocal de Hylodes phyllodes (Amphibia, Anura, Hylodidae). Papeis Avulsos de Zoologia, 46 (17), 203–209.

    Heyer, W.R., Rand, A.S., Cruz, C.A.G., Peixoto, O.L. & Nelson, C.E. (1990) Frogs of Boraceia. Arquivos de Zoologia, 31 (4), 231–410.

    Hödl, W. & Amézquita, A. (2001) Visual signalling in anuran amphibians. In: Ryan, M.J. (Ed.). Anuran Communication. Smithsonian Institution Press, Washington, DC, pp. 121–141.

    Hothorn, T., Hornik, K., Van de Wiel, M.A. & Zeileis, A. (2008) Implementing a Class of Permutation Tests: The coin Package. Journal of Statistic Software, 28 (8), 1

    https://doi.org/10.18637/jss.v028.i08

    Izecksohn, E. & Carvalho-e-Silva, S.P. (2001) Anfíbios do Município do Rio de Janeiro. Editora UFRJ, Rio de Janeiro, 158 pp.

    Jombart, T. (2008) Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24 (11), 1403–1405.
    https://doi.org/10.1093/bioinformatics/btn129

    Jombart, T., Devillard, S. & Balloux, F. (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics, 2010, 11–94.
    https://doi.org/10.1186/1471-2156-11-94

    Laia, R.C. & Rocha, C.F.D. (2012) Adults and tadpoles of species of Hylodidae (Anura): Hystory and taxonomy perspectives. Zoologia, 29 (1), 89−94.
    https://doi.org/10.1590/S1984-46702012000100012

    Liaw, A. & Wiener, M. (2002) Classification and regression by randomForest. R News, 2 (3), 18−22. Available from: http://CRAN.R-project.org/doc/Rnews/ (accessed 1 August 2015)

    Lingnau, R. & Bastos, R.P. (2007) Vocalizations of the Brazilian torrent frog Hylodes heyeri (Anura: Hylodidae): repertoire and influence of air temperature on advertisement call variation. Journal of Natural History, 41 (17–20), 1227–1235.
    https://doi.org/10.1080/00222930701395626

    Lingnau, R., Canedo, C.C. & Pombal Jr., J.P. (2008) A new species of Hylodes (Anura: Hylodidae) from the Brazilian Atlantic Forest. Copeia, 2008 (3), 595–602.
    https://doi.org/10.1643/CH-07-091

    Lutz, A. (1925) Batraciens du Brésil. Comptes Rendus et Mémoires Hebdomadaires des Séances de la Société de Biologie et des ses Filiales, 93 (2), 137–139.

    Müller, L. (1924) Neue Batrachier aus Ost-Brasilien. Senckenbergiana Biologica, 6, 169–177.

    Nascimento, L.B., Cruz, C.A.G. & Feio, R.N. (2005) A new species of diurnal frog in the genus Crossodactylus Duméril and Bibron, 1841 (Anura, Leptodactylidae) from southeastern Brazil. Amphibia-Reptilia, 26 (1), 497–505.
    https://doi.org/10.1163/156853805774806214

    Palumbi, S.R., Martin, A., Romano, S., McMillan, W.O., Sticc, L. & Grabowski, G. (1991) The simple fools guide to PCR. Version 2.0. Privately published document compiled by S. Palumbi, Department of Zoology, University of Hawaii, Honolulu, HI, 45 pp.

    Pimenta, B.V.S., Wachlevsky, M. & Cruz, C.A.G. (2008) Morphological and acoustical variation, geographic distribution, and conservation status of the spinythumb frog Crossodactylus bokermanni Caramaschi & Sazima, 1985 (Anura, Hylodidae). Journal of Herpetology, 42 (1), 481–492.
    https://doi.org/10.1670/07-164.1

    Pimenta, B.V.S., Cruz, C.A.G. & Caramaschi, U. (2014) Taxonomic review of the species complex of Crossodactylus dispar A. Lutz, 1925 (Anura, Hylodidae). Arquivos de Zoologia, 45 (1), 1–33.
    https://doi.org/10.11606/issn.2176-7793.v45i1p1-33

    Pimenta, B.V.S., Caramaschi, U. & Cruz, C.A.G. (2015) Synonymy of Crossodactylus bokermanni Caramaschi & Sazima, 1985 with Crossodactylus trachystomus (Reinhardt & Lütken, 1862) and description of a new species from Minhas Gerais, Brazil (Anura: Hylodidae). Zootaxa, 3955 (1), 65–82.
    https://doi.org/10.11646/zootaxa.3955.1.3

    R Development Core Team (2015) R Foundation for Statistical Computing. Vienna, Austria. Available from: http://www.Rproject.org (accessed 14 July 2015)

    Ribeiro, R.S., Egito, G.T.B.T. & Haddad, C.F.B. (2005) Chave de identificação: Anfíbios anuros da vertente de Jundiaí da Serra do Japi, Estado de São Paulo. Biota Neotropica, 5 (2), 1–15.
    https://doi.org/10.1590/S1676-06032005000300017

    Silva-Soares, T., Nogueira-Costa, P., Borges Júnior, V.N.T., Weber, L.N. & Rocha, C.F.D. (2015) The larva of Crossodactylus aeneus Müller, 1924: Morphology and Ecological Aspects. Herpetologica, 71 (1), 46–57.
    https://doi.org/10.1655/HERPETOLOGICA-D-13-00048

    Sueur, J., Aubin, T. & Simonis, C. (2008) 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., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) Mega6: molecular evolutionary genetic analysis version 6.0. Molecular Biology and Evolution, 30 (12), 2725–2729.
    https://doi.org/10.1093/molbev/mst197

    Toledo, L.F., Martins, I.A., Bruschi, D.P., Passos, M.A., Alexandre, C. & Haddad, C.F.B. (2015) The anuran calling repertoire in the light of social context. Acta Ethologica, 18 (2), 87–99.
    https://doi.org/10.1007/s10211-014-0194-4

    Weygoldt, P. (1986) Beobachtungen zur Ökologie und Biologie von Fröschen an einem neotropischen Bergbach. Zoologische Jahrbücher, Abteilung für Systematik, Ökologie und Geographie der Tiere, 113 (3), 429–454.

    Weygoldt, P. & Carvalho-e-Silva, S.P. (1992) Mating and oviposition in the Hylodine frog Crossodactylus gaudichaudii (Anura: Leptodactylidae). Amphibia-Reptilia, 13 (1), 35−45.
    https://doi.org/10.1163/156853892X00210

    Yang, Z. (2006) Computational Molecular Evolution. Oxford University Press, Oxford, 374 pp.
    https://doi.org/10.1093/acprof:oso/9780198567028.001.0001