Skip to main content Skip to main navigation menu Skip to site footer
Article
Published: 2022-06-23

On the stream-dwelling Crossodactylus timbuhy (Anura, Hylodidae): taxonomy, natural history, and geographic distribution

National Institute of the Atlantic Forest (INMA), 29650-000, Santa Teresa, ES, Brazil. Projeto Bromélias, Instituto de Ensino, Pesquisa e Preservação Ambiental Marcos Daniel, Av. Eugênio Pachêco de Queirós, s/n Jardim Camburi, 29090-160, Vitória, ES, Brazil
Programa de Pós-Graduação em Zoologia, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270901, Belo Horizonte, MG, Brazil. Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil
National Institute of the Atlantic Forest (INMA), 29650-000, Santa Teresa, ES, Brazil 2Projeto Bromélias, Instituto de Ensino, Pesquisa e Preservação Ambiental Marcos Daniel, Av. Eugênio Pachêco de Queirós, s/n Jardim Camburi, 29090-160, Vitória, ES, Brazil
Mapinguari Lab, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul–UFMS, 79070-900, Campo Grande, MS, Brazil
Mapinguari Lab, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul–UFMS, 79070-900, Campo Grande, MS, Brazil
National Institute of the Atlantic Forest (INMA), 29650-000, Santa Teresa, ES, Brazil 2Projeto Bromélias, Instituto de Ensino, Pesquisa e Preservação Ambiental Marcos Daniel, Av. Eugênio Pachêco de Queirós, s/n Jardim Camburi, 29090-160, Vitória, ES, Brazil
Amphibia Atlantic Forest Santa Teresa tadpole vocalization

Abstract

The genus Crossodactylus has taxonomic problems due to the difficulty in properly identifying some populations to the species level. The deficient species diagnosis rises mostly due to high intraspecific variation and lack of information on topotypes. Crossodactylus timbuhy was described based only on external morphology of preserved adult specimens. Based on topotypic specimens, we provide further information on C. timbuhy regarding color in life (both adult and larvae), tadpole external morphology, vocal repertoire, natural history, and geographic distribution. The species identification was confirmed through comparison to the type series, 16S rRNA analysis, and bioacoustics. Crossodactylus timbuhy vocalizes during daylight along shallow slow-flowing streams. The advertisement call has ascendant amplitude modulation, duration of 2.1–8.4 s, 23–75 pulsed notes, and peak frequency of 3.6–4.8 kHz. Our report on male unilateral sac inflation is the first within Crossodactylus. Although overall tadpole external morphology and coloration resemble other species of hylodids, we report ventral depression and golden iridophores also for the first time within Crossodactylus. Adult males display five antipredator mechanisms (interrupt calling, escape, aggression, posture, and aposematism). Finally, we restrict its geographic distribution to the Municipality of Santa Teresa, State of Espírito Santo, Southeastern Brazil.

 

References

  1. Altig, R. & McDiarmid, R.W. (1999) Body plan: development and morphology. In: McDiarmid, R.W. & Altig, R. (Eds.), Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago, Illinois, pp. 24–51.
    Augusto-Alves, G., Dena, S.A. & Toledo, L.F. (2018) Visual communication and aggressive behavior in a giant mute torrent-frog, Megaelosia apuana (Anura; Hylodidae). Amphibia-Reptilia, 39, 260–264. https://doi.org/10.1163/15685381-20181000
    Bastos, R.P. & Pombal, J.P. (1995) New species of Crossodactylus (Anura: Leptodactylidae) from the Atlantic Rain Forest of southeastern Brazil. Copeia, 1995, 436–439. https://doi.org/10.2307/1446907
    Bioacoustics Research Program (2014) Raven Pro: Interactive Sound Analysis Software. Version 1.5. The Cornell Lab of Ornithology, Ithaca, New York. Available from: http://www.birds.cornell.edu/raven (accessed November 2019)
    Bokermann, W.C.A. (1963) Girinos de anfíbios brasileiros – 2 (Amphibia, Salientia). Revista Brasileira de Zoologia, 23, 349–353.
    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, 118–124.
    Caldart, V.M., Iop, S. & Cechin, S.Z. (2014) Social interactions in a Neotropical stream frog reveal a complex repertoire of visual signals and the use of multimodal communication. Behaviour, 151, 719–739. https://doi.org/10.1163/1568539X-00003165
    Caramaschi, U. & Sazima, I. (1985) Uma nova espécie de Crossodactylus da Serra do Cipó, Minas Gerais, Brasil (Amphibia, Leptodactylidae). Revista Brasileira de Zoologia, 3, 43–49. https://doi.org/10.1590/S0101-81751985000100005
    Caramaschi, U. & Kisteumacher, G. (1989) O girino de Crossodactylus trachystomus (Reinhardt e Luetken, 1862) (Anura, Leptodactylidae). Revista Brasileira de Biologia, 49, 237–239.
    Cocroft, R.B. & Ryan, M.J. (1995) Patterns of advertisement call evolution in toads and chorus frogs. Animal Behaviour, 49, 283–303. https://doi.org/10.1006/anbe.1995.0043
    Costa, T.R.N., Lingnau, R. & Toledo, L.F. (2009) The tadpole of the Brazilian torrent frog Hylodes heyeri (Anura, Hylodidae). Zootaxa, 2222 (1), 66–68. https://doi.org/10.11646/zootaxa.2222.1.6
    Costa, P.N., Silva-Soares, T., Weber, L.N. & Carvalho-e-Silva, A.M.P.T. (2010) Redescription of tadpole of the hylodid frog Hylodes asper (Müller, 1924). Zootaxa, 2521 (1), 65–68. https://doi.org/10.11646/zootaxa.2521.1.5
    Cruz, C.A.G. & Peixoto, O.L. (1987 “1985”) Especies verdes de Hyla: o complexo “Albofrenata” (Amphibia, Anura, Hylidae). Arquivos de Universidade Federal Rural do Rio de Janeiro, 8, 59–70.
    de Sá, F.P., Canedo, C., Lyra, M.L. & Haddad, C.F.B. (2015) A new species of Hylodes (Anura, Hylodidae) and its secretive underwater breeding behavior. Herpetologica, 71, 58–71. https://doi.org/10.1655/HERPETOLOGICA-D-13-00053
    de Sá, F.P., Zina, J. & Haddad, C.F.B. (2016) Sophisticated communication in the Brazilian torrent frog Hylodes japi. PLoS One, 11, e0145444. https://doi.org/10.1371/journal.pone.0145444
    de Sá, F.P., Pupin, N. & Haddad, C.F.B. (2018) Notes on agonistic communication by the Neotropical torrent frog Hylodes meridionalis (Hylodidae). Herpetology Notes, 11, 919–923.
    Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113. https://doi.org/10.1186/1471-2105-5-113.
    Elias-Costa, A.J, Montesinos, R., Grant, T. & Faivovich, J. (2017) The vocal sac of Hylodidae (Amphibia, Anura): phylogenetic and functional implications of a unique morphology. Journal of Morphology, 278, 1506–1516. https://doi.org/10.1002/jmor.20727
    Elias-Costa, A.J. & Faivovich, J. (2019) Convergence to the tiniest detail: vocal sac structure in torrent-dwelling frogs. Biological Journal of the Linnean Society, 128, 390–402. https://doi.org/10.1093/biolinnean/blz068
    Eterovick, P.C. & Barros, I.S. (2003) Niche occupancy in southeastern Brazilian tadpole communities in montane meadow streams. Journal of Tropical Ecology, 19, 439–448. https://doi.org/10.1017/S026646740300347X
    Faivovich, J. (1998) Comments on the larvae of Argentine species of the genus Crossodactylus (Leptodactylidae, Hylodinae). Alytes, 16, 61–67.
    Ferreira, R.B, Lourenço-de-Moraes, R., Zocca, C.Z., Duca, C., Beard, K.H. & Brodie Jr, E.D. (2019) Antipredator mechanisms of post-metamorphic anurans: a global database and classification system. Behavioral Ecology and Sociobiology, 73, 69. https://doi.org/10.1007/s00265-019-2680-1
    Forti, L.R. & Castanho, L.M. (2012) Behavioural repertoire and a new geographical record of the torrent frog Hylodes cardosoi (Anura: Hylodidae). Herpetological Bulletim, 121, 17–22.
    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
    Francioni, E. & Carcerelli, L.C. (1993) Descrição do girino de Crossodactylus gaudichaudii Duméril & Bibron, 1841 (Anura, Leptodactylidae). Memórias do Instituto Butantan, 55, 63–67.
    Furtado, R., Lermen, L.N., Márquez, R. & Hartz, S.M. (2019) Neotropical dancing frog: the rich repertoire of visual displays in a hylodine species. Journal of Ethology, 37, 291–300. https://doi.org/10.1007/s10164-019-00600-x
    Gallardo, J.M. (1961) Anfibios anuros de Misiones con la descripcion de una nueva especie de Crossodactylus. Neotropica, 7, 33–38.
    Gerhardt, H.C. (1994) The evolution of vocalization in frogs and toads. Annual Review of Ecology and Systematics, 25, 293–324. https://doi.org/10.1146/annurev.es.25.110194.001453
    Gerhardt, H.C. (1998) Acoustic signals of animals: recording, field measurements, analysis and description. In: Hopp, S.L., Owren, M.J. & Evans, C.S. (Eds.), Animal acoustic communication. Springer Verlag, Berlin, pp. 1–25.
    Gosner, K.L. (1960) A simplified table for staging anuran embryo and larvae with notes on identification. Herpetologica, 16, 183–190.
    Grosjean, S., Vences, M. & Dubois, A. (2004) Evolutionary significance of oral morphology in the carnivorous tadpoles of tiger frogs, genus Hoplobatrachus (Ranidae). Biological Journal of the Linnean Society, 81, 171–181. https://doi.org/10.1111/j.1095-8312.2003.00272.x
    Grosjean, S. (2005) The choice of external morphological characters and developmental stages for tadpole-based anuran taxonomy: a case study in Rana (Sylvirana) nigrovittata (Blyth, 1855) (Amphibia, Anura, Ranidae). Contributions to Zoology, 74, 61–76. https://doi.org/10.1163/18759866-0740102005
    Grosjean, S., Bordoloi, S., Chuaynkern, Y., Chakravarty, P. & Ohler, A. (2015) When young are more conspicuous than adults: a new ranid species (Anura: Ranidae) revealed by its tadpole. Zootaxa, 4058 (4), 471–498. https://doi.org/10.11646/zootaxa.4058.4.2
    Haddad, C.F.B. & Pombal Jr., J.P. (1995) A new species of Hylodes from southeastern Brazil (Amphibia: Leptodactylidae). Herpetologica, 51, 279–286.
    Haddad, C.F.B. & Giaretta, A.A. (1999) Visual and acoustic communication in the Brazilian torrent frog, Hylodes asper (Anura: Leptodactylidae). Herpetologica, 55, 324–333.
    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, 245–254.
    Hartmann, M.T., Giasson, L.O.M., Hartmann, P.A. & Haddad, C.F.B. (2005) Visual communication in Brazilian species of anurans from the Atlantic Forest. Journal of Natural History, 39, 1675–1685. https://doi.org/10.1080/00222930400008744
    Hödl, W., Rodrigues, M.T., Accacio, G.M, Lara, P.H, Pavan, D., Schiesari, L.C. & Skuk, G. (1997) Foot-flagging display in the Brazilian stream-breeding frog Hylodes asper (Leptodactylidae). Scientific film CTf 2703 ÖWF, Wien. Available from: https://amphibiaweb.org/cgi/amphib_query?where-genus=Hylodes&where-species=asper (accessed 23 June 2020)
    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
    Köhler, J., Jansen, M., Rodríguez, A., Kok, P.J.R., Toledo, L.F., Emmrich, M., Glaw, F., Haddad, C.F.B., Rödel, M.O. & Vences, M. (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa, 4251 (1), 1–124. https://doi.org/10.11646/zootaxa.4251.1.1
    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Mo­lecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549. https://doi. org/10.1093/molbev/msy096
    Laia, R.C., Fatorelli, P., Hatano, F.H. & Rocha, C.F.D. (2010) Tadpole of Hylodes fredi (Anura; Hylodidae), a frog endemic to an Atlantic Forest island (Ilha Grande, Rio de Janeiro State), Brazil. Zootaxa, 2640 (1), 62–64. https://doi.org/10.11646/zootaxa.2640.1.5
    Lannoo, M.J. (1987) Neuromast topography in anuran amphibians. Journal of Morphology, 191, 115–129. https://doi.org/10.1002/jmor.1051910203
    Lavilla, E.O. & Scrocchi, G.J. (1986) Morfometría larval de los géneros de Telmatobiinae (Anura: Leptodactylidae) de Argentina y Chile. Physis, 44, 39–43.
    Leigh, J.W. & Bryant, D. (2015). Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110–1116. https://doi.org/10.1111/2041-210X.12410
    Lyra, M.L., Haddad, C.F.B. & de Azeredo-Espin, A.M.L. (2017) Meeting the challenge of DNA barcoding Neotropical amphibians: polymerase chain reaction optimization and new COI primers. Molecular Ecology Resources, 17, 966–980. https://doi.org/10.1111/1755-0998.12648
    Nascimento, L.B., Pombal Jr., J.P. & Haddad, C.F.B. (2001) A new frog of the genus Hylodes (Amphibia: Leptodactylidae) from Minas Gerais, Brazil. Journal of Zoology, 254, 421–428. https://doi.org/10.1017/S0952836901000917
    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, 497–505. https://doi.org/10.1163/156853805774806214
    Narvaes, P. & Rodrigues, M.T. (2005) Visual communication, reproductive behavior, and home range of Hylodes dactylocinus (Anura, Leptodactylidae). Phyllomedusa, 4, 147–158. https://doi.org/10.11606/issn.2316-9079.v4i2p147-158
    Naz, S., Akbar, H., Habib, S.S., Faiq, M., Rais, M., Malik, M.A. & Shafiq, A. (2019) Role of anuran tadpoles as biological control for dengue larvae. International Journal of Mosquito Research, 6, 22–26.
    Palumbi, S.R., Martin, A., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The simple fool’s guide to PCR. Version 2.0. Available from: http://palumbi.stanford.edu/SimpleFoolsMaster.pdf (accessed 30 March 2016)
    Pimenta, B.V.S., Wachlevski, M. & Cruz, C.A.G. (2008) Morphological and acoustical variation, geographic distribution, and conservation status of the spinythumb frog Crossodactylus bokermanni Caramaschi and Sazima, 1985 (Anura, Hylodidae). Journal of Herpetology, 42, 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, 1–33. 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
    Pombal Jr., J.P., Sazima, I. & Haddad, C.F.B. (1994) Breeding behavior of the Pumpkin Toadlet, Brachycephalus ephippium (Brachycephalidae). Journal of Herpetology, 28, 516–519. https://doi.org/10.2307/1564972
    Pombal Jr., J.P., Feio, R.N. & Haddad, C.F.B. (2002) A new species of torrent frog genus Hylodes (Anura: Leptodactylidae) from southeastern Brazil. Herpetologica, 58, 462–471. https://www.jstor.org/stable/3893302
    Robillard, T., Höbel, G. & Gerhardt, H.C. (2006) Evolution of advertisement signal in North American hylid frogs: vocalizations as end products of calling behavior. Cladistics, 22, 533–545. https://doi.org/10.1111/j.1096-0031.2006.00118.x
    Rossa-Feres, D.C. & Nomura, F. (2006) Characterization and taxonomic key for tadpoles (Amphibia: Anura) from the northwestern region of São Paulo State, Brazil. Biota Neotropica, 6, BN00706012006. https://doi.org/10.1590/S1676-06032006000100014
    Salinas, A.S., Costa, R.N., Orrico, V.G.D. & Solé, M. (2018) Tadpoles of the bromeliad-dwelling frog Phyllodytes luteolus are able to prey on mosquito larvae. Ethology Ecology & Evolution, 30, 485–496. https://doi.org/10.1080/03949370.2018.1438518
    Sambrook, J. & Russell, D.W. (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor, New York, New York, 2100 pp.
    Sherratt, E., Vidal-García, M., Anstis, M. & Keogh, J.S. (2017) Adult frogs and tadpoles have different macroevolutionary patterns across the Australian continent. Nature Ecology & Evolution, 1, 1385–1391. https://doi.org/10.1038/s41559-017-0268-6
    Silva, H.R. & Benmaman, P. (2008) Uma nova espécie de Hylodes Fitzinger da Serra da Mantiqueira, Minas Gerais, Brasil (Anura: Hylodidae). Revista Brasileira de Zoololgia, 25, 89–99. https://doi.org/10.1590/S0101-81752008000100013
    Silva-Soares, T., Nogueira-Costa, P., Borges-Jr., V.N.T., Weber, L.N. & Rocha, C.F.D. (2015) The larva of Crossodactylus aeneus Müller, 1924: morphology and ecological aspects. Herpetologica, 71, 46–57. https://doi.org/10.1655/HERPETOLOGICA-D-13-00048
    Struett, M.M., Confetti, A.E. & Leivas, P.T. (2021) The Brazilian torrent frog controls its paired vocal sacs independently: implications for acoustic parameters. South American Journal of Herpetology, 21, 65–69. https://doi.org/10.2994/SAJH-D-19-00103.1
    Thurnheer, S. & Reyer, H.U. (2000) Spatial distribution and survival rate of waterfrog tadpoles in relation to biotic and abioticfactors: a field experiment. Amphibia-Reptilia, 22, 21–32. https://doi.org/10.1163/156853801750096150
    Toledo, L.F., Llusia, D., Vieira, C.A., Corbo, M. & Márquez, R. (2015) Neither convergence nor divergence in the advertisement call of sympatric congeneric Neotropical treefrogs. Bioacoustics, 24, 31–47. https://doi.org/10.1080/09524622.2014.926831
    Toscano, N.P., Freitas, N.H.A., Rezende, M.R.C., Provete, D.B., Lyra, M., Haddad, C.F.B., Rossa-Feres, D.C. & Silva, F.R. (2019) External morphology and internal oral features of the tadpole of Crossodactylus caramaschii (Anura: Hylodidae). Journal of Herpetology, 53, 263–271. https://doi.org/10.1670/18-155
    Vidigal, I., Carvalho, T.R., Clemente-Carvalho, R.G. & Giaretta, A.A. (2018) Vocalizations, tadpole, and natural history of Crossodactylus werneri Pimenta, Cruz & Caramaschi, 2014 (Anura: Hylodidae), with comments on distribution and intraspecific variation. Zootaxa, 4388 (1), 61–75. https://doi.org/10.11646/zootaxa.4388.1.4
    Vittorazzi, S.E., Lourenço, L.B., Zattera, M.L., Weber, L.N., Recco-Pimentel, S.M. & Bruschi, D.P. (2021) Cytogenetic and genetic data support Crossodactylus aeneus Müller, 1924 as a new junior synonym of C. gaudichaudii Duméril and Bibron, 1841 (Amphibia, Anura). Genetics and Molecular Biology, 44, e20200301. https://doi.org/10.1590/1678-4685-GMB-2020-0301
    Weygoldt, P. (1986) Beobachtungen Zur Ökologie und biologie von fröschen an einem neotropischen bergbach. Zoologische Jahrbücher (Systematik), 113, 429–454.
    Weygoldt, P. (1989) Changes in the composition of mountain stream frog communities in the Atlantic mountains of Brazil: frogs as indicators of environmental deterioration?. Studies on Neotropical Fauna and Environment, 243, 249–255. https://doi.org/10.1080/01650528909360795
    Weygoldt, P. & Carvalho-e-Silva, S.P. (1992) Mating and oviposition in the Hylodine frog Crossodactylus gaudichaudii (Anura: Leptodactylidae). Amphibia-Reptilia, 13, 35−45. https://doi.org/10.1163/156853892X00210
    Wilczynskia, W.A., Rand, S. & Ryan, M.J. (2001) Evolution of calls and auditory tuning in the Physalaemus pustulosus species group. Brain, Behavior and Evolution, 58, 137–151. https://doi.org/10.1159/000047268
    Wogel, H., Abrunhosa, P.A. & Weber, L.N. (2004) The tadpole, vocalizations and visual displays of Hylodes nasus (Anura: Leptodactylidae). Amphibia-Reptilia, 25, 219–227. https://doi.org/10.1163/1568538041231184