Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2018-04-12
Page range: 483–505
Abstract views: 175
PDF downloaded: 1

A new species of Brachycephalus (Anura, Brachycephalidae) from the coast of Santa Catarina State, southern Atlantic Forest, Brazil

Departamento de Zoologia and Centro de Aquicultura, Instituto de Biociências, Campus Rio Claro, Av. 24-A 1515, caixa postal 199, Universidade Estadual Paulista, 13506-900, Rio Claro, São Paulo, Brazil
Departamento de Zoologia and Centro de Aquicultura, Instituto de Biociências, Campus Rio Claro, Av. 24-A 1515, caixa postal 199, Universidade Estadual Paulista, 13506-900, Rio Claro, São Paulo, Brazil
Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Ciências Biológicas, Av. Antônio Carlos 6627, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, Minas Gerais, Brazil Programa de Pós-Graduação em Zoologia, Instituto de Ciências Biológicas, Av. Antônio Carlos 6627, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, Minas Gerais, Brazi
Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Ciências
Centro Nacional de Pesquisa e Conservação de Répteis e Anfíbios, Rua 229 95, Instituto Chico Mendes de Conservação da Biodiversidade, 74605-090, Goiânia, Goiás, Brazil
Departamento de Zoologia and Centro de Aquicultura, Instituto de Biociências, Campus Rio Claro, Av. 24-A 1515, caixa postal 199, Universidade Estadual Paulista, 13506-900, Rio Claro, São Paulo, Brazil
Amphibia Brachycephaloidea elevational range morphology taxonomy

Abstract

We describe a new species of Brachycephalus from municipality of São Francisco do Sul and municipality of Itapoá, in the state of Santa Catarina, Brazil, southern Atlantic Forest. The new species is known from six localities from near sea level up to 250 meters and represents the first record of a “pumpkin-toadlet” occurring in the lowlands. Morphological traits and phylogenetic analysis of a fragment the 16S mtDNA gene place the new species in the Brachycephalus pernix group. The new species is supported by external morphology, osteology, advertisement call, and mtDNA divergence. It is characterized, among other traits by a dorsal body color dark green with a dark brown vertebral stripe, and an orange background; snout-vent length of 9.2–10.8 mm in males and 11.1–12.4 mm in females; and advertisement call short (0.02–0.03 seconds), composed of one high-frequency note (dominant frequency 6.6–7.3 kHz). We observed synchronized alternation in the emission of vocalizations among neighbor males, indicating that males of the new species are able to hear and use vocalizations to interact with each other. We provide descriptions of clutch, eggs, and juvenile and observations on parental care. The new species has not been recorded within any protected area and can be threatened by human-induced habitat loss and modification.

 

References

  1. Abegg, A.D., Ortiz, F.R., Rocha, B. & Condez, T.H. (2015) A new record for Brachycephalus nodoterga (Amphibia, Anura, Brachycephalidae) in the state of São Paulo. Brazil. Check List, 11 (1769), 1–3.
    https://doi.org/10.15560/11.5.1769

    Alves, A.C.R., Ribeiro, L.F., Haddad, C.F.B. & Reis, S.F. (2006) Two new species of Brachycephalus (Anura: Brachycephalidae) from the Atlantic Forest in Paraná state, southern Brazil. Herpetologica, 62 (2), 221–233.
    https://doi.org/10.1655/05-41.1

    Araújo, C.B., Guerra, T.J., Amatuzzi, M.C.O. & Campos, L.A. (2012) Advertisement and territorial calls of Brachycephalus pitanga (Anura: Brachycephalidae). Zootaxa, 3302, 66–67.

    Arcanjo, D.D.R., Vasconcelos, A.G., Comerma-Steffensen, S.G., Jesus, J.R., Silva, L.P., Pires Junior, O.R., Costa-Neto, C.M., Oliveira, E.B., Migliolo L., Franco, O.L., Restini, C.B.A., Paulo, M., Bendhack, L.M., Bemquerer, M.P., Oliveira, A.P., Simonsen, U. & Leite, J.R.S.A. (2015) A novel vasoactive proline-rich oligopeptide from the skin secretion of the frog Brachycephalus ephippium. PLoS ONE, 10 (12), 1–19.
    https://doi.org/10.1371/journal.pone.0145071

    Bioacoustics Research Program (2011) Raven Pro: interactive sound analysis software, Version 1.5. The Cornell Lab of Ornithology, New York, USA. Available from: http://www.birds.cornell.edu/raven (accessed 8 December 2016)

    Bornschein, M.R., Firkowski, C.R., Belmonte-Lopes, R., Corrêa, L., Ribeiro, L.F., Morato, S.A.A., Antoniazzi-Junior, R.L., Reinert, B.L., Meyer, A.L.S., Cini, F.A. & Pie, M. R. (2016a). Geographical and altitudinal distribution of Brachycephalus (Anura: Brachycephalidae) endemic to the Brazilian Atlantic Rainforest. PeerJ, 4 (e2490), 1–41.
    https://doi.org/10.7717/peerj.2490

    Bornschein, M.R., Ribeiro, L.F., Blackburn, D.C., Stanley, E.L. & Pie, M.R. (2016b). A new species of Brachycephalus (Anura: Brachycephalidae) from Santa Catarina, southern Brazil. PeerJ, 4 (e2629), 1–19.
    https://doi.org/10.7717/peerj.2629

    Cei, J.M. (1980) Amphibians of Argentina. Monitore Zoologico Italiano, Nuova Serie, Monographs, 2, 1–609.

    Clemente-Carvalho, R.B.G., Monteiro, L., Bonato, V., Rocha, H., Pereira, G., Oliveira, D., Lopes, R., Haddad, C.F.B., Martins, E. & Reis, S.F. (2008) Geographic variation in cranial shape in the pumpkin toadlet (Brachycephalus ephippium): a geometric analysis. Journal of Herpetology, 42 (1), 176–185.
    https://doi.org/10.1670/07-141R1.1

    Clemente-Carvalho, R.B.G., Antoniazzi, M.M., Jared, C., Haddad, C.F.B., Alves, A.C.R., Rocha, H.S., Pereira, G.R., Oliveira, D.F., Lopes, R.T. & Reis, S.F. (2009) Hyperossification in miniaturized toadlets of the genus Brachycephalus (Amphibia: Anura: Brachycephalidae): Microscopic structure and macroscopic patterns of variation. Journal of Morphology, 270 (11), 1285–1295.
    https://doi.org/10.1002/jmor.10755

    Clemente-Carvalho, R.G.B., Klaczo, J., Perez, I., Alves, A.C.R., Haddad, C.F.B. & Reis, S.F. (2011) Molecular phylogenetic relationships and phenotypic diversity in miniaturized toadlets, genus Brachycephalus (Amphibia: Anura: Brachycephalidae). Molecular Phylogenetics and Evolution, 61, 79–89.
    https://doi.org/10.1016/j.ympev.2011.05.017

    Clemente-Carvalho, R.B.G., Perez, S.I., Tonhati, C.H., Condez, T.H., Sawaya, R.J., Haddad, C.F.B. & Reis, S.F. (2015) Boundaries of morphological and molecular variation and the distribution range of a miniaturized froglet, Brachycephalus nodoterga (Anura: Brachycephalidae). Journal of Herpetology, 50 (1), 169–178.
    https://doi.org/10.1670/14-119

    Condez, T.H., Clemente-Carvalho, R.B.G., Haddad, C.F.B. & Reis, S.F. (2014) A new species of Brachycephalus (Anura: Brachycephalidae) from the highlands of the Atlantic Forest, southeastern Brazil. Herpetologica, 70 (1), 89–99.
    https://doi.org/10.1655/HERPETOLOGICA-D-13-00044

    Condez, T.H., Monteiro, J.P.C., Comitti, E.J., Garcia, P.C.A., Amaral, I.B. & Haddad, C.F.B. (2016) A new species of flea-toad (Anura: Brachycephalidae) from southern Atlantic Forest, Brazil. Zootaxa, 4083 (1), 40–56.
    https://doi.org/10.11646/zootaxa.4083.1.2

    Condez, T.H., Monteiro, J.P.C. & Haddad, C.F.B. (2017) Comments on the current taxonomy of Brachycephalus (Anura: Brachycephalidae). Zootaxa, 4290 (2), 395–400.
    https://doi.org/10.11646/zootaxa.4290.2.12

    Duellman, W.E. (1970) Hylid frogs of Middle America. Monograph of the Museum of Natural History, The University of Kansas, Lawrence, Kansas, 753 pp.

    Duellman, W.E. & Trueb, L. (1986) Biology of amphibians. McGraw-Hill, New York, 670 pp.

    Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797.
    https://doi.org/10.1093/nar/gkh340

    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

    Firkowski, C.R., Bornschein, M.R., Ribeiro, L.F. & Pie, M.R. (2016) Species delimitation, phylogeny and evolutionary demography of co-distributed, montane frogs in the southern Brazilian Atlantic Forest. Molecular Phylogenetics and Evolution, 100, 345–60.
    https://doi.org/10.1016/j.ympev.2016.04.023

    Frost, D.R. (2017) Amphibian species of the world: an online reference. Version 6.0. American Museum of Natural History, New York, USA. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 28 September 2017)

    Garey, M.V., Lima, A.M.X., Hartmann, M.T. & Haddad, C.F.B. (2012) A new species of miniaturized toadlet, genus Brachycephalus (Anura: Brachycephalidae), from southern Brazil. Herpetologica, 68 (2), 266–271.
    https://doi.org/10.1655/HERPETOLOGICA-D-11-00074.1.

    Giaretta, A.A. & Sawaya, R.J. (1998) Second species of Psyllophryne (Anura: Brachycephalidae). Copeia, 1998, 985–987.
    https://doi.org/10.2307/1447345

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

    Goloboff, P., Farris, J. & 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

    Goutte, S., Mason, M.J., Christensen-Dalsgaard, J., Montealegre-Z, F., Chivers, B.D., Sarria-S, F.A., Antoniazzi, M.M., Jared, C., Sato, L.A. & Toledo, L.F. (2017) Evidence of auditory insensitivity to vocalization frequencies in two frogs. Scientific Reports, 7, 12121.
    https://doi.org/10.1038/s41598-017-12145-5

    Guimarães, C.S., Luz, S., Rocha, P.C. & Feio, R.N. (2017) The dark side of pumpkin toadlet: a new species of Brachycephalus (Anura: Brachycephalidae) from Serra do Brigadeiro, southeastern Brazil. Zootaxa, 4258 (4), 327–344.
    https://doi.org/10.11646/zootaxa.4258.4.2

    Haddad, C.F.B., Giovanelli, J.G.R. & Alexandrino, J.M.B. (2008) O aquecimento global e seus efeitos na distribuição e declínio dos anfíbios. In: Buckeridge, M. (Ed.), A biologia e as mudanças climáticas no Brasil. Ed. RIMA, São Carlos, pp. 195–206.

    Haddad, C.F.B., Alves, A.C.R., Clemente-Carvalho, R.B.G. & Reis, S.F. (2010) A new species of Brachycephalus from the Atlantic Rain Forest in São Paulo state, southeastern Brazil (Amphibia: Anura: Brachycephalidae). Copeia, 2010, 410–420.
    https://doi.org/10.1643/CH-09-102

    Hanifin, C.T. (2010) The chemical and evolutionary ecology of tetrodotoxin (TTX): toxicity in terrestrial vertebrates. Marine Drugs, 8, 577–593.
    https://doi.org/10.3390/md8030577

    Hanken, J. & Wake, D.B. (1993) Miniaturization of body size: organismal consequences and evolutionary significance. Annual Review of Ecology and Systematics, 24, 501–519.
    https://doi.org/10.1146/annurev.es.24.110193.002441

    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.

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

    Izecksohn, E. (1971) Novo gênero e nova espécie de Brachycephalidae do estado do Rio de Janeiro, Brasil. Boletim do Museu Nacional, Zoologia, 280, 1–12.

    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 bioacustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa, 4251 (1), 001–124.
    https://doi.org/10.11646/zootaxa.4251.1.1

    Leite, Y.L.R., Costa, L.P., Loss, A.C., Rocha, R.G., Batalha-Filho, H., Bastos, A.C., Quaresma, V.S., Fagundes, V., Paresque, R., Passamani, M. & Pardini, R. (2015) Neotropical forest expansion during the last glacial period challenges refuge hypothesis. Proceedings of the National Academy of Sciences of United States of America, 113 (4), 1008–1013.
    https://doi.org/10.1073/pnas.1513062113

    Maniatis, T., Fritsch, E.F. & Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York, 585 pp.

    Napoli, M.F., Caramaschi, U., Cruz, C.A.G. & Dias, I.R. (2011) A new species of flea-toad, genus Brachycephalus Fitzinger (Amphibia: Anura: Brachycephalidae), from the Atlantic rainforest of southern Bahia, Brazil. Zootaxa, 2739 (1), 33–40.
    https://doi.org/10.11646/zootaxa.2739.1.3

    Nixon, K.C. (1999-2002) WinClada, v. 1.00.08. Ithaca, New York, USA. Available from: http://www.cladistics.com/wincDownload.htm (accessed 10 January 2016)

    Oliveira, J.C.F., Coco, L., Pagotto, R.V., Pralon, E., Vrcibradic, D., Pombal, J.P. & Rocha, C.F.D. (2012) Amphibia, Anura, Brachycephalus didactylus (Izecksohn, 1971) and Zachaenus parvulus (Girard, 1853): Distribution extension. Check List, 8 (2), 242–244.
    https://doi.org/10.15560/8.2.242

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

    Palumbi, S., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The simple fool’s guide to PCR. Version 2. Privately published, Honolulu, HI, 45 pp.

    Pie, M.R., Meyer, A.L.S., Firkowski, C.R., Ribeiro, L.F. & Bornschein, M.R. (2013) Understanding the mechanisms underlying the distribution of microendemic montane frogs (Brachycephalus spp., Terrarana: Brachycephalidae) in the Brazilian Atlantic Rainforest. Ecological Modelling, 250, 165–176.
    https://doi.org/10.1016/j.ecolmodel.2012.10.019

    Pie, M.R. & Ribeiro, L.F. (2015) A new species of Brachycephalus (Anura: Brachycephalidae) from the Quiriri mountain range of southern Brazil. PeerJ, 3 (e1179), 1–9.
    https://doi.org/10.7717/peerj.1179

    Pimenta, B.V.S., Bérnils, R.S. & Pombal, J.P. (2007) Amphibia, Anura, Brachycephalidae, Brachycephalus hermogenesi: filling gap and geographic distribution map. Check List, 3 (3), 277–279.
    https://doi.org/10.15560/3.3.277

    Pires Jr, O.R., Sebben, A., Schwartz, E.F., Largura, S.W.R., Bloch Jr, C., Morales, R.A.V. & Schwartz, C.A. (2002) Occurrence of tetrodotoxin and its analogues in the Brazilian frog Brachycephalus ephippium (Anura: Brachycephalidae). Toxicon, 40, 761–766.
    https://doi.org/10.1016/S0041-0101(01)00279-3

    Pires Jr, O.R., Sebben, A., Schwartz, E.F., Morales, R.A.V., Bloch Jr., C. & Schwartz, C.A. (2005) Further report of the occurrence of tetrodotoxin and new analogues in the anuran family Brachycephalidae. Toxicon, 45, 73–79.
    https://doi.org/10.1016/j.toxicon.2004.09.016.

    Pombal, J.P., Wistuba, E.M. & Bornschein, M.R. (1998) A new species of brachycephalid (Anura) from the Atlantic Rain Forest of Brazil. Journal of Herpetology, 32 (1), 70–74.
    https://doi.org/10.2307/1565481

    Pombal, J.P. (2010) A posição taxonômica das "variedades" de Brachycephalus ephippium (Spix, 1824) descritas por Miranda-Ribeiro, 1920 (Amphibia, Anura, Brachycephalidae). Boletim do Museu Nacional, Zoologia, 526, 1–12.

    Pombal, J.P. & Izecksohn, E. (2011) Uma nova espécie de Brachycephalus (Anura: Brachycephalidae) do estado do Rio de Janeiro. Papéis Avulsos de Zoologia, 51 (28), 443–451.
    https://doi.org/10.1590/S0031-10492011002800001

    R Development Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.R-project.org (accessed 5 Aug 2017)

    Ribeiro, L.F., Alves, A.C.R., Haddad, C.F.B. & Reis, S.F. (2005) Two new species of Brachycephalus Günther, 1985 from the state of Paraná, southern Brazil (Amphibia, Anura, Brachycephalidae). Boletim do Museu Nacional, Zoologia, 519, 1–18.

    Ribeiro, L.F., Bornschein, M.R., Belmonte-Lopes, R., Firkowski, C.R., Morato, S.A.A. & Pie, M.R. (2015) Seven new microendemic species of Brachycephalus (Anura: Brachycephalidae) from southern Brazil. PeerJ, 3 (e1011), 1–36.
    https://doi.org/10.7717/peerj.1011

    Ribeiro, L.F., Blackburn, D.C., Stanley, E.L., Pie, M.R. & Bornschein M.R. (2017) Two new species of the Brachycephalus pernix group (Anura: Brachycephalidae) from the state of Paraná, southern Brazil. PeerJ, 5 (e3603), 1–28.
    https://doi.org/10.7717/peerj.3603

    Sebben, A., Schwartz, C.A., Valente, D. & Mendes, E.G.A. (1986) Tetrodotoxin-like substance found in the Brazilian frog Brachycephalus ephippium. Toxicon, 24, 799–806.
    https://doi.org/10.1016/0041-0101(86)90105-4

    Sueur, J., Aubin, T. & Simonis, C. (2008) Seewave, a free modular tool for sound analysis and synthesis. Bioacoustics-The international Journal of Animal Sound and its Recording, 18, 213–226.
    http://doi.org/10.1080/09524622.2008.9753600

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
    https://doi.org/10.1093/molbev/mst197

    Taylor, W.R. &Van Dyke, G.C. (1985) Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9, 107–119.

    Trueb, L. (1993) Patterns of cranial diversity among the Lissamphibia. In: Hanken, J. & Hall, B.K. (Eds.), The skull. Vol. 2. The University of Chicago Press, Chicago and London, pp. 255–343.

    Vences, M., Thomas, M., Meijden, A.V.D., Chiari, Y. & Vieites, D.R. (2005) Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Frontiers in Zoology, 2 (5), 1–12.
    https://doi.org/10.1186/1742-9994-2-5

    Verdade, V.K., Rodrigues, M.T., Cassimiro, J., Pavan, D., Liou, N. & Lange, M. (2008) Advertisement call, vocal activity, and geographic distribution of Brachycephalus hermogenesi (Giaretta and Sawaya, 1998) (Anura, Brachycephalidae). Journal of Herpetology, 42 (3), 542–549.
    https://doi.org/10.1670/07-287.1

    Wistuba, E.M. (1998) História natural de Brachycephalus pernix Pombal, Wistuba & Borschein, 1998 (Anura) no Morro Anhangava, Município de Quatro Barras, Estado do Paraná. Ms. Thesis, Federal University of Paraná, Curitiba, 89 pp.

    Yeh, J. (2002) The effect of miniaturized body size on skeletal morphology in frogs. Evolution, 56, 628–641.
    https://doi.org/10.1111/j.0014-3820.2002.tb01372.x