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Article
Published: 2020-07-23

Rediscovery of the toadlet Brachycephalus bufonoides Miranda-Ribeiro, 1920 (Anura: Brachycephalidae) with osteological and acoustic descriptions

Universidade Federal do Rio de Janeiro, Departamento de Vertebrados, Museu Nacional, Quinta da Boa Vista, 20940–040 Rio de Janeiro, RJ, Brazil. Universidade Federal do Rio de Janeiro, Laboratório de Anfíbios e Répteis, Departamento de Zoologia, Caixa Postal 68044, 21944-970, Rio de Janeiro, RJ, Brazil.
Universidade Federal do Rio de Janeiro, Laboratório de Anfíbios e Répteis, Departamento de Zoologia, Caixa Postal 68044, 21944-970, Rio de Janeiro, RJ, Brazil.
Universidade Federal do Rio de Janeiro, Laboratório de Anfíbios e Répteis, Departamento de Zoologia, Caixa Postal 68044, 21944-970, Rio de Janeiro, RJ, Brazil.
Universidade Federal do Rio de Janeiro, Departamento de Vertebrados, Museu Nacional, Quinta da Boa Vista, 20940–040 Rio de Janeiro, RJ, Brazil.
Atlantic Forest Brachycephaloidea Morphology Natural History Taxonomy Anura

Abstract

Brachycephalus bufonoides was described as a “variety” of B. ephippium based on two specimens which 90 years later was considered full species. Besides its brief original description, nothing else is known for this species. Herein we report the rediscovery of the pumpkin-toadlet Brachycephalus bufonoides from Nova Friburgo, State of Rio de Janeiro, the second most populous area within the Atlantic Forest in Brazil. A detailed osteological description of this species was also provided, including skull, hyolaryngeal skeleton and postcranium skeleton. The laryngeal skeleton of Brachycephalus genus was depicted for the first time. We conducted a molecular phylogenetic analysis of Brachycephalus using DNA sequences comprising two fragments of mitochondrial gene (16S). Both analysis with Bayesian inference and maximum parsimony supported the recognition of B. bufonoides as an exclusive lineage, allocated within the B. ephippium species group in B. vertebralis lineage. We improved the diagnosis and variation of the species, including more collected specimens, coloration in vivo and advertisement call description. Compared with its congeners, B. bufonoides has skin on head and dorsum with dermal hyperossification; skull with hyperossification of postorbital crests; a pair of hyperossified bulges about equidistant between postorbital crests; fourth presacral vertebra with transverse process hyperossified, ornamented and sacral diapophyses hyperossified, which can be seen externally (lineage of B. vertebralis sensu Condez et al. 2020); presence of dermal ossification as separated bulges of each vertebrae; general background color orange with different intensities of dark orange blotches on dorsum, including bordering of sacral region; absence of osteoderms and presence of warts on the dorsolateral surface of body; medium body size (SVL of adults: 12.0–14.5 mm for males and 14.7–16.3 mm for females; Table 1); rough dorsum; advertisement calls with 13 to 17 pulses; presence of pulse period modulation; and advertisement calls with notes longer than 0.2 s (0.22 to 0.31 s). Herein an important contribution for the taxonomy and systematics of this genus is provided, including a large amount of novel information for B. bufonoides from different sources (i.e., molecular, morphological variation, bioacoustic), allowing it to be included in future studies of species delimitation and relationships within Brachycephalus. Also, the discovery of this species reiterates the importance of Nova Friburgo for the conservation of the Atlantic Forest biodiversity.

References

  1. Alberch, P. & Gale, E.A. (1985) A developmental analysis of an evolutionary trend: digital reduction in amphibians. Evolution, 39, 8–23.

    https://doi.org/10.1111/j.1558-5646.1985.tb04076.x

    Almeida-Santos, M. Siqueira, C.C., Van Sluys, M. & Rocha, C.F.D. (2011) Ecology of the Brazilian flea frog Brachycephalus didactylus (Terrarana: Brachycephalidae). Journal of Herpetology, 45 (2), 251–255.

    https://doi.org/10.1670/10-015.1

    Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25 (17), 3389–3402.

    https://doi.org/10.1093/nar/25.17.3389

    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

    Alves, A.C.R., Sawaya, R., Reis, S.F. & Haddad, C.B.F. (2009) A new species of Brachycephalus (Anura: Brachycephalidae) from the Atlantic Rain Forest in São Paulo State, Southeastern Brazil. Journal of Herpetology, 43 (2), 212–219.

    https://doi.org/10.1670/0022-1511-43.2.212

    Andersen, M.L. (1978) The comparative myology and osteology of the carpus and tarsus of selected anurans. Ph.D. dissertation, University of Kansas, Lawrence, Kansas, 295 pp.

    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 (1), 59–77.

    https://doi.org/10.1111/j.1096-3642.2007.00338.x

    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 (1), 66–67.

    https://doi.org/10.11646/zootaxa.3302.1.5

    Bokermann, W.C.A. (1966) Lista anotada das localidades tipo de anfíbios brasileiros. Serviço de Documentação, São Paulo, 183 pp.

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

    https://doi.org/10.7717/peerj.2629

    Bornschein, M.R., Ribeiro, L.F., Rollo Jr., M.M., Confetti, A.E. & Pie, M.R. (2017) Advertisement call of Brachycephalus albolineatus (Anura: Brachycephalidae). PeerJ, 6 (e5273), 1–18.

    https://doi.org/10.7287/peerj.preprints.3461v1

    Bornschein, M.R., Pie, M.R. & Teixeira, L. (2019a) Conservation Status of Brachycephalus Toadlets (Anura: Brachycephalidae) from the Brazilian Atlantic Rainforest. Diversity, 11, 150, 1–29.

    https://doi.org/10.3390/d11090150

    Bornschein, M.R., Rollo, M.M., Pie, M.R., Confetti, A.E. & Ribeiro, L.F. (2019b) Redescription of the advertisement call of Brachycephalus tridactylus (Anura: Brachycephalidae). Phyllomedusa, 18 (1), 3–12.

    https://doi.org/10.11606/issn.2316-9079.v18i1p3-12

    Brown, J.H. (1978) The theory of insular biogeography and the distribution of boreal birds and mammals. Great Basin Naturalist Memoirs, 2, 209–227.

    Campos, L.A., Silva, H.R. & Sebben, A. (2010) Morphology and development of additional bony elements in the genus Brachycephalus (Anura: Brachycephalidae). The Biological Journal of the Linnean Society, 99 (4), 752–767.

    https://doi.org/10.1111/j.1095-8312.2010.01375.x

    Canedo, C. & Pombal, J.P. Jr. (2007) Two new species of torrent frog of the genus Hylodes (Anura, Hylodidae) with nuptial thumb tubercles. Herpetologica, 63 (2), 224–235.

    https://doi.org/10.1655/0018-0831(2007)63[224:TNSOTF]2.0.CO;2

    Carvalho, T.R. & Giaretta, A.A. (2013) Taxonomic circumscription of Adenomera martinezi (Bokermann, 1956) (Anura: Leptodactylidae: Leptodactylinae) with the recognition of a new cryptic taxon through a bioacoustic approach. Zootaxa, 3701 (2), 207–237.

    https://doi.org/10.11646/zootaxa.3701.2.5

    Cei, J.M. (1980) Amphibians of Argentina. Monitore Zoologico Italiano. New Series. Monograph 2. Instituto de Biologia Animal, Facultad de Ciencias Agrarias, Universidad Nacional de Cuyo, Mendoz, 609 pp.

    Clemente-Carvalho, R.B., Antoniazzi, M.M., Jared, C., Haddad, C.F., Alves, A.C., Rocha, H.S., Pereira, G.R., Oliveira, D.F., Lopes, R.T. & dos 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.B.G., Klaczko, J., Perez, S.I., Alves, A.C.R., Haddad, C.F.B. & dos Reis, S.F. (2011) Molecular phylogenetic relationships and phenotypic diversity in miniaturized toadlets, genus Brachycephalus (Amphibia: Anura: Brachycephalidae). Molecular Phylogenetics and Evolution, 61 (1), 79–89.

    https://doi.org/10.1016/j.ympev.2011.05.017

    Clemente-Carvalho, R.B.G., Giaretta, A.A., Condez, T.H., Haddad, C.F.B. & dos Reis, S.F. (2012) A new species of miniaturized toadlet, genus Brachycephalus (Anura: Brachycephalidae), from the Atlantic forest of Southeastern Brazil. Herpetologica, 68 (3), 365–374.

    https://doi.org/10.1655/HERPETOLOGICA-D-11-00085.1

    Cochran, D.M. (1955) Frogs of southeastern Brazil. Bulletin of the United States National Museum, 206, 1–423.

    https://doi.org/10.5479/si.03629236.206.1

    Condez, T.H., Clemente-Carvalho, R.B.G., Haddad, C.F.B. & dos 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., Haddad, C.F.B. & Zamudio, K.R. (2020) Historical biogeography and multi-trait evolution in miniature toadlets of the genus Brachycephalus (Anura: Brachycephalidae), Biological Journal of the Linnean Society, 129 (3), 664–686.

    https://doi.org/10.1093/biolinnean/blz200

    Dirnböck, T., Essl, F. & Rabitsch, W. (2011) Disproportional risk for habitat loss of high-altitude endemic species under climate change. Global Change Biology, 17 (2), 990–996.

    https://doi.org/10.1111/j.1365-2486.2010.02266.x

    Dorigo, T.A., Siqueira, C.C., Vrcibradic, D., Maia-Carneiro, T., Almeida-Santos, M. & Rocha, C.F.D. (2012) Ecological aspects of the pumpkin toadlet, Brachycephalus garbeanus Miranda-Ribeiro, 1920 (Anura: Neobatrachia: Brachycephalidae), in a highland forest of southeastern Brazil. Journal of Natural History, 46 (39–40), 2497–2507. https://doi.org/10.1080/00222933.2012.713525

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

    Duellman, W.E. (1999) Global distribution of amphibians: patterns, conservation, and future challenges. In: Duellman, W.E. (Ed.), Patterns of distribution of amphibians: a global perspective. Johns Hopkins University Press, Baltimore, Maryland, pp. 1–30

    Fabrezi, M. (1992) El carpo de los anuros. Alytes, 10, 1–36.

    Fabrezi, M. (1993) The anuran tarsus. Alytes, 11, 47–63.

    Fabrezi, M. (2001) A survey of prepollex and prehallux variation in anuran limbs. Zoological Journal of the Linnean Society, 131 (2), 227–248.

    https://doi.org/10.1111/j.1096-3642.2001.tb01316.x

    Felsenstein, J. (1985) Confidence limits on phylogenies, an approach using bootstrap. Evolution, 39 (4), 783–791.

    https://doi.org/10.1111/j.1558-5646.1985.tb00420.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, 345–360.

    https://doi.org/10.1016/j.ympev.2016.04.023

    Folly, M., Hepp, F., Carvalho-e-Silva, S.P. & Duellman, W.E. (2014) Taxonomic status and redescription of Flectonotus ulei (Anura: Hemiphractidae), with a key for the species of Fritziana. Zoologia, 31 (4), 393–399. https://doi.org/10.1590/S1984-46702014000400011

    Folly, M., Hepp, F. & Carvalho-e-Silva, S.P. (2018) A new bromeligenous species of Fritziana Mello-Leitão, 1937 (Amphibia: Anura: Hemiphractidae) from high elevations in the Serra dos Órgãos, Rio de Janeiro, Brazil. Herpetologica, 74 (1), 58–72.

    https://doi.org/10.1655/Herpetologica-D-16-00035

    Frost, D.R. (2019) Amphibian Species of the World: An Online Reference. American Museum of Natural History, New York, USA. 21 May 2019. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 21 December 2019)

    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 (4), 985–987.

    https://doi.org/10.2307/1447345

    Goloboff, P.A., Farris, J.S. & Nixon, K.C. (2003) T.N.T.: Tree analysis using new technology. Program and documentation. Available from: http:www.zmuc.dk/public/phylogeny (accessed 21 December 2019)

    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), 1–9.

    https://doi.org/10.1038/s41598-017-12145-5

    Guimarães, C. da 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., Alves, A.C.R., Clemente-Carvalho, R.B.G. & dos 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 (3), 410–420.

    https://doi.org/10.1643/CH-09-102

    Haddad, C.F.B. & Pombal, J.P. Jr. (1998) Redescription of Physalaemus spiniger (Anura: Leptodactylidae) and description of two new reproductive modes. Journal of Herpetolology, 32 (4), 557–565.

    https://doi.org/10.2307/1565210

    Hedges, S.B., Duellman, W.E. & Heinicke, M.P. (2008) New World direct-development frogs (Anura: Terrarana): Molecular phylogeny, classification, biogeography, and conservation. Zootaxa, 1737 (1), 1–182.

    https://doi.org/10.11646/zootaxa.1737.1.1

    Hedges, S.B. (1994) Molecular evidence for the origin of birds. Proceedings of the National Academy of Sciences of the United States of America, 91 (7), 2621–2624.

    https://doi.org/10.1073/pnas.91.7.2621

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

    Hepp, F. & Pombal, J.P. Jr. (2019) Naming structures and qualifying properties of anuran bioacoustical signals: a call for homology-based nomenclature and equality for quantitative data. Anais da Acadêmia Brasileira de Ciências, 91 (4), e20190965.

    https://doi.org/10.1590/0001-3765201920190965

    Ihering, H.V. & Ihering, R.V. (1911) O Museu Paulista nos anos de 1906 a 1909. Revista do Museu Paulista, 8, 1–22.

    https://doi.org/10.5962/bhl.part.20998

    Instituto Brasileiro de Geografia e Estatística—IBGE (1959) Enciclopédia dos municípios brasileiros. IBGE, Rio de Janeiro, 467 pp.

    Izecksohn, E. (1971) Novo gênero e nova espécie de Brachycephalidae do Estado do Rio de Janeiro, Brasil (Amphibia, Anura). Boletim do Museu Nacional, Boletim do Museu Nacional (N.S.), Zoologia, New Series, Zoologia, 280, 1–12.

    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780.

    https://doi.org/10.1093/molbev/mst010

    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., Meintjes, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649.

    https://doi.org/10.1093/bioinformatics/bts199

    Köhler, J., Jansen, M., Rodrígues, 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 form best practice. Zootaxa, 4251 (1), 1–124.

    https://doi.org/10.11646/zootaxa.4251.1.1

    Koichiro, T., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30 (12), 2725–2729.

    https://doi.org/10.1093/molbev/mst197

    Littlejohn, M.J. (2001) Patterns of differentiation in temporal properties of acoustic signals of anurans. In: Ryan, M.J. (Ed.), Anuran Communication. Smithsonian Institution Press, Washington, pp. 102–120.

    McDonald, K. & Brown, J.H. (1992) Using montane mammals to model extinctions due to global change. Conservation Biology, 6 (3), 409–415.

    https://doi.org/10.1046/j.1523-1739.1992.06030409.x

    Merckx, V.S.F.T., Hendriks, K.P., Beentjes, K.K., Mennes, C.B., Becking, L.E., Peijnenburg, K.T.C.A., Afendy, A., Arumugam, N., de Boer, H., Biun, A., Buang, M.M., Chen, P., Chung, A.Y.C., Dow, R., Feijen, F.A.A., Feijen, H., Soest, C.F., Geml, J., Geurts, R., Gravendeel, B., Hovenkamp, P., Imbun, P., Ipor, I., Janssens, S.B., Jocqué, M., Kappes, H., Khoo, E., Koomen, P., Lens, F., Majapun, R.J., Morgado, L.N., Neupane, S., Nieser, N., Pereira, J.T., Rahman, H., Sabran, S., Sawang, A., Schwallier, R.M., Shim, P., Smit, H., Sol, N., Spait, M., Stech, M., Stokvis, F., Sugau, J.B., Suleiman, M., Sumail, S., Thomas, D.C., van Tol, J., Tuh, F.Y.Y., Yahya, B.E., Nais, J., Repin, R., Lakim, M. & Schilthuizen, M. (2015) Evolution of endemism on a young tropical mountain. Nature, 524, 347–350.

    https://doi.org/10.1038/nature14949

    Miranda-Ribeiro, A. (1920) Os Brachycephalideos do Museu Paulista (com três especes novas). Revista do Museu Paulista, 12, 307–316.

    https://doi.org/10.5962/bhl.part.22255

    Monteiro, J.P.C., Condez, T.H., Garcia, P.C.A., Comitti, E.J., Amaral, I.B. & Haddad, C.F.B. (2018a) A new species of Brachycephalus (Anura, Brachycephalidae) from the coast of Santa Catarina State, southern Atlantic Forest, Brazil. Zootaxa, 4407 (4), 483–505.

    https://doi.org/10.11646/zootaxa.4407.4.2

    Monteiro, J.P.C., Condez, T.H., Garcia, P.C.A. & Haddad, C.F.B. (2018b) The advertisement calls of two species of Brachycephalus (Anura: Brachycephalidae) from southern forest Brazil. Zootaxa, 4415 (1), 183–188.

    https://doi.org/10.11646/zootaxa.4415.1.10

    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

    Oliveira, E.G. & Haddad, C.F.B. (2015) Diet Seasonality and Feeding Preferences of Brachycephalus pitanga (Anura: Brachycephalidae). Journal of Herpetology, 49 (2), 252–256.

    https://doi.org/10.1670/13-211

    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.R., Martin, A., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The simple fool’s guide to PCR. Version 2.0. Privately published, compiled by Palumbi S., Department of Zoology, University of Hawaii, Honolulu, 47 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

    Pie, M.R., Ribeiro, L.F., Confetti, A.E., Nadaline, M.J. & Bornschein, M.R. (2018) A new species of Brachycephalus (Anura: Brachycephalidae) from southern Brazil. PeerJ, 6 (e5683), 1–27.

    https://doi.org/10.7717/peerj.5683

    Pombal, J.P. Jr. (1999) Oviposição e desenvolvimento de Brachycephalus ephippium (Spix) (Anura: Brachycephalidae). Revista Brasileira de Zoologia, 16 (4), 947–956.

    https://doi.org/10.1590/S0101-81751999000400004

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

    Pombal, J.P. Jr. & Gasparini, J.L. (2006) A new Brachycephalus (Anura: Brachycephalidae) from the Atlantic Rainforest of Espírito Santo, southeastern Brazil. South American Journal of Herpetology, 1 (2), 87–93.

    https://doi.org/10.2994/1808-9798(2006)1[87:ANBABF]2.0.CO;2

    Pombal, J.P. Jr. & 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

    Pombal, J.P. Jr., Sazima, I. & Haddad, C.F.B. (1994) Breeding behavior of the pumpkin toadlet, Brachycephalus ephippium (Brachycephalidae). Journal of Herpetology, 28 (4), 516–519.

    https://doi.org/10.2307/1564972

    Pombal, J.P. Jr., 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. Jr., Siqueira, C.C., Dorigo, T.A., Vrcibradic, D. & Rocha, C.F.D. (2008) A third species of the rare frog genus Holoaden (Terrarana, Strabomantidae) from a montane rainforest area of southeastern Brazil. Zootaxa, 1938 (1), 61–68.

    https://doi.org/10.11646/zootaxa.1938.1.4

    Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25 (7), 1253–1256.

    https://doi.org/10.1093/molbev/msn083

    Pounds, J.A., Bustamante, M.R., Coloma, L.A., Consuegra, J.A., Fodgen, M.P.L., Foster, P.N., La Marca, E., Masters, K.L., Merino-Viteri, A., Puschendorf, R., Ron, S.R., Sánchez-Azofeifa, G.A., Still, C.J. & Young, B.E. (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature, 439, 161–167.

    https://doi.org/10.1038/nature04246

    Pugener, L.A. & Maglia, A.M. (1997) Osteology and skeletal development of Discoglossus sardus (Anura: Discoglossidae). Journal of Morphology, 233 (3), 267–286.

    https://doi.org/10.1002/(SICI)1097-4687(199709)233:3<267::AID-JMOR6>3.0.CO;2-0

    R Core Team R (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.r-project.org/ (accessed 24 December 2019)

    Rambaut, A. & Drummond, A. (2007) TRACER. MCMC trace analysis tool. Version 1.4. University of Oxford, Oxford. Available from: http://tree.bio.ed.ac.uk/software/tracer (accessed 24 December 2019)

    Ribeiro, L.F., Alves, A.C.R., Haddad, C.F.B. & Reis, S.F. dos (2005) Two new species of Brachycephalus Günther, 1858 from the State of Paraná, southern Brazil (Amphibia, Anura, Brachyephalidae). Boletim do Museu Nacional, New Series, 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.

    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.

    https://doi.org/10.7717/peerj.3603

    Ronquist, F., Teslenko, M., Mark, P. van der, Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MRBAYES 3.2: Efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic Biology, 61 (3), 539–542.

    https://doi.org/10.1093/sysbio/sys029

    Sabaj, M.H. (2016) Standard symbolic codes for institutional resource collections in herpetology and ichthyology: an online reference. Version 6.5. American Society of Ichthyologists and Herpetologists, Washington, D.C. Available from: http://www.asih.org/ (accessed 16 August 2016)

    Siqueira, C.C., Vrcibradic, D., Nogueira-Costa, P., Martins, A.R., Dantas, L., Gomes, V.L.R., Bergallo, H.G. & Rocha, C.F.D. (2014) Environmental parameters affecting the structure of leaf-litter frog (Amphibia: Anura) communities in tropical forests: a case study from an Atlantic Rainforest area in Southeastern Brazil. Iheringia, Zoologia, 31 (2), 147–152.

    https://doi.org/10.1590/S1984-46702014000200005

    Spehn, E.M., Rudmann-Maurer, K., Körner, C. & Maselli, D. (2010) Mountain biodiversity and global change. GMBA-DIVERSITAS, University of Basel, Basel, 59 pp.

    Tandel, M.C.F.F., Loibel, S., Oliveira, E.G. & Haddad, C.F.B. (2014) Diferenciação de 3 tipos de vocalizações (cantos) na espécie Brachycephalus pitanga. Revista da Estatística da Universidade Federal de Ouro Preto, 3, 374–386.

    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.

    Trewavas, E. (1933) The hyoid and larynx of the Anura. Philosophical transactions of the Royal Society of London, Series B, 222, 410–527.

    https://doi.org/10.1098/rstb.1932.0020

    Trueb, L. (1973) Bones, frogs, and evolution. In: Vial, J.L. (Ed.), Evolutionary biology of anurans: contemporary research on major problems. University of Missouri Press, Columbia, Missouri, pp. 65–132.

    Trueb, L. (2015) Osteology. In: Duellman, W.E. (Ed.), Marsupial frog: Gastrotheca and allied genera. Johns Hopkins University Press, Baltimore, Maryland, pp. 31–51.

    Verdade, V.K., Rodrigues, M.T., Cassimiro, J., Pavan, D., Liou, N. & Lange, M.C. (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

    Weber, L.N., Verdade, V.K., Salles, R.O.L., Fouquet, A. & Carvalho-e-Silva, S.P. de (2008) A new species of Cycloramphus Tschudi (Anura: Cycloramphidae) from the Parque Nacional da Serra dos Órgãos, southeastern Brazil. Zootaxa, 2737 (1), 19–33.

    https://doi.org/10.11646/zootaxa.2737.1.2

    Wilkinson, J.A., Matsui, M. & Terachi, T. (1996) Geographic variation in a Japanese tree frog (Rhacophorus arboreus) revealed by PCR-aided restriction site analysis of mtDNA. Journal of Herpetology, 30 (3), 418–423.

    https://doi.org/10.2307/1565184

    Wistuba, E.M. (1998) História natural de Brachycephalus pernix Pombal, Wistuba and Bornschein, 1998 (Anura) no Morro Anhangava, Município de Quatro Barras, Estado do Paraná. M.Sc. dissertation, Universidade Federal do Paraná, Curitiba, 89 pp.

    Yeh, J. (2002) The effect of miniaturized body size on skeletal morphology in frogs. Evolution, 56 (3), 628–641.

    https://doi.org/10.1111/j.0014-3820.2002.tb01372.x

    Zeileis, A. & Grothendieck, G. (2005) Zoo: s3 Infrastructure for Regular and Irregular Time Series. Journal of Statistical Software, 14 (6), 1–7.

    https://doi.org/10.18637/jss.v014.i06

How to Cite

FOLLY, M., AMARAL, L. C., CARVALHO-E-SILVA, S. P. D., & POMBAL JR., J. P. (2020). Rediscovery of the toadlet <em>Brachycephalus bufonoides</em> Miranda-Ribeiro, 1920 (Anura: Brachycephalidae) with osteological and acoustic descriptions. Zootaxa, 4819(2), 265–294. https://doi.org/10.11646/zootaxa.4819.2.3