Abstract
A new species of Paratelmatobius is described from the Brazilian Atlantic Forest in the state of Paraná in southern Brazil. Adults, tadpoles, and vocalizations are described. Morphological traits and phylogenetic analysis place the new species within the P. cardosoi group. The new species can be readily distinguished from its congeners by its advertisement call being composed of two note types and comprised of a series of 2–4 notes. The new species is classified as an explosive breeder, having reproductive activity strongly associated with heavy rainfall. This discovery highlights the importance of intensifying survey efforts in the Atlantic Forest, a domain with high levels of species richness and endemism.
References
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, pp. 24–51.
Audacity Team (2017) Audacity (R): Free Audio Editor and Recorder. Version 2.2.1. Boston, Massachusetts. [program]
Bioacoustics Research Program (2014) Raven Pro: Interactive Sound Analysis Software. Version 1.5. The Cornell Lab of Ornithology, Ithaca, New York. [program]
Bornschein, M.R., Firkowski, C.R., Baldo, D., Ribeiro, L.F., Belmonte-Lopes, R., Corrêa, L., Morato, S.A.A. & Pie, M.R. (2015) Three new species of phytotelm-breeding Melanophryniscus from the Atlantic Rainforest of southern Brazil (Anura: Bufonidae). PLOS ONE, 10, e0142791.
https://doi.org/10.1371/journal.pone.0142791
Cardoso, A.J. & Haddad, C.F.B. (1990) Redescrição e biologia de Paratelmatobius gaigeae (Anura, Leptodactylidae). Papéis Avulsos de Zoologia, 37, 125–132.
Cochran, D.M. (1938) Diagnoses of new frogs from Brazil. Proceedings of the Biological Society of Washington, 51, 41–42.
Cocroft, R.B. & Rian, 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
Domenico, E.A., Haddad, C.F.B. & Zaher, H. (2014) Natural history of Paratelmatobius gaigeae (Amphibia, Anura, Leptodactylidae): description of the tadpole and advertisement call. Journal of Herpetology, 48, 430–433.
https://doi.org/10.1670/12-275
Duellman, W.E. (1970) Hylid frogs of Middle America. Monographs of the Museum of Natural History. University of Kansas, Lawrence, Kansas, xi + 753 pp., 72 pls.
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, The University of Kansas, 3, 1–41.
https://doi.org/10.5962/bhl.title.48689
Duellman, W.E. & Lehr, E. (2009) Terrestrial Breeding Frogs (Strabomantidae) in Peru. Natur und Tier-Verlag, Münster, 382 pp.
Faivovich, J., Haddad, C.F.B., Garcia, P.C.A., Frost, D.R., 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.
https://doi.org/10.1206/0003-0090(2005)294[0001:SROTFF]2.0.CO;2
Feller, A.E. & Hedges, S.B. (1998) Molecular evidence for the early history of living amphibians. Molecular Phylogenetics and Evolution, 9, 509–516.
https://doi.org/10.1006/mpev.1998.0500
Fouquet, A., Blotto, B.L., Maronna, M.M., Verdade, V.K., Junc, F.A., De S, R. & Rodrigues, M.T. (2013a) Unexpected phylogenetic positions of the genera Rupirana and Crossodactylodes reveal insights into the biogeography and reproductive evolution of leptodactylid frogs. Molecular Phylogenetics and Evolution, 67, 445–457.
https://doi.org/10.1016/j.ympev.2013.02.009
Fouquet, A., Pineau, K., Rodrigues, M.T., Mailles, J., Schneider, J.B., Ernst, R. & Dewynter, M. (2013b) Endemic or exotic: the phylogenetic position of the Martinique volcano frog Allobates chalcopis (Anura: Dendrobatidae) sheds light on its origin and challenges current conservation strategies. Systematics and Biodiversity, 11, 87–101.
https://doi.org/10.1080/14772000.2013.764944
Frost, D.R., Grant, T., Faivovich, J., Bain, R., Haas, A., Haddad, C.F.B, de Sá, R.O., Donnellan, S.C., Raxworthy, C.J., Wilkinson, M., Channing, A., Campbell, J.A., Blotto, B.L., Moler, P., Drewes, R.C., Nussbaum, R.A., Lynch, J.D., Green, D. & Wheeler, W.C. (2006) The amphibian tree of life. Bulletin of the American Museum of Natural History, 297, 1–370.
https://doi.org/10.1206/0003-0090(2006)297[0001:TATOL]2.0.CO;2
Garcia, P.C.A., Berneck, B.V.M. & Costa, C.O.R. (2009) A new species of Paratelmatobius (Amphibia, Anura, Leptodactylidae) from Atlantic Rain Forest of Southeastern Brazil. South American Journal of Herpetology, 4, 217–224.
https://doi.org/10.2994/057.004.0303
Garcia, P.C.A., Vinciprova, G. & Haddad, C.F.B. (2003) The taxonomic status of Hyla pulchella joaquini (Anura: Hylidae) with description of its tadpole and vocalization. Herpetologica, 59, 350–363.
Giaretta, A.A. & Castanho, L.M. (1990) Nova espécie de Paratelmatobius (Amphibia, Anura, Leptodactylidae) da Serra do Mar, Brasil. Papéis Avulsos de Zoologia, São Paulo, 37, 133–139.
Giaretta, A.A. & Magrini, L. (2013) Calls of Paratelmatobius gaigeae (Cochran 1938) (Anura, Leptodactylidae). Herpetology Notes, 6, 171–176.
Giasson, L.O.M. (2008) Atividade sazonal e uso do ambiente por anfíbios da Mata Atlântica no alto da Serra do Mar. Ph.D. thesis, Universidade Estadual Paulista, São Paulo, 132 pp.
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, 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, 183–190.
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
Grant, T., Frost, D.R., Caldwell, J.P., Gagliardo, R., Haddad, C.F.B. & Kok, P.J.R. (2006) Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of the American Museum of Natural History, 299, 1–262.
https://doi.org/10.1206/0003-0090(2006)299[1:PSODFA]2.0.CO;2
Graybeal, A. (1997) Phylogenetic relationships of bufonid frogs and tests of alternate macroevolutionary hypotheses characterizing their radiation. Zoological Journal of the Linnean Society, 119, 297–338.
https://doi.org/10.1111/j.1096-3642.1997.tb00139.x
Greene, A.E. & Funk, W.C. (2009) Sexual selection on morphology in an explosive breeding amphibian, the columbia spotted frog (Rana luteiventris). Journal of Herpetology, 43, 244–251.
https://doi.org/10.1670/08-112R.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, 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. (1990) Frogs of Boracéia. Arquivos de Zoologia do Estado de São Paulo, 31, 271–272.
Heyer, W.R. (1999) A new genus and species of frog from Bahia, Brazil (Amphibia: Anura: Leptodactylidae) with comments on the zoogeography of the Brazilian campos rupestres. Proceedings of the Biological Society of Washington, 112, 19–30.
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software Version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
https://doi.org/10.1093/molbev/mst010
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolotionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
https://doi.org/10.1093/molbev/msw054
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses. Molecular Biology and Evolution, 34, 772–773.
https://doi.org/10.1093/molbev/msw260
Lavilla, E.O. & Scrocchi, G.J. (1986) Morfometría larval de los géneros de Telmatobiinae (Anura: Leptodactylidae) de Argentina y Chile. Physis, 44, 39–43.
Lourenço, L.B., Garcia, P.C.A. & Recco-Pimentel, S.M. (2003) Cytogenetics of a new species of Paratelmatobius cardosoi group (Anura: Leptodactylidae), with the description of an apparent case of pericentric inversion. Amphibia-Reptilia, 24, 47–55.
https://doi.org/10.1163/156853803763806939
Lourenço, L.B., Bacci-Júnior, M., Martins, V.G., Recco-Pimentel, S.M. & Haddad, C.F.B. (2008) Molecular phylogeny and karyotype differentiation in Paratelmatobius and Scythrophrys (Anura, Leptodactylidae). Genetica, 132, 255–266.
https://doi.org/10.1007/s10709-007-9169-y
Lourenço, L.B., Targueta, C.P., Baldo, D., Nascimento, J., Garcia, P.C.A., Andrade, G.V., Haddad, C.F.B. & Recco-Pimentel, S.M. (2015) Phylogeny of frogs from the genus Physalaemus (Anura, Leptodactylidae) inferred from mitochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution, 92, 204–216.
https://doi.org/10.1016/j.ympev.2015.06.011
Lutz, B. & Carvalho, A.L. (1958) Novos anfíbios anuros das Serras Costeiras do Brasil. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro, 56, 239–249.
https://doi.org/10.1590/S0074-02761958000100012
Lyra, M.L., Haddad, C.F.B. & 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
Lynch, J.D. (1971) Evolutionary relationships, osteology, and zoogeography of leptodactyloid frogs. Miscellaneous Publication. Museum of Natural History, University of Kansas, 53, 1–238.
Malagoli, L.R., De Sá, F.P., Canedo, C. & Haddad, C.F.B. (2017) A New Species of Hylodes (Anura, Hylodidae) from Serra do Mar, Southeastern Brazil: The Fourth with Nuptial Thumb Tubercles. Herpetologica, 73, 136–147.
https://doi.org/10.1655/HERPETOLOGICA-D-16-00069
Maniatis, T., Fritsch, E.F. & Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, X + 545S.
McDiarmid, R.W. & Altig, R. (1999) Research: materials and techniques. In: McDiarmid, R.W. & Altig, R. (Eds.), Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago, pp. 7–23.
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop, 2010, 1–8.
https://doi.org/10.1109/GCE.2010.5676129
Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.
https://doi.org/10.1038/35002501
Ohler, A. & Dubois, A. (2012) Validation of two familial nomina nuda of Amphibia Anura. Alytes, 28, 162–167.
Palumbi, S.R., Martin, A.P., Kessing, B.D. & McMillan, W.O. (1991) Detecting population structure using mitochondrial DNA. In: Hoelzel, A.R. (Ed.), Genetic Ecology of Whales and Dolphins. International Whaling Comission, Cambridge, pp. 271–278.
Pinheiro, P.D.P., Pezzuti, T.L. & Garcia, P.C.A. (2012) The tadpole and vocalizations of Hypsiboas polytaenius (Cope, 1870) (Anura, Hylidae, Hylinae). South American Journal of Herpetology, 7, 123–133.
https://doi.org/10.2994/057.007.0202
Pombal, Jr.J.P. & Haddad, C.F.B. (1999) Frogs of the genus Paratelmatobius (Anura: Leptodactylidae) with descriptions of two new species. Copeia, 1999, 1014–1026.
https://doi.org/10.2307/1447976
Pyron, R.A. & Wiens, J.J. (2011) A large-scale phylogeny of Amphibia with over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61, 543–583.
https://doi.org/10.1016/j.ympev.2011.06.012
Pyron, R.A. (2014) Biogeographic analysis reveals ancient continental vicariance and recent oceanic dispersal in amphibians. Systematic Biology, 63, 779–797.
https://doi.org/10.1093/sysbio/syu042
R Core Team (2015) R: a language and environment for statistical computing. Version 3.2.2. R foundation for statistical computing, Vienna. [program]
Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer. Version 1.6. Available from: http://tree.bio.ed.ac.uk/software/tracer (accessed 16 June 2019)
Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J. & Hirota, M.M. (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142, 1141–1153.
https://doi.org/10.1016/j.biocon.2009.02.021
Ronquist, F., Teslenko, M., van der Mark, P., 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 choice across a large model space. Systematic Biology, 61, 539–542.
https://doi.org/10.1093/sysbio/sys029
Schacht, M.C. & McBrayer, L.D. (2009) A Method for Constructing an Adjustable Plataform to Obtain Lateral Photographs of Larval Anurans. Herpetological review, 40, 303–304.
Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nature methods, 9, 671–675.
https://doi.org/10.1038/nmeth.2089
Sueur, J., Aubin, T. & Simonis, C. (2008) Seewave, a new modular tool for sound analysis and synthesis. Bioacoustics, 18, 213–226.
https://doi.org/10.1080/09524622.2008.9753600
Vrcibradic, D., Ariani, C.V., Van Sluys, M. & Rocha, C.F.D. (2010) Amphibia, Leptodactylidae, Paratelmatobius mantiqueira: Distribution extension. Check List, 6, 1–2.
https://doi.org/10.15560/6.1.001
Walker, M., Lyra, M.L. & Haddad, C.F.B. (2018) Phylogenetic relationships and cryptic species diversity in the Brazilian eggbrooding tree frog, genus Fritziana Mello-Leitão 1937 (Anura: Hemiphractidae). Molecular Phylogenetics and Evolution, 123, 59–72.
https://doi.org/10.1016/j.ympev.2018.02.012
Wells, K.D. (1977) The social behaviour of anuran amphibians. Animal Behaviour, 25, 666–693.
https://doi.org/10.1016/0003-3472(77)90118-X
Zaher, H., Aguiar, E. & Pombal Jr., J.P. (2005) Paratelmatobius gaigeae (Cochran, 1938) re-discovered (Amphibia, Anura, Leptodactylidae). Arquivos do Museu Nacional, 63, 321–328.