Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2020-12-09
Page range: 206–220
Abstract views: 104
PDF downloaded: 5

Advertisement call of two threatened red-bellied-toads, Melanophryniscus cambaraensis and M. macrogranulosus (Anura: Bufonidae), from the Atlantic Rainforest, southern Brazil

Programa de Pós-Graduação em Biologia Animal, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, 91501-970 - Porto Alegre, RS, Brazil.
Programa de Pós-Graduação em Biologia Animal, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, 91501-970 - Porto Alegre, RS, Brazil.
Fonoteca Zoológica, Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), 28006, Madrid, Spain.
Programa de Pós-Graduação em Biologia Animal, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, 91501-970 - Porto Alegre, RS, Brazil.
Amphibia Taxonomy Bioacoustics Amphibian Endemic species Endangered species

Abstract

In anuran amphibians, acoustic signals are fundamental mechanisms of mate recognition and mate choice, which makes frog calls a fundamental tool for anuran taxonomy. In this work, we describe the advertisement call of two species for the genus Melanophryniscus, M. cambaraensis and M. macrogranulosus and use the descriptions to try to solve a taxonomic problem between them. We collected data after heavy rains in three different sample sites in Rio Grande do Sul, Brazil, between 2012 and 2013. The advertisement call of both species is composed of two segments. It always begins with part A (about 0.44–6 seconds) composed of single modulated pulses separated by long time intervals. It is followed by part B, a long train of unmodulated pulses with short time intervals, lasting from 9 to 32.2 seconds. Principal Component Analysis (PCA) indicated some variation between temporal parameters of the two species, but Multivariate Analysis of Variance showed no significant differences. Within-individual Coefficient of Variation (CV) showed only two static parameters: pulse rate and peak frequency, both in the part B of the call. Despite intra-male variation in some acoustic parameters, it is not possible to differentiate between M. cambaraensis and M. macrogranulosus species only using bioacoustics.

 

References

  1. Achaval, F. & Olmos, A. (2007) Anfibios y Reptiles del Uruguay. 3 ed. Graphis Impresora, Montevideo, 136 pp.

    Alström, P. & Ranft, R. (2003) The use of sounds in avian systematics and the importance of bird sound archives. Bulletin of the British Ornithologists’ Club, 123, 114–135.

    Baldo, D. & Basso, N.G. (2004) A new species of Melanophryniscus Gallardo, 1961 (Anura: Bufonidae), with comments on the species of the genus reported for Misiones, northeastern Argentina. Journal of Herpetology, 38 (3), 393–404.

    https://doi.org/10.1670/144-03A

    Baldo, D., Borteiro, C., Kolenc, F., Rosset, S. & Prigioni, C. (2012) The taxonomic status of Melanophryniscus orejasmirandai Prigioni & Langone, 1987 “1986” (Anura: Bufonidae). Zootaxa, 3235 (1), 45–61.

    https://doi.org/10.11646/zootaxa.3235.1.4

    Barrio, A. (1964) Peculiaridades del canto nupcial de Melanophryniscus stelzneri (Weyenbergh) (Anura: Brachicephalidae). Physis, 24, 435–437.

    Bee, M.A., Kozich, C.E., Blackwell, K.J. & Gerhardt, H.C. (2001) Individual variation in advertisement calls of territorial male green frogs, Rana clamitans: implications for individual discrimination. Ethology, 107, 65–84.

    https://doi.org/10.1046/j.1439-0310.2001.00640.x

    Bioacoustics Research Program (2011) Raven Pro: interactive sound analysis software. Version 1.4. The Cornell Lab of Ornithology Ithaca, New York. [program]

    Brasil. (2014) Portaria do Ministério do Meio Ambiente Nº 444 de 17 de dezembro de 2014. Lista Nacional Oficial de Espécies da Fauna Ameaçadas de Extinção. Diário Oficial da União, 245, 12–126.

    Braun, P.C. (1973) Nova espeìcie do gênero Melanophryniscus Gallardo, 1961 do Estado do Rio Grande do Sul, Brasil (Anura, Brachycephalidae). Iheringia, Série Zoology, 44, 3–13.

    Braun, P.C. & Braun, C.A.S. (1979) Nova espécie de Melanophryniscus Gallardo, 1961 do Estado do Rio Grande do Sul, Brasil (Anura, Bufonidae). Iheringia, Série Zoology, 54, 7–16.

    Cairo, S.L., Zalba, S.M. & Úbeda, C.A. (2013) Reproductive pattern in the southernmost populations of South American redbelly toads. Journal of Natural History, 47, 2125–2134.

    https://doi.org/10.1080/00222933.2013.769644

    Caldart, V.M., Santos, T.G. dos & Maneyro, R. (2013) The advertisement and release calls of Melanophryniscus pachyrhynus (Miranda-Ribeiro, 1920) from the central region of Rio Grande do Sul, southern Brazil. Acta Herpetologica, 8, 115–122.

    Caorsi, V.Z., Colombo, P., Freire, M.D., Amaral, I.B., Zank, C., Borges-Martins, M. & Grant, T. (2014) Natural history, coloration pattern and conservation status of the threatened South Brazilian red bellied toad, Melanophryniscus macrogranulosus Braun, 1973 (Anura, Bufonidae). Herpetology Notes, 7, 585–598.

    Castellano, S., Rosso, A., Doglio, S. & Giacoma, C. (1999) Body size and calling variation in the green toad (Bufo viridis). Journal of Zoology, 248, 83–90.

    https://doi.org/10.1111/j.1469-7998.1999.tb01025.x

    Cruz, C.A.G. & Caramaschi, U. (2003) Taxonomic status of Melanophryniscus stelzneri dorsalis (Mertens, 1933) and Melanophryniscus stelzneri fulvoguttatus (Mertens, 1937) (Amphibia, Anura, Bufonidae). Boletim do Museu Nacional, Rio de Janeiro, 500, 1–11.

    Duré, M.I., Schaefer, E.F. & Kehr, A.I. (2015) Acoustic repertoire of Melanophryniscus cupreuscapularis (Céspedez and Álvarez 2000) (Anura: Bufonidae): advertisement, encounter, and release calls. Journal of Herpetology, 49 (1), 53–59.

    https://doi.org/10.1670/13-115

    Escobar, A., Maneyro, R. & Di-Bernardo, M. (2004) Rediscovery of Melanophryniscus macrogranulosus (Anura, Bufonidae), an endangered species of Amphibia from the State of Rio Grande do Sul, Brazil. Biociências, 12 (1). [published online]

    Esteban, M. & Sánchez-Herráiz, M. (2002) Effects of age, size and temperature on the advertisement calls of two Spanish populations of Pelodytes punctatus. Amphibia-Reptilia, 23, 249–258.

    https://doi.org/10.1163/15685380260449135

    Ferrari, L. & Vaira, M. (2008) Análisis comparativo de la estructura del canto del anuncio de tres poblaciones de Melanophryniscus rubriventris (Vellar, 1947) (Anura: Bufonidae). Cuadernos de Herpetología, 22, 25–34.

    Forti, L.R., Haddad, C.F.B., Leite, F., de Oliveira, D.L., de Assis, C., Crivellari, L.B., Mello, C.M., Garcia, P.C.A., Zornosa-Torres, C. & Toledo, L.F. (2019) Notes on vocalizations of Brazilian amphibians IV: advertisement calls of 20 Atlantic Forest frog species. PeerJ, 7, e7612.

    https://doi.org/10.7717/peerj.7612

    Friedl, T.W.P. & Klump, G.M. (2002) The vocal behaviour of male european treefrogs (Hyla arborea): implications for inter- and intrasexual selection. Behaviour, 139, 113–136.

    https://doi.org/10.1163/15685390252902319

    Frost, D.R. (2019) Amphibian Species of the World: an Online Reference. Version 6.0. American Museum of Natural History, New York. Available from: https://amphibiansoftheworld.amnh.org/ (accessed 16 September 2019)

    Garcia, P.C.A. & Vinciprova, G. (2003) Anfiìbios. In: Fontana, C.S., Bencke, G.A., Reis, R.E., (Eds.), Livro vermelho da fauna ameaçada extinçaÞo no Rio Grande do Sul. EDIPUCRS, Porto Alegre, pp. 147–164.

    Garcia, P., Kwet, A. & Silvano, D. (2004) Melanophryniscus cambaraensis. The IUCN Red List of Threatened Species, 2004, e.T54817A11208173.

    https://doi.org/10.2305/IUCN.UK.2004.RLTS.T54817A11208173.en

    Gerhardt, H.C. (1991) Female mate choice in treefrogs: static and dynamic acoustic criteria. Animal Behaviour, 42, 615–635.

    https://doi.org/10.1016/S0003-3472(05)80245-3

    Giacoma, C. & Castellano, S. (2001) Advertisement call variation and speciation in the Bufo viridis complex. In: Ryan, M.J. (Ed.), Anuran Communication. Smithsonian Institution Press, Washington, D.C., pp. 205–219.

    Haad, B., Vera Candioti, F. & Baldo, D. (2011) Shape variation in lentic and lotic tadpoles of Melanophryniscus (Anura: Bufonidae). Studies on Neotropical Fauna and Environment, 46, 91–99.

    https://doi.org/10.1080/01650521.2011.593124

    Kohler, J., Jansen, M., Rodriguez, A., Kok, P.J.R., Toledo, L.F., Emmrich, M., Glaw, F., Haddad, C.F.B., Rodel, M.O. & Vences, M. (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa, 4251, 1–124.

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

    Kurth, M., Hornes, S. & Rodder, D. (2013) Notes on the acoustic repertoire of Melanophryniscus klappenbachi Prigioni & Langone, 2000. Zootaxa, 3626, 597–600.

    https://doi.org/10.11646/zootaxa.3626.4.15

    Kwet, A. & Di-Bernardo, M. (1999) Pró-Mata. Anfíbios—Amphibien—Amphibian. EDIPUCRS, Porto Alegre, 107 pp.

    Kwet, A., Maneyro, R., Zillikens, A. & Mebs, D. (2005) Advertisement call of Melanophryniscus dorsalis (Mertens, 1933) and M. montevidensis (Phillipi, 1902), two parapatric species from southern Brazil and Uruguay, with comments on morphological variation in the Melanophryniscus stelzneri group (Anura: Bufonidae). Salamandra, 41, 3–20.

    Kwet, A. & Miranda, T. (2001) Zur biologie und taxonomie der Schwarz-Kröte Melanophryniscus atroluteus (Miranda-Ribeiro, 1920). Herpetofauna, 23, 19–27.

    Littlejohn, M.J. (1969) The systematic significance of isolating mechanisms. Systematic Biology, 459–482.

    Mângia, S., Santana, D.J. & Mariotto, L.R. (2019) The advertisement call of the phytotelm-breeding Melanophryniscus xanthostomus (Anura: Bufonidae). Zoologia, 36, 1–7.

    https://doi.org/10.3897/zoologia.36.e25662

    Márquez, R. & Eekhout, X. (2006) Advertisement calls of six species of anurans from Bali, Republic of Indonesia. Journal of Natural History, 40 (9–10), 571–588.

    https://doi.org/10.1080/00222930600712129

    Márquez, R. & Tejedo, M. (1990) Size-based mating pattern in the tree-frog Hyla arborea. Herpetologica, 46, 176–182.

    Márquez, R., De la Riva, I. & Bosch, J. (1995) Advertisement Calls of Bolivian Leptodactylidae (Amphibia, Anura). Journal of Zoology, London, 237, 313–336.

    https://doi.org/10.1111/j.1469-7998.1995.tb02765.x

    McClelland, B.E., Wilczynski, W. & Ryan, M.J. (1998) Intraspecific variation in laryngeal and ear morphology in male cricket frogs (Acris crepitans). Biological Journal of the Linnean Society, 63, 51–67.

    https://doi.org/10.1111/j.1095-8312.1998.tb01638.x

    Naya, D.E., Langone, J.A. & de Sá, R.O. (2004) Características histológicas de la tumefacción frontal de Melanophryniscus (Amphibia: Anura: Bufonidae). Revista Chilena de Historia Natural, 77, 593–59.

    https://doi.org/10.4067/S0716-078X2004000400002

    Rio Grande do Sul (2014) Decreto Estadual Nº 51.797 de 8 de setembro de 2014. Lista das Espécies da Fauna Silvestre Ameaçadas de Extinção do Rio Grande do Sul. Diário Oficial do Estado, 2014, 9.

    Robisson, P., Aubin, T. & Bremond, J.C. (1993) Individuality in the voice of the emperor penguin Aptenodytes forsteri: adaptation to a noisy environment. Ethology, 94, 279–290.

    https://doi.org/10.1111/j.1439-0310.1993.tb00445.x

    Ryan, M.J. & Wilczynski, W. (1991) Evolution of intraspecific variation in the advertisement call of a cricket frog (Acris crepitans, Hylidae). Biological Journal of the Linnean Society, 44, 249–271.

    https://doi.org/10.1111/j.1095-8312.1991.tb00619.x

    Santos, R.R., Leonardi, S.B., Caorsi, V.Z. & Grant, T. (2010) Directional orientation of migration in an aseasonal explosive-breeding toad from Brazil. Journal of Tropical Ecology, 26, 415–421.

    https://doi.org/10.1017/S0266467410000180

    Silvano, D. & Garcia, P. (2010) Melanophryniscus macrogranulosus. The IUCN Red List of Threatened Species, 2010, e.T54823A11210082.

    https://doi.org/10.2305/IUCN.UK.2010-2.RLTS.T54823A11210082.en

    Sueur, J., Aubin, T. & Simonis, C. (2008) Equipment review: seewave, a free modular tool for sound analysis and synthesis. Bioacoustics, 18, 213–226.

    https://doi.org/10.1080/09524622.2008.9753600

    Teixeira, B.F.V., Giaretta, A.A. & Pansonato, A. (2013) The advertisement call of Dendropsophus tritaeniatus (Bokermann, 1965) (Anura: Hylidae). Zootaxa, 3669, 189–192.

    https://doi.org/10.11646/Zootaxa.3669.2.12

    Tishechkin, D.Y. (2014) The use of bioacoustic characters for distinguishing between cryptic species in insects: Potentials, restrictions, and prospects. Entomological Review, 94, 289–309.

    https://doi.org/10.1134/S0013873814030014

    Vaira, M. (2005) Annual variation of breeding patterns of the toad, Melanophryniscus rubriventris (Vellard, 1947). Amphibia-Reptilia, 26, 193–199.

    https://doi.org/10.1163/1568538054253519

    Wells, K.D. (2007) The ecology and behavior of amphibians. The University of Chicago Press, Chicago, Illinois, 1148 pp.

    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

    Zank, C., Becker, F., Abadie, M., Baldo, D., Maneyro, R. & Borges-Martins, M. (2014) Climate Change and the Distribution of Neotropical Red Bellied Toads (Melanophryniscus, Anura, Amphibia): How to Prioritize Species and Populations? PLoS One, 9, e94625.

    https://doi.org/10.1371/journal.pone.0094625