Abstract
The Rhinella granulosa group is composed of 13 species widely distributed in South America and Panama. The richness of the group may be poorly characterized due to limited characterizations caused by a lack of topotype data. This is the case for Rhinella mirandaribeiroi, which lacks topotypical (from Marajó Island, Pará state, Brazil) characterization in terms of acoustics and molecular data, as well as interpopulation variation, considering specimens from the Cerrado, including its junior synonym Bufo granulosus lutzi (Pirapora, Minas Gerais state, Brazil). At the same time, morphological and acoustic differences seem scarce and subtle compared to R. granulosa, a sister species with contiguous distribution areas. Therefore, an integrative taxonomic approach arises as necessary to assess the status of these species and differentiate them. Here, we present morphological data from recently collected topotypes of R. mirandaribeiroi, as well as acoustic and genetic data from this population. We found acoustic, molecular, and morphological evidence that B. g. lutzi and individuals distributed in the Cerrado belong to the same species of R. mirandaribeiroi, maintaining its condition of synonym. We also found that R. granulosa and R. mirandaribeiroi exhibit a conserved phenotype (morphology and acoustics) and that the presence/absence of a clear vertebral line is not a diagnostic character for both named species. However, R. granulosa and R. mirandaribeiroi show a significant genetic distance and therefore should be maintained as valid species until a better understanding of the distribution of both species is achieved.
References
- Archer, E. (2016) Estimate permutation p-values for random forest importance metrics. R package. Version 2.1. Available from: http://CRAN.R–project.org/package=rfPermute (accessed 20 January 2022)
- Brito, E.D.S. & Ilkiu-Borges, A.L. (2013) Bryoflora of the municipalities of Soure and Cachoeira do Arari, on Marajó Island, in the state of Pará, Brazil. Acta Botanica Brasilica, 27, 124–141. https://doi.org/10.1590/S0102-33062013000100013 DOI: https://doi.org/10.1590/S0102-33062013000100013
- Brown, W.M., George Jr., M. & Wilson, A.C. (1979) Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences, 76 (4), 1967–1971. https://doi.org/10.1073/pnas.76.4.1967 DOI: https://doi.org/10.1073/pnas.76.4.1967
- 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 (10), 1109. https://doi.org/10.1371/journal.pone.0001109 DOI: https://doi.org/10.1371/journal.pone.0001109
- Fouquet, A., Marinho, P., Réjaud, A., Carvalho, T.R., Caminer, M.A., Jansen, M., Rainha, R., Rodrigues, M., Werneck, F., Lima, A., Hrbek, T., Giaretta, A., Venegas, P., Chávez, G. & Ron, S. (2021) Systematics and biogeography of the Boana albopunctata species group (Anura, Hylidae), with the description of two new species from Amazonia. Systematics and Biodiversity, 19 (4), 375–399. https://doi.org/10.1080/14772000.2021.1873869 DOI: https://doi.org/10.1080/14772000.2021.1873869
- Gallardo, J.M. (1965) The species Bufo granulosus Spix (Salientia: Bufonidae) and its geographic variation. Bulletin of the Museum of Comparative Zoology, 134, 107–138.
- Giaretta, A.A., Haga, I.A. & De Andrade, F.S. (2018) The advertisement call of two species of the Rhinella granulosa group (Anura: Bufonidae). Phyllomedusa: Journal of Herpetology, 17 (2), 255–265. https://doi.org/10.11606/issn.2316–9079.v17i2p255–265 DOI: https://doi.org/10.11606/issn.2316-9079.v17i2p255-265
- Hothorn, T., Hornik, K., Van De Wiel, M.A. & Zeileis, A. (2008) Implementing a class of permutation tests: the coin package. Journal of Statistical Software, 28 (8), 1–23. https://doi.org/10.18637/jss.v028.i08 DOI: https://doi.org/10.18637/jss.v028.i08
- Jombart, T. (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403–1405. https://doi.org/10.1093/bioinformatics/btn129 DOI: https://doi.org/10.1093/bioinformatics/btn129
- Jombart, T., Devillard, S. & Balloux, E. (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. Genetics, 11, 1–15. https://doi.org/10.1186/1471-2156-11–94 DOI: https://doi.org/10.1186/1471-2156-11-94
- Köhler, J., Martin, J., Rodríguez, A., Philippe, J.R.K., Toledo, L., Emmrich, M., Glaw, F., Haddad, C.F., Rödel, M. & 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 DOI: https://doi.org/10.11646/zootaxa.4251.1.1
- Liaw, A. & Wiener, M. (2002) Classification and regression by randomForest. R News, 2, 18–22.
- Montag, L.F.D.A., Albuquerque, A.A.D., Freitas, T.M.D.S. & Barthem, R.B. (2009) Ictiofauna de campos alagados da Ilha do Marajó, Estado do Pará, Brasil. Biota Neotropica, 9, 241–253. https://doi.org/10.1590/S1676–06032009000300024 DOI: https://doi.org/10.1590/S1676-06032009000300024
- Morais, A.R., Pereira, R., Annunziata, B.B., Kokubum, M.N.C. & Maciel, N.M. (2012) Description of the advertisement call of Rhinella mirandaribeiroi (Gallardo, 1965) (Anura: Bufonidae). Zootaxa, 68 (3265), 66–68. https://doi.org/10.11646/zootaxa.3265.1.5 DOI: https://doi.org/10.11646/zootaxa.3265.1.5
- Narvaes, P. & Rodrigues, M.T. (2009) Taxonomic revision of Rhinella granulosa species group (Amphibia, Anura, Bufonidae), with a description of a new species. Arquivos de Zoologia, 40 (1), 1–73. https://doi.org/10.11606/issn.2176-7793.v40i1p1-73 DOI: https://doi.org/10.11606/issn.2176-7793.v40i1p1-73
- Palumbi, S.R. & Benzie, J. (1991) Large mitochondrial DNA differences between morphologically similar penaeid shrimp. Molecular Marine Biology and Biotechnology, 1 (1), 27–34.
- Pereyra, M.O., Baldo, D., Blotto, B.L., Iglesias, P.P., Thomé, M.T.C., Haddad, C.F.B., Barrio-Amorós, C., Ibáñez, R. & Faivovich. J. (2016) Phylogenetic relationships of toads of the Rhinella granulosa group (Anura: Bufonidae): A molecular perspective with comments on hybridization and introgression. Cladistics, 32 (1), 36–53. https://doi.org/10.1111/cla.12110 DOI: https://doi.org/10.1111/cla.12110
- Pereyra, M.O., Blotto, B.L., Baldo, D., Chaparro, J.C., Ron, S.R., Elias- Costa, A.J., Iglesias, P., Venegas, P., Thome, M., Ospina-Sarria, J., Maciel, N., Rada, M., Kolenc, F., Borteiro, C., Rivera-Correa, M., Rojas-Runjaic, F., Moravec , J., de la Riva, I., Wheeler, W., Castroviejo-Fisher, S., Grant, T., Haddad, C. & Faivovich, J. (2021) Evolution in the Genus Rhinella: A Total Evidence Phylogenetic Analysis of Neotropical True Toads (Anura: Bufonidae). Bulletin of the American Museum of Natural History, 447, 1–156. https://doi.org/10.1206/0003-0090.447.1.1 DOI: https://doi.org/10.1206/0003-0090.447.1.1
- Pramuk, J.B. (2006) Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence. Zoological Journal of the Linnean Society, 146, 407–452. https://doi.org/10.1111/j.1096-3642.2006.00212.x DOI: https://doi.org/10.1111/j.1096-3642.2006.00212.x
- R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.R-project.org/ (accessed 9 December 2024)
- Rivera, D., Prates, I., Firneno Jr., T.J., Rodrigues, M.T., Caldwell, J.P. & Fujita, M.K. (2022) Phylogenomics, introgression, and demographic history of South American true toads (Rhinella). Molecular Ecology, 31 (3), 978–992. https://doi.org/10.1111/mec.16280 DOI: https://doi.org/10.1111/mec.16280
- Rodrigues, G.M., Maschio, G.F. & Prudente, A.L.D.C. (2016) Snake assemblages of Marajó Island, Pará state, Brazil. Zoologia, Curitiba, 33 (01). [published online] https://doi.org/10.1590/S1984-4689zool-20150020 DOI: https://doi.org/10.1590/S1984-4689zool-20150020
- Rossetti, D.F. & De Toledo, P.M. (2006) Biodiversity from a historical geology perspective: a case study from Marajó Island, lower Amazon. Geobiology, 4 (3), 215–223. https://doi.org/10.1111/j.1472-4669.2006.00080.x DOI: https://doi.org/10.1111/j.1472-4669.2006.00080.x
- Sueur, J., Aubin, T. & Simonis, C. (2008) Seewave, a free modular tool for sound analysis and synthesis. Bioacoustics, 18, 213–226. https://doi.org/10.1080/09524622.2008.9753600 DOI: https://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 DOI: https://doi.org/10.1093/molbev/mst197
- Vasconcelos, B., Dos santos Campos, E.R., De sena, V.M.A., Cardoso, A.G.T., Dos santos, J.M.D.N. & Brandão, R.A. (2022) New records of Boana raniceps (Cope, 1862) (Anura, Hylidae) in Distrito Federal, Central Brazil: evidence of recent distribution expansion? Heringeriana, 16, e917969. https://doi.org/10.17648/heringeriana.v16i1.917969 DOI: https://doi.org/10.17648/heringeriana.v16i1.917969
- Vences, M. & Köhler, J. (2005) Global diversity of amphibians (Amphibia) in freshwater. In: Vences, M. & Köhler, J. (Eds.), Freshwater Animal Diversity Assessment, 2005, pp. 569–580. https://doi.org/10.1007/978-1-4020-8259-7_54 DOI: https://doi.org/10.1007/978-1-4020-8259-7_54
- Vences, M., Meike, T., Bonett, R.M. & Vieites, D.R. (2005) Deciphering Amphibian Diversity through DNA Barcoding: Chances and Challenges. Philosophical Transactions of the Royal Society B. Biological Sciences, 360 (1462), 1859–68. https://doi.org/10.1098/rstb.2005.1717 DOI: https://doi.org/10.1098/rstb.2005.1717
- Vieites, D.R., Wollenberg, K.C., Andreone, F., Köhler, J., Glaw, F. & Vences, M. (2009) Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences, 106, 8267–8272. https://doi.org/10.1073/pnas.0810821106 DOI: https://doi.org/10.1073/pnas.0810821106