Abstract
Neotropical toads from the Rhinella margaritifera species group have been considered a taxonomic puzzle for a long time. Because of the high morphological similarity and an unknown number of undescribed taxa among the species of this group, we did an extensive search for character distribution within all nominal taxa. Herein we describe Rhinella parecis sp. nov. a new species from Southern Brazilian Amazon. We provide a morphological diagnosis, morphometric comparisons with similar species, and a molecular phylogenetic hypothesis on the relationships of the new species. Rhinella parecis sp. nov. is assigned to the R. margaritifera group and differs from others species by snout-vent length ranging 40.7–53.5 mm in males (n=12) and 44.9–54.8 mm in females (n=4), snout rounded in dorsal view, acute with fleshy ridge extending to tip of snout in lateral view, canthal and pre-orbital crests absent, supra-orbital, parietal and supra-tympanic crests present and low, dorsolateral row of tubercles present, bony protrusion at the angle of jaws absent, tympanum evident, vertebral apophyses absent and toes half-webbed. The new species is the 20th species associated to the R. margaritifera group distributed in the Chapada dos Parecis, a probable center of endemism in states of Rondônia and Mato Grosso, Brazil.
References
Ávila, R.W., Pansonato, A. & Strüssmann, C. (2010) A New Species of the Rhinella margaritifera group (Anura: Bufonidae) from Brazilian Pantanal. Zootaxa, 2339 (1), 57–68.
https://doi.org/10.11646/zootaxa.2339.1.3
Ávila, R.W., Pansonato, A., Perez, R., Carvalho, V.T., Roberto, I.J., Morais, D.H., Almeida, A.P. Rojas, R., Gordo, M. & Farias, I.P. (2018) On Rhinella gildae Vaz-Silva, Maciel, Bastos & Pombal 2015 (Anura: Bufonidae): Phylogenetic relationship, morphological variation, advertisement and release calls and geographic distribution. Zootaxa, 4462 (2), 274–290.
https://doi.org/10.11646/zootaxa.4462.2.9
Azevedo, J.A.R., Valdujo, P.H. & Nogueira. C.C. (2016) Biogeography of anurans and squamates in the Cerrado hotspot: coincident endemism patterns in the richest and most impacted savanna on the globe. Journal of Biogeography, 43 (12), 2454–2464.
https://doi.org/10.1111/jbi.12803
Caldwell, J.P. (1991) A new species of toad in the genus Bufo from Pará, Brasil, with an unusual breeding site. Papéis Avulsos de Zoologia, 37 (26), 389–400.
Caramaschi, U. & Niemeyer, H. (2003) Nova espécie do complexo de Bufo margaritifer (Laurenti, 1768) do Estado do Mato Grosso do Sul, Brasil (Amphibia, Anura, Bufonidae). Boletim do Museu Nacional, 501, 1–16.
Caramaschi, U. & Pombal Jr., J.P. (2006) A new species of Rhinella Fitzinger, 1826 from the Atlantic Rain Forest, eastern Brazil (Amphibia, Anura, Bufonidae). Papéis Avulsos de Zoologia, 46, 251–259.
https://doi.org/10.1590/S0031-10492006002300001
Cardozo, N.R.R., Arriaga, N.C. & Ricaurte, J.C.D. (2016) Diversidad de anuros en la Reserva Natural Comunitaria El Manantial, Florencia, Caquetá, Colombia. Revista Biodiversidade Neotropical, 6, 212–220.
https://doi.org/10.18636/bioneotropical.v6i2.328
Colli, G.R., Costa, G.C., Garda, A.A., Kopp, K.A., Mesquita, D.O., Peres, A.K., Valdujo, P.H., Vieira, G.H.C. & Wiederhecker, H.C. (2003) A critically endangered new species of Cnemidophorus (Squamata, Teiidae) from a Cerrado enclave in southwestern Amazonia, Brazil. Herpetologica, 59 (1), 76–88.
https://doi.org/10.1655/0018-0831(2003)059[0076:ACENSO]2.0.CO;2
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
https://doi.org/10.1038/nmeth.2109
Fouquet, A., Noonan, B.P., Rodrigues, M.T., Pech, N., Gilles, A. & Gemmell, N.J. (2012a) Multiple quaternary refugia in the eastern Guiana Shield revealed by comparative phylogeography of 12 frog species. Systematic Biology, 61, 461–489.
https://doi.org/10.1093/sysbio/syr130
Fouquet, A., Recoder, R., Teixeira, M., Cassimiro Da Silva, J., Amaro, R.C., Camacho, A.G., Damasceno, R., Carnaval, A.C., Moritz, C. & Rodrigues, M.T. (2012b) Molecular phylogeny and morphometric analyses reveal deep divergence between Amazonia and Atlantic Forest species of Dendrophryniscus. Molecular Phylogenetics and Evolution, 62, 826–838.
https://doi.org/10.1016/j.ympev.2011.11.023
Fouquet A., Vences, M., Salducci, M.D., Meyer, A., Marty, C., Blanc, M. & Gilles, A. (2007a) Revealling cryptic diversity using molecular phylogenetics and phylogeography in frogs of the Scinax ruber and Rhinella margaritifera species groups. Molecular Phylogenetics and Evolution, 43 (2), 567–582.
https://doi.org/10.1016/j.ympev.2006.12.006
Fouquet, A., Gaucher, P., Blanc, M. & Velez-Rodriguez, C.M. (2007b) Description of two new species of Rhinella (Anura: Bufonidae) from the lowlands of the Guiana shield. Zootaxa, 1663, 17–32.
https://doi.org/10.5281/zenodo.180003
Freitas J.L., Strüssmann, C., Carvalho, M.A., Kawashita-Ribeiro, R.A. & Mott, T. (2011) A new species of Bachia Gray, 1845 (Squamata: Gymnophthalmidae) from the Cerrado of Midwestern Brazil. Zootaxa, 2737 (1), 61–68.
https://doi.org/10.11646/zootaxa.2737.1.5
Frost D.R. (2019) Amphibian Species of the World: an Online Reference. American Museum of Natural History, USA. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 26 March 2019) [archived by WebCite at http://www.webcitation.org/77AQIcR6V]
Günther, A.C.L.G. (1858) Neue Batrachier in der Sammlung des britischen Museums. Archiv für Naturgeschichte. Berlin, 24, 319–328.
https://doi.org/10.5962/bhl.part.5288
Heyer, W.R. & Crombie, R.I. (2005) Leptodactylus lauramiriamae, a distinctive new species of frog (Amphibia: Anura: Leptodactylidae) from Rondônia, Brazil. Proceedings of the Biological Society of Washington, 118, 590–595.
https://doi.org/10.2988/0006-324X(2005)118[590:LLADNS]2.0.CO;2
Heyer, W.R., Rand, A.S., Cruz, C.A.G., Peixoto, O.L. & Nelson, C.E. (1990) Frogs of Boracéia. Arquivos de Biologia, 31, 231–410.
Hoogmoed, M.S. (1986) Biosystematic studies of the Bufo “typhonius” group. A preliminary progress report. In: Rocek, Z. (Ed.), Studies in Herpetology. Charles University, Prague, pp. 14–150.
Hoogmoed, M.S. (1989) South American bufonids (Amphibia: Anura: Bufonidae), an enigma for taxonomists. In: Fontanet, X. & Horta, N. (Eds.), Treballs d’Ictiologia i Herpetologia, Barcelona, 1989, pp. 167–180.
Hoogmoed, M.S. (1990). Biosystematics of South American Bufonidae, with special reference to the Bufo “typhonius” group. In: Peters, G. & Hutterer, R. (Eds.), Vertebrates in the Tropics. Museum Alexander Koening, Bonn, pp. 113–123.
Instituto Chico Mendes de Conservação da Biodiversidade—ICMBio (2018) Unidades de conservação. ICMBio, Brasília. Available from: http://www.icmbio.gov.br/portal/biodiversidade/unidades-de-conservacao/biomas-brasileiros.html (accessed 29 January 2020)
Katoh, S. (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.
Köhler, J., Vietes, D.R., Bonett, R.M., Hita Garcia, F., Glaw, F., Steinke, D. & Vences, M. (2005) New amphibians and global conservation: a boost in species discoveries in a highly endangered vertebrate group. BioScience, 55, 693–696.
https://doi.org/10.1641/0006-3568(2005)055[0693:NAAGCA]2.0.CO;2
Kumar, S., Stecher, G, Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549.
https://doi.org/10.1093/molbev/msy096
Laurenti, J.N. (1768) Specimen medicum, exhibens synopsin reptilium emendatam cum experimentis circa venena et antidota reptilium austriacorum. Joan Thomae, Viennae, 214 pp., 5 pls.
https://doi.org/10.5962/bhl.title.5108
Lavilla, E.O., Caramaschi, U., Langone, J.A., Pombal Jr, J.P. & De Sá, R.O. (2013) The identity of Rana margaritifera Laurenti, 1768 (Anura, Bufonidae). Zootaxa, 3646 (3), 251–264.
https://doi.org/10.11646/zootaxa.3646.3.4
Lavilla, E.O., Langone, J.A., Caramaschi, U., Pombal Jr. J.P. & De Sá, R.O. (2017) Comments on the neotype of Rana margaritifera Laurenti, 1768 (Anura, Bufonidae). Zootaxa, 4286 (1), 113–114.
https://doi.org/10.11646/zootaxa.4286.1.5
Leão, A.T. & Cochran, D.M. (1952) Revaldidation and re-description of Bufo ocellatus Günther, 1858 (Anura: Bufonidae). Memórias do Instituto Butantan, 24, 271–280.
Lema, T. (2004). Nova espécie de Apostolepis COPE do estado de Rondônia, Brasil (Serpentes, Elapomorphinae). Comunicações do Museu Ciência Tecnologia, 17 (2), 81–89.
Lima, A.P., Menin, M. & Araújo, M.C. (2007) A new species of Rhinella (Anura: Bufonidae) from Brazilian Amazon. Zootaxa, 1663 (1), 1–15.
https://doi.org/10.11646/zootaxa.1663.1.1
Lötters, S. & Köhler, J. (2000). A new toad of the Bufo typhonius complex from humid montane forests of Bolivia. Spixiana, 23 (3), 293–303.
Lyra, M.L., Azeredo-Espin, A. M. L. & Haddad, C.F.B. (2017) Meeting the challenge of DNA barcoding Neotropical amphibians: polymerase chain reaction optimization and new COI primers. Molecular Ecology Resource, 17, 966–980.
https://doi.org/10.1111/1755-0998.12648
Melin, D.E. (1941) Contributions to the knowledge of the Amphibia of South America. Göteborgs Kungl. Vetenskaps-och Vitterhets-samhälles. Handlingar. Serien B. Matematiska och Naturvetenskapliga Skrifter, Göteborg, pp. 1–71.
Mijares-Urrutia A. & Arends, A. (2001) A new toad of the Bufo margaritifer complex (Amphibia: Bufonidae) from northwestern Venezuela. Herpetologica, 57 (4), 523–531
Milto, K.D. & Barbanov, A.V. (2011) An annotated catalogue of the amphibian types in the collection of the Zoological Institute, Russian Academy of Sciences, St. Petersburg. Russian Journal of Herpetology, 18 (2), 137–153.
Moravec, J., Lehr, E., Cusi, J.C., Córdova, J.H. & Gvozdík, V. (2014) A new species of the Rhinella margaritifera species group (Anura, Bufonidae) from the montane forest of the Selva Central, Peru. Zookeys, 371, 35–56.
https://doi.org/10.3897/zookeys.371.6580
Myers, G.S. & Carvalho, A.L. (1945) Notes on some new or little-known Brazilian amphibians, with an examination of the history of the plata salamander, Ensatina platensis. Boletim do Museu Nacional do Rio de Janeiro, 35, 1–24, 18 pls.
Myers, C.W. & Duellman, W.E. (1982) A new species of Hyla from Cerro Colorado, and other tree frog records and geographical notes from western Panama. American Museum Novitates, 2752, 1–32.
Ohara, W.M. & Lima, F.C.T. (2015) Moenkhausia uirapuru, a new species from the upper rio Guaporeì, Chapada dos Parecis, Mato Grosso, Brazil (Teleostei: Characidae). Ichthyological Exploration of Freshwaters, 26, 159–170.
Pereira, T.N.A. & Castro, R.M.C. (2014) A new species of Utiaritichthys Miranda Ribeiro (Characiformes: Serrasalmidae) from the Serra dos Parecis, Tapajoìs drainage. Neotropical Ichthyology, 12, 397–402.
https://doi.org/10.1590/1982-0224-20130137
Pramuk, J.B. (2006) Phylogeny of South American Bufo (Anura, Bufonidae) inferred from combined evidence. Zoological Journal of Linnean Society, 146, 407–452.
https://doi.org/10.1111/j.1096-3642.2006.00212.x
Ramalho, W.P., Andrade, M.S., Matos, L.R.A. & Vieira, L.J.S. (2016) Amphibians of varzea environments and floating meadows of the oxbow lakes of the Middle Purus River, Amazonas, Brazil. Biota Neotropica, 16 (1), e20150093.
https://doi.org/10.1590/1676-0611-BN-2015-0093.
Rambaut, A. (2016). FigTree v1.4.3, http://tree.bio.ed.ac.uk/software/figtree/. Edinburgh, UK: University of Edinburgh.
Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Systematic Biology, 67 (5), 901–904.
https://doi.org/10.1093/sysbio/syy032
Roberto, I.J, Brito, L. & Cascon, P. (2011) Temporal and spatial patterns of reproductive activity in Rhinella hoogmoedi (Anura: Bufonidae) from a tropical rainforest in northeastern brazil, with the description of it’s advertisement call. South American Journal of Herpetology, 6 (2), 87–97.
https://doi.org/10.2994/057.006.0207
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 selection across a large model space. Systematic Biology, 61, 539–542.
https://doi.org/10.1093/sysbio/sys029
Santos, S.P., Ibánez, R. & Ron, S.R. (2015) Systematics of the Rhinella margaritifera complex (Anura, Bufonidae) from western Ecuador and Panama with insights in the biogeography of Rhinella alata. Zookeys, 501 (501), 109–145.
https://doi.org/10.3897/zookeys.501.8604
Savage, J.M. & Heyer, W.R. (1967) Variation and distribution in the tree-frog genus Phyllomedusa in Costa Rica, Central America. Beiträge zur Neotropischen Fauna, 5, 111–131.
https://doi.org/10.1080/01650526709360400
Silva, J.M., Linhares, D.P., Nunes, D.D., Assunção, A.G., Lima, T.R., Furlan, D.N., Carvalho, A.C. & Souza, R.C. (2005) Evolution of deforestation and natural resources degradation in Rondonia. Sociedade & Natureza, 1, 502–511.
Spix, J.B. von (1824) Animalia nova sive Species novae Testudinum et Ranarum quas in itinere per Brasiliam annis MDCCCXVII–MDCCCXX jussu et auspiciis Maximiliani Josephi I. Bavariae Regis. F. S. Hübschmann, München, 53 pp., XXII Tabs.
https://doi.org/10.5962/bhl.title.63182
StatSoft, Inc. (2011). STATISTICA (data analysis software system). Version 10. Available from: http://www.statsoft.com (accessed 12 October 2020)
Struwe, L., Kinkade M. & Maas, P.J.M. (2005) Two new Brazilian species of Tachia (Gentianaceae: Helieae). Blumea, 50, 457–462.
https://doi.org/10.3767/000651905X622707
Thominot, A. (1884) Note sur un batracien d’espèce nouvelle provenant de Panama. Bulletin de la Société Philomathique de Paris, Series 7 (8), 151–152.
Vacher, J., Chave, J., Ficetola, F., Sommeria-Klein, G., Tao, S., Thébaud, C., Blanc, M., Camacho, A., Cassimiro, J., Colston, T.J., Dewynter, M., Ernst, R., Gaucher, P., Gomes, J.O., Jairam, R., Kok, P.J.R., Lima, J.D., Martinez, Q., Marty, M., Noonan, B.P., Nunes, P., Ouboter, P., Recoder, R., Rodrigues, M.T., Snyder, A., Marques-Souza, S. & Fouquet, A. (2020) Large-scale DNA-based survey of frogs in Amazonia suggests a vast underestimation of species richness and endemism. Journal of Biogeography, 47, 1781–1791.
https://doi.org/10.1111/jbi.13847
Vanzolini, P.E. (1986) Levantamento herpetológico da área do Estado de Rondônia sob a influência da rodovia BR 364. Programa Polonoroeste, Subprograma Ecologia Animal, Relatório de Pesquisa #1. CNPq, Brasília, 50 pp.
Vaz-Silva, W., Maciel, N.M., Bastos, R.P. & Pombal Jr., J.P. (2015) Revealing two new species of the Rhinella margaritifera species group (Anura, Bufonidae): An enigmatic taxonomic group of Neotropical toads. Herpetologica, 71 (3), 212–222.
https://doi.org/10.1655/HERPETOLOGICA-D-14-00039
Vences, M., Thomas, M., van der Meijden, A., Chiari, Y. & Vieites, D. (2005). Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Frontiers in Zoology, 2 (1), 5.
https://doi.org/10.1186/1742-9994-2-5
Villacampa, J., Serrano-Rojas, S. & Whitworth, A. (2017) Amphibians of the Manu Learning Centre and other areas of the Manu region. The Crees Foundation. Cusco, Peru. pp. 282.
Zar, J.H. (1999) Biostatistical Analysis. 4a edição. Prentice Hall Inc., Upper Saddle River, New Jersey, 929 pp.