Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2022-06-09
Page range: 487-515
Abstract views: 1279
PDF downloaded: 36

Two new surprising species of leaf-litter toad of the Rhinella margaritifera species group (Anura: Bufonidae) from the Peruvian Amazon, Loreto—Peru

Facultad de Ciencias Biológicas, Departamento académico de ecología y fauna, Universidad Nacional de la Amazonia Peruana-UNAP. Av. Grau 1072, Iquitos, Perú.
Instituto de Investigaciones de la Amazonía Peruana (IIAP), Dirección de Investigación en Diversidad Biológica Terrestre Amazónica. Av. Abelardo Quiñones km 2.5, Iquitos, Perú.
Departamento de Biologia, Centro de Ciências, Campus do Pici, Universidade Federal do Ceará, Fortaleza, Ceará, Brazil.
Programa de Pós-Graduação em Diversidade Biológica e Recursos Naturais, Universidade Regional do Cariri, Crato, Ceará, Brazil.
Unidade Descentralizada de Campos Sales, Universidade Regional do Cariri, Campos Sales, Ceará, Brazil.
Laboratório de Evolução e Genética Animal, Departamento de Genética, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Av. Rodrigo Octávio Jordão Ramos, 6200, Mini–Campus, Coroado I, 69077–000, Manaus, Amazonas, Brazil.
Departamento de Biologia, Programa de Pós Graduação em Zoologia, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil.
Laboratório de Evolução e Genética Animal, Departamento de Genética, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Av. Rodrigo Octávio Jordão Ramos, 6200, Mini–Campus, Coroado I, 69077–000, Manaus, Amazonas, Brazil. Department of Biology, Trinity University, San Antonio, TX 78212, USA
Amphibia Amazonia cryptic species conservation leaf litter frog

Abstract

We describe two new species of Rhinella (Anura: Bufonidae) from the department of Loreto, Peru. We integrate morphological and phylogenetic analyses to provide evidence of new species. R. angeli sp. nov. is diagnosable from all congeners by its pronounced fleshy proboscis and R. unapensis sp. nov. by the small size (mean snout-vent length=37.7 ± 4.1 mm) of adult males, snout pointed in dorsal view, nearly acute in lateral view, and small bony protrusion at the angle of jaws among other characters. The two species are allopatric, where the first species is known to be associated inhabits upland (=terra firme) forests, while the second white sand forests (=varillales) around Iquitos city. The two new species represent the 20th and 21st species of the Rhinella margaritifera species group.

 

References

  1. Ávila, R.W., Honorio Morais, D., Perez, R., Pansonato, A., Carvalho, V., Rojas, R., Gordo, M. & Farias, I. (2020) A new species of the Rhinella margaritifera (Laurenti 1768) species group (Anura, Bufonidae) from southern Brazilian Amazonia. Zootaxa, 4868 (3), 368–388. https://doi.org/10.11646/zootaxa.4868.3.3
    Ávila, R.W., Pansonato, A., Perez, R., De Carvalho, V.T., Roberto, I.J., Morais, D.H., De 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
    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
    Baum, D.A. & Donoghue, M.J. (1995) Choosing among alternative “Phylogenetic” Species Concepts. Systematic Botany, 20, 560–573. https://doi.org/10.2307/2419810
    Bruschi, D.P., Sousa, D.Y., Soares, A., de Carvalho, K.A., Busin, C.S., Ficanha, N.C., Lima, A.P., Andrade, G.V. & Recco-Pimentel, S.M. (2019) Comparative cytogenetics of nine populations of the Rhinella genus (Anura, Bufonidae) with a highlight on their conservative karyotype. Genetics and Molecular Biology, 42, 445–451. https://doi.org/10.1590/1678-4685-gmb-2018-0139
    Caldwell, J.P. (1991) A new species of toad in the genus Bufo from Pará, Brazil, with an unusual breedind site. Papéis Avulsos de Zoologia, 37, 389–400.
    Caramaschi, U. & Niemeyer, H. de (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 do Rio de Janeiro, 501, 1–16.
    Caramaschi, U. & Pombal, J.P. (2006) A new species of Rhinella Fitzinger, 1826 from the Atlantic Rain Forest, Eastern Brazil (Amphibia, Anura, Bufonidae). Papeis Avulsos de Zoologia, 46, 251–259. https://doi.org/10.1590/S0031-10492006002300001
    Felsenstein, J. (1981) Evolutionary trees from DNA sequences: A maximum likelihood approach. Journal of Molecular Evolution, 17, 368–376. https://doi.org/10.1007/BF01734359
    Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791. https://doi.org/10.2307/2408678
    Ferrão, M., Lima, A.P., Ron, S., Santos, S.P. & Hanken, J. (2020) New species of leaf-litter toad of the Rhinella margaritifera species group (Anura: Bufonidae) from Amazonia. Copeia, 108, 967–986. https://doi.org/10.1643/CH2020043
    Fouquet, A., Gaucher, P., Blanc, M. & Velez-Rodriguez, C.M. (2007a) Description of two new species of Rhinella (Anura: Bufonidae) from the lowlands of the Guiana shield. Zootaxa, 1663, 17–32.
    Fouquet, A., Vences, M., Salducci, M.D., Meyer, A., Marty, C., Blanc, M. & Gilles, A. (2007b) Revealing cryptic diversity using molecular phylogenetics and phylogeography in frogs of the Scinax ruber and Rhinella margaritifera species groups. Molecular Phylogenetics and Evolution, 43, 567–582.
    Fouquet, A., Noonan, B.P., Rodrigues, M.T., Pech, N., Gilles, A. & Gemmell, N.J. (2012b) 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, J., Amaro, R.C., Camacho, A., Damasceno, R., Carnaval, A.C., Moritz, C. & Rodrigues, M.T. (2012a) Molecular phylogeny and morphometric analyses reveal deep divergence between Amazonia and Atlantic Forest species of Dendrophryniscus. Molecular Phylogenetics and Evolution, 62, 826–38. https://doi.org/10.1016/j.ympev.2011.11.023
    Frost D.R. (2022) Amphibian Species of the World: an Online Reference. American Museum of Natural History, New York, New York. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 12 January 2022) [archived by WebCite at http://www.webcitation.org/77AQIcR6V]
    Gordo, M. (2006) s.n. In: Vriesendorp, C., Pitman, N., Rojas, M., Pawlak, B.A., Rivera, C., Calixto, M., Vela, C.P. & Fasabi, R. (Eds.), Perú: Matsés. Rapid Biological Inventories. Report 16. The Field Museum, Chicago, Illinois, pp. 1–336.
    Günther, A.C.L.G. (1858) Neue Batrachier in der Sammlung des Britischen Museums. Archiv für Naturgeschichte, 24, 319–328. https://doi.org/10.5962/bhl.part.5288
    Hall, T. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
    Heyer, W.R., Rand, A.S., Cruz, C.A.G., Peixoto, O.L. & Nelson, C.E. (1991) Frogs of Boracéia. Arquivos de Biologia, 31, 231–410. https://doi.org/10.2307/1446606
    Jansen, M., Bloch, R., Schulze, A. & Pfenninger, M. (2011) Integrative inventory of Bolivia’s lowland anurans reveals hidden diversity. Zoologica Scripta, 40, 567–583. https://doi.org/10.1111/j.1463-6409.2011.00498.x
    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, Oxford, England, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
    Kok, P. & Kalamandeen, M. (2008) Introduction to the taxonomy of the amphibians of Kaieteur National Park, Guyana. Abc Taxa, 5, 1–288.
    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Molecular biology and evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054
    Laurenti, J.N. (1768) Specimen Medicum, Exhibens Synopsin Reptilium emendatum cum experimentis circa venena at antidota reptilium austriacorum. Joan Thomae, Viennae, 214 pp., 5 pls.
    Lavilla, E.O., Caramaschi, U., Langone, J.A., Pombal, 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, 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
    Lima, A.P., Menin, M. & De Araújo, M.C. (2007) A new species of Rhinella (Anura: Bufonidae) from Brazilian Amazon. Zootaxa, 1663, 1–15.
    Lötters, S. & Köhler, J. (2000) A new toad of the Bufo typhonius complex from humid montane forest of Bolivia. Spixiana, 23, 293–303.
    Lyra, M.L., Haddad, C.F.B. & de 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
    Melin, D. (1941) Contributions to the knowledge of the Amphibia of South America. Göteborgs Kungl. Vetenskaps-och Vitterhets- samhälles. Handlingar. Serien B. Matematiska och Naturvetenskapliga Skrifter (Ed), Göteborg, 71 pp.
    Mendelson, J.R., Mulcahy, D.G., Williams, T.S. & Sites, J.W. (2011) A phylogeny and evolutionary natural history of mesoamerican toads (Anura: Bufonidae: Incilius) based on morphology, life history, and molecular data. Zootaxa, 3138 (1), 1–34. https://doi.org/10.11646/zootaxa.3138.1.1
    Mijares-Urrutia, A. & Arends, A. (2001) A new toad of the Bufo margaritifer complex (Amphibia: Bufonidae) from northwestern Venezuela. Herpetologica, 57, 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, 137–153.
    Moravec, J., Lehr, E., Cusi, J.C., Córdova, J.H. & Gvoždík, 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
    Motta, J., Menin, M., Almeida, A.P., Hrbek, T. & Pires Farias, I. (2018) When the unknown lives next door: A study of central Amazonian anurofauna. Zootaxa, 4438 (1), 79–104. https://doi.org/10.11646/zootaxa.4438.1.3
    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.
    Padial, J.M. & Riva, I.D.E.L.A. (2009) Integrative taxonomy reveals cryptic Amazonian species of Pristimantis (Anura : Strabomantidae). Zoological Journal of the Linnean Society, 155, 97–122.
    Posada, D. (2008) jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256. https://doi.org/10.1093/molbev/msn083
    Peréz, P., Bodmer, R. & Puertas, P. (2006) In: Fang, T., Bodmer, R., Aquino, R. & Valqui, M. (Ed.), Manejo de Fauna Silvestre en la Amazonia. Quito, Ecuador. Anuros y Saurios del Interfluvio Yavarí- Tahuayo y su comparación con las áreas naturales protegidas en la región Loreto, Perú, pp. 1–15.
    Pereyra, M., Blotto, B., Baldo, D., Chaparro, J., Ron, S., Elias-Costa, A., Iglesias, P., Venegas, P., Thomeí, M., Ospina-Sarria, J., Maciel, N., Rada, M., Kolenc, F., Borteiro, C., Rivera-Correa, M., Rojas Runjaic, F.,Moravec, J., Riva, I. de la; 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. Available from: http://digitallibrary.amnh.org/handle/2246/7260 (accessed 9 May 2022)
    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
    Riveira-Gonzales, C., Von May, R., Aguilar, C., Arista, I., Curo, A., Schulte, R. Una evaluación preliminar de la Herpetofauna en la Zona Reservada Allpahuayo Mishana, Loreto, Perú (2003). Folia Amazónica, 1, 138–147.
    Ribeyro, S. & Layche, J. (2008) Herpetofauna en el bosque de varillal del centro de enseñanza forestal (CIEFOR)-Puerto Almendra, Iquitos-Perú. Bachelor dissertation. Universidad Nacional de la Amazonia Peruana-UNAP, Iquitos. [unknown pagination]
    Rivera, D., Prates, I., Firneno Jr., T.J., Rodrigues, M.T., Caldwell, J.P. & Fujita, M.K. (2021) Phylogenomics, introgression, and demographic history of South American true toads (Rhinella). Molecular Ecology. [in press] https://doi.org/10.1111/mec.16280
    Roberto, I., 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, 87–97. https://doi.org/10.2994/057.006.0207
    Rodriguez, L.O. & Knell, G. (2003) In: Pitman, N., Vriesendorp, C. & Moskovits, D. (Eds.), 2006. Perú: Yavarí. Rapid Biological Inventories. Report 11. The Field Museum, Chicago, Illinois, pp. 1–336.
    Sambrook, J. & Russell, D.W. (2006) Purification of nucleic acids by extraction with phenol:chloroform. Cold Spring Harbor Protocols. [published online] https://doi.org/10.1101/pdb.prot4455
    Santos, S.P., Ibáñez, 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, 109–145. https://doi.org/10.3897/zookeys.501.8604
    Savage, J. & Heyer, W. (1967) Variation and distribution in the tree-frog genus Phyllomedusa in Costa Rica, Central America. Studies on Neotropical Fauna and Environment, 5, 111–131. https://doi.org/10.1080/01650526709360400
    Sequeira, F., Sodré, D., Ferrand, N., Bernardi, J.A.R., Sampaio, I., Schneider, H. & Vallinoto, M. (2011) Hybridization and massive mtDNA unidirectional introgression between the closely related Neotropical toads Rhinella marina and R . schneideri inferred from mtDNA and nuclear markers. BMC Evolutionary Biology, 11, 264.
    Spix, J.B. von (1824) s.n. In: Hübschmann, F.S. (Ed.), Animalia nova sive species novae testudinum et ranarum : quas in itinere per Brasiliam annis 1817–1820 jussu et auspiciis Maximiliani Josephi I. Bavariae regis. F. S. Hübschmann, München, pp. 1–53, XXII tabs.
    Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30 (9), 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
    Thominot, A. (1884) Note sur un batracien d’espèce nouvelle provenant de Panama. Bulletin de la Société Philomathique de Paris, 7 (8), 151–152.
    Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2002) Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics, Chapter 2, Unit 2, 3, 2.3.1–2.3.22 https://doi.org/10.1002/0471250953.bi0203s00
    Vacher, J.P., Chave, J., Ficetola, F.G., 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, C., Noonan, B.P., Nunes, P.M.S., 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
    Vaz-Silva, W., Maciel, N.M., Bastos, R.P. & Pombal, J.P. (2015) Revealing two new species of the Rhinella margaritifera species group (Anura, Bufonidae): an enigmatic taxonomic group of Neotropical toads. Herpetologica, 71, 212–222. https://doi.org/10.1655/Herpetologica-D-14-00039
    Vences, M., Thomas, M., van der Meijden, A., Chiari, Y. & Vieites, D.R. (2005) Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Frontiers in Zoology, 2, 5. https://doi.org/10.1186/1742-9994-2-5

  2.