Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-06-06
Page range: 533-561
Abstract views: 645
PDF downloaded: 29

Two new species of Allobates of the trilineatus clade (Anura: Aromobatidae) from the Eastern Guiana Shield

Laboratoire Evolution et Diversité Biologique; UMR 5174; CNRS; IRD; Université Paul Sabatier; Bâtiment 4R1 31062 cedex 9; 118 Route de Narbonne; 31077 Toulouse; France
Museum of Comparative Zoology; Harvard University; Cambridge; MA; 02138; USA
National Zoological Collection Suriname (NZCS); Anton de Kom University of Suriname; Paramaribo; Suriname
Amphibia Acoustics Amazonia AmphibiaMorphology Neotropics Taxonomy

Abstract

The actual diversity of anurans occurring in Amazonia remains only partly described. This is notably the case of the species of the genus Allobates despite a fast rate of species description in this genus during the last decade. This increasing taxonomic effort has been particularly facilitated by the availability of DNA sequences throughout the region. These data suggest for instance the existence of three lineages in the Guiana Shield that may correspond to unnamed species. We examined morphology and calls of these putative species and compared them to related nominal species, which confirmed that two of these lineages not only differ genetically but also morphologically and bioacoustically. These two species are thus named and described herein. Allobates vicinus sp. nov. from northern Suriname forms a clade with another candidate species from southern Suriname and Northern Pará, (Brazil) and with A. granti that occurs in French Guiana. Allobates ripicolus sp. nov. occurs throughout the eastern Guiana Shield and is nested within the A. tapajos complex which otherwise occurs in southeastern Amazonia and comprises A. tapajos and A. kamilae, along with three additional candidate species.

 

References

  1. Amézquita, A., Lima, A.P., Jehle, R., Castellanos, L., Ramos, O, Crawford, A.J., Gasser, H. & Hödl, W. (2009) Calls, colours, shape, and genes: a multi-trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis. Biological Journal of the Linnean Society, 98, 826–838. https://doi.org/10.1111/j.1095-8312.2009.01324.x DOI: https://doi.org/10.1111/j.1095-8312.2009.01324.x
  2. Antonelli, A., Quijada-Mascareñas, A., Crawford, A.J., Bates, J.M., Velazco, P.M. & Wüster, W. (2010) Molecular studies and phylogeography of Amazonian tetrapods and their relation to geological and climatic models. In: Hoorn, C. & Wesselingh, F. (Eds.), Amazonia, landscape and species evolution 1st ed. Wiley-Blackwell, Chichester, West Sussex, UK, pp. 386–404. https://doi.org/10.1002/9781444306408.ch24 DOI: https://doi.org/10.1002/9781444306408.ch24
  3. Ávila-Pires, T.C.S.D., Hoogmoed, M.S. & Rocha, W.A.D. (2010) Notes on the Vertebrates of northern Pará, Brazil: a forgotten part of the Guianan Region, I. Herpetofauna. Boletim do Museu Paraense Emílio Goeldi. Ciências Naturais, 5, 13–112. https://doi.org/10.46357/bcnaturais.v5i1.647 DOI: https://doi.org/10.46357/bcnaturais.v5i1.647
  4. Boulenger, G.A. (1884) "1883". On a collection of frogs from Yurimaguas, Huallaga River, Northern Peru. Proceedings of the Zoological Society of London, 1883, 635–638. https://doi.org/10.1111/j.1469-7998.1883.tb06669.x DOI: https://doi.org/10.1111/j.1469-7998.1883.tb06669.x
  5. Caldwell, J.P., Lima, A.P. & Keller, C. (2002) Redescription of Colostethus marchesianus from its type locality. Copeia, 2002, 157–165. https://doi.org/10.1643/0045-8511(2002)002[0157:ROCMMF]2.0.CO;2 DOI: https://doi.org/10.1643/0045-8511(2002)002[0157:ROCMMF]2.0.CO;2
  6. Carnaval, A.C. & Bates, J.M. (2007) Amphibian DNA shows marked genetic structure and tracks Pleistocene climate change in Northeastern Brazil. Evolution, 61, 2942–2957. https://doi.org/10.1111/j.1558-5646.2007.00241.x DOI: https://doi.org/10.1111/j.1558-5646.2007.00241.x
  7. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791. https://doi.org/10.2307/2408678 DOI: https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
  8. Ferrão, M., Hanken, J. & Lima, A.P. (2022) A new nurse frog of the Allobates tapajos species complex (Anura: Aromobatidae) from the upper Madeira River, Brazilian Amazonia. PeerJ, 10 (e13751), 1–36. https://doi.org/10.7717/peerj.13751 DOI: https://doi.org/10.7717/peerj.13751
  9. Fouquet, A., Courtois, E.A., Baudain, D., Lima, J.D., Souza, S.M., Noonan, B.P. & Rodrigues, M.T. (2015b) The trans-riverine genetic structure of 28 Amazonian frog species is dependent on life history. Journal of Tropical Ecology, 31, 361–373. https://doi.org/10.1017/S0266467415000206 DOI: https://doi.org/10.1017/S0266467415000206
  10. 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), e1109. https://doi.org/10.1371/journal.pone.0001109 DOI: https://doi.org/10.1371/journal.pone.0001109
  11. Fouquet, A., Noonan, B.P., Rodrigues, M.T., Pech, N., Gilles, A. & Gemmell, N.J. (2012) 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 DOI: https://doi.org/10.1093/sysbio/syr130
  12. Fouquet, A., Peloso, P., Jairam, R., Lima, A.P., Mônico, A.T., Ernst, R. & Kok, P.J.R. (2022) Back from the deaf: Integrative taxonomy confirms a new species of Pristimantis Jiménez de la Espada, 1870 (Anura, Strabomantidae) endemic to the eastern Guiana Shield and revalidates Hylodes grandoculis van Lidth de Jeude, 1904. Organisms Diversity & Evolution, 22, 1065–1098. https://doi.org/10.1007/s13127-022-00564-w DOI: https://doi.org/10.1007/s13127-022-00564-w
  13. Fouquet, A., Vacher J.P., Kadosoe, V., Jairam, R. & Ouboter, P. (2015a) Checklist of the Amphibians of the Sipaliwini area, Suriname. Herpetology Notes, 8, 63–68.
  14. Fouquet, A., Vidal, N. & Dewynter, M. (2019) The Amphibians of the Mitaraka massif, French Guiana. Zoosystema, 41, 359–374. https://doi.org/10.5252/zoosystema2019v41a19 DOI: https://doi.org/10.5252/zoosystema2019v41a19
  15. Frost, D.R. (2023) Amphibian Species of the World: an Online Reference. Version 6.1, American Museum of Natural History, New York, USA. Available from: https://amphibiansoftheworld.amnh.org/index.php/ (accessed 01 January 2023)
  16. Gagliardi-Urrutia, L.A.G., Castroviejo-Fisher, S., Rojas-Runjaic, F.J.M., Jaramillo-Martinez, A.F., Solís, S. & Simões, P.I. (2021) A new species of nurse-frog (Aromobatidae, Allobates) from the Amazonian forest of Loreto, Peru. Zootaxa, 5026 (3), 375–404. https://doi.org/10.11646/zootaxa.5026.3.3 DOI: https://doi.org/10.11646/zootaxa.5026.3.3
  17. Grant, T., Frost, D.R., Caldwell, J.P., Gagliardo, R., Haddad, C.F.B., Kok, P.J.R., Means, D. B., Noonan, B.P., Schargel, W.E. & Wheeler, W.C. (2006) Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of the American Museum of Natural History, 299, 1–262 DOI: https://doi.org/10.1206/0003-0090(2006)299[1:PSODFA]2.0.CO;2
  18. Grant, T., Rada, M., Anganoy-Criollo, M., Batista, A., Dias, P.H., Jeckel, A.M., Machado, D.J. & Rueda-Almonacid, J.V. (2017) Phylogenetic systematics of dart-poison frogs and their relatives revisited (Anura: Dendrobatoidea). South American Journal of Herpetology, 12, 1–262. https://doi.org/10.2994/SAJH-D-17-00017.1 DOI: https://doi.org/10.2994/SAJH-D-17-00017.1
  19. Grant, T. & Rodríguez, L.O. (2001) Two new species of frogs of the genus Colostethus (Dendrobatidae) from Peru and a redescription of C. trilineatus (Boulenger, 1883). American Museum Novitates, 2001, 1–24. https://doi.org/10.1206/0003-0082(2001)355%3C0001:TNSOFO%3E2.0.CO;2 DOI: https://doi.org/10.1206/0003-0082(2001)355<0001:TNSOFO>2.0.CO;2
  20. Guerra, V., Jardim, L., Llusia, D., Marquez, R. & Bastos, R.P. (2020) Knowledge status and trends in description of amphibian species in Brazil. Ecological Indicators, 118, p.106754. https://doi.org/10.1016/j.ecolind.2020.106754 DOI: https://doi.org/10.1016/j.ecolind.2020.106754
  21. IUCN (2022) The IUCN Red List of Threatened Species. Version 2022-1. Available from: https://www.iucnredlist.org (accessed 01 August 2022)
  22. Katoh, K., Rozewicki, J. & Yamada, K.D. (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20, 1160–1166. https://doi.org/10.1093/bib/bbx108 DOI: https://doi.org/10.1093/bib/bbx108
  23. Koehler, J., Jansen, M., Rodriguez, A., Kok, P.J.R., Toledo, L. F., Emmrich, M., Glaw, F., Haddad, C.F.B., Rödel, M.-O. & 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
  24. Kok, P.J.R. & Ernst, R. (2007) A new species of Allobates (Anura: Aromobatidae: Allobatinae) exhibiting a novel reproductive behavior. Zootaxa, 1555 (1), 21–38. https://doi.org/10.11646/zootaxa.1555.1.2 DOI: https://doi.org/10.11646/zootaxa.1555.1.2
  25. Kok, P.J.R., Hölting, M. & Ernst, R. (2013) A third microendemic to the Iwokrama Mountains of central Guyana: a new “cryptic” species of Allobates Zimmerman and Zimmerman, 1988 (Anura: Aromobatidae). Organisms, Diversity & Evolution, 13, 621–638. https://doi.org/10.1007/s13127-013-0144-4 DOI: https://doi.org/10.1007/s13127-013-0144-4
  26. Kok, P.J.R., MacCulloch, R.D., Gaucher, P., Poelman, E.H., Bourne, G.R., Lathrop, A. & Lenglet, G.L. (2006) A new species of Colostethus (Anura, Dendrobatidae) from French Guiana with a redescription of Colostethus beebei (Noble, 1923) from its type locality. Phyllomedusa, 5, 43–66. https://doi.org/10.11606/issn.2316-9079.v5i1p43-66 DOI: https://doi.org/10.11606/issn.2316-9079.v5i1p43-66
  27. Lê, S., Josse, J. & Husson, F. (2008) FactoMineR: an R package for multivariate analysis. Journal of Statistical Software, 25, 1–18. https://doi.org/10.18637/jss.v025.i01 DOI: https://doi.org/10.18637/jss.v025.i01
  28. Lescure, J. & Marty, C. (2000) Atlas des amphibiens de Guyane. Collection patrimoines naturels (45), Muséum national d'Histoire naturelle, Paris, 392 pp.
  29. Lima, A.P., Simoes, P.I. & Kaefer, I.L. (2015) A new species of Allobates (Anura: Aromobatidae) from Parque Nacional da Amazonia, Pará State, Brazil. Zootaxa, 3980 (4), 501–525. https://doi.org/10.11646/zootaxa.3980.4.3 DOI: https://doi.org/10.11646/zootaxa.3980.4.3
  30. Lima, A.P., Ferrão, M. & da Silva, D.H. (2020) Not as widespread as thought: Integrative taxonomy reveals cryptic diversity in the Amazonian nurse frog Allobates tinae Melo-Sampaio, Oliveira and Prates, 2018 and description of a new species. Journal of Zoological Systematics and Evolutionary Research, 58, 1173–1194. https://doi.org/10.1111/jzs.12406 DOI: https://doi.org/10.1111/jzs.12406
  31. Lundberg, J.G., Marshall, L.G., Guerrero, J., Horton, B., Malabarba, M.C.S.L. & Wesselingh, F. (1998) The stage for neotropical fish diversification: a history of South American rivers. In: Malabarba M.C.S.L., Reis, R.E., Vari R.P., Lucena Z.M., Lucena C.A.S., (Eds.), Phylogeny and classification of neotropical fishes. Edipucrs, Porto Alegre, Brazil, pp. 13–48.
  32. Malhi, Y., Roberts, J.T., Betts, R.A., Killeen, T.J., Li, W. & Nobre, C.A. (2008) Climate change, deforestation, and the fate of the Amazon. Science, 319, 169–172. https://doi.org/10.1126/science.1146961 DOI: https://doi.org/10.1126/science.1146961
  33. Mayle, F.E. & Power, M.J. (2008) Impact of a drier Early–Mid-Holocene climate upon Amazonian forests. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 1829–1838. https://doi.org/10.1098/rstb.2007.0019 DOI: https://doi.org/10.1098/rstb.2007.0019
  34. Melo-Sampaio, P.R., Prates, I., Peloso, P.L.V., Recoder, R.S., Vechio, F.D., Marques-Souza, S. & Rodrigues, M.T. (2020) A new nurse frog from southwestern Amazonian highlands, with notes on the phylogenetic affinities of Allobates alessandroi (Aromobatidae). Journal of Natural History, 54, 43–62. https://doi.org/10.1080/00222933.2020.1727972 DOI: https://doi.org/10.1080/00222933.2020.1727972
  35. Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 gateway computing environments workshop (GCE), Ieee, pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129 DOI: https://doi.org/10.1109/GCE.2010.5676129
  36. Moraes, L.J.C.L. & Lima, A.P. (2021) A new Nurse Frog (Allobates, Aromobatidae) with a cricket-like advertisement call from eastern Amazonia. Herpetologica, 77, 146–163. https://doi.org/10.1655/Herpetologica-D-20-00010.1 DOI: https://doi.org/10.1655/Herpetologica-D-20-00010.1
  37. Moraes, L.J.C.L., Werneck, F.P., Réjaud, A., Rodrigues, M.T., Prates, I., Glaw, F., Kok, P.J.R., Ron, S.R., Chaparro, J.C., Osorno-Muñoz, M., Dal Vechio, F., Recoder, R.S., Marques-Souza, S., Rojas, R.R., Demay, L., Hrbek, T. & Fouquet, A. (2022) Diversification of tiny toads (Bufonidae: Amazophrynella) sheds light on ancient landscape dynamism in Amazonia. Biological Journal of the Linnean Society, 136, 75–91. https://doi.org/10.1093/biolinnean/blac006 DOI: https://doi.org/10.1093/biolinnean/blac006
  38. Morales, V.R. (2002) Sistematica y biogeografía del grupo trilineatus (Amphibia, Anura, Dendrobatidae, Colostethus), con descripción de once nuevas especies. Publicaciones de la Asociación de Amigos de Doñana, 13, 1–59.
  39. Noble, G.K. (1923) New batrachians from the Tropical Research Station British Guiana. Zoologica, 3, 289–299. https://doi.org/10.5962/p.184633 DOI: https://doi.org/10.5962/p.184633
  40. Padial, J.M., Miralles, A., De la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, 1–14. https://doi.org/10.1186/1742-9994-7-16 DOI: https://doi.org/10.1186/1742-9994-7-16
  41. Réjaud, A., Rodrigues, M.T., Crawford, A.J., Castroviejo-Fisher, S., Jaramillo, A.F., Chaparro, J.C., Glaw, F., Gagliardi-Urrutia, G., Moravec, J., Ignacio, J., Perez, P., Lima, A.P., Werneck, F.P., Hrbek, T., Ron, S.R., Ernst, R., Kok, P.J.R., Driskell, A., Chave, J. & Fouquet A. (2020) Historical biogeography identifies a possible role of Miocene wetlands in the diversification of the Amazonian rocket frogs (Aromobatidae: Allobates). Journal of Biogeography, 47, 2472–2482. https://doi.org/10.1111/jbi.13937 DOI: https://doi.org/10.1111/jbi.13937
  42. Rivera-Correa, M., Baldo, D., Candioti, F.V., Orrico, V.G.D., Blackburn, D.C., Castroviejo-Fisher, S., Chan, K.O., Gambale, P., Gower, D.J., Quah, E.S. & Rowley, J.J. (2021) Amphibians in Zootaxa: 20 years documenting the global diversity of frogs, salamanders, and caecilians. Zootaxa, 4979 (1), 57–69. https://doi.org/10.11646/zootaxa.4979.1.9 DOI: https://doi.org/10.11646/zootaxa.4979.1.9
  43. Silva, L.A., Marques, R., Folly, H. & Santana, D.J. (2022) A new Amazonian species of Allobates Zimmermann & Zimmermann, 1988 (Aromobatidae) with a trilled advertisement call. PeerJ, 10, p.e13026. https://doi.org/10.7717/peerj.13026 DOI: https://doi.org/10.7717/peerj.13026
  44. Simões, P.I., Kaefer, Í.L., Farias, I.P. & Lima, A.P. (2013) An integrative appraisal of the diagnosis and distribution of Allobates sumtuosus (Morales, 2002) (Anura, Aromobatidae). Zootaxa, 3746 (3), 401–421. https://doi.org/10.11646/zootaxa.3746.3.1 DOI: https://doi.org/10.11646/zootaxa.3746.3.1
  45. Souza, J.R.D., Ferrão, M., Hanken, J. & Lima, A.P. (2020) A new nurse frog (Anura: Allobates) from Brazilian Amazonia with a remarkably fast multi-noted advertisement call. PeerJ, 8, e9979. https://doi.org/10.7717/peerj.9979 DOI: https://doi.org/10.7717/peerj.9979
  46. Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033 DOI: https://doi.org/10.1093/bioinformatics/btu033
  47. Strauss, R.E. (1985) Evolutionary allometry and variation in body form in the South American catfish genus Corydoras (Callichthyidae). Systematic Biology, 34, 381–396. https://doi.org/10.1093/sysbio/34.4.381 DOI: https://doi.org/10.1093/sysbio/34.4.381
  48. 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 DOI: https://doi.org/10.1111/jbi.13847
  49. Vences, M., Kosuch, J., Boistel, R., Haddad, C.F., La Marca, E., Lötters, S. & Veith, M. (2003) Convergent evolution of aposematic coloration in Neotropical poison frogs: a molecular phylogenetic perspective. Organisms, Diversity & Evolution, 3, 215–226. https://doi.org/10.1078/1439-6092-00076 DOI: https://doi.org/10.1078/1439-6092-00076
  50. Zimmermann, H. & Zimmermann, E. (1988) Etho-Taxonomie und zoogeographische Artengruppenbildung bei Pfeilgiftfroschen (Anura: Dendrobatidae). Salamandra, 24, 125–160.