Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5514 No. 1: 25 Sept. 2024
Type: Article
Published: 2024-09-25
DOI: 10.11646/zootaxa.5514.1.5
Page range: 73-90
Abstract views: 577
PDF downloaded: 30

A new species of Neblinaphryne (Anura: Brachycephaloidea: Neblinaphrynidae) from Serra do Imeri, Amazonas state, Brazil

Centre de Recherche sur la Biodiversité et l’Environnement (CRBE); UMR 5300 CNRS-IRD-TINP-UT3; Université Toulouse III – Paul Sabatier; Bât. 4R1; 118 route de Narbonne; 31062 Toulouse cedex 9; France
Universidade de São Paulo; Instituto de Biociências; Departamento de Zoologia; São Paulo; SP; Brazil
Universidade de São Paulo; Instituto de Biociências; Departamento de Zoologia; São Paulo; SP; Brazil
Universidade de São Paulo; Instituto de Biociências; Departamento de Zoologia; São Paulo; SP; Brazil
Universidad Autónoma de Madrid. Facultad de Ciencias (Edificio Biología). C. Darwin; 2; Fuencarral-El Pardo; 28049; Madrid
Universidade de São Paulo; Instituto de Biociências; Departamento de Zoologia; São Paulo; SP; Brazil
Universidade de São Paulo; Instituto de Biociências; Departamento de Zoologia; São Paulo; SP; Brazil
Universidade de São Paulo; Instituto de Biociências; Departamento de Zoologia; São Paulo; SP; Brazil
Amphibia Amazonia Amphibian Biodiversity Frog Guiana Shield Pantepui Taxonomy Systematics

Abstract

The highlands of the Guiana Shield (Pantepui) in northern South America harbor a unique fauna and flora. However, this diversity remains poorly documented, as many Pantepui massifs remain little explored or unexplored, mainly because their access is very challenging. Considering amphibians, 11 genera are endemic or sub-endemic to Pantepui, and one of them, Neblinaphryne, is monospecific and was recently described from the Neblina massif, at the border between Brazil and Venezuela. We recently undertook an expedition in the nearby, previously uninventoried Imeri massif and discovered a new species of this genus. We describe this new species herein as Neblinaphryne imeri sp. nov., combining molecular, external morphological, acoustic, osteological and myological data. The new species shares with the other Neblinaphryne species (N. mayeri) minuscule septomaxillae and pointed terminal phalanges, confirming the morphological diagnostic characters of the genus. Nevertheless, the new species can promptly be distinguished from N. mayeri by having the head wider than long, a distinct color pattern, and prominent tubercles on the eyelid and humeral region, as well as osteological and genetic differences. These two species are likely endemic to their respective massifs, providing a striking new example of speciation by isolation within Pantepui, which was possibly mediated by climate and elevation, as previously hypothesized for many other lineages endemic to this region.

 

References

  1. Abdala, V., Vera, M.C., Amador, L.I., Fontanarrosa, G., Fratani, J. & Ponssa, M.L. (2019) Sesamoids in tetrapods: the origin of new skeletal morphologies. Biological Reviews, 94, 2011–2032. https://doi.org/10.1111/brv.12546
  2. Berry, P.E. & Riina, R. (2005) Insights into the diversity of the Pantepui flora and the biogeographic complexity of the Guayana Shield. Biologiske Skrifter, 55, 145–167.
  3. Cervino, N.G., Elias-Costa, A.J., Pereyra, M.O. & Faivovich, J. (2021) A closer look at pupil diversity and evolution in frogs and toads. Proceedings of the Royal Society B, 288 (1957), 20211402. https://doi.org/10.1098/rspb.2021.1402
  4. Duellman, W.E. & Lehr, E. (2009) Terrestrial-breeding frogs (Strabomantidae) in Peru. Natur und Tier Verlag GmbH, Münster, 384 pp.
  5. Dunlap, D.G. (1960) The comparative myology of the pelvic appendage in the Salientia. Journal of Morphology, 106, 1–76. https://doi.org/10.1002/jmor.1051060102
  6. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39 (4), 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
  7. 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
  8. Fouquet, A., Kok, P.J.R., Recoder, R.S., Prates, I., Camacho, A., Marques-Souza, S., Ghellere, J.M., McDiarmid, R.W. & Rodrigues, M.T. (2024) Relicts in the mist: Two new frog families, genera and species highlight the role of Pantepui as a biodiversity museum throughout the Cenozoic. Molecular Phylogenetic & Evolution, 191, 107971. https://doi.org/10.1016/j.ympev.2023.107971
  9. Heinicke, M.P., Duellman, W.E., Trueb, L., Means, D.B., MacCulloch, R.D. & Hedges, S.B. (2009) A new frog family (Anura: Terrarana) from South America and an expanded direct-developing clade revealed by molecular phylogeny. Zootaxa, 2211 (1), 1–35. https://doi.org/10.11646/zootaxa.2211.1.1
  10. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
  11. Katoh, K. & Standley, D.M. (2013) MAFFT Multiple sequence alignment software Version 7: Improvements in performance and usability. Molecular Biology & Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
  12. Köhler, J., Jansen, M., Rodriguez, A., Kok, P.J., 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
  13. Kok, P.J.R. (2005) A new genus and species of gymnophthalmid lizard (Squamata: Gymnophthalmidae) from Kaieteur National Park, Guyana. Bulletin de l’Institut Royal des Sciences Naturelles de Belgique Biologie, 75, 35–45.
  14. Kok, P.J.R. (2009) Lizard in the clouds: a new highland genus and species of Gymnophthalmidae (Reptilia: Squamata) from Maringma tepui, western Guyana. Zootaxa, 1992, 53–67. https://doi.org/10.11646/zootaxa.1992.1.4
  15. Kok, P.J.R. (2013) Islands in the Sky: Species Diversity, Evolutionary History, and Patterns of Endemism of the Pantepui Herpetofauna. PhD thesis, Leiden University, Leiden. [unknown pagination]
  16. Kok, P.J.R. (2015) A new species of the Pantepui endemic genus Riolama (Squamata: Gymnophthalmidae) from the summit of Murisipán-tepui, with the erection of a new gymnophthalmid subfamily. Zoological Journal of the Linnean Society, 174 (3), 500–518. https://doi.org/10.1111/zoj.12241
  17. Kok, P.J.R., MacCulloch, R.D., Means, D.B., Roelants, K., Van Bocxlaer, I. & Bossuyt, F. (2012) Low genetic diversity in tepui summit vertebrates. Current Biology, 22 (15), R589–90. https://doi.org/10.1016/j.cub.2012.06.034
  18. Kok, P.J.R., Ratz, S., MacCulloch, R.D., Lathrop, A., Dezfoulian, R., Aubret, F. & Means, D.B. (2018) Historical biogeography of the palaeoendemic toad genus Oreophrynella (Amphibia: Bufonidae) sheds a new light on the origin of the Pantepui endemic terrestrial biota. Journal of Biogeography, 45 (1), 26–36. https://doi.org/10.1111/jbi.13093
  19. Kok, P.J.R., Russo, V.G., Ratz, S., Means, D.B., MacCulloch, R.D., Lathrop, A., Aubret, F. & Bossuyt, F. (2017) Evolution in the South American ‘Lost World’: insights from multilocus phylogeography of stefanias (Anura, Hemiphractidae, Stefania). Journal of Biogeography, 44, 170–181. https://doi.org/10.1111/jbi.12860
  20. Kok, P.J.R., van Doorn, L. & Dezfoulian, R. (2019) Predation by non-bioluminescent firefly larvae on a tepui-summit endemic toad. Current Biology, 29 (22), R1170–R1171. https://doi.org/10.1016/j.cub.2019.10.001
  21. Kok, P.J.R. & Means, D.B. (2023) Hiding in the mists: Molecular phylogenetic position and description of a new genus and species of snake (Dipsadidae: Xenodontinae) from the remote cloud forest of the Lost World. Zoological Journal of the Linnean Society, zlad082. [published online] https://doi.org/10.1093/zoolinnean/zlad082
  22. Leite, Y.L., Kok, P.J.R. & Weksler, M. (2015) Evolutionary affinities of the ‘Lost World’mouse suggest a late Pliocene connection between the Guiana and Brazilian shields. Journal of Biogeography, 42 (4), 706–715. https://doi.org/10.1111/jbi.12461
  23. Lynch, J.D. (1979) A new genus for Elosia duidensis Rivero (Amphibia, Leptodactylidae) from southern Venezuela. American Museum Novitates, 2680, 1–8
  24. Lynch, J.D. & Duellman, W.E. (1997) Frogs of the genus Eleutherodactylus in western Ecuador. University of Kansas Special Publication, 23, 1–236. https://doi.org/10.5962/bhl.title.7951
  25. Mayr, E. & Phelps, W.H. (1967) The origin of the bird fauna of the south Venezuelan highlands. Bulletin of the American Museum of Natural History, 136, 273–327.
  26. Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., von Haeseler, A. & Lanfear, R. (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology & Evolution, 37, 1530–1534. https://doi.org/10.1093/molbev/msaa015
  27. Myers, C.W. (1987) New generic names from some neotropical poison frogs (Dendrobatidae). Papéis Avulsos de Zoologia, 36, 301–306. https://doi.org/10.11606/0031-1049.1983.36.p301-306
  28. Myers, C.W. & Donnelly, M.A. (2001) Herpetofauna of the Yutajé-Corocoro Massif, Venezuela: second report from the Robert G. Goelet American Museum - Terramar Expedition to the Northwestern Tepuis. Bulletin of the American Museum of Natural History, 261, 1–85. https://doi.org/10.1206/0003-0090(2001)261<0001:HOTYCM>2.0.CO;2
  29. Ortiz, D.A., Hoskin, C.J., Werneck, F.P., Réjaud, A., Manzi, S., Ron, S.R. & Fouquet, A. (2022) Historical biogeography of a diverse tree frog clade highlights a key role of Miocene landscape changes on Amazonian diversification. Organisms Diversity and Evolution, 23 (2), 395–414. https://doi.org/10.1007/s13127-022-00588-2
  30. Ospina-Sarria, J.J. & Grant, T. (2022) New phenotypic synapomorphies delimit three molecular-based clades of New World direct-developing frogs (Amphibia: Anura: Brachycephaloidea). Zoological Journal of the Linnean Society, 195 (3), 976–994. https://doi.org/10.1093/zoolinnean/zlab071
  31. Pellegrino, K.C.M., Brunes, T.O., Souza, S.M., Laguna, M.M., Avila-Pires, T.C.S., Hoogmoed, M.S. & Rodrigues, M.T. (2018) On the distinctiveness of Amapasaurus, its relationship with Loxopholis Cope 1869, and description of a new genus for L. guianensis and L. hoogmoedi (Gymnophthalmoidea/Ecpleopodini: Squamata). Zootaxa, 4441 (2), 332–346. https://doi.org/10.11646/zootaxa.4441.2.8
  32. Pinheiro, P.D., Kok, P.J.R., Noonan, B.P., Means, D.B., Haddad, C.F. & Faivovich, J. (2019) A new genus of Cophomantini, with comments on the taxonomic status of Boana liliae (Anura: Hylidae). Zoological Journal of the Linnean Society, 185 (1), 226–245. https://doi.org/10.1093/zoolinnean/zly030
  33. Recoder, R., Prates, I., Marques-Souza, S., Camacho, A., Nunes, P.M.S., Dal Vechio, F., Ghellere, J.M., McDiarmid, R.W. & Rodrigues, M.T. (2020) Lizards from the Lost World: two new species and evolutionary relationships of the Pantepui highland Riolama (Gymnophthalmidae). Zoological Journal of the Linnean Society, 190 (1), 271–297. https://doi.org/10.1093/zoolinnean/zlz168
  34. Rueden, C.T., Schindelin, J., Hiner, M.C., DeZonia, B.E., Walter, A.E., Arena, E.T. & Eliceiri, K.W. (2017) ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics, 18. https://doi.org/10.1186/s12859-017-1934-z
  35. Rull, V., Montoya, E., Nogué, S., Safont, E. & Vegas-Vilarrúbia, T. (2019) Climatic and ecological history of Pantepui and surrounding areas. In: Rull, V., Montoya, E., Nogué, S., Safont, E. & Vegas-Vilarrúbia, T. (Eds.), Biodiversity of Pantepui. The Pristine “Lost World” of the Neotropical Guiana Highlands. Academic press, Cambridge, pp. 33–54. https://doi.org/10.1016/B978-0-12-815591-2.00002-1
  36. Rull, V. & Vegas-Vilarrúbia, T. (2020) The Pantepui “Lost World”: towards a biogeographical, ecological and evolutionary synthesis of a pristine Neotropical sky-island archipelago. In: Rull, V. & Carnaval, A.C.Q (Eds.), Neotropical Diversification: Patterns and Processes. Springer, Cham, pp. 369–413. https://doi.org/10.1007/978-3-030-31167-4_15
  37. Santos, J.C., Coloma, L.A., Summers, K., Caldwell, J.P., Ree, R. & Cannatella, D.C. (2009) Amazonian amphibian diversity is primarily derived from later Miocene Andean lineages. PLoS Biology, 7, 448–461. https://doi.org/10.1371/journal.pbio.1000056
  38. Señaris, J.C., Ayarzagüena, J. & Gorzula, S.J. (1994) Los sapos de la familia Bufonidae (Amphibia: Anura) de las tierras altas de la Guayan Venezolana: Descripción de un nuevo genero y tres especies. Publicaciones de la Asociación de Amigos de Doñana, 3, 1–37.
  39. Steyermark, J.A. (1986) Holstianthus, a new genus of Rubiaceae from the Guayana highland. Annals of the Missouri Botanical Garden, 73 (2), 495–497. https://doi.org/10.2307/2399130
  40. Vacher, J.-P., Kok, P.J.R., Rodrigues, M.T., Lima, A.P., Hrbek, T., Werneck, F.P., Manzi, S., Thébaud, C. & Fouquet, A. (2024) Diversification of terrestrial frogs within the Guiana Shield: from highlands to lowlands and successive loss and reacquisition of endotrophy in Anomaloglossus (Aromobatidae). Molecular Phylogenetics & Evolution, 192, 108008. https://doi.org/10.1016/j.ympev.2023.108008
  41. Vanzolini, P.E. & Williams, E.E. (1981) The vanishing refuge: a mechanism for ecogeographic speciation. Papéis Avulsos de Zoologia, 34 (23), 251–255. https://doi.org/10.11606/0031-1049.1980.34.p251-255