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Type: Article
Published: 2024-02-22
Page range: 351-391
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Lost in time: Unraveling the identity of Vitreorana parvula (Boulenger, 1895) (Anura: Centrolenidae)

Laboratório de Sistemática de Vertebrados; Pontifícia Universidade Católica do Rio Grande do Sul; Av. Ipiranga 6681; CEP 90619- 900; Porto Alegre; Rio Grande do Sul; Brasil
Laboratório de Sistemática de Vertebrados; Pontifícia Universidade Católica do Rio Grande do Sul; Av. Ipiranga 6681; CEP 90619- 900; Porto Alegre; Rio Grande do Sul; Brasil; Departamento de Zoología; Universidad de Sevilla; Av. Reina Mercedes; 41012; Sevilla; España
Amphibia Atlantic Forest bioacoustics Brazil glassfrogs integrative taxonomy morphology

Abstract

Vitreorana parvula was the first glassfrog described for the Atlantic Forest. The species, however, has become a taxonomic puzzle as the only known individual is the lectotype from the 19th century, which is not particularly well-preserved or accompanied by a detailed original description. To solve this problem, we collected topotypic specimens, as well as advertisement calls, tissue samples, and natural history data, and compared them to other Vitreorana species. Our results show clear morphological, acoustic, and genetic differences between V. parvula and other species of Vitreorana, except for V. uranoscopa. Following our results, we consider V. uranoscopa as a junior synonym of V. parvula and redescribe the species based on topotypic material, while summarizing relevant variation from across its distribution.

 

References

  1. Alberch, P. & Gale E. (1985) A developmental analysis of an evolutionary trend: Digital reduction in amphibians. Evolution, 39 (1), 8–23. https://doi.org/10.1111/j.1558-5646.1985.tb04076.x
  2. Arias-Cárdenas, A., Barrientos, L.S., Pardo-Diaz, C., Paz, A., Crawford, A.J. & Salazar, C. (2023) Taxonomic inflation and a reconsideration of speciation in the Andes: the case of the high-elevation tree frog Dendropsophus molitor (Anura: Hylidae). Zoological Journal of the Linnean Society, zlad085. https://doi.org/10.1093/zoolinnean/zlad085
  3. Bang, D.L., Lisboa, B.S., Teixeira, B.F.V., Giaretta, A.A. & Carvalho, T.R. (2020) A comparative acoustic analysis of species of Vitreorana (Anura: Centrolenidae) from Brazilian Atlantic Forest and Cerrado, with a description of the call of V. baliomma and insights into the taxonomic status of Cerrado populations. Phyllomedusa, 19 (1), 35–47. https://doi.org/10.11606/issn.2316-9079.v19i1p35-47
  4. Boulenger, G.A. (1895 “1894”) Third report on additions to the batrachian collection in the Natural-History Museum. Proceedings of the Zoological Society of London, 1894, 640–646.
  5. Brower, A.V. (2018) Going rogue. Cladistics, 34 (4), 467–468. https://doi.org/10.1111/cla.12211
  6. Brusquetti, F. & Lavilla, E.O. (2006) Lista comentada de los anfíbios de Paraguay. Cuadernos de Herpetología, 20 (2), 3–79.
  7. Castroviejo-Fisher, S., Guayasamin, J.M., Gonzalez-Voyer, A. & Vilà, C. (2014) Neotropical disversification seen through glassfrogs. Journal of Biogeography, 41 (1), 66–80. https://doi.org/10.1111/jbi.12208
  8. Castroviejo-Fisher, S., Vilà, C., Ayarzagüena, J., Blanc, M. & Ernst, R. (2011) Species diversity of Hyalinobatrachium glassfrog (Amphibia: Centrolenidae) from the Guiana Shield, with the description of two new species. Zootaxa, 3132 (1), 1–55. https://doi.org/10.11646/zootaxa.3132.1.1
  9. Chernomor, O., von Haeseler, A. & Minh, B.Q. (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology, 65 (6), 997–1008. https://doi.org/10.1093/sysbio/syw037
  10. Cisneros-Heredia, D.F. & McDiarmid, R.W. (2007) Revision of the characters of Centrolenidae (Amphibia: Anura: Athesphatanura), with comments on its taxonomy and the description of new taxa of glassfrogs. Zootaxa, 1572 (1), 1–82. https://doi.org/10.11646/zootaxa.1572.1.1
  11. Crawford, A.J., Lips, K.R. & Bermingham, E. (2010) Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Academy of Sciences of the USA, 107 (31), 13777–13782. https://doi.org/10.1073/pnas.0914115107
  12. Delia, J., Bravo-Valencia, L. & Warkentin, K.M. (2017) Patterns of parental care in Neotropical glassfrogs: fieldwork alters hypotheses of sex-role Evolution. Journal of Evolutionary Biology, 30 (5), 898–914. https://doi.org/10.1111/jeb.13059
  13. Dias, P.H.d.S., Anganoy-Criollo, M., Rada, M.A. & Grant, T. (2020) Comparative larval buccopharyngeal morphology of two glass frog species (Anura: Centrolenidae: Vitreorana), Zoologischer Anzeiger, 289, 118–122. https://doi.org/10.1016/j.jcz.2020.10.007.
  14. Duarte-Marín, S., Rada, M., Rivera-Correa, M., Caorsi, V., Barona, E., González-Durán, G. & Vargas-Salinas, F. (2022) Tic, Tii and Trii calls: advertisement call descriptions for eight glass frogs from Colombia and analysis of structure of auditory signals in Centrolenidae. Bioacoustics, 32 (2), 143–180. https://doi.org/10.1080/09524622.2022.2077833
  15. Duellman, W.E. (1977) Liste der rezenten Amphibien und Reptilien. Hylidae, Centrolenidae, Pseudidae. Das Tierreich, 95, 1–225. https://doi.org/10.1515/9783112420348
  16. Edgar, R.C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797. https://doi.org/10.1093/nar/gkh340
  17. Fabrezi, M. & Alberch, P. (1996) The carpal elements of anurans. Herpetologica, 52 (2), 188–204.
  18. Fernandes, I.Y., Cândido-Junior, J.F. & Kaefer, I.L. (2018) Combat behaviour in the glassfrog Vitreorana uranoscopa (Müller, 1924). Herpetology Notes, 11, 671–673.
  19. Flores, G. (1985) A new Centrolenella (Anura) from Ecuador, with comments on nuptial pads and prepollical spines in Centrolenella. Journal of Herpetology, 19 (3), 313–320. https://doi.org/10.2307/1564260
  20. 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
  21. Frost, D.R. (2023) Amphibian Species of the World: an Online Reference. Version 6.2. American Museum of Natural History, New York, New York. Available from: https://amphibiansoftheworld.amnh.org/index.php. (acessed 28 November 2023) https://doi.org/10.5531/db.vz.0001
  22. Gerhardt, H.C. (1994) The evolution of vocalization in frogs and toads. Annual Review of Ecology and Systematics, 25, 293–324. https://doi.org/10.1146/annurev.es.25.110194.001453
  23. Guayasamin, J.M., Bustamante, M.R., Almeida-Reinoso, D. & Funk, W.C. (2006) Glass frogs (Centrolenidae) of Yanayacu Biological Stations, Ecuador, with the description of a new species and comments on centrolenid systematics. Zoological Journal of the Linnean Society, 147 (4), 489–513. https://doi.org/10.1111/j.1096-3642.2006.00223.x
  24. Guayasamin, J.M., Castroviejo-Fisher, S., Ayarzagüena, J., Trueb, L. & Vilà, C. (2008) Phylogenetic relationships of glassfrogs (Centrolenidae) based on mithocondrial and nuclear genes. Molecular Phylogenetics and Evolution, 48 (2), 574–595. https://doi.org/10.1016/j.ympev.2008.04.012
  25. Guayasamin, J.M., Castroviejo-Fisher, S., Trueb, L., Ayarzagüena, J., Rada, M. & Vilà, C. (2009) Phylogenetic systematics of glassfrogs (Amphibia: Centrolenidae) and their sister táxon Allophryne ruthveni. Zootaxa, 2100 (1), 1–97. https://doi.org/10.11646/zootaxa.2100.1.1
  26. Guayasamin, J.M., Cisneros-Heredia, D.F., McDiarmid, R.W., Peña, P. & Hutter C.R. (2020) Glassfrogs of Ecuador: diversity, evolution, and conservation. Diversity, 12 (6), 222. https://doi.org/10.3390/d12060222
  27. Haga, I.A., Andrade, F.S., Toscano, N.P., Kwet, A. & Giaretta, A.A. (2014) Advertisement call and habitat of Vitreorana uranoscopa (Anura: Centrolenidae) in Brazil. Salamandra, 50 (4), 236–240.
  28. Hepp, F. & Pombal Jr., J.P. (2019) Naming structures and qualifying properties of anuran bioacoustical signals: a call for homology-based nomenclature and equality for quantitative data. Anais da Academia Brasileira de Ciências, 91 (4), e20190965. https://doi.org/10.1590/0001-3765201920190965
  29. Hepp, F. & Pombal Jr., J.P. (2020) Review of bioacoustical traits in the genus Physalaemus Fitzinger, 1826 (Anura: Leptodactylidae: Leiuperinae). Zootaxa, 4725 (1), 1–106. https://doi.org/10.11646/zootaxa.4725.1.1
  30. Heyer, W.R. (1978) Variation in members of the Centrolenella eurygnatha complex (Amphibia: Centrolenidae) from Serra do Mar and Serra da Mantiqueira, Brazil. Papéis Avulsos de Zoologia, 32 (2), 15–33.
  31. Heyer, W.R. (1985) Taxonomic and natural history notes on frogs of the genus Centrolenella (Amphibia: Centrolenidae) from southeastern Brasil and Adjacent Argentina. Papéis Avulsos de Zoologia, 36 (1), 1–21.
  32. Instituto Brasileiro de Geografia e Estatística—IBGE (2019) Biomas e Sistemas Costeiro-Marinha do Brasil: compatível com a escala 1:250000. IBGE, Cordenação de Recursos Naturais e Estudos Ambientais, Rio de Janeiro. Available from: https://www.ibge.gov.br/geociencias/informacoes-ambientais/estudos-ambientais/15842-biomas.html?=&t=downloads (accessed 3 December 2023)
  33. International Commission on Zoological Nomenclature (2000) International Code of Zoological Nomenclature. Available from: https://www.iczn.org/the-code/the-code-online/ (accessed 3 December 2023)
  34. Jaramillo, A.F., Gagliardi-Urrutia, G., Simões, P.I. & Castroviejo-Fisher, S. (2021) Redescription and phylogenetics of Allobates trilineatus (Boulenger 1884 “1883”) (Anura: Aromobatidae) based on topotypic specimens. Zootaxa, 4951 (2), 201–235. https://doi.org/10.11646/zootaxa.4951.2.1
  35. K. Lisa Yang Center for Conservation Bioacoustics (2023) Raven Pro: Interactive Sound Analysis Software. Version 1.6.5. The Cornell Lab of Ornithology, Ithaca, New York, computer software. Available from: https://ravensoundsoftware.com/ (accessed 30 January 2024)
  36. 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
  37. Kearney, M. (2002) Fragmentary taxa, missing data, and ambiguity: mistaken assumptions and conclusions. Systematic Biology, 51, 369–381. https://doi.org/10.1080/10635150252899824
  38. Köhler, J., Jansen, M. Rodríguez, 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
  39. Larsson, A. (2014) AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics, 30 (22), 3276–3278. https://doi.org/10.1093/bioinformatics/btu531
  40. Lutz, A. (1925) Batraciens du Brésil. Comptes rendus et mémories hebdomadaires des séances de la société de biologie et des ses filiales, Paris, 93, 137–139.
  41. Lynch, J.D. & Duellman, W.E. (1973) A review of the centrolenid frogs of Ecuador, with descriptions of new species. Occasional Papers University of Kansas Museum of Natural History, 16, 1–66.
  42. Lyra, M.L., Haddad, C.F.B. & 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 (5), 966–980. https://doi.org/10.1111/1755-0998.12648
  43. Machado, I.F., Bühler, D., Abadie, M., Júnior, A.P.S.-Jr. & Santos, R.R. (2014) Distribution extension of Vitreorana uranoscopa (Anura: Centrolenidae) in the state of Rio Grande do Sul, southern Brazil. Herpetology Notes, 7, 443–446.
  44. Machado, D.J., Castroviejo-Fisher, S. & Grant, T. (2021) Evidence of absence treated as absence of evidence: The effects of variation in the number and distribution of gaps treated as missing data on the results of standard maximum likelihood analysis. Molecular Phylogenetics and Evolution, 154, 106966. https://doi.org/10.1016/j.ympev.2020.106966
  45. Minh, B.Q., Schimidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., von Haeseler, A. & Lanfear, R. (2020) IQ-TREE 2: New models and eficiente methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37 (5), 1530–1534. https://doi.org/10.1093/molbev/msaa015
  46. Montilla, S.O., Arcila-Pérez, L.F., Toro-Gómez, M.P., Vargas-Salinas, F. & Rada, M. (2023) A multidisciplinar approach reveals a new species of glassfrogs from Colombia (Anura: Centrolenidae: Nymphargus). Zootaxa, 5271 (1), 1–48. https://doi.org/10.11646/zootaxa.5271.1.1
  47. Müller, L. (1924) Neue laubfrösche aus dem Staate Santa Catharina, S. O. Brasilien. Zoologischer Anzeiger, 59, 233–238.
  48. Noble, G.K. (1926) An analysis of the remarkable cases of distribution among the Amphibia, with description of new genera. American Museum Novitates, 212, 1–24.
  49. Palumbi, S.R., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The simple fool’s guide to PCR. Version 2.0. Privately published document compiled by S. Palumbi, Dept. Zoology, University Hawaii, Honolulu, 43 pp.
  50. Pontes, R.C., Caramaschi, U., Pombal Jr., J.P. (2014) A remarkable new glass frog (Centrolenidae: Vitreorana) from the northeast Atlantic Forest, Brazil. Herpetologica, 70 (3), 298–308. https://doi.org/10.1655/HERPETOLOGICA-D-13-00024
  51. R Core Team (2023) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: https://www.R-project.org/ (accessed 30 January 2024)
  52. Rada, M., Dias, P.H.d.S., Pérez-Gonzalez, J.L., Anganoy-Criollo, M., Rueda-Solano, L.A., Pinto-E, M.A., Quintero, L.M., Vargas-Salinas, F. & Grant, T. (2019) The poverty of adult morphology: Bioacoustics, genetics, and internal tadpole morphology reveal a new species of glassfrog (Anura: Centrolenidae: Ikakogi) from the Sierra Nevada de Santa Marta, Colombia. PLoS one, 14 (5), e0215349. https://doi.org/10.1371/journal.pone.0215349
  53. Renner, S.S., Scherz, M.D., Schoch, C.L., Gottschling, M. & Vences, M. (2023) DNA sequences from type specimens and type strains–how to increase their number and improve their annotation in NCBI GenBank and related databases. Systematic Biology, syad068. https://doi.org/10.1093/sysbio/syad068
  54. Ruíz-Carranza, P.M. & Lynch, J.D. (1991) Ranas Centrolenidae de Colombia I: propuesta de una nueva clasificación genérica. Lozania, 57, 1–30.
  55. Sabaj, M.H. (2020) Codes for natural history collections in ichthyology and herpetology. Copeia, 108 (3), 593–669. https://doi.org/10.1643/ASIHCODONS2020
  56. Santana, D.J., Barros, A.B., Pontes, R.C. & Feio R.N. (2015) A new species of Glassfrog genus Vitreorana (Anura: Centrolenidae) from the Cerrado Domain, southeastern Brazil. Herpetologica, 71 (4), 289–298. https://doi.org/10.1655/HERPETOLOGICA-D-14-00066
  57. Savage, J.M. & Heyer, W.R. (1997) Digital webbing formulae for anurans: a refinement. Herpetological Review, 28 (3), 131.
  58. Sukumaran, J.M. & Holder, T. (2010) DendroPy: A Python library for phylogenetic computing. Bioinformatics, 26 (12), 1569–1571. https://doi.org/10.1093/bioinformatics/btq228
  59. Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution, 38 (7), 3022–3027. https://doi.org/10.1093/molbev/msab120
  60. Taylor, E.H. & Cochran, D.M. (1953) Frogs of the family Centrolenidae from Brasil. University of Kansas Science Bulletin, 35, 1625–1656. https://doi.org/10.5962/bhl.part.26735
  61. Vaidya, G., Lohman, D.J. & Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with Character set and códon information. Cladistics, 27 (2), 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
  62. Vences, M., Thomas, M., 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, 1859–1868. https://doi.org/10.1098/rstb.2005.1717
  63. Watters, J.L., Cummings, S.T., Flanagan, R.L. & Siler, C.D. (2016) Review of morphometric measurements used in anuran species description and recommendations for a standardized approach. Zootaxa, 4072 (4), 477–495. https://doi.org/10.11646/zootaxa.4072.4.6
  64. Wells, K.D. (2007) The ecology and behavior of amphibians. The University of Chicago Press, Chicago, Illinois, 416 pp. https://doi.org/10.7208/chicago/9780226893334.001.0001
  65. Wilkinson, M. (1995) Coping with abundant missing entries in phylogenetic inference using parsimony. Systematic Biology, 44 (4), 501–514. https://doi.org/10.2307/2413657
  66. Zaracho, V.H. (2014) Re-description of the advertisement call of Vitreorana uranoscopa (Müller, 1924) (Anura: Centrolenidae) from the Argentinean Atlantic Forest, with notes on natural history. South American Journal of Herpetology, 9 (2), 83–89. https://doi.org/10.2994/SAJH-D-14-00005.1
  67. Zucchetti, V.M., Rojas-Padilla, O., Días, I.R., Solé, M. & Castroviejo-Fisher, S. (2021) Reproductive biology and phylogenetic relationships of Vitreorana baliomma (Anura: Centrolenidae). Salamandra, 57 (3), 353–370.
  68. Zucchetti, V.M., Rojas-Padilla, O., Dias, I.R., Solé, M., Orrico, V.G.D. & Castroviejo-Fisher, S. (2023) An elusive giant: A new species of Vitreorana Guayasamin et al., 2009 (Anura: Centrolenidae) from the northern Atlantic Forest with an osteological description and comments on integumentary spicules. Zootaxa, 5249 (3), 301–334. https://doi.org/10.11646/zootaxa.5249.3.1