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
- 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
- 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
- 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
- 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.
- Brower, A.V. (2018) Going rogue. Cladistics, 34 (4), 467–468. https://doi.org/10.1111/cla.12211
- Brusquetti, F. & Lavilla, E.O. (2006) Lista comentada de los anfíbios de Paraguay. Cuadernos de Herpetología, 20 (2), 3–79.
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- Duellman, W.E. (1977) Liste der rezenten Amphibien und Reptilien. Hylidae, Centrolenidae, Pseudidae. Das Tierreich, 95, 1–225. https://doi.org/10.1515/9783112420348
- 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
- Fabrezi, M. & Alberch, P. (1996) The carpal elements of anurans. Herpetologica, 52 (2), 188–204.
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- 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.
- 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.
- 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)
- 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)
- 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
- 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)
- 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
- Kearney, M. (2002) Fragmentary taxa, missing data, and ambiguity: mistaken assumptions and conclusions. Systematic Biology, 51, 369–381. https://doi.org/10.1080/10635150252899824
- 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
- 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
- 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.
- 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.
- 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
- 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.
- 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
- 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
- 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
- Müller, L. (1924) Neue laubfrösche aus dem Staate Santa Catharina, S. O. Brasilien. Zoologischer Anzeiger, 59, 233–238.
- 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.
- 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.
- 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
- 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)
- 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
- 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
- Ruíz-Carranza, P.M. & Lynch, J.D. (1991) Ranas Centrolenidae de Colombia I: propuesta de una nueva clasificación genérica. Lozania, 57, 1–30.
- Sabaj, M.H. (2020) Codes for natural history collections in ichthyology and herpetology. Copeia, 108 (3), 593–669. https://doi.org/10.1643/ASIHCODONS2020
- 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
- Savage, J.M. & Heyer, W.R. (1997) Digital webbing formulae for anurans: a refinement. Herpetological Review, 28 (3), 131.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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