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Type: Article
Published: 2024-06-26
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Forty years later: a new Andean stream treefrog of the genus Hyloscirtus (Anura: Hylidae) from Ecuador, with comments on arm hypertrophy in the H. larinopygion group

Grupo Herpetológico de Antioquia; Instituto de Biología; Universidad de Antioquia; Medellín; Colombia
Museo de Zoología; Escuela de Biología; Pontificia Universidad Católica del Ecuador; Av. 12 de Octubre y Roca; Apartado 17-01-2184; Quito; Ecuador
Laboratório de Herpetologia (LHERP); Instituto de Biociências; Campus do Litoral Paulista; UNESP; São Vicente; São Paulo; Brazil
Laboratório de Herpetologia; Departamento de Biodiversidade and Centro de Aquicultura (CAUNESP); Universidade Estadual Paulista-UNESP; Av. 24 A; 1515; Bela Vista; 13506-970; Rio Claro; São Paulo; Brazil
Division of Amphibians & Reptiles; Department of Vertebrate Zoology; National Museum of Natural History; Smithsonian Institution; Washington; D.C.; 20560; U.S.A.
Departamento de Zoologia; Instituto de Biociências; Universidade de São Paulo; Rua do Matão; Trav. 14; no. 101; Cidade Universitária; 05508-090; São Paulo; SP; Brazil
Amphibia Andes Biological Collections Biodiversity Morphology Systematics Taxonomy

Abstract

We present the description of a novel treefrog species inhabiting the Andean streams in southeastern Ecuador that has been erroneously identified as Hyloscirtus lindae for four decades. The new species is closely related to H. tapichalaca and is part of the southern clade of the H. larinopygion group, which comprises five species confined to the southeastern Andes of Ecuador to the northeastern Andes of Peru. It is diagnosed from its close relatives by a unique combination of characteristics, including hypertrophied forelimbs in males, a pronounced, curved, and protruding spine-shaped prepollex, a substantial supracloacal flap, supratympanic fold, digital discs colored in shades of orange-red or bright-red, and the concealed surfaces of limbs displaying a bluish-gray hue and dorsal spicules in males. We briefly explore the implications of this discovery for the evolution of arm morphology in the H. larinopygion group. Our findings underscore the continued importance of periodically reviewing historical specimens, leading to unexpected discoveries; once again confirming the importance of natural history museums and their custodian biological collections.

 

References

  1. Almendaìriz, A., Brito M.J., Batallas, R.D. & Ron, S.R. (2014) Una especie nueva de rana arboìrea del geìnero Hyloscirtus (Amphibia: Anura: Hylidae) de la Cordillera del Coìndor. Papeis Avulsos de Zoologia, 54, 33–49. https://doi.org/10.1590/0031-1049.2014.54.04
  2. Ardila-Robayo, M.C., Ruiz-Carranza P.M. & Roa-Trujillo, S.H. (1993) Una nueva especie de Hyla del grupo larinopygion (Amphibia: Anura: Hylidae) del sur de la Cordillera Central de Colombia. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 18, 559–565.
  3. Barrio-Amorós, C.L. & Brewer-Carias, C. (2008) Herpetological results of the 2002 expedition to Sarisariñama, a tepui in Venezuelan Guayana, with the description of five new species. Zootaxa, 1942 (1), 1–68. https://doi.org/10.11646/zootaxa.1942.1.1
  4. Boulenger, G.A. (1902) Descriptions of new batrachians and reptiles from the Andes of Peru and Bolivia. Annals and Magazine of Natural History, Series 7, 10, 394–402. https://doi.org/10.1080/00222930208678691
  5. Boulenger, G.A. (1908) Descriptions of new batrachians and reptiles discoverd by Mr. M.G. Palmer in south-western Colombia. Annals and Magazine of Natural History, Series 8, 2, 515–522. https://doi.org/10.1080/00222930808692531
  6. Caramaschi, U., Pimenta, B.V.S. & Feio, R.N. (2004) Nova especie do grupo de Hyla geographica Spix, 1824 da floresta Atlântica, Brasil (Amphibia, Anura, Hylidae). Boletim do Museu Nacional, Nova Serie, Zoologia, 518, 1–14.
  7. Coloma, L.A., Carvajal-Endara, S., Dueñas, J.F., Paredes-Recalde, A., Morales-Mite, M., Almeida-Reinoso, D., Tapia, E.E., Hutter, C.R., Toral, E. & Guayasamin, J.M. (2012) Molecular Phylogenetics of stream treefrogs of the Hyloscirtus larinopygion group (Anura: Hylidae), and description of two new species from Ecuador. Zootaxa, 3364 (1), 1–78. https://doi.org/10.11646/zootaxa.3364.1.1
  8. Cope, E.D. (1871) “1870”. Eighth contribution to the herpetology of tropical America. Proceedings of the American Philosophical Society, 11, 553–559.
  9. Darst, C.R. & Cannatella, D.C. (2004) Novel relationships among hyloid frogs inferred from 12S and 16S mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 31, 462–475. https://doi.org/10.1016/j.ympev.2003.09.003
  10. Duellman, W.E. (1970) Hylid frogs of Middle America. Monographs of the Museum of Natural History, University of Kansas, 1–2, 1–753. https://doi.org/10.5962/bhl.title.2835
  11. Duellman, W.E. (1972) A review of the neotropical frogs of the Hyla bogotensis group. Occasional Papers of the Museum of Natural History, University of Kansas, 11, 1–31. https://doi.org/10.5962/bhl.part.15140
  12. Duellman, W.E. (1973) Descriptions of new hylid frogs from Colombia and Ecuador. Herpetologica, 29, 219–227.
  13. Duellman, W.E. (1989) New species of hylid frogs from the Andes of Colombia and Venezuela. Occasional Papers of the Museum of Natural History, University of Kansas, 131, 1–12.
  14. Duellman, W.E. (2001) Hylid frogs of Middle America. Society for the Study of Amphibians and Reptiles, Ithaca, New York, 1159 pp.
  15. Duellman, W.E. & Altig, R. (1978) New species of tree frogs (family Hylidae) from the Andes of Colombia and Ecuador. Herpetologica, 34 (2), 177–185.
  16. Duellman, W.E. & Berger, T.J. (1982) A new species of Andean treefrog (Hylidae). Herpetologica, 38, 456–460.
  17. Duellman, W.E. & Hillis, D.M. (1990) Systematics of frogs of the Hyla larinopygion group. Occasional Papers of the Museum of Natural History, The University of Kansas, 134, 1–23.
  18. Duellman, W.E. & Coloma, L.A. (1993) Hyla staufferorum, a new species of treefrog in the Hyla larinopygion group from the cloud forest of Ecuador. Occasional Papers of the Museum of Natural History, University of Kansas, 161, 1–11. https://doi.org/10.5962/bhl.part.15140
  19. Duellman, W.E., De la Riva, I. & Wild, E.R. (1997) Frogs of the Hyla armata and Hyla pulchella groups in the Andes of South America, with definitions and analyses of phylogenetic relationships of Andean groups of Hyla. Scientific Papers of the Natural History Museum, The University of Kansas, 3, 1–41. https://doi.org/10.5962/bhl.title.48689
  20. Faivovich, J. & De la Riva, I. (2006) On‘‘Hyla’’ chlorostea Reynolds and Foster, 1992, a hylid of uncertain relationships, with some comments on Hyloscirtus (Anura: Hylidae). Copeia, 2006, 785–791. https://doi.org/10.1643/0045-8511(2006)6[785:OHCRAF]2.0.CO;2
  21. Faivovich, J., Haddad, C.F.B., Garcia, P.C. de A., Frost, D.R., Campbell, J.A. & Wheeler, W.C. (2005) Systematic review of the frog family Hylidae, with special reference to Hylinae: a phylogenetic analysis and taxonomic revision. Bulletin of the American Museum of Natural History, 294, 1–240. https://doi.org/10.1206/0003-0090(2005)294[0001:SROTFF]2.0.CO;2
  22. Faivovich, J., Lugli, L., Lourenço, A.C.C. & Haddad, C.F.B. (2009) A new species of the Bokermannohyla martinsi group from central Bahia, Brazil with comments on Bokermannohyla (Anura: Hylidae). Herpetologica, 65, 303–310. https://doi.org/10.1655/0018-0831-65.3.303
  23. Faivovich, J., McDiarmid, R.W. & Myers, C.W. (2013) Two new species of Myersiohyla (Anura: Hylidae) from Cerro de la Neblina, Venezuela, with comments on other species of the genus. American Museum Novitates, 3792, 1–63. https://doi.org/10.1206/3792.1
  24. Farris, J.S. (1983) The logical basis of phylogenetic analysis. In: Platnick, N.I. & Funk V.A. (Eds.), Advances in Cladistics: Proceedings of the Third Meeting of the Willi Hennig Society. Columbia University Press, New York, New York, pp. 7–36,
  25. Farris, J.S., Albert, V.A., Källersjo, M., Lipscomb, D. & Kluge, A.G. (1996) Parsimony jackknifing outperforms neighbor-joining. Cladistics, 12, 99–124. https://doi.org/10.1111/j.1096-0031.1996.tb00196.x
  26. Frost, D.R. (2024) Amphibian Species of the World: an Online Reference. Version 6.2 (13 April 2024). Electronic Database. American Museum of Natural History, New York, New York. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 4 June 2024)
  27. Goebel, A.M., Donnelly, J.M. & Atz, M.E. (1999) PCR Primers and amplification methods for 12S Ribosomal DNA, the Control Region, Cytochrome Oxidase I, and Cytochrome b in bufonids and other frogs, and an overview of PCR primers which have amplified DNA in amphibians successfully. Molecular Phylogenetics and Evolution, 11, 163–199. https://doi.org/10.1006/mpev.1998.0538
  28. Goloboff, P.A. (2003) Parsimony, likelihood, and simplicity. Cladistics, 19, 91–103. https://doi.org/10.1111/j.1096-0031.2003.tb00297.x
  29. Goloboff, P.A. & Pol, D. (2005) Parsimony and Bayesian phylogenetics. In: Albert, V.A. (Ed.), Parsimony, Phylogeny, and Genomics. Oxford University Press, London, pp. 148–159. https://doi.org/10.1093/acprof:oso/9780199297306.003.0008
  30. Goloboff, P.A. & Morales, M.E. (2023) TNT. Version 1.6, with a graphical interface for MacOS and Linux, including new routines in parallel. Cladistics, 39, 144–153. https://doi.org/10.1111/cla.12524
  31. Goin, C.J. & Woodley, J.D. (1969) A new tree-frog from Guyana. Zoological Journal of the Linnean Society, 48, 135–140. https://doi.org/10.1111/j.1096-3642.1969.tb00709.x
  32. Grant, T. & Kluge, A.G. (2009) Perspective: Parsimony, explanatory power, and dynamic homology testing. Systematics and Biodiversity, 7, 357–363. https://doi.org/10.1017/S147720000999017X
  33. Gray, J.E. (1825) A synopsis of the genera of reptiles and Amphibia, with a description of some new species. Annals of Philosophy, Series 2, 10, 193–217.
  34. Graybeal, A. (1997) Phylogenetic relationships of bufonid frogs and tests of alternate macroevolutionary hypotheses characterizing their radiation. Zoological Journal of the Linnean Society, 119, 297–338. https://doi.org/10.1111/j.1096-3642.1997.tb00139.x
  35. Guayasamin, J.M., Rivera-Correa, M., Arteaga, A., Culebras, J., Bustamante, L., Pyron, R.A., Peñafiel, N., Morochze, C. & Hutter, C.R. (2015) Molecular phylogeny of stream treefrogs (Hylidae: Hyloscirtus bogotensis Group), with a new species from the Andes of Ecuador. Neotropical Biodiversity, 1, 2–21. https://doi.org/10.1080/23766808.2015.1074407
  36. Hall, T.A. (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
  37. Hedges, S.B. (1994) Molecular evidence for the origin of birds. Proceedings of the National Academy of Sciences, 91, 2621–2624. https://doi.org/10.1073/pnas.91.7.2621
  38. Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
  39. Kluge, A.G. & Grant, T. (2006) From conviction to anti-superfluity: old and new justifications of parsimony in phylogenetic inference. Cladistics, 22, 276–288. https://doi.org/10.1111/j.1096-0031.2006.00100.x
  40. Kizirian, D., Coloma, L.A. & Paredes-Recalde, A. (2003) A new treefrog (Hylidae: Hyla) from southern Ecuador and a description of its antipredator behavior. Herpetologica, 59, 339–349. https://doi.org/10.1655/02-41
  41. Lugli, L. & Haddad, C.F.B. (2006) A new species of the Bokermannohyla pseudopseudis group from central Bahia, Brazil (Amphibia, Hylidae). Herpetologica, 62, 453–465. https://doi.org/10.1655/0018-0831(2006)62[453:ANSOTB]2.0.CO;2
  42. Lutz, B. (1950) Anfíbios anuros da coleção Adolpho Lutz do Instituto Oswaldo Cruz. V/ Frogs in the Adolpho Lutz collection of the Instituto Oswaldo Cruz. V. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro, 48, 599–637. https://doi.org/10.1590/S0074-02761950000100022
  43. Lyra, M.L., Lourenço, A.C.C., Pinheiro, P.D.P., Pezzuti, T.L., Baêta, D., Barlow, A., Hofreiter, M., Pombal, J.P. Jr., Haddad, C.F.B. & Faivovich, J. (2020) High-throughput DNA sequencing of museum specimens sheds light on the long-missing species of the Bokermannohyla claresignata group (Anura: Hylidae: Cophomantini). Zoological Journal of the Linnean Society, 190, 1235–1255. https://doi.org/10.1093/zoolinnean/zlaa033
  44. Mangiamele, L.A., Fuxjager, M.J., Schuppe, E.R., Taylor, R.S., Hödl, W. & Preininger, D. (2016) Increased androgenic sensitivity in the hind limb muscular system marks the evolution of a derived gestural display. Proceedings of the National Academy of Sciences of the USA, 113, 5664–5669. https://doi.org/10.1073/pnas.1603329113
  45. Melin, D.E. (1941) Contributions to the knowledge of the Amphibia of South America. Göteborgs Kungl. Vetenskaps-och Vitterhets-samhälles. Handlingar. Serien B, Matematiska och Naturvetenskapliga Skrifter, 1, 1–71.
  46. Müller, E.R., Galavazi, G. & Szirmai, J.A. (1969) Effect of castration and testosterone treatment on fiber width of the flexor carpi radialis muscle in the male frog (Rana temporaria). General and Comparative Endocrinology, 13, 275–284. https://doi.org/10.1016/0016-6480(69)90249-4
  47. Mueses-Cisneros, J.J. & Anganoy-Criollo, M.A. (2008) Una nueva especie del grupo Hyloscirtus larinopygion (Amphibia: Anura: Hylidae) del suroccidente de Colombia. Papéis Avulsos de Zoologia, 48, 129–138. https://doi.org/10.1590/S0031-10492008001500001
  48. Myers, C.W. & Duellman, W.E. (1982) A new species of Hyla from Cerro Colorado, and other tree frog records and geographical notes from western Panama. American Museum Novitates, 2752, 1–32.
  49. Palumbi, S.R., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabawski, G. (1991) The Simple Fool’s Guide to PCR. 2nd Edition. University of Hawaii, Honolulu, 45 pp.
  50. Peters, W.C.H. (1882) Der namen der Batrachiergattung Hylonomus in Hyloscirtus zu Ändern und legte zwei neue Arten von Schlangen, Microsoma notatum und Liophis Ygraecum. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, 1882, 127–129. https://doi.org/10.5962/bhl.part.15223
  51. Pinheiro, P.D.P., Kok, P.J.R., Noonan, B.P., Means, D.B., Haddad, C.F.B. & 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, 226–245. https://doi.org/10.1093/zoolinnean/zly030
  52. Pinheiro, P.D.P., Blotto, B.L., Ron, S.R., Stanley, E.L., Garcia, P.C., Haddad, C.F., Grant, T. & Faivovich, J. (2022) Prepollex diversity and evolution in Cophomantini (Anura: Hylidae: Hylinae). Zoological Journal of the Linnean Society, 195 (3), 995–1021. https://doi.org/10.1093/zoolinnean/zlab079
  53. Pyron, A. & Wiens, J.J. (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61, 543–583. https://doi.org/10.1016/j.ympev.2011.06.012
  54. Rambaut, A. (2014) FigTree. Tree figure drawing tool. Version 1.4.2. Available from: http://tree.bio.ed.ac.uk/software/figtree (accessed 28 May 2024)
  55. Regnier, M. & Herrera, A.A. (1993) Changes in contractile properties by androgen hormones in sexually dimorphic muscles of male frogs (Xenopus laevis). Journal of Physiology, 461, 565–581. https://doi.org/10.1113/jphysiol.1993.sp019529
  56. Reyes-Puig, J.P., Recalde, D., Recalde, F., Koch, C., Guayasamin, J.M., Cisneros-Heredia, D.F., Jost, L. & Yánez-Muñoz, M.H. (2022) A spectacular new species of Hyloscirtus (Anura: Hylidae) from the Cordillera de Los Llanganates in the eastern Andes of Ecuador. PeerJ, 10, e14066. https://doi.org/10.7717/peerj.14066
  57. Rivera-Correa, M. & Faivovich, J. (2013) A new species of Hyloscirtus (Anura: Hylidae) from Colombia with a rediagnosis of Hyloscirtus larinopygion (Duellman, 1973). Herpetologica, 69, 298–313. https://doi.org/10.1655/HERPETOLOGICA-D-12-00059
  58. Rivera-Correa, M., García-Burneo, K. & Grant, T. (2016) A new red-eyed of stream treefrog of Hyloscirtus (Anura: Hylidae) from Peru, with comments on the taxonomy of the genus. Zootaxa, 4061 (1), 29–40. https://doi.org/10.11646/zootaxa.4061.1.3
  59. Rojas-Runjaic, F.J.M., Infante-Rivero, E.E., Salerno, P.E. & Meza-Joya, F.L. (2018) A new species of Hyloscirtus (Anura, Hylidae) from the Colombian and Venezuelan slopes of Sierra de Perijá, and the phylogenetic position of Hyloscirtus jahni (Rivero, 1961). Zootaxa, 4382 (1), 121–146. https://doi.org/10.11646/zootaxa.4382.1.4
  60. Ron, S.R., Caminer, M.A., Varela-Jaramillo, A. & Almeida-Reinoso, D. (2018) A new treefrog from Cordillera del Cóndor with comments on the biogeographic affinity between Cordillera del Cóndor and the Guianan Tepuis (Anura, Hylidae, Hyloscirtus). ZooKeys, 809, 97–124. https://doi.org/10.3897/zookeys.809.25207
  61. Ron, S.R., Merino-Viteri, A. & Ortiz, D.A. (2022) Anfibios del Ecuador. Version 2022.0. Museo de Zoología, Pontificia Universidad Católica del Ecuador. Available from https://bioweb.bio/faunaweb/amphibiaweb (accessed 13 May 2024)
  62. Sánchez, D.A. (2010) Larval development and synapomorphies for species groups of Hyloscirtus Peters, 1882 (Anura: Hylidae: Cophomantini). Copeia, 2010, 351–363. https://doi.org/10.1643/CH-10-010
  63. Sánchez-Nivicela, J.C., Falcón-Reibán, J.M. & Cisneros-Heredia, D.F. (2023) A new stream treefrog of the genus Hyloscirtus (Amphibia, Hylidae) from the Río Negro-Sopladora National Park, Ecuador. ZooKeys, 1141, 75–92. https://doi.org/10.3897/zookeys.1141.90290
  64. Sabaj, M.H. (2023) Codes for Natural History Collections in Ichthyology and Herpetology. Online Supplement. Version 9.5. 10 November 2023. Available from: https://asih.org (accessed 17 February 2024)
  65. Savage, J.M. & Heyer, R.W. (1967) Variation and distribution of the tree-frog genus Phyllomedusa in Costa Rica. Beiträge zur Neotropical Fauna, 5, 111–131. https://doi.org/10.1080/01650526709360400
  66. Sierra, R., Cerón, C., Palacios, W. & Valencia, R. (1999) Mapa de vegetación del Ecuador Continental 1:1’000.000. Proyecto INEFAN/GEF-BIRF, Wildlife Conservation Society y Ecociencia, Quito. [map]
  67. Swofford, D.L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Sinauer Associates, Sunderland, Massachusetts. [program]
  68. Vellard, J. (1970) Contribución al estudio de los batracios Andinos. Revista del Museo Argentino de Ciencias Naturales «Bernardino Rivadavia» Zoología, 10, 1–21.
  69. Yánez-Muñoz, M.H., Reyes-Puig, J.P., Batallas-Revelo, D., Broaddus, C., Urgilés-Merchán, M., Cisneros-Heredia, D.F. & Guayasamin, J.M. (2021) A new Andean treefrog (Amphibia: Hyloscirtus bogotensis group) from Ecuador: An example of community involvement for conservation. PeerJ, 9 (e11914), 1–33. https://doi.org/10.7717/peerj.11914
  70. Watters, J.L., Cummings, S.T., Flanagan, R.L. & Siler, C.D. (2016) Review of morphometric measurements used in anuran species descriptions and recommendations for a standardized approach. Zootaxa, 4072 (4), 477–495. https://doi.org/10.11646/zootaxa.4072.4.6
  71. Wied-Neuwied, M.A.P. zu (1821) Reise nach Brasilien in den Jahren 1815 bis 1817. Vol. 2. Henrich Ludwig Brönner, Franfurt a.M, 345 pp. https://doi.org/10.5962/bhl.title.85967
  72. Wiens, J.J., Fetzner, J.W. Jr., Parkinson, C.L. & Reeder, T.W. (2005) Hylid frog phylogeny and sampling strategies for speciose clades. Systematic Biology, 54, 719–748. https://doi.org/10.1080/10635150500234625
  73. Wiens, J.J., Graham, C.H., Moen, D.S., Smith, S.A. & Reeder, T.W. (2006) Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity. The American Naturalist, 168, 579–596. https://doi.org/10.1086/507882
  74. Wiens, J.J., Kuczynski, C.A., Hua, X. & Moen, D.S. (2010) An expanded phylogeny of treefrogs (Hylidae) based on nuclear and mitochondrial sequence data. Molecular Phylogenetics and Evolution, 55 (3), 871–882. https://doi.org/10.1016/j.ympev.2010.03.013