Abstract
Using different sources of evidence (i.e., integrative taxonomy), we describe a new species of Hyloxalus, Hyloxalus arliensis sp. nov. The new species occurs in the middle Magdalena River valley on slopes between the Cordillera Central and Cordillera Oriental of the Andes of Colombia. Previously, the new species was referred to as Hyloxalus “Ibagué” but was not formally described. Phylogenetic re-analyses of 2440 base pairs (bp) of mitochondrial DNA (mtDNA), revealed the species to be a sister taxon of H. lehmanni, within a monophyletic clade also comprising H. delatorreae lineage 1, H. pulchellus and H. vertebralis. The adult males of H. arliensis sp. nov. have a pale arm gland, which differentiates it from all other species of the genus, except for H. saltarius. The new species also differs from other species of Hyloxalus by its smaller size, disc on Finger III not expanded, toes unwebbed, dorsolateral stripe absent, oblique lateral stripe present, white spots on ventrolateral flanks in life and cloacal tubercles absent. The advertisement call consists of long trains of a single note repeated at a rate of 89–132 notes/min with a dominant frequency ranging from 4808–6387 Hz. The new species is a tiny frog that inhabits the sheltered areas around streams in sub-Andean forests. Aspects of its natural history are described.
References
Acosta-Galvis, A.R. & Vargas-Ramírez, M. (2018) A new species of Hyloxalus Jiménez De La Espada, 1871 ‘‘1870’’ (Anura: Dendrobatidae: Hyloxalinae) from a cloud forest near Bogotá, Colombia, with comments on the subpunctatus clade. Vertebrate Zoology, 68 (2),123–14. [http://www.senckenberg.de/files/content/forschung/publikationen/vertebratezoology/vz68-2/02_vertebrate_zoology_68_2_acosta-vargas_123-141.pdf]
Acosta-Galvis, A.R. & Pinzón, A. (2018) Una nueva rana nodriza (Anura: Dendrobatidae) de los bosques de niebla asociados a la cuenca del Orinoco de Colombia. Biota Colombiana, 19 (Supplement 1), 160–190.
https://doi.org/10.21068/c2018.v19s1a12
Charif, R.A., Waack, A.M. & Strickman, L.M. (2010) Raven Pro 1.4 user’s manual. Cornell Lab of Ornithology, Ithaca, New York, 25506974.
Chen, M. & Combs, C. (1999) An alternative anesthesia for amphibians: ventral application of benzocaine. Herpetological Review, 30 (1), 34.
Cisneros-Heredia, D.F. & Mcdiarmid, R. (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. [http://www.mapress.com/zootaxa/2007f/zt01572p082.pdf]
https://doi.org/10.11646/zootaxa.1572.1.1
Cocroft, R.B. & Ryan, M.J. (1995) Patterns of advertisement call evolution in toads and chorus frogs. Animal Behaviour, 49 (2), 283−303.
https://doi.org/10.1006/anbe.1995.0043
Coloma, L.A. (1995) Ecuadorian frogs of the genus Colostethus (Anura: Dendrobatidae). Natural History Museum, Kansas, 82 pp.
https://doi.org/10.5962/bhl.title.16171
Dinerstein, E., Olson, D.M., Graham, D.J., Webster, A.L., Primm., S.A., Bookbinder, M.P. & Young, K.R. (1995) A conservation assessment of the terrestrial ecoregions of Latin America and the Caribbean. World Bank, Washington, D.C., 174 pp. https://doi.org/10.1596/0-8213-3295-3
Duellman, W.E. & Pyles, R.A. (1983) Acoustic resource partitioning in anuran communities. Copeia, 1893 (3), 639−649.
https://doi.org/10.2307/1444328
Duellman, W.E. & Lynch, J.D. (1988) Anuran amphibians from the Cordillera de Cutuc, Ecuador. Proceedings of the Academy of Natural Sciences of Philadelphia, 140 (2), 125–142. [http://www.jstor.org/stable/4064938]
Edwards, S.R. (1971) Taxonomic notes on South American Colostethus with Descriptions of two new species (Amphibia, Dendrobatidae). Proceedings of the Biological Society of Washington, 84 (18), 147–162. [http://www.biodiversitylibrary.org/page/34563199#page/179/mode/1up]
Edwards, S.R. (1974) Taxonomic notes on South American dendrobatid frogs of the genus Colostethus. Museum of Natural History, University of Kansas, 30, 1–14.
https://doi.org/10.5962/bhl.part.22165
Frost, D.R. (2019) Amphibian species of the world: an online reference. Version 6.0. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 20 January 2019)
Grant, T. (2004) On the identities of Colostethus inguinalis (Cope, 1868) and C. panamensis (Dunn, 1933), with comments on C. latinasus (Cope, 1863) (Anura: Dendrobatidae). American Museum Novitates, 3444, 1–24. [http://hdl.handle.net/2246/2809]
Grant, T. (2007) A new, toxic species of Colostethus (Anura: Dendrobatidae: Colostethinae) from the Cordillera Central of Colombia. Zootaxa, 1555 (1), 39–51. [http://www.mapress.com/zootaxa/2007f/z01555p051f.pdf]
Grant, T., Acosta-Galvis, A.R. & Rada, M. (2007) A name for the species of Allobates (Anura: Dendrobatoidea: Aromobatidae) from the Magdalena Valley of Colombia. Copeia, 2007 (4), 844–854.
https://doi.org/10.1643/0045-8511(2007)7[844:ANFTSO]2.0.CO;2
Grant, T. & Ardila–Robayo, M.C. (2002) A new species of Colostethus (Anura: Dendrobatidae) from the eastern slopes of the Cordillera Oriental of Colombia. Herpetologica, 58 (2), 252–260.
https://doi.org/10.1655/0018–0831(2002)058[0252:ANSOCA]2.0.CO;2
Grant, T. & Castro–Herrera, F. (1998) The cloud forest Colostethus (Anura, Dendrobatidae) of a region of the Cordillera Occidental of Colombia. Journal of Herpetology, 32 (3), 378–392.
https://doi.org/10.2307/1565452
Grant, T., Frost, D.R., Caldwell, J.P., Gagliardo, R., Haddad, C.F., Kok, P.J. & 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. [http://hdl.handle.net/2246/5803]
https://doi.org/10.1206/0003-0090(2006)299[1:PSODFA]2.0.CO;2
Grant, T., Humphrey, E.C. & Myers, C.W. (1997) The median lingual process of frogs: a bizarre character of Old World ranoids discovered in South American dendrobatids. American Museum of Natural History, 3212, 1–40.
[http://hdl.handle.net/2246/3611]
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), S1–S90.
https://doi.org/10.2994/SAJH-D-17-00017.1
IUCN Species Survival Commission. (2003) Guidelines for Application of IUCN Red List Criteria at Regional Levels. IUCN. Available from: http://www.iucnredlist.org/technical-documents/red-list-training/red-list-guidance-docs, (accessed 20 July 2017)
Jiménez De La Espada, M. (1870) 1. Faunae neotropicalis species quaedam nondum cognitae. Jornal de Sciencias Mathematicas Physicas e Naturaes, 3 ,57–65. [http://www.biodiversitylibrary.org/part/55205#/summ.ary]
Kaplan, M. (1997) A new species of Colostethus from the Sierra Nevada de Santa Marta (Colombia) with comments on intergeneric relationships within the Dendrobatidae. Journal of Herpetology, 31 (3), 369–375.
https://doi.org/10.2307/1565665
Koch, C., Venegas, P.J. & Rödder, D. (2011) Advertisement call of Hyloxalus elachyhistus (Edwards, 1971) (Anura, Dendrobatidae). Salamandra, 47 (2), 116–119.
Kok, P.J.R. (2010) A redescription of Anomaloglossus praderioi (La Marca,1998) (Anura: Aromobatidae: Anomaloglossinae), with description of its tadpole and call. Papéis Avulsos de Zoologia, 50 (4), 51–68.
https://doi.org/10.1590/S0031-10492010000400001
Kok, P.J.R., Willaert, B. & Means, D.B. (2013) A new diagnosis and description of Anomaloglossus roraima (La Marca, 1998) (Anura:Aromobatidae: Anomaloglossinae), with description of its tadpole and call. South American Journal of Herpetology, 8 (1), 29–45.
https://doi.org/10.2994/SAJH-D-12-00021.1
Köhler, J., Jansen, M., Rodriguez, A., Kok, P.J., Toledo, L.F., Emmrich, M., Glaw, F., Haddad, C.F., Roede, M.O. & Vences, M. (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa, 4251 (1), 001–124.
https://doi.org/10.11646/zootaxa.4251.1.1
Kumar, S., Stecher, G. & Amura, K.T. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7), 1870–1874.
https://doi.org/10.1093/molbev/msw054
Lanfear, R., Calcott, B., Ho, S.Y. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29 (6),1695–1701.
https://doi.org/10.1093/molbev/mss020
Lynch, J.D. (1982) Two new species of poison-dart frogs (Colostethus) from Colombia. Herpetologica, 38 (3), 366–374. [http://www.jstor.org/stable/3892419?seq=1#page_scan_tab_contents]
Lynch, J.D. & Duellman, W.E. (1997) Frogs of the genus Eleutherodactylus (Leptodactylidae) in western Ecuador: systematics, ecology and biogeography. University of Kansas, Natural History Museum Special Publication, 23, 1–236. [http://www.biodiversitylibrary.org/bibliography/7951#/summary]
https://doi.org/10.5962/bhl.title.7951
Myers, C.W., Paolillo, O.A. & Daly, J.W. (1991) Discovery of a defensively malodorous and nocturnal frog in the family Dendrobatidae: phylogenetic significance of a new genus and species from the Venezuelan Andes. American Museum of Natural History, 3002, 1–33. [http://digitallibrary.amnh.org/handle/2246/5084]
Olson, D.M. & Dinerstein, E. (2002) The Global 2000: Priority ecoregions for global conservation. Annals of the Missouri Botanical Garden, 89, 199–224. [https://www.worldwildlife.org/publications/the–global–200–priority–ecoregions–for–global–conservation]
https://doi.org/10.2307/3298564
Rambaut, A. & Drummond, A.J. (2007) Tracer. Version 1.4. Available from: http://beast.bio.ed.ac.uk/software/tracer/ (accessed 20 August 2019)
Rivero, J.A. (1991) New Colostethus (Amphibia, Dendrobatidae) from South America. Breviora, 493, 1–28. [http://www.biodiversitylibrary.org/part/6018#/summary]
Rivero, J.A. & Granados-Diaz, H. (1989) Nuevos Colostethus (Amphibia, Dendrobatidae) del departamento de Cauca, Colombia. Caribbean Journal of Science, 25,148–152.
Rivero, J.A. & Serna, M.A. (1986) Dos nuevas especies de Colostethus (Amphibia, Dendrobatidae) de Colombia. Caldasia, 15, 525–531.
https://doi.org/10.15446/caldasia
Rivero, J.A. & Serna, M.A. (1991) Tres nuevas especies de Colostethus (Amphibia–Dendrobatidae) de Colombia. Trianea, (4), 481–495.
Rivero, J.A. & Serna, M.A. (1995) Nuevos Colostethus (Amphibia, Dendrobatidae) del Departamento de Antioquia, Colombia, con la descripción del renacuajo de Colostethus fraterdanieli. Revista de Ecologia Latino Americana, 2, 45–58.
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539–542.
https://doi.org/10.1093/sysbio/sys029
Santos, J.C., Coloma, L.A., Summers, K., Caldwell, J.P., Ree, R. & Cannatella, D.C. (2009) Amazonian amphibian diversity is primarily derived from late Miocene Andean lineages. PLoS Biology, 7 (3), 448–461, e1000056.
https://doi.org/10.1371/journal.pbio.1000056
Santos, J.C. & Cannatella, D.C. (2011) Phenotypic integration emerges from aposematism and scale in poison frogs. Proceedings of the National Academy of Sciences U.S.A., 108 (15), 6175–6180.
https://doi.org/10.1073/pnas.1010952108
Santos, J.C., Baquero, M., Barrio-Amoros, C., Coloma, L.A., Erdtmann, L.K., Lima, A.P. & Cannatella, D.C. (2014) Aposematism increases acoustic diversification and speciation in poison frogs. Proceedings of the Royal Society B, 281, 20141761. https://doi.org/10.1098/rspb.2014.1761
Silverstone, P.A. (1971) Status of certain frogs of the genus Colostethus with descriptions of new species. Contributions in Science, Natural History Museum. Los Angeles County, 215, 1–8. [https://nhm.org/site/sites/default/files/pdf/contrib_science/CS215.pdf]
Silverstone, P.A. (1975) A revision of the poison-arrow frogs of the genus Dendrobates Wagler. Natural History Museum of Los Angeles County Science Bulletin, 21, 1–55.
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22 (21), 2688–2690.
https://doi.org/10.1093/bioinformatics/btl446
Tarvin, R.D., Borghese, C.M., Sachs, W., Santos, J.C., Lu, Y., O’Connell, L.A., Cannatella, D.C., Harris, R.A. & Zakon, H.H. (2017) Interacting amino acid replacements allow poison frogs to evolve epibatidine resistance. Science, 357 (6357), 1261–1266.
https://doi.org/10.1126/science.aan5061