Abstract
Telmatobius halli was the first endemic Telmatobius species described in Chile, reported by Noble in 1938 near the locality of Ollagüe, in the high Andean zone of the Antofagasta region. To this date, there are no specimens assignable to this species other than the type series; although many expeditions have tried to search for T. halli, they have been unsuccessful, but they have found and described new species around this area. In order to clarify the origin of the enigmatic T. halli, we reviewed the itinerary of the expedition carried out by F. G. Hall in the Chilean Altiplano, to place a putative type locality. We contrast the morphology of the holotype, with that of recently collected specimens from the new putative type locality, to confirm the population’s identity; and finally, we perform phylogenetic analyses in order to clarify the systematic position of this taxon. The historical review of the expedition that collected these frogs shows that it is likely that Telmatobius halli had been collected near Collahuasi, about 50 km northwest of Ollagüe, site that we have assigned as a putative type locality for T. halli. The morphological analyses support this hypothesis, while phylogenetic results show that the specimens assigned to this species form a monophyletic group, and is a sister clade of T. chusmisensis. Thus, we propose that the type locality of T. halli be changed from “around Ollagüe” to the area of the Copaquire ravine, so its distribution would be restricted to this system and Choja-Chijlla ravine, both in the high Andean zone of the Región de Tarapacá, Chile.
References
Barrionuevo, J.S. & Mangione, S. (2006) Chytridiomycosis in two species of Telmatobius (Anura: Leptodactylidae) from Argentina. Diseases of Aquatic Organisms, 73, 171–174.
https://doi.org/10.3354/dao073171Barrionuevo, J.S. (2017) Frogs at the summits: phylogeny of the Andean frogs of the genus Telmatobius (Anura, Telmatobiidae) based on phenotypic characters. Cladistics, 33, 41–68.
https://doi.org/10.1111/cla.12158Benavides, E., Ortiz, J.C. & Formas, J.R. (2002) A new species of Telmatobius (Anura: Leptodactylidae) from northern Chile. Herpetologica, 58 (2), 210–220.
https://doi.org/10.1655/0018-0831(2002)058[0210:ANSOTA]2.0.CO;2Cei, J.M. (1962) Batracios de Chile. Universidad de Chile, Santiago, 240 pp.
Cei, J.M. (1986) Speciation and adaptative radiation in Andean Telmatobius frogs. In: Vuilleumier, F. & Monasterio, M. (Eds.), High altitude tropical biogeography. Oxford University Press, New York, pp. 374–386.
Correa, C. (2017) Refuting the revalidation of Telmatobius laevis Philippi 1902. Herpetological Journal, 27, 69–78.
Cuevas, C. & Formas, J.R. (2002) Telmatobius philippii, una nueva especie de rana acuática de Ollagüe, norte de Chile (Leptodactylidae). Revista Chilena de Historia Natural, 75, 245–258.
https://doi.org/10.4067/S0716-078X2002000100022Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
De la Riva, I., García-París, M. & Parra-Olea, G. (2010) Systematics of Bolivian frogs of the genus Telmatobius (Anura, Ceratophryidae) based on mtDNA sequences. Systematics and Biodiversity, 8, 49–61.
https://doi.org/10.1080/14772000903526454De la Riva, I. & Harvey, M.B. (2003) A new species of Telmatobius from Bolivia and a redescription of T. simonsi Parker, 1940 (Amphibia: Anura: Leptodactylidae). Herpetologica, 59, 127–142.
https://doi.org/10.1655/0018-0831(2003)059[0127:ansotf]2.0.co;2Dill, D.B. (1979) Case history of a physiologist: F. G. Hall. Physiologist, 22, 8–21.
Fibla, P., Sáez, P.A., Salinas, H., Araya, C., Sallaberry, M. & Méndez, M.A. (2017) The taxonomic status of two Telmatobius (Anura: Telmatobiidae) frog species from the western Andean slopes of northernmost Chile. Zootaxa, 4250 (4), 301–314.
https://doi.org/10.11646/zootaxa.4250.4.1Formas, J.R., Northland, I., Capetillo, J., Nuñez, J.J., Cuevas, C.C. & Brieva, L. (1999) Telmatobius dankoi, una nueva especie de rana acuática del norte de Chile (Leptodactylidae). Revista Chilena de Historia Natural, 72, 427–445.
Formas, J.R., Benavides, E. & Cuevas, C. (2003) A new species of Telmatobius (Anura: Leptodactylidae) from Río Vilama, northern Chile, and the redescription of T. halli Noble. Herpetologica, 59, 253–270.
https://doi.org/10.1655/0018-0831(2003)059[0253:ANSOTA]2.0.CO;2Formas, J.R., Cuevas, C. & Nuñez, J.J. (2006) A New Species of Telmatobius (Anura: Leptodactylidae) from northern Chile, Herpetologica, 62, 173–183.
https://doi.org/10.1655/05-08.1Frost, D. R. (2017) Amphibian Species of the World: an Online Reference. Version 6.0 (9 February 2018). American Museum of Natural History, New York, USA.Electronic Database accessible. Available from: http://research.amnh.org/herpetology/amphibia/index.html.
Hall, T. (1999) Bioedit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Version 5.0.9. Nucleic Acids Symposium Series, 41, 95–98.
Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica, 4, 1–9.
Hall, F.G., Dill, D.B. & Guzman-Barron, E.S. (1936) Comparative Physiology in high altitudes. Journal of Cellular and Comparative Physiology, 8, 301–313.
https://doi.org/10.1002/jcp.1030080302IUCN SSC Amphibian Specialist Group (2015) Telmatobius halli. The IUCN Red List of Threatened Species, 2015, e.T21582A79809691.
https://doi.org/10.2305/IUCN.UK.2015-4.RLTS.T21582A79809691.enJowett, T. (1986) Preparation of nucleic acids. In: Roberts, D.B. (Eds.), Drosophila: A Practical Approach. IRL Press, Oxford, pp. 275–286.
Keys, A., Matthews, B., Forbes, W.H. & McFarland, R. (1938) Individual variations in ability to acclimatize to high altitude. Proceedings of the Royal Society B: Biological Sciences, 126, 1–24.
https://doi.org/10.1098/rspb.1938.0043Lobos, G., Rebolledo, N., Sandoval, M., Canales, C. & Perez-Quezada, J.F. (2018) Temporal gap between knowledge and conservation needs in high Andean anurans: the case of the Ascotán salt flat frog in Chile (Anura: Telmatobiidae: Telmatobius). South American Journal of Herpetology, 13 (1), 33–43.
https://doi.org/10.2994/SAJH-D-16-00062.1Márquez-García, M., Vila, I., Hinojosa L. F., Méndez M.A., Carvajal J.L. & Sabando, M.C. (2009) Distribution and seasonal fluctuations in the aquatic biodiversity of the southern Altiplano. Limnologica, 39 (4), 314–318.
https://doi.org/10.1016/j.limno.2009.06.007Merino-Viteri, A., Coloma, L.A. & Almendáriz, A. (2005) Los Telmatobius de los Andes de Ecuador y su disminución poblacional. Monografías de Herpetología, 7, 9–37.
Millán, A. (2006) La minería metálica en Chile en el siglo XX. Editorial Universitaria, Santiago, 180 pp.
Mitchell, M.A. (2009) Anesthetic Considerations for Amphibians. Journal of Exotic Pet Medicine, 18, 40–49.
https://doi.org/10.1053/j.jepm.2008.11.006Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop (GCE). New Orleans, LA, pp. 1–8.
https://doi.org/10.1109/GCE.2010.5676129Noble, G.K. (1938) A new species of frog of the genus Telmatobius from Chile. American Museum Novitates, 973, 1–3.
Northland, I., Capetillo, J., Iturra, P. & Veloso A. (1990) Nuclear DNA content and karyosystematic relationships of species grouped in primitive tribes of Leptodactylidae (Amphibia-Anura). Revista Brasileira de Genetica, 13, 247–254.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180Sáez, P.A., Fibla, P., Correa, C., Sallaberry, M., Salinas, H., Veloso, A., Mella, J., Iturra, P. & Méndez, M.A. (2014) A new endemic lineage of Andean frog genus Telmatobius (Anura, Telmatobiidae) from the western slope of the Central Andes. Zoological Journal of the Linnean Society, 171, 769–782.
https://doi.org/10.1111/zoj.12152Seimon, T.A., Seimon, A., Daszak, P., Halloy, S.R.P., Schloegel, L.M., Aguilar, C.A., Sowell, P., Hyatt, A.D., Konecky, B. & Simmons, J.E. (2007) Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Global Change Biology, 13, 288–299.
https://doi.org/10.1111/j.1365-2486.2006.01278.xSinsch, U. & Lehr, E. (2010) Geographical variation in the high Andean frog Telmatobius carrillae Morales, 1988 (Ceratophryidae, Telmatobiinae): size, skin texture, and coloration. Journal of Herpetology, 44, 495–505.
https://doi.org/10.1670/09-081.1Stamatakis, A. (2014) RAxML version 8: A tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. Bioinformatics, 30, 1312−1313.
https://doi.org/10.1093/bioinformatics/btu033Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis using parsimony (* and other methods). Version 4. Sinauer, Sunderland, Massachusetts. [software]
Trueb, L. (1979) Leptodactylid frogs of the genus Telmatobius in Ecuador with the description of a new species. Copeia, 1979, 714–733.
Veloso, A., Sallaberry, M., Navarro, J., Iturra, P., Valencia, J., Penna, M. & Díaz, N. (1982) Contribución sistemática al conocimiento de la herpetofauna del extremo norte de Chile. In: Veloso, A. & Bustos, E. (Eds.), La Vegetación y vertebrados ectotérmicos del transecto Arica-Lago Chungará. ROSTLAC, Montevideo, pp. 135–268.
West, J. (1998) Permanent residents of high altitude. In: West, J. (Eds.), Highlife: A history of high-altitude physiology and medicine. American Physiology Society, Washington, D.C., pp. 194–227.
https://doi.org/10.1007/978-1-4614-7573-6_7Wiens, J.J. (1993) Systematics of the leptodactylid frog genus Telmatobius in the Andes of northern Peru. Occasional Papers of the Museum of Natural History, 162, 1–76.