Abstract
We describe a new harlequin frog (genus Atelopus) from the cloud forest near Anchihuay (Anco District, Ayacucho Department) from 2000 to 2150 m elevation in southern Peru, representing the first record for the genus in the Department of Ayacucho. The new species has a maximum snout-vent length of 21.5 mm in females and 21.6 mm in males, and resembles A. erythropus in general appearance, small size, and dorsal coloration. The new species can be distinguished from A. erythropus by its unique pattern of ventral coloration, dorsal skin texture, and snout shape. We detected the presence of the pathogenic fungus Batrachochytrium dendrobatidis in individuals of the new species. This pathogen is threatening the survival of harlequin frogs throughout the Neotropics. In addition to chytridiomycosis, habitat loss further threatens the single locality where the new species is known to occur.
References
Asquith, A. & Altig, R. (1987) Life history notes. Atelopus spumarius. Vocalization. Herpetological Review, 18, 32–33.
Boulenger, G.A. (1903) Descriptions of new batrachians in the British Museum. Journal of Natural History, 12, 552–557.
https://doi.org/10.1080/00222930308678892
Boyle, D.G., Boyle, D.B., Olsen, V., Morgan, J.A.T. & Hyatt, A.D. (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms, 60, 141–148.
https://doi.org/10.3354/dao060141
Catenazzi, A., Lehr, E. & von May, R. (2013) The amphibians and reptiles of Manu National Park and its buffer zone, Amazon basin and eastern slopes of the Andes, Peru. Biota Neotropica, 13, 269–283.
https://doi.org/10.1590/S1676-06032013000400024
Catenazzi, A., Lehr, E., Rodriguez, L.O. & Vredenburg, V.T. (2011) Batrachochytrium dendrobatidis and the collapse of anuran species richness and abundance in the upper Manu National Park, southeastern Peru. Conservation Biology, 25, 382–391.
https://doi.org/10.1111/j.1523-1739.2010.01604.x
Catenazzi, A., Lehr, E. & Vredenburg, V.T. (2014) Thermal physiology, disease, and amphibian declines on the eastern slopes of the Andes. Conservation Biology, 28, 509–517.
https://doi.org/10.1111/cobi.12194
Catenazzi, A. & Ttito, A. (2019) Noblella thiuni sp. n., a new (singleton) species of minute terrestrial-breeding frog (Amphibia, Anura, Strabomantidae) from the montane forest of the Amazonian Andes of Puno, Peru. PeerJ, 7, e6780.
https://doi.org/10.7717/peerj.6780
Catenazzi, A., Ttito, A., Diaz, M.I. & Shepack, A. (2017) Bryophryne phuyuhampatu sp. n., a new species of Cusco Andes frog from the cloud forest of the eastern slopes of the Peruvian Andes (Amphibia, Anura, Craugastoridae). ZooKeys, 685, 65–81.
https://doi.org/10.3897/zookeys.685.12152
Coloma, L.A. (1997) Morphology, systematics, and phylogenetic relationships among frogs of the genus Atelopus (Anura: Bufonidae). Ph. D. dissertation, Lawrence, University of Kansas, 287 pp.
Coloma, L.A., Lötters, S., Duellman, W.E. & Miranda-Leiva, A. (2007) A taxonomic revision of Atelopus pachydermus, and description of two new (extinct?) species of Atelopus from Ecuador (Anura: Bufonidae). Zootaxa, 1557 (1), 1–32.
https://doi.org/10.11646/zootaxa.1557.1.1
Coloma, L.A., Lötters, S. & Salas, A.W. (2000) Taxonomy of the Atelopus ignescens complex (Anura: Bufonidae): Designation of a neotype of Atelopus ignescens and recognition of Atelopus exiguus. Herpetologica, 56, 303–324.
Duellman, W.E. & Lehr, E. (2009) Terrestrial-breeding frogs (Strabomantidae) in Peru. Natur und Tier Verlag, Münster, 382 pp.
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
Frost, D. (2020) Amphibian Species of the World: an Online Reference. Version 6.1. American Museum of Natural History, New York. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed July 20, 2020)
Gray, P. & Cannatella, D.C. (1985) A new species of Atelopus (Anura, Bufonidae) from the Andes of Northern Peru. Copeia, 4, 910–917.
https://doi.org/10.2307/1445241
Guayasamin, J.M., Bonaccorso, E., Duellman, W.E. & Coloma, L.A. (2010) Genetic differentiation in the nearly extinct harlequin frogs (Bufonidae: Atelopus), with emphasis on the Andean Atelopus ignescens and A. bomolochos species complexes. Zootaxa, 2574 (1), 55–68.
https://doi.org/10.11646/zootaxa.2574.1.2
Hazzi, N.A., Moreno, J.S., Ortiz-Movliav, C. & Palacio, R.D. (2018) Biogeographic regions and events of isolation and diversification of the endemic biota of the tropical Andes. Proceedings of the National Academy of Sciences, 115 (31), 7985–7990.
https://doi.org/10.1073/pnas.1803908115
Hyatt, A.D., Boyle, D.G., Olsen, V., Boyle, D.B., Berger, L., Obendorf, D., Dalton, A., Kriger, K., Hero, M., Hines, H., Phillott, R., Campbell, R., Marantelli, G., Gleason, F. & Colling, A. (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms, 73, 175–192.
https://doi.org/10.3354/dao073175
IUCN (2020) The IUCN Red List of Threatened Species. Version 2020-1. Available from: https://www.iucnredlist.org (accessed 20 July 2020)
De la Riva, I., Castroviejo-Fisher, S., Chaparro, J.C., Boistel, R. & Padial, J.M. (2011) A new species of Atelopus (Anura: Bufonidae) from the Amazonian slopes of the Andes in south-eastern Peru. Salamandra, 47, 161–168.
Köhler, J., Koscinski, D., Padial, J.M., Chaparro, J.C., Handford, P., Lougheed, S.C. & De la Riva, I. (2010) Systematics of Andean gladiator frogs of the Hypsiboas pulchellus species group (Anura, Hylidae). Zoologica Scripta, 39 (6), 572–590.
https://doi.org/10.1111/j.1463-6409.2010.00448.x
La Marca, E., Lips, K.R., Lötters, S., Puschendorf, R., Ibáñez, R., Rueda-Almonacid, J.V., Schulte, R., Marty, C., Castro, F., Manzanilla-Puppo, J., Garcia-Pérez, J.E., Bolaños, F., Chaves, G., Pounds, J.A., Toral, E. & Young, B.E. (2005) Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica, 37, 190–201.
https://doi.org/10.1111/j.1744-7429.2005.00026.x
Lanfear, R., Calcott, B., Ho, S. & Guindon, S. (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
https://doi.org/10.1093/molbev/mss020
Lehr, E. & Catenazzi, A. (2008) A new species of Bryophryne (Amphibia: Strabomantidae) from southern Peru. Zootaxa, 1784 (1), 1–10.
https://doi.org/10.11646/zootaxa.1784.1.1
Lehr, E., Lötters, S. & Lundberg, M. (2008) A New Species of Atelopus (Anura: Bufonidae) from the Cordillera Oriental of Central Peru. Herpetologica, 64, 368–378.
https://doi.org/10.1655/07-076.1
Lips, K.R., Diffendorfer, J., Mendelson, J.R. & Sears, M.W. (2008) Riding the wave: Reconciling the roles of disease and climate change in amphibian declines. PLoS Biology, 6 (3), e72.
https://doi.org/10.1371/journal.pbio.0060072
Lötters, S. (2003) On the systematics of the harlequin frogs (Amphibia: Bufonidae: Atelopus) from Amazonia. III: A new, remarkably dimorphic species from the Cordillera Azul, Peru. Salamandra, 39, 169–180.
Lötters, S. (2007) The fate of the harlequin toads—Help through a synchronous multi-disciplinary approach and the IUCN ‘Amphibian conservation action plan’? Zoosystematics and Evolution, 83, 69–73.
https://doi.org/10.1002/mmnz.200600028
Lötters, S., Haas, W., Schick, S. & Böhme, W. (2002) On the systematics of the harlequin frogs (Amphibia: Bufonidae: Atelopus) from Amazonia. II: Redescription of Atelopus pulcher (Boulenger, 1882) from the eastern Andean versant in Peru. Salamandra, 38, 165–184.
Lötters, S. & Henzl, M.J. (2000) A New Species of Atelopus (Anura: Bufonidae) from the Serrania de Sira, Amazonian Peru. Journal of Herpetology, 34, 169–173.
https://doi.org/10.2307/1565411
Lötters, S., Meijden, A.V., Coloma, L.A., Boistel, R., Cloetens, P., Ernst, R., Lehr, E. & Veith, M. (2011) Assessing the molecular phylogeny of a near extinct group of vertebrates: The Neotropical harlequin frogs (Bufonidae; Atelopus). Systematics and Biodiversity, 9, 45–57.
https://doi.org/10.1080/14772000.2011.557403
Lötters, S. & De la Riva, I. (1998) Redescription of Atelopus tricolor Boulenger from southeastern Peru and adjacent Bolivia, with comments on related forms. Journal of Herpetology, 32, 481–488.
https://doi.org/10.2307/1565201
Lynch, J.D. & Duellman, W.E. (1997) Frogs of the genus Eleutherodactylus in western Ecuador. Special Publications, Natural History Museum, University of Kansas, 23, 1–236.
Nguyen, L.T., Schmidt, H.A, von Haeseler, A., & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274.
https://doi.org/10.1093/molbev/msu300
Palumbi, S.R., Martin, A., Romano, S., McMillan, W.O, Stice, L. & Grabawski, G. (2002) The Simple Fool’s Guide to PCR. Version 2.0. Privately published, compiled by S. Palumbi. Departament of Zoology, University of Hawaii, Honolulu, 45 pp.
Pounds, J.A., Bustamante, M.R., Coloma, L.A., Consuegra, J.A., Fogden, M.P.L., Foster, P.N., La Marca, E., Masters, K.L., Merino-Viteri, A., Puschendorf, R., Ron, S.R., Sánchez-Azofeifa, G.A., Still, C.J. & Young, B.E. (2007) Global warming and amphibian losses; The proximate cause of frog declines? (Reply). Nature, 447, E5–E6.
https://doi.org/10.1038/nature05942
Rodríguez, L.O., Córdova, J.H. & Icochea, J. (1993) Lista preliminar de los anfibios del Perú. Publicaciones del Museo de Historia Natural. Universidad Nacional Mayor de San Marcos (A), 45, 1–22.
Rodríguez, L.O. & Catenazzi, A. (2005) Amphibians and reptiles. In: Vriesendorp, C., Rivera Chávez, L., Moskovits, D. & Shopland, J. (Eds.), Peru: Megantoni. Rapid Biological Inventories, Chicago, Illinois, pp. 199–204.
Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Lötters, S., La Marca, E., Kahn, T. & Angulo, A. (2005) Ranas Arlequines. Conservación Internacional, Panamericana Formas e Impresos S. A., Bogotá, 202 pp.
Savage, J.M. & Heyer, W.R. (1967) Variation and distribution in the tree‐frog genus Phyllomedusa in Costa Rica, Central America. Beitrage zur Neotropischen Fauna, 5, 111–131.
https://doi.org/10.1080/01650526709360400
Savage, J.M. & Heyer, W.R. (1997) Digital webbing formulae for anurans: a refinement. Herpetological Review, 28, 131.
Scheele, B.C., Pasmans, F., Skerratt, L.F., Berger, L., Martel, A., Beukema, W., Acevedo, A.A., Burrowes, P.A., Carvalho, T., Catenazzi, A., De La Riva, I., Fisher, M.C., Flechas, S.V., Foster, C.N., Frías-Álvarez, P., Garner, T.W.J., Gratwicke, B., Guayasamin, J.M., Hirschfeld, M., Kolby, J.E., Kosch, T.A., Marca, E. La, Lindenmayer, D.B., Lips, K.R., Longo, A. V., Maneyro, R., McDonald, C.A., Mendelson, J., Palacios-Rodriguez, P., Parra-Olea, G., Richards-Zawacki, C.L., Rödel, M.O., Rovito, S.M., Soto-Azat, C., Toledo, L.F., Voyles, J., Weldon, C., Whitfield, S.M., Wilkinson, M., Zamudio, K.R. & Canessa, S. (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science, 363, 1459–1463.
https://doi.org/10.1126/science.aav0379
Ttito, A. & Catenazzi, A. (2019) Geographic and altitudinal range extension of Oreobates amarakaeri Padial et al. 2012 (Anura: Craugastoridae). Zootaxa, 4543 (4), 584–586.
https://doi.org/10.11646/zootaxa.4543.4.6
Venegas, P., Catenazzi, A., Siu Ting, K. & Carrillo, J. (2008) Two new species of harlequin frogs (Anura: Bufonidae: Atelopus) from the Andes of northern Peru. Salamandra, 44, 163–176.