Abstract
We studied populations of frogs of the genus Atelopus from the Pasto Massif of the Andes in southern Colombia and northern Ecuador, and from the Huancabamba depression in southern Ecuador and northern Perú and conclude that they belong to six species, five of which are described as new to science. Atelopus angelito is recorded for the first time from Ecuador and its range is extended 183 km (airline) southwest of its type locality in Departamento del Cauca, Colombia. We distinguish the five new species from similar ones using features of coloration, skin texture, and morphometrics. We also include osteological data for four of the new species. A putative hybrid zone at Provincia Imbabura, Ecuador, is proposed to exist between the non-sister taxa A. ignescens and one of the new species. Because recent records of four of the new species and A. angelito are lacking despite search efforts, we hypothesize that they are possibly extinct, as are many other Andean Atelopus. Thus, we categorize these species, applying IUCN Red List criteria, as Critically Endangered (Possibly Extinct). No search efforts have been carried out for one new species (from La Victoria, Colombia); thus, it is included under the Data Deficient category. The conservation of Atelopus is briefly discussed.References
Adler, K. (2007) Orcés V., Gustavo (1903–1999). In: Adler, K. (Ed.) Contributions to the History of Herpetology. Society for the Study of Amphibians and Reptiles, Dexter, USA, 394 pp.
Albuja, V.L. (2004) Dr. Gustavo Orcés Villagómez (1903–1999). Politécnica, 25, 7–10.
Almendáriz, A. (2005) Atelopus sp. 15. In: Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Lötters, S., La Marca, E., Kahn, T. & Angulo, A. (Eds.) Ranas arlequines. Conservación Internacional. Panamericana Formas e Impresos S. A., Bogotá, Colombia, 151 pp.
Almendáriz, A. & Cisneros, D. (2005) Atelopus sp. 17. In: Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Lötters, S., La Marca, E., Kahn, T. & Angulo, A. (Eds.) Ranas arlequines. Conservación Internacional. Panamericana Formas e Impresos S. A., Bogotá, 153 pp.
Alméndariz, A. & Orcés, G. (2004) Distribución de algunas especies de la herpetofauna de los pisos: altoandino, temperado y subtropical. Politécnica, 25, 97–150.
AmphibiaWeb. (2009) AmphibiaWeb: information on amphibian biology and conservation. [Web application] 8 June 2009. University of California Berkeley. Berkeley, California: AmphibiaWeb. Available from http://amphibiaweb.org (Accessed 2 July 2009).
Ardila-Robayo, M.C. (2005) Atelopus angelito. In: Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Lötters, S., La Marca, E., Kahn, T. & Angulo, A. (Eds.) Ranas arlequines. Conservación Internacional. Panamericana Formas e Impresos S. A., Bogotá, Colombia, 56 pp.
Ardila-Robayo, M.C. & Maldonado-Silva, R.A. (2004) Sapito arlequín de Nariño <<Atelopus ignescens>>. In: Rueda-Almonacid, J.V., Lynch, J.D., & Amézquita, A. (Eds.) Libro rojo de los anfibios de Colombia. Serie Libros Rojos de Especies Amenazadas de Colombia. Conservación Internacional Colombia, Instituto de Ciencias Naturales-Universidad Nacional de Colombia, Ministerio de Medio Ambiente, Panamericana Formas e Impresos S. A., Bogotá, Colombia, 384 pp.
Ardila-Robayo, M.C. & Ruiz-Carranza, P.M. (1998) Una nueva especie de Atelopus A.M.C. Duméril & Bribon 1841 (Amphibia: Bufonidae) de la Cordillera Central Colombiana. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 83, 281–285.
Barinaga, M. (1990) Where have all the froggies gone? Science, 274, 1034–1035.
Blaustein, A.R. & Wake, D.B. (1990) Declining amphibian populations: A global phenomenon? Trends in Ecology & Evolution, 5, 203–204.
Cannatella, D.C. (1986) A new genus of bufonid (Anura) from South America, and phylogenetic relationships of the neotropical genera. Herpetologica, 42, 197–205.
Cañadas-Cruz, L. (1983) El mapa bioclimático y ecológico del Ecuador. Ministerio de Agricultura y Ganadería. Programa Nacional de Regionalización Agraria. Banco Central del Ecuador, Quito, Ecuador, 209 pp.
Cepeda-Quilindo, B. & Rueda-Almonacid, J.V. (2005) Atelopus complejo ignescens. In: Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Lötters, S., La Marca, E., Kahn, T. & Angulo, A. (Eds.) Ranas arlequines. Conservación Internacional. Panamericana Formas e Impresos S. A., Bogotá, 135 pp.
Chan, K.M.A. (2008) Conservation: in a rut, we need rut-inspired solutions. Nature 451, 127.
Chapron, G. & Arlettaz, R. (2008) Conservation: academics should "conserve or perish". Nature 451, 127.
Collins, J.P. & Storfer, A. (2003) Global amphibian declines: sorting the hypotheses. Diversity and Distributions, 9, 89–98.
Collins, J.P. & Crump, M.L. (2009) Extinction in Our Times: Global Amphibian Decline. 273 pp.
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. (2002) Two new species of Atelopus (Anura: Bufonidae) from Ecuador. Herpetologica, 58, 229–252.
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, 1–32.
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.
Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2003) Infectious disease and amphibian population declines. Diversity and Distributions, 9, 141–150.
Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.
Del Castillo Ch., B. (1982) Comportamiento reproductor y primeros estadios embrionarios de Atelopus ignescens (Cornalia). In: II Congreso Grancolombiano y VI Jornadas Nacionales de Ciencias Biológicas. Vol. I. Sociedad Ecuatoriana de Biología (ed.). Editorial Escuela Superior Politécnica del Litoral, Guayaquil, Ecuador. 127–132 pp.
Dingerkus, G. & Uhler, L.D. (1977) Enzyme clearing of alcian blue stained whole small vertebrates for demostration of cartilage. Stain Technology, 52, 229–232.
Duellman, W.E. (1979) The herpetofauna of the Andes: Patterns of distribution, origins, differentiation, and present communities In: Duellman, W.E. (Ed.) The South American herpetofauna: Its origin, evolution, and dispersal. Monographs of the Museum of Natural History, The University of Kansas, Lawrence, 371–459 pp.
Duellman, W.E. & Lynch, J.D. (1969) Descriptions of Atelopus tadpoles and their relevance to atelopodid classification. Herpetologica, 25, 231–240.
Duellman, W.E. & Trueb, L. (1986) Biology of Amphibians. McGraw-Hill, New York, 670 pp.
Emerson, S.B. (1979) The ilio-sacral articulation in frogs: form and function. Biological Journal of the Linnean Society, 11, 153–168.
ESRI (2008-) ArcMap v. 9.3. ESRI. California, USA.
Fabrezi, M. & Alberch, P. (1996) The carpal elements of anurans. Herpetologica, 52, 188–204.
Frost, D.R. (2009) Amphibian Species of the World: an Online Reference. Version 5.3 (12 February, 2009). American Museum of Natural History. New York, USA. Available at: http://research.amnh.org/herpetology/amphibia/index.html (accessed 8 June 2009).
Gascon, C., Collins, J.P., Moore, R.D., Church, D.R., McKay, J.E. & Mendelson III, J.R. (2007) Amphibian Conservation Action Plan. Gland, IUCN/SSC Amphibian Specialist Group, 64 pp.
Gómez, C.L. & Ramos, O.A. (1982) Alimento de las ranas Atelopus ignescens (Cornalia) de Nariño y Putumayo (Colombia). In: II Congreso Grancolombiano y VI Jornadas Nacionales de Ciencias Biológicas. Vol. I. Sociedad Ecuatoriana de Biología (ed.). Editorial Escuela Superior Politécnica del Litoral, Guayaquil, Ecuador. 167–173 pp.
Gómez Castillo, L. (1982) Aspectos ecológicos, morfológicos y de conducta de las ranas del género Atelopus del Departamento de Nariño, Colombia. Revista Humboldt, 1, 53–64.
Gómez Castillo, L. (1993) Aspectos de la ecología y ciclo vital de la rana Atelopus ignescens (Cornalia) de los alrededores del Lago Guamuez, Nariño Colombia. Revista de Investigaciones Universidad de Nariño, Pasto, 7(VI), 168–177.
Gómez, L. & Ramos, O.A. (1982) Contenido estomacal de Atelopus ignescens (Cornalia) de Nariño y Putumayo, República de Colombia. In: II Congreso Grancolombiano y VI Jornadas Nacionales de Biología. Vol. I. Sociedad Ecuatoriana de Biología (ed.). Editorial Escuela Superior Politécnica del Litoral, Guayaquil, Ecuador. 163–165 pp.
Gray, P. (1983) Morphometrics of the Atelopus ignescens Complex (Anura: Bufonidae). M. Sc. dissertation, Lawrence, University of Kansas. 225 pp.
Gray, P. & Cannatella, D.C. (1985) A new species of Atelopus (Anura, Bufonidae) from the Andes of northern Peru. Copeia, 910–917.
Graybeal, A. & Cannatella, D.C. (1995) A new taxon of Bufonidae from Peru, with descriptions of two new species and a review of the phylogenetic status of supraspecific bufonid taxa. Herpetologica, 51, 105-–131.
Guayasamin, J.M. & Trueb, L. (2007) A new species of glass frog (Anura: Centrolenidae) from the lowlands of northwestern Ecuador, with comments on centrolenid osteology. Zootaxa, 1447, 27–45.
Guayasamin, J.M., Bonaccorso, E., Duellman, W.E. & Coloma, L.A. (2010) Genetic differentiation in the nearly extinct harlequin toads (Bufonidae: Atelopus), with emphasis on the Atelopus ignescens and A. bomolochos species complexes. Zootaxa, 2574, 55–68.
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978.
Hoffmann, M., Brooks, T.M., Da Fonseca, G.A.B., Gascon, C., Hawkins, A.F.A., James, R.E., Langhammer, P., Mittermeier, R.A., Pilgrim, J.D., Rodrigues, A.S.L. & Silva, J.M.C. (2008) Conservation planning and the IUCN Red List. Endangered Species Research, 6, 113–125.
IUCN. (2001) Red list categories: version 3.1. UICN Species Survival Comission, Gland 30 pp.
IUCN Standards and Petitions Working Group. (2008) Guidelines for using the IUCN Red List Categories and Criteria. Version 7.0. (August 2008). Standards and Petitions Working Groups of the IUCN SSC Biodiversity Assesment Sub-Committe. Available from http://intranet.iucn.org/webfiles/doc/SSC/RedList/RedListGuidelines.pd (accessed 15 May 2009).
Jarrín-V, P. & Kunz, T.H. (2008) Taxonomic history of the genus Anoura (Chiroptera: Phyllostomidae) with insights into the challenges of morphological species delimitation. Acta Chiropterologica, 10, 257–269.
Kiesecker, J.M., Blaustein, A.R. & Belden, L.K. (2001) Complex causes of amphibian population declines. Nature, 410, 681–684.
La Marca, E., Lips, K.R., Lötters, S., Puschendorf, R., Ibañez, R., Rueda-Almonacid, J.V., Schulte, R., Marty, C., Castro, F., Manzanilla-Puppo, J., García-Perez, 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.
Lemmon, E.M., Lemmon, A.R., Collins, J.T., Lee-Yaw, J.A. & Cannatella, D.C. (2007) Phylogeny-based delimitation of species boundaries and contact zones in the trilling chorus frogs (Pseudacris). Molecular Phylogenetics and Evolution, 44, 1068-–82.
Lips, K.R., Diffendorfer, J., Mendelson III, J.R. & Sears, M.W. (2008) Riding the wave: Reconciling the roles of disease and climate change in amphibian declines. PLoS Biology, 6, 441–454.
Lötters, S. (1996) The Neotropical Toad Genus Atelopus. Checklist - Biology - Distribution. M. Vences & F. Glaw, Köln, Germany, 143 pp.
Lötters, S., Schulte, R., Córdova, J.H. & Veith, M. (2005) Conservation priorities for harlequin frogs (Atelopus spp.) of Peru. Oryx, 39 (3), 343–346.
Lötters, S. (2007) The fate of the harlequin toads – help through a synchronous multidisciplinary approach and the IUCN “Amphibian Conservation Action Plan”. Mitteilungen Museum Für Naturkunde Berlin, Zoologische Reihe, 83, 69–73.
Luger, M., Garner, T.W.J., Ernst, R., Hödl, W. & Lötters, S. (2008) No evidence for precipitous declines of harlequin frogs (Atelopus) in the Guyanas. Studies on Neotropical Fauna and Environment, 43, 177–180.
Mallet, J. (2007) Hybrid speciation. Nature, 466, 279–283.
Mendelson III, J.R. & Mulcahy, D.G. (2010) A new species of toad (Bufonidae: Incilius) from central Panama. Zootaxa, 2396, 61–68.
Merino-Viteri, A. (2001) Análisis de posibles causas de las disminuciones de poblaciones de anfibios en los Andes del Ecuador. Tesis de Licenciatura, Quito, Ecuador, Pontificia Universidad Católica del Ecuador. 66 pp.
Mueses-Cisneros, J.J. (2005) Fauna anfibia del valle de Sibundoy, Putumayo-Colombia. Caldasia, 27, 229–242.
Nature Editorial. (2007) The great divide. Nature, 450, 136.
Noonan, B.P. & Gaucher, P. (2005) Phylogeography and demography of Guianan harlequin toads (Atelopus): diversification within a refuge. Molecular Ecology, 14, 3017–3031.
Poole, V. (2008) Project golden frog. Endangered Species Bulletin, 33, 7–10.
Pounds, J.A., Bustamante, M.R., Coloma, L.A., Consuegra, J.A., Fogden, M.P., 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. (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature, 439, 161–7.
Pounds, J.A. & Coloma, L.A. (2008) Beware the lone killer: Why are harlequin frogs disappearing across the American tropics? A resifiting of the evidence backs up the conclusion that global warming is a key conspirator in the losses. Nature Reports Climate Change, Nature Publishing Group, 0804, 10.1038/climate.2008.37.
Rivera-Rosi, J. (2007) Parque Nacional Podocarpus. In: ECOLAP & MAE (Eds.) Guía del patrimonio de áreas naturales protegidas del Ecuador. ECOFUND, FAN, Darwin Net, IGM, Quito, Ecuador, 185–192 pp.
Ron, S.R. & Merino, A. (2000) Amphibian declines in Ecuador: overview and first report of chytridiomycosis from South America. Froglog, 42, 2–3.
Ron, S.R., Duellman, W.E., Coloma, L.A. & Bustamante, M.R. (2003) Population decline of the Jambato toad Atelopus ignescens (Anura: Bufonidae) in the Andes of Ecuador. Journal of Herpetology, 37, 116–126.
Ron, S.R., Guayasamin, J.M., Coloma, L.A. & Menéndez-Guerrero, P.A. (in press) Decline and conservation of amphibians in Ecuador. In: Heatwole, H., Barrio-Amoros, C. & Wilkinson, J. (Eds.) Status of conservation and decline of amphibians. Surrey Beatty & Sons Pty. Ltd., Australia, xx pp.
Rueda-Almonacid, J.V. (2005a) Atelopus sp. 16. In: Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Lötters, S., La Marca, E., Kahn, T. & Angulo, A. (Eds.) Ranas arlequines. Conservación Internacional. Panamericana Formas e Impresos S. A., Bogotá, Colombia, 152 pp.
Rueda-Almonacid, J.V. & Acosta, A.R. (2005) Atelopus sp. 6. In: Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Lötters, J.V., La Marca, E., Kahn, T. & Angulo, A. (Eds.) Ranas arlequines. Conservación Internacional. Panamericana Formas e Impresos S. A., Bogotá, Colombia, 142 pp.
Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Lötters, S., La Marca, E., Kahn, T. & Angulo, A. (Eds.). (2005) Ranas arlequines. Conservación Internacional. Panamericana Formas e Impresos S. A., Bogotá, Colombia, 158 pp.
SAS Institute Inc. (2009) Statitistical discovery software, JMP® 8, Cary, North Carolina, USA.
Savage, J.M.H. & Heyer, W.R. (1997) Digital webbing formulae for anurans: a refinement. Herpetological Review, 28, 131.
Starrett, P.H. (1967) Observations on the life history of frogs of the family Atelopodidae. Herpetologica, 3, 195–204.
Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L. & Waller, R.W. (2004) Status and trends of amphibian declines and extinctions worldwide. Science, 306, 1783–1786.
Szymura, J.M. (1993) Analysis of hybrid zones with Bombina. New York and Oxford, Oxford University Press, 261–289 pp.
Valencia, R., Cerón, C., Palacios, W. & Sierra, R. (1999) Las formaciones naturales de la Sierra del Ecuador. In: Sierra, R. (Ed.) Propuesta preliminar de un sistema de clasificación de vegetación para el Ecuador continental. Proyecto INEFAN/GERF-BIRF y Ecociencia, Quito, 79–108 pp.
Venegas, P. ( 2005) Atelopus peruensis. In: Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Marca, E.L., Lötters, S., Kahn, T. & Angulo, A. (Eds.) Ranas Arlequines. Conservación Internacional. Panamericana Formas e Impresos S. A., Bogotá, Colombia, 150 pp.
von May, R., Catenazzi, A., Angulo, A., Brown, J.L., Carrillo, J., Chávez, G., Córdova, J.H., Curo, A., Delgado, A., Enciso, M.A., Gutiérrez, R., Lehr, E., Martínez, J.L., Medina-Müller, M., Miranda, A., Neira, D.R., Ochoa, J.A., Aarón, J.Q., Rodríguez, D.A., Rodríguez, L.O., Salas, A.W., Seimon, T., Seimon, A., Siu-Ting, K., Suárez, J., Torres, C. & Twomey, E. (2008) Current state of conservation knowledge on threatened amphibian species in Perú. Tropical Conservation Science, 1, 376–396.
Wiens, J.J. (2007) Species delimitation: new approaches for discovering diversity. Systematic Biology, 56, 875–878.
Yánez-Muñoz, M. & Altamirano B., M. (2005) Atelopus sp. 14. In: Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V., Lötters, S., La Marca, E., Kahn, T. & Angulo, A. (Eds.) Ranas arlequines. Conservación Internacional. Panamericana Formas e Impresos S. A., Bogotá, 150 pp.
Zippel, K.C. & Mendelson III, J.R. (2008) The amphibian extincion crisis: A call to action. Herpetological Review, 39, 23–29.