Abstract
The amphibian chytrid fungus, Batrachochytrium dendrobatidis, Bd, has been implicated in the decimation and extinction of many amphibian populations worldwide, especially at mid and high elevations. Recent studies have demonstrated the presence of the pathogen in the lowlands from Australia and Central America. We extend here its elevational range by demonstrating its presence at the sea level, in the lowland forests of Gorgona Island, off the Pacific coast of Colombia. We conducted two field surveys, separated by four years, and diagnosed Bd by performing polymerase chain reactions on swab samples from the skin of five amphibian species. All species, including the Critically Endangered Atelopus elegans, tested positive for the pathogen, with prevalences between 3.9 % in A. elegans (in 2010) and 52 % in Pristimantis achatinus. Clinical signs of chytridiomycosis were not detected in any species. To our knowledge, this is the first report of B. dendrobatidis in tropical lowlands at sea level, where temperatures may exceed optimal growth temperatures of this pathogen. This finding highlights the need to understand the mechanisms allowing the interaction between frogs and pathogen in lowland ecosystems.
References
Annis SL, Dastoor FP, Ziel H, Daszak P, Longcore JE (2004) A DNA-based assay identifies Batrachochytrium dendrobatidis in amphibians. Journal of Wildlife Diseases 40:420–428.
Atuesta N (2003) Estimación de la distribución y densidad de Atelopus elegans (Boluenger 1882), y su relación con el hábitat en la isla continental Gorgona. Master Dissertation, Universidad Nacional de Colombia.
Beard KH, O’Neill EM (2005) Infection of an invasive frog Eleutherodactylus coqui by the chytrid fungus Batrachochytrium dendrobatidis in Hawaii. Biological Conservation 126:591–595.
Becker CG, Fonseca CR, Haddad CFB, Batista RF, Prado PI (2007) Habitat split and the global decline of amphibians. Science 318:1775–1777.
Bielby J, Cooper N, Cunningham AA, Garner TWJ, Purvis A (2008) Predicting susceptibility to future declines in world’s frogs. Conservation Letters 1:82–90.
Blanco JF (2009) The hydroclimatology of Gorgona Island: seasonal and ENSO-related patterns. Actualidades Biológicas 31:111–121.
Blaustein AR, Dobson A (2006) A message from the frogs. Nature 439:143–144.
Bosch J, Carrascal LM, Durán L, Walker S, Fisher MC (2007) Climate change and outbreaks of amphibian chytridiomycosis in a montane area of Central Spain; is there a link? Proceedings of the Royal Society of London Series B 274:253–260.
Brem FMR, Lips KR (2008) Batrachochytrium dendrobatidis infection patterns among Panamanian amphibian species, habitats and elevations during epizootic and enzootic stages. Diseases of Aquatic Organisms 81:189–202.
Bustamante HM, Livo LJ, Carey C (2010) Effects of temperature and hydric environment on survival of the Panamanian Golden Frog infected with a pathogenic chytrid fungus. Integrative Zoology 5:143–153.
Carey C, Cohen N, Rollins-Smith L (1999) Amphibian declines: an immunological perspective. Developmental and Comparative Immunology 23:459–472.
Carnaval ACOQ, Puschendorf R, Peixoto OL, Verdade VK, Rodrigues MT (2006) Amphibian chytrid fungus broadly distributed in the Brazilian Atlantic rain forest. EcoHealth 3:41–48.
Coloma LA, Ron S, Bolívar W, Cisneros-Heredia D, Lötters S (2010) Atelopus elegans. IUCN Red List of Threatened Species. Version 2011.2. Downloaded on 23 March 2012.
Crawford AJ, Lips KR, Bermingham E (2010) Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Academy of Sciences 107:13777–13782.
Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R (1999) Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5:735–748.
Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9:141–150.
Duellman WE (1999) Global distribution of amphibians: Patterns, conservation, and future challenges. Patterns of Distribution of Amphibians: A Global Perspective, Duellman WE (editor), Baltimore, John Hopkins University Press pp. 1–30.
Eterovick PC, Carnaval ACOQ, Borges-Nojosa DM, Silvano DL, Segalla MV (2005) Amphibian declines in Brazil: an overview. Biotropica 37:166–179.
Green DE, Gray MJ, Miller DL (2010) Disease monitoring and biosecurity. Amphibian Ecology and Conservation: A Handbook of Techniques, Dood KCJ (editor), New York, Oxford University Press pp. 481–505.
Hero JM, Morrison C (2004) Frog declines in Australia: global implications. Herpetological Journal 14:175–186.
Kilburn VL, Ibáñez R, Sanjur O, Bermingham E, Suraci JP, Green DM (2010) Ubiquity of the pathogenic chytrid fungus, Batrachochytrium dendrobatidis, in anuran communities in Panama. EcoHealth 4:537–548.
Kriger KM, Hero JM (2007) The chytrid fungus Batrachochytrium dendrobatidis is non-randomly distributed across amphibian breeding habitats. Diversity and Distributions 13:781–788.
Kriger KM, Hero JM (2008) Altitudinal distribution of chytrid (Batrachochytrium dendrobatidis) infection in subtropical Australian frogs. Austral Ecology 33:1022–1033.
La Marca E, Lips KR, Lötters S, Puschendorf R, Ibáñez R, Rueda-Almonacid JV, et al. (2005) Catastrophic population declines and extinctions in Neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica 37:190–201.
Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, et al. (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences 103:3165–3170.
Lips KR, Burrowes PA, Mendelson JRI, Parra-Olea G (2005) Amphibian population declines in Latin America: a synthesis. Biotropica 37:222–226.
Lips KR, Reeve JD, Witters LR (2003) Ecological traits predicting amphibian population declines in Central America. Conservation Biology 37:222–226.
Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227.
Lötters S (1996) The Neotropical Toad Genus Atelopus. M. Vences & F. Glaw Verlags GbR, Köln
Lötters S, Kielgast J, Bielby J, Schmidtlein S, Bosch J, Veith M, et al. (2009) The link between rapid enigmatic amphibian decline and the globally emerging chytrid fungus. EcoHealth 6:358–372.
Morgan JA, Vredenburg VT, Rachowicz LJ, Knapp RA, Stice MJ, Tunstall T, et al. (2007) Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences 104:13845–13850.
Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15.
Pounds AJ, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, et al. (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167.
Pounds AJ, Coloma LA (2008) Beware the lone killer. Nature 2:57–59.
Puschendorf R, Bolaños F, Chaves G (2006) The amphibian chytrid fungus along a latitudinal transect before the first reported declines in Costa Rica. Biological Conservation 132:136–142.
Rangel JO (1995) Islas de Gorgona y Gorgonilla. Colombia: Diversidad Biótica I, Rangel JO (editor), Bogotá, Editora Guadalupe pp. 145–154.
Richards CL, Zellmer AJ, Martens LM (2008) Batrachochytrium dendrobatidis not detected in Oophaga pumilio on Bastimentos Island, Panama. Herpetological Review 39:200–202.
Rödder D, Kielgast J, Bielby J, Schmidtlein S, Bosch J, Garner TWJ, et al. (2009) Global amphibian extinction risk assessment for the panzootic chytrid fungus. Diversity 1:52–66.
Rueda-Almonacid JV, Rodríguez-Mahecha JV, La Marca E, Lötters S, Kahn T, Angulo A (2005) Ranas Arlequines. Panamerica Formas e Impresos S. A., Bogotá.
Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillot AD, et al. (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125–134.
Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fuischman DL, et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786.
Urbina-C JN, Londoño-M MC (2003) Distribución de la comunidad de herpetofauna asociada a cuatro áreas con diferente grado de perturbación en la Isla Gorgona, pacífico colombiano. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales 27:105–113.
Woodhams DC, Bosch J, Briggs CJ, Cashins S, Davis LR, Muths E, et al. (2011) Mitigating amphibian diseases: strategies to maintain wild populations. Frontiers in Zoology 8:8.
Acknowledgments
This study was completed with financial support from Conservation International’s Critically Endangered Species Fund and the Association of Zoos and Aquariums’ Conservation Endowment Fund. For assistance in the field, we thank A. J. Crawford, C. Silva, J. Méndez, and J. A. Hernández. Thanks to A. J. Crawford, D. M. Hudson, S. LÖtters and R. Ibáñez for helpful comments and suggestions that greatly improved this manuscript. Research permits were provided by the Unidad Administrativa del Sistema de Parques Nacionales Naturales (PIDB DTSO 001-09 and PIDB DTSO 019-09).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Flechas, S.V., Sarmiento, C. & Amézquita, A. Bd on the Beach: High Prevalence of Batrachochytrium dendrobatidis in the Lowland Forests of Gorgona Island (Colombia, South America). EcoHealth 9, 298–302 (2012). https://doi.org/10.1007/s10393-012-0771-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-012-0771-9