Abstract
The role of the chytrid fungus Batrachochytrium dendrobatidis (Bd), which is the causal agent of chytridiomycosis, in the declines of Central American bolitoglossine salamanders is unknown. Here we establish a swabbing protocol to maximize the detection probability of Bd in salamanders. We then used this protocol to examine captive and wild Mexican bolitoglossine salamanders of 14 different species for the presence of Bd. Of the seven body parts sampled, the pelvic region, hindlimbs, forelimbs, and the ventral side of the tail had the most Bd per surface area and thus might provide the best sampling regions of salamanders to detect Bd infections. Sixteen out of 33 (48%) of the dead captive salamanders had Bd infections and epidermal hyperkeratosis, whereas none of the 28 clinically healthy captive animals were infected. Nine out of 17 (53%) of the wild salamanders carried low zoospore loads of Bd but had no clinical signs of disease. The high prevalence of Bd in dead captive salamanders, its absence in clinically healthy living ones and its presence in wild salamanders is consistent with Bd being involved in recent bolitoglossine population declines, but further studies would be required to draw a causal link.
References
Bandi C, Damiani G, Magrassi L, Grigolo A, Fani R, Sacchi L, et al. (1994) Flavobacteria as intracellular symbionts in cockroaches. Proceedings of the Royal Society B-Biological Sciences 257:43–48.
Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, et al. (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Science of the USA 95:9031–9036.
Berger L, Hyatt AD, Olsen V, Hengstberger SG, Boyle D, Marantelli G, et al. (2002) Production of polyclonal antibodies to Batrachochytrium dendrobatidis and their use in an immunoperoxidase test for chytridiomycosis in amphibians. Diseases of Aquatic Organisms 48:213–220.
Berger L, Speare R, Skerratt LF (2005) Distribution of Batrachochytrium dendrobatidis and pathology in the skin of green tree frogs Litoria caerulea with severe chytridiomycosis. Diseases of Aquatic Organisms 68:65–70.
Boyle DG, Boyle DB, Olsen V, Morgan JA, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms 60:141–148.
Cheng TL, Rovito SM, Wake DB, Vredenburg VT (2011) Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Science of the USA. doi:10.1073/pnas.1105538108 (early online edition, May 19, 2011)
Hyatt AD, Boyle DG, Olsen V, Boyle DB, Berger L, Obendorf D et al. (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 73:175–192.
La Marca E, Lips KR, Lötters S, Puschendorf R, Ibanez R, Rueda-Almonacid JV, et al. (2005) Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica 37:190–201.
Larson L, Wake D, Devitt T (2006) Plethodontidae. Lungless salamanders. http://tolweb.org/Plethodontidae/15441/2006.09.26 in The Tree of Life Web Project, http://tolweb.org. Accessed February 3, 2010.
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 Science of the USA 103:3165–3170.
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.
Parra-Olea G, Garcia-Paris M, Wake DB (1999) Status of some populations of Mexican salamanders (Amphibia: Plethodontidae). Revista de Biologia Tropical 47:217–223.
Pasmans F, Zwart R, Hyatt AD (2004) Chytridiomycosis in the Central American bolitoglossine salamander (Bolitoglossa dofleini). Veterinary Record 154:153.
Puschendorf R, Bolaños F (2006) Detection of Batrachochytrium dendrobatidis in Eleutherodactylus fitzingeri: effects of skin sample location and histologic stain. Journal of Wildlife Diseases 42: 301–306.
Rohr JR, Raffel TR (2010) Linking global climate and temperature viability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Science of the USA 107: 8269–8274.
Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ (2008) Evaluating the links between climate, disease spread and amphibian declines. Proceedings of the National Academy of Science of the USA 105:17436–17441.
Rovito SM, Parra-Olea G, Vasquez-Almazan CR, Papenfuss TJ, Wake DB (2009) Dramatic declines in Neotropical salamander populations are an important part of the global amphibian crisis. Proceedings of the National Academy of Science of the USA 106:3231–3236.
Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786.
Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Science of the USA 105:11466–11473.
Acknowledgments
This study was funded by a research grant from Ghent University to Pascale Van Rooij (BOF08/24J/004). Polyclonal antibodies against B. dendrobatidis were kindly provided by Dr. Alex D. Hyatt (Australian Animal Health Laboratory, CSIRO, Victoria, Australia). We are grateful to Arnaud Jamin and Eike Amthauer for kindly providing Plethodontid specimens, David Van Rooij (RCMG, Ghent University, Belgium) for providing help in mapping of the sampling localities and two anonymous referees for providing helpful suggestions that greatly improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Van Rooij, P., Martel, A., Nerz, J. et al. Detection of Batrachochytrium dendrobatidis in Mexican Bolitoglossine Salamanders Using an Optimal Sampling Protocol. EcoHealth 8, 237–243 (2011). https://doi.org/10.1007/s10393-011-0704-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-011-0704-z