Stream tadpoles present high prevalence but low infection loads of Batrachochytrium dendrobatidis (Chytridiomycota)
Tadpoles can be found in different lentic and lotic habitats, including permanent and ephemeral water bodies. Characteristics from these habitats influence both the tadpole assemblages and the co-occurring amphibian-killing fungus Batrachochytrium dendrobatidis (Bd). However, this intricate relationship has not been fully addressed. Bd causes depigmentation of tooth rows and jaw sheaths, but infection is usually nonlethal in tadpoles. We herein investigate how Bd interacted with tadpoles from different habitats in a high elevation site in the Brazilian Atlantic forest. Our results revealed that Bd was more prevalent in tadpoles from lotic habitats (streams) as expected, even though the infection intensity was greater in tadpoles from lentic habitats (ponds), especially on those sampled in permanent ponds. Also, because tadpoles may act as Bd reservoirs, influencing the infection rates of adult amphibians, we hypothesized that at sites where Bd was very prevalent on tadpoles, it would also be very prevalent on adults. However, we did not find such interaction. Even so, Bd has the potential to rapidly spread in water and understanding its dynamics in this environment could be the key to prevent die-offs events, already reported from amphibian populations worldwide.
KeywordsAnuran Batrachochytrium dendrobatidis Brazilian Atlantic forest Larvae Lentic Lotic
We thank A. B. Carollo, C. Lambertini, and P. Morão for laboratory assistance at Unicamp, and all colleagues from the lab at UFRJ for the feedback on earlier versions of the manuscript. We also thank C. Luna, J. Kirchmeyer, and V. Rademaker for helping with fieldwork. We thank all reviewers and the editor for their comments and great suggestions. Access to parks was possible through the collecting permits provided by ICMBio/SISBIO (35779–7) and INEA/RJ (053/2012).
LFT has received research grants from the Brazilian National Council of Technological and Scientific Development (CNPq 302589/2013–9; 405285/2013–2) and from the São Paulo Research Foundation (FAPESP 2014/23388–7), and SPCS from the Brazilian National Council of Technological and Scientific Development (CNPq 311156/2013–4).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Berger, L., R. Speare, P. Daszak, D. E. Green, A. A. Cunningham, C. L. Goggin, R. Slocombe, M. A. Ragan, A. D. Hyatt, K. R. McDonald, H. B. Hines, K. R. Lips, G. Marantelli & H. Parke, 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rainforests of Australia and Central America. Proceedings of the National Academy of Sciences USA 95: 9031–9036.CrossRefGoogle Scholar
- Borges-Junior, V. N. T. & C. F. D. Rocha, 2013. Tropical tadpole assemblages: which factors affect their structure and distribution? Oecologia Australis 17: 27–38.Google Scholar
- Conradie, W., C. Weldon, K. G. Smith & L. H. D. Preez, 2011. Seasonal pattern of chytridiomycosis in common river frog (Amietia angolensis) tadpoles in the South African Grassland Biome. African Zoology 46: 95–102.Google Scholar
- Gründler, M. C., L. F. Toledo, G. Parra Olea, C. F. B. Haddad, L. O. M. Giasson, R. J. Sawaya, C. P. A. Prado, O. G. S. Araújo, F. J. Zara, F. C. Centeno & K. R. Zamudio, 2012. Interaction between breeding habitat and elevation affects prevalence but not infection intensity of Batrachochytrium dendrobatidis in Brazilian anuran assemblages. Diseases of Aquatic Organisms 97: 173–184.CrossRefPubMedGoogle Scholar
- Haddad, C. F. B., L. F. Toledo, C. P. A. Prado, D. Loebmann, J. L. Gasparini & I. Sazima, 2013. Guide to the Amphibians of the Atlantic Forest: Diversity and Biology. Anolis Books, São Paulo.Google Scholar
- Hoff, K. S., A. R. Blaustein, R. W. McDiarmid & R. Altig, 1999. Behaviour: interactions and their consequences. In McDiarmid, R. W. & R. Altig (eds), Tadpoles: The Biology of Anuran Larva. University of Chicago Press, Chicago: 215–239.Google Scholar
- Hyatt, A. D., D. G. Boyle, V. Olsen, D. B. Boyle, L. Berger, B. Obendorf, A. Dalton, K. M. Kriger, J. M. Hero, H. Hines, R. Phillott, R. Campbell, G. Marantelli, F. Gleason & A. Colling, 2007. Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 73: 175–192.CrossRefPubMedGoogle Scholar
- James, T. Y., L. F. Toledo, D. Rödder, D. S. Leite, A. M. Belasen, C. M. Betancourt-Román, T. S. Jenkinson, C. Soto-Azat, C. Lambertini, A. V. Longo, J. Ruggeri, J. P. Collins, P. A. Burrowes, K. R. Lips, K. R. Zamudio & J. E. Longcore, 2015. Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecology and Evolution 5: 4079–4097.CrossRefPubMedPubMedCentralGoogle Scholar
- Jenkinson, T. S., C. M. Betancourt-Román, C. Lambertini, A. Valencia-Aguilar, D. Rodriguez, C. H. L. Nunes-de-Almeida, J. Ruggeri, A. M. Belasen, D. S. Leite, K. R. Zamudio, J. E. Longcore, L. F. Toledo & T. Y. James, 2016. Amphibian-killing chytrid in Brazil comprises both locally endemic and globally expanding populations. Molecular Ecology 28: 1302–1311.Google Scholar
- Kilpatrick, A. M., C. J. Briggs & P. Daszak, 2010. The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends in Ecology & Evolution 30: 1–10.Google Scholar
- Lambertini, C., D. Rodriguez, F. B. Brito, D. S. Leite & L. F. Toledo, 2013. Diagnóstico do fungo quitrídio: Batrachochytrium dendrobatidis. Herpetologia Brasileira 2: 12–17.Google Scholar
- Lips, K. R., F. Brem, R. Brenes, J. D. Reeve, R. A. Alford, J. Voyles, C. Carey, L. Livo, A. P. Pessier & J. P. Collins, 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences USA 103: 3165–3170.CrossRefGoogle Scholar
- McDiarmid, R. W. & R. Altig, 1999. Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago.Google Scholar
- McKenzie, V. J., R. M. Bowers, N. Fierer, R. Knight & C. L. Lauber, 2011. Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. Multidisciplinary Journal of Microbial Ecology 6: 588–596.Google Scholar
- Mittermeier, C. G., W. R. Turner, F. W. Larsen, T. M. Brooks & C. Gascon, 2011. Global biodiversity conservation: the critical role of hotspots. In Zachos, F. E. & J. C. Habel (eds), Biodiversity Hotspots: Distribution and Protection of Priority Conservation Areas. Springer, Berlin: 3–22.CrossRefGoogle Scholar
- R Development Core Team, 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Austria.Google Scholar
- Rollins-Smith, L. A., 1998. Metamorphosis and the amphibian immune system. Immunological Reviews 166: 221–230Google Scholar
- Rowley, J. J. L. & R. A. Alford, 2013. Hot bodies protect amphibians against chytrid infection in nature. Nature 3: 1515.Google Scholar
- Salla, R. F., F. U. Gamero, L. R. Ribeiro, G. M. Rizzi, S. E. D. Medico, R. Z. Rissoli, C. A. Vieira, E. C. M. Silva-Zacarin, D. S. Leite, F. C. Addalla, L. F. Toledo & M. J. Costa, 2015. Cardiac adaptations of bullfrog tadpoles in response to chytrid infection. Journal of Experimental Zoology A 323: 487–496.CrossRefGoogle Scholar
- Scott, N. J., 1993. Postmetamorphic death syndrome. Froglog 7: 1–2.Google Scholar
- Ultsch, G. R., D. F. Bradford & J. Freda, 1999. Physiology: coping with the environment. In McDiarmid, R. W. & R. Altig (eds), Tadpoles: the Biology of Anuran Larvae. University of Chicago Press, Chicago: 215–239.Google Scholar