, Volume 806, Issue 1, pp 303–311 | Cite as

Stream tadpoles present high prevalence but low infection loads of Batrachochytrium dendrobatidis (Chytridiomycota)

  • Joice RuggeriEmail author
  • Luís Felipe Toledo
  • Sergio Potsch de Carvalho-e-Silva
Primary Research Paper


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.


Anuran 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.

Supplementary material

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Supplementary material 1 (PDF 112 kb)
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Supplementary material 2 (PDF 17 kb)
10750_2017_3367_MOESM3_ESM.pdf (69 kb)
Supplementary material 3 (PDF 69 kb)


  1. Becker, C. G., D. Rodriguez, C. Lambertini, L. F. Toledo & C. F. B. Haddad, 2015. Historical dynamics of Batrachochytrium dendrobatidis in Amazonia. Ecography 38: 1–7.CrossRefGoogle Scholar
  2. 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
  3. Berger, L., A. D. Hyatt, R. Speare & J. E. Longcore, 2005. Life cycle of the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 68: 51–63.CrossRefPubMedGoogle Scholar
  4. Blaustein, A., J. M. Romansic, E. A. Schessele, B. A. Han, A. P. Pessier & J. E. Longcore, 2005. Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conservation Biology 19: 1460–1468.CrossRefGoogle Scholar
  5. 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
  6. Boyle, D. G., D. B. Boyle, V. Olsen, J. A. T. Morgan & A. D. Hyatt, 2004. Rapid quantitative detection of chytridiomycosis. Diseases of Aquatic Organisms 60: 141–148.CrossRefPubMedGoogle Scholar
  7. Briggs, C. J., R. A. Knapp & V. T. Vredenburg, 2010. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences USA 107: 9695–9700.CrossRefGoogle Scholar
  8. Catenazzi, A., R. Von May & V. T. Vredenburg, 2013. High prevalence of infection in tadpoles increases vulnerability to fungal pathogen in high-Andean amphibians. Biological Conservation 159: 413–421.CrossRefGoogle Scholar
  9. Carey, C., J. E. Bruzgul, L. J. Livo, M. L. Walling, K. A. Kuehl, B. F. Dixon, A. P. Pessier, R. D. Alford & K. B. Rogers, 2006. Experimental exposures of Boreal Toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3: 5–21.CrossRefGoogle Scholar
  10. Carvalho, T., C. G. Becker & L. F. Toledo, 2017. Historical amphibian declines extinctions in Brazil linked to chytridiomycosis. Proceedings of the Royal Society B 284: 20162254.CrossRefPubMedGoogle Scholar
  11. 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
  12. Corey, S. J. & T. A. Waite, 2008. Phylogenetic autocorrelation of extinction threat in globally imperiled amphibians. Diversity and Distribution 14: 614–629.CrossRefGoogle Scholar
  13. Courtois, E. A., A. Loyau, M. Bourgain & D. S. Schmeller, 2016. Initiation of Batrachochytrium dendrobatidis infection in the absence of physical contact with infected hosts – a field study in a high altitude lake. Oikos. doi: 10.1111/oik.03462.Google Scholar
  14. Daszak, P., A. A. Cunningham & A. D. Hyatt, 2003. Infectious disease and amphibian population declines. Diversity and Distribution 9: 141–150.CrossRefGoogle Scholar
  15. Fellers, G. M., D. E. Green & J. E. Longcore, 2001. Oral Chytridiomycosis in the mountain yellow-legged frog (Rana muscosa). Copeia 2001: 945–953.CrossRefGoogle Scholar
  16. Garner, T. W. J., S. Walker, J. Bosch, S. Leech, J. M. Rowcliffe, A. A. Cunningham & M. C. Fisher, 2009. Life tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118: 783791.CrossRefGoogle Scholar
  17. Gervasi, S., C. Gondhalekar, D. H. Olson & A. R. Blaustein, 2013. Host identity matters in the Amphibian-Batrachochytrium dendrobatidis system: fine-scale patterns of variation in responses to a multi-host pathogen. PloS ONE 8: e54490.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Grant, E. H. C., L. L. Bailey, J. L. Ware & K. L. Duncan, 2008. Prevalence of the amphibian pathogen Batrachochytrium dendrobatidis in stream and wetland amphibians in Maryland, USA. Applied Herpetology 5: 233–241.CrossRefGoogle Scholar
  19. Greenspan, S. E., A. J. Calhoun, J. E. Longcore & M. G. Levy, 2012. Transmission of Batrachochytrium dendrobatidis to wood frogs (Lithobates sylvaticus) via a bullfrog (L. catesbeianus) vector. Journal of Wildlife Diseases 48: 575–582.CrossRefPubMedGoogle Scholar
  20. 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
  21. 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
  22. Hagman, M. & R. A. Alford, 2015. Patterns of Batrachochytrium dendrobatidis transmission between tadpoles in high-elevation rainforest in tropical Australia. Diseases of Aquatic Organisms 115: 213–221.CrossRefPubMedGoogle Scholar
  23. Haydon, D. T., S. Cleaveland, L. H. Taylor & M. K. Laurenson, 2002. Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8: 1468–1473.CrossRefPubMedGoogle Scholar
  24. Hero, J. M., S. E. Williams & W. E. Magnusson, 2005. Ecological traits of declining amphibians in upland areas of Eastern Australia. Journal of Zoology 267: 221–232.CrossRefGoogle Scholar
  25. 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
  26. 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
  27. 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
  28. 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
  29. Johnson, M. L. & R. Speare, 2003. Survival of Batrachochytrium dendrobatidis in water: quarantine and control implications. Emerging Infectious Diseases 9: 922–925.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Johnson, M. L. & R. Speare, 2005. Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Diseases of Aquatic Organisms 65: 181–186.CrossRefPubMedGoogle Scholar
  31. 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
  32. Knapp, R. A. & J. A. T. Morgan, 2006. Tadpole mouthpart depigmentation as an accurate indicator of chytridiomycosis, an emerging disease of amphibians. Copeia 2006: 188–197.CrossRefGoogle Scholar
  33. Kolby, J. E., S. D. Ramirez, L. Berger, K. L. Richards-Hrdlicka, M. Jocque & L. F. Skerratt, 2015a. Terrestrial dispersion and potential environmental transmission of the amphibian chytrid fungus (Batrachochytrium dendrobatidis). PLoS ONE 10: e0125386.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kolby, J. E., S. D. Ramirez, L. Berger, D. W. Griffin, M. Jocque & L. F. Skerratt, 2015b. Presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) in rainwater suggests aerial dispersal is possible. Aerobiologia. doi: 10.1007/s10453-015-9374-6.Google Scholar
  35. Kriger, K. M. & J. M. Hero, 2007. The chytrid fungus Batrachochytrium dendrobatidis in non-randomly distributed across amphibian breeding habitats. Diversity and Distributions 13: 781–788.CrossRefGoogle Scholar
  36. Kriger, K. M., J. M. Hero & K. J. Ashton, 2006. Cost efficiency in the detection of chytridiomycosis using PCR assay. Diseases of Aquatic Organisms 71: 149–154.CrossRefPubMedGoogle Scholar
  37. Kueneman, J. G., D. C. Woodhams, W. Van Treuren, H. M. Archer, R. Knight & V. J. McKenzie, 2016. Inhibitory bacteria reduce fungi on early life stages of Colorado boreal toads (Anaxyrus boreas). The ISME Journal 10: 934–944.CrossRefPubMedGoogle Scholar
  38. 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
  39. 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
  40. Longcore, J. E., A. P. Pessier & D. K. Nichols, 1999. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91: 219–227.CrossRefGoogle Scholar
  41. McDiarmid, R. W. & R. Altig, 1999. Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago.Google Scholar
  42. 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
  43. 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
  44. Padgett-Flohr, G. E. & R. L. Hopkins, 2010. Landscape epidemiology of Batrachochytrium dendrobatidis in central California. Ecography 33: 688–697.CrossRefGoogle Scholar
  45. Peterson, A. C. & V. J. McKenzie, 2014. Investigating differences across host species and scales to explain the distribution of the amphibian pathogen Batrachochytrium dendrobatidis. PLoS ONE 9: e107441.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Piotrowski, J. S., S. L. Annis & J. E. Longcore, 2004. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96: 9–15.CrossRefPubMedGoogle Scholar
  47. R Development Core Team, 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Austria.Google Scholar
  48. Rachowicz, L. J. & V. T. Vredenburg, 2004. Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Diseases of Aquatic Organisms 61: 75–83.CrossRefPubMedGoogle Scholar
  49. Richards-Zawacki, C. L., 2010. Thermoregulatory behavior affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proceedings of the Royal Society of London B 277: 519–528.CrossRefGoogle Scholar
  50. Rollins-Smith, L. A., 1998. Metamorphosis and the amphibian immune system. Immunological Reviews 166: 221–230Google Scholar
  51. Rowley, J. J. L. & R. A. Alford, 2007. Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. Diseases of Aquatic Organisms 677: 1–9.CrossRefGoogle Scholar
  52. Rowley, J. J. L. & R. A. Alford, 2013. Hot bodies protect amphibians against chytrid infection in nature. Nature 3: 1515.Google Scholar
  53. Ruano-Farjado, G., L. F. Toledo & T. Mott, 2016. Jumping into a trap: high prevalence of chytrid fungus in the preferred microhabitats of a bromeliad-specialist frog. Diseases of Aquatic Organisms 121: 223–232.CrossRefGoogle Scholar
  54. 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
  55. Scott, N. J., 1993. Postmetamorphic death syndrome. Froglog 7: 1–2.Google Scholar
  56. Smith, K. G., C. Weldon, W. Conradie & L. H. D. Preez, 2007. Relationships among size, development, and Batrachochytrium dendrobatidis infection in African tadpoles. Diseases of Aquatic Organisms 74: 159–164.CrossRefPubMedGoogle Scholar
  57. Toledo, L. F., F. B. Britto, O. G. S. Araújo, L. M. O. Giasson & C. F. B. Haddad, 2006. The occurrence of Batrachochytrium dendrobatidis in Brazil and the inclusion of 17 new cases of infection. South American Journal of Herpetology 1: 185–191.CrossRefGoogle Scholar
  58. 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
  59. Valencia-Aguilar, A., G. Ruano-Fajardo, C. Lambertini, D. S. Leite, L. F. Toledo & T. Mott, 2015. Chytrid fungus acts as a generalist pathogen infecting species-rich amphibian families in Brazilian rainforests. Diseases of Aquatic Organisms 114: 61–67.CrossRefPubMedGoogle Scholar
  60. Valencia-Aguilar, A., L. F. Toledo, M. V. Vital & T. Mott, 2016. Seasonality, environmental factors, and host behavior linked to disease risk in stream-dwelling tadpoles. Herpetologica 72: 98–106.CrossRefGoogle Scholar
  61. Vieira, C. A., L. F. Toledo, J. E. Longcore & J. R. Longcore, 2013. Body length of Hylodes cf. ornatus and Lithobates catesbeianus tadpoles, depigmentation of mouthparts, and presence of Batrachochytrium dendrobatidis are related. Brazilian Journal of Biology 73: 195–199.CrossRefGoogle Scholar
  62. Wells, K. D., 2007. The ecology and behavior of amphibians. University of Chicago Press, Illinois.CrossRefGoogle Scholar
  63. Woodhams, D. C. & R. A. Alford, 2005. Ecology of chytridiomycosis in rainforest stream frog assemblage of tropical Queensland. Conservation Biology 19: 449–1459.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Joice Ruggeri
    • 1
    • 3
    Email author
  • Luís Felipe Toledo
    • 2
  • Sergio Potsch de Carvalho-e-Silva
    • 3
  1. 1.Museu Nacional, Universidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Laboratório de História Natural de Anfíbios Brasileiros (LaHNAB), Departamento de Biologia Animal, Instituto de BiologiaUniversidade Estadual de CampinasCampinasBrazil
  3. 3.Instituto de BiologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil

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