Presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) in rainwater suggests aerial dispersal is possible

Abstract

Global spread of the pathogenic amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) may involve dispersal mechanisms not previously explored. Weather systems accompanied by strong wind and rainfall have been known to assist the dispersal of microbes pathogenic to plants and animals, and we considered a similar phenomenon might occur with Bd. We investigated this concept by sampling rainwater from 20 precipitation events for the presence of Bd in Cusuco National Park, Honduras: a site where high Bd prevalence was previously detected in stream-associated amphibians. Quantitative PCR analysis confirmed the presence of Bd in rainwater in one (5 %) of the weather events sampled, although viability cannot be ascertained from molecular presence alone. The source of the Bd and distance that the contaminated rainwater traveled could not be determined; however, this collection site was located approximately 600 m from the nearest observed perennial river by straight-line aerial distance. Although our results suggest atmospheric Bd dispersal is uncommon and unpredictable, even occasional short-distance aerial transport could considerably expand the taxonomic diversity of amphibians vulnerable to exposure and at risk of decline, including terrestrial and arboreal species that are not associated with permanent water bodies.

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References

  1. Barker, J., & Jones, M. (2005). The potential spread of infection caused by aerosol contamination of surfaces after flushing a domestic toilet. Journal of Applied Microbiology, 99, 339–347.

    CAS  Article  Google Scholar 

  2. Berger, L., Speare, R., Daszak, P., Green, D. E., Cunningham, A. A., Goggin, C. L., 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 Sciences USA, 95, 9031–9036.

  3. Berger, L., Speare, R., Hines, H. B., Marantelli, G., Hyatt, A. D., McDonald, K. R., et al. (2004). Effects of season and temperature on mortality in amphibians due to chytridiomycosis. Australian Veterinary Journal, 82, 434–439.

    CAS  Article  Google Scholar 

  4. Blooi, M., Martel, A., Vercammen, F., & Pasmans, F. (2013). Combining ethidium monoazide treatment with real-time PCR selectively quantifies viable Batrachochytrium dendrobatidis cells. Fungal Biology, 117, 56–162.

    Article  Google Scholar 

  5. Boyle, D. G., Boyle, D. B., Olsen, V., Morgan, J. A. T., & Hyatt, A. D. (2004). Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms, 60, 133–139.

    Article  Google Scholar 

  6. Caruso, N. M., & Lips, K. R. (2013). Truly enigmatic declines in terrestrial salamander populations in Great Smoky Mountains National Park. Diversity and Distributions, 19, 34–48.

    Article  Google Scholar 

  7. Chatigny, M. A., Dimmick, R. L., & Harrington, J. B. (1979). Deposition. In R. L. Edmonds (Ed.), Aerobiology, a systems approach (pp. 111–150). Hutchinson and Ross: Dowden.

    Google Scholar 

  8. Chestnut, T., Anderson, C., Popa, R., Blaustein, A. R., Voytek, M., et al. (2014). Heterogeneous occupancy and density estimates of the pathogenic fungus Batrachochytrium dendrobatidis in waters of North America. PLoS One, 9, e106790. doi:10.1371/journal.pone.0106790.

    Article  Google Scholar 

  9. Cummer, M., Green, D., & O’Neill, E. (2005). Aquatic chytrid pathogen detected in terrestrial plethodontid salamander. Herpetological Review, 36, 248–249.

    Google Scholar 

  10. Fellers, G. M., Bradford, D. F., Pratt, D., & Wood, L. L. (2007). Demise of repatriated populations of mountain yellow-legged frogs (Rana muscosa) in the Sierra Nevada of California. Herpetological Conservation and Biology, 2, 5–21.

    Google Scholar 

  11. Fisher, M. C., & Garner, T. W. J. (2007). The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biology Reviews, 21, 2–9.

    Article  Google Scholar 

  12. Garcia, G., Lopez, J., Fa, J. E., & Gray, G. A. L. (2009). Chytrid fungus strikes mountain chickens in Montserrat. Oryx, 4, 323–328.

    Google Scholar 

  13. Garmyn, A., Van Rooij, P., Pasmans, F., Hellebuyck, T., Van Den Broeck, W., Haesebrouck, F., et al. (2012). Waterfowl: Potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLoS ONE, 7, e35038.

  14. Gloster, J. (1982). Risk of airborne spread of foot-and-mouth disease from the continent to England. Veterinary Record, 111, 290–295.

    CAS  Article  Google Scholar 

  15. Gottwald, T. R., & Irey, M. (2007). Post-hurricane analysis of citrus canker II: Predictive model estimation of disease spread and area potentially impacted by various eradication protocols following catastrophic weather events. Plant Health Progress,. doi:10.1094/PHP-2007-0906-01-RV.

    Google Scholar 

  16. Gower, D. J., Doherty-Bone, T., Loader, S. P., Wilkinson, M., Kouete, M. T., Tapley, B., et al. (2013). Batrachochytrium dendrobatidis infection and lethal chytridiomycosis in caecilian amphibians (Gymnophiona). EcoHealth,. doi:10.1007/s10393-013-0831-9.

    Google Scholar 

  17. Griffin, D. W. (2007). Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clinical Microbiology Reviews, 20, 459–477.

    Article  Google Scholar 

  18. Hyman, O. J., & Collins, J. P. (2011). Evaluation of a filtration-based method for detecting Batrachochytrium dendrobatidis in natural bodies of water. Diseases of Aquatic Organisms, 97, 185–195.

    Article  Google Scholar 

  19. Irey, M., Gottwald, T. R., Graham, J. H., Riley, T. D., & Carlton, G. (2006). Post-hurricane analysis of citrus canker spread and progress towards the development of a predictive model to estimate disease spread due to catastrophic weather events. Plant Health Progress,. doi:10.1094/PHP-2006-0822-01-RS.

    Google Scholar 

  20. Johnson, M. L., & Speare, R. (2003). Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases, 9, 922–925.

    Article  Google Scholar 

  21. Johnson, M.L., & Speare, R. (2005). Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Diseases of Aquatic Organisms, 65, 181–186.

  22. Kellogg, C. A., & Griffin, D. W. (2006). Aerobiology and the global transport of desert dust. Trends in Ecology and Evolution, 21, 638–644.

    Article  Google Scholar 

  23. Kirshtein, J. D., Anderson, C. W., Wood, J. S., Longcore, J. E., & Voytek, M. A. (2007). Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. Diseases of Aquatic Organisms, 77, 11–15.

    CAS  Article  Google Scholar 

  24. Kolby, J. E., Padgett-Flohr, G. E., & Field, R. (2010). Amphibian chytrid fungus Batrachochytrium dendrobatidis in Cusuco national Park, Honduras. Diseases of Aquatic Organisms, 92, 245–251.

    Article  Google Scholar 

  25. Kolby, J. E., Smith, K. M., Berger, L., Karesh, W. B., Preston, A., Pessier, A. P., et al. (2014). First evidence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) and ranavirus in Hong Kong amphibian trade. PLoS One, 9, e90750. doi:10.1371/journal.pone.0090750.

    Article  Google Scholar 

  26. LaMarca, E., Lips, K. R., Lotters, S., Puschendorf, R., Ibanez, R., Rueda-Almonacid, J. V., et al. (2005). Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae : Atelopus). Biotropica, 37, 190–201.

    Article  Google Scholar 

  27. Laurance, W. F. (1996). Catastrophic declines of Australian rainforest frogs: Is unusual weather responsible? Biological Conservation, 77, 203–212.

    Article  Google Scholar 

  28. Lips, K. R., Diffendorfer, J., Mendelson, J. R., & Sears, M. W. (2008). Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biology, 6, e72.

    Article  Google Scholar 

  29. Longcore, J. E., Pessier, A. P., & Nichols, D. K. (1999). Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia, 91, 219–227.

    Article  Google Scholar 

  30. Longo, A. V., & Burrowes, P. A. (2010). Persistence with chytridiomycosis does not assure survival of direct-developing frogs. EcoHealth, 7, 185–195.

    Article  Google Scholar 

  31. Longo, A. V., Rodriguez, D., da Silva Leite, D., Toledo, L. F., Mendoza Almeralla, C., et al. (2013). ITS1 copy number varies among Batrachochytrium dendrobatidis strains: Implications for qPCR estimates of infection intensity from field-collected amphibian skin swabs. PLoS One, 8, e59499. doi:10.1371/journal.pone.0059499.

    CAS  Article  Google Scholar 

  32. McMahon, T. A., Brannelly, L. A., Chatfield, M. W. H., Johnson, P. T. J., Joseph, M. B., McKenzie, V. J., et al. (2013). Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. Proceedings of the National Academy of Sciences USA, 110, 210–215.

  33. Murray, K. A., Rosauer, D., McCallum, H., & Skerratt, L. F. (2011). Integrating species traits with extrinsic threats: Closing the gap between predicting and preventing species declines. Proceedings of the Royal Society B Biological Sciences, 278, 1515–1523.

    Article  Google Scholar 

  34. Olson, D. H., Aanensen, D. M., Ronnenberg, K. L., Powell, C. I., Walker, S. F., Bielby, J., et al. (2013). Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS One, 8, e56802.

    CAS  Article  Google Scholar 

  35. Piotrowski, J. S., Annis, S. L., Longcore, J. F. (2004). Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia, 96, 9–15.

  36. Puschendorf, R., & Bolanos, F. (2006). Detection of Batrachochytrium dendrobatidis in Eleutherodactylus fitzingeri: Effects of skin sample location and histologic stain. Journal of Wildlife Diseases, 42, 301–306.

    Article  Google Scholar 

  37. Reeder, N. M., Pessier, A. P., & Vredenburg, V. T. (2012). A reservoir species for the emerging amphibian pathogen Batrachochytrium dendrobatidis thrives in a landscape decimated by disease. PLoS One, 7, e33567.

    CAS  Article  Google Scholar 

  38. Rosenblum, E. B., James, T. Y., Zamudio, K. R., Poorten, T. J., Ilut, D., Rodriguez, D., et al. (2013). Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proceedings of the National Academy of Sciences USA, 110, 9385–9390.

  39. Schloegel, L. M., Toledo, L. F., Longcore, J. E., Greenspan, S. E., Vieira, C. A., Lee, M., et al. (2012). Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology, 21, 5162–5177.

    Article  Google Scholar 

  40. Schoegel, L. M., Hero, J. M., Berger, L., Speare, R., McDonald, K., & Daszak, P. (2006). The decline of the sharp-snouted day frog (Taudactylus acutirostris): The first documented case of extinction by infection in a free-ranging wildlife species? EcoHealth, 3, 35–40.

    Article  Google Scholar 

  41. Seimon, T. A., Seimon, A., Daszak, P., Halloy, S. R. P., Schloegel, L. M., Aguilar, C. A., et al. (2007). Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Global Change Biology, 13, 288–299.

    Article  Google Scholar 

  42. Skerratt, L. F., Berger, L., Speare, R., Cashins, S., McDonald, K. R., Phillott, A. D., et al. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth, 4, 125–134.

    Article  Google Scholar 

  43. Skerratt, L. F., McDonald, K. R., Hines, H. B., Berger, L., Mendez, D., Phillott, A. D., et al. (2010). Application of the survey protocol for chytridiomycosis to Queensland, Australia. Diseases of Aquatic Organisms, 92, 117–129.

    Article  Google Scholar 

  44. Smith, K. G., et al. (2007). Use of quantitative PCR assay for amphibian chytrid detection: Comment on Kriger et al. (2006a,b). Diseases of Aquatic Organisms, 73, 253–255.

    CAS  Article  Google Scholar 

  45. Vredenburg, V. T., Knapp, R. A., Tunstall, T. S., & Briggs, C. J. (2010). Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences of the USA, 107, 9689–9694.

    CAS  Article  Google Scholar 

  46. Wake, D. B., & Vredenburg, V. T. (2008). Colloquium paper: Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences of the USA, 105, 11466–11473.

    CAS  Article  Google Scholar 

  47. Weinstein, S. B. (2009). An aquatic disease on a terrestrial salamander: Individual and population level effects of the amphibian chytrid fungus, Batrachochytrium dendrobatidis, on Batrachoseps attenuatus (Plethodontidae). Copeia, 4, 653–660.

    Article  Google Scholar 

  48. Wilson, L. D., & McCranie, J. R. (2004). The herpetofauna of Parque Nacional El Cusuco, Honduras (reptilia, amphibia). Herpetological Bulletin, 87, 13–24.

    Google Scholar 

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Acknowledgments

This research was supported, in part, by the Mohamed Bin Zayed Species Conservation Fund, Rufford Small Grants for Nature Conservation, Chicago Zoological Society/Chicago Board of Trade Endangered Species Fund, and the Columbus Zoo and Aquarium. Sampling was performed in Cusuco National Park with permission from the Instituto Nacional de Conservacion y Desarollo Forestal Areas Protegidas y Vida Silvestre (ICF) as part of the long-term biodiversity monitoring program performed by Operation Wallacea. We thank Operation Wallacea for orchestrating fieldwork logistics and are grateful for the many volunteers and local guides who assisted with sample collection. We also thank D. Calhoun, K. Richards-Hrdlicka, J. Kirshtein, and B. Scheele for their helpful advice on field methods and earlier manuscript drafts. Any use of trade, firm, or product names in this manuscript is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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The authors declare that they have no conflict of interest.

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Correspondence to Jonathan E. Kolby.

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Kolby, J.E., Ramirez, S.D., Berger, L. et al. Presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) in rainwater suggests aerial dispersal is possible. Aerobiologia 31, 411–419 (2015). https://doi.org/10.1007/s10453-015-9374-6

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Keywords

  • Amphibian chytrid fungus
  • Batrachochytrium dendrobatidis
  • Chytridiomycosis
  • Dispersal
  • Atmospheric
  • Rain