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EcoHealth

, Volume 13, Issue 1, pp 145–150 | Cite as

Invasion of the Fungal Pathogen Batrachochytrium dendrobatidis on California Islands

  • Tiffany A. Yap
  • Lauren Gillespie
  • Silas Ellison
  • Sandra V. Flechas
  • Michelle S. Koo
  • Ari E. Martinez
  • Vance T. VredenburgEmail author
Short Communication

Abstract

Batrachochytrium dendrobatidis (Bd), an amphibian fungal pathogen, has infected >500 species and caused extinctions or declines in >200 species worldwide. Despite over a decade of research, little is known about its invasion biology. To better understand this, we conducted a museum specimen survey (1910–1997) of Bd in amphibians on 11 California islands and found a pattern consistent with the emergence of Bd epizootics on the mainland, suggesting that geographic isolation did not prevent Bd invasion. We propose that suitable habitat, host diversity, and human visitation overcome isolation from the mainland and play a role in Bd invasion.

Keywords

amphibian pathogen Batrachochytrium dendrobatidis chytridiomycosis emerging infectious disease California islands 

Notes

Acknowledgments

This research was supported by a graduate fellowship from UCLA-Charles F. Scott Fellowship (TAY), National Science Foundation Post-doctoral Fellowship PRFB1309320 (AEM), and National Science Foundation IOS-1258133 (VTV). We thank the Museum of Vertebrate Zoology at UC Berkeley for access to their permanent collection and technical support. We thank the anonymous reviewers. Specimens examined are listed in the Supplemental Materials.

Supplementary material

10393_2015_1071_MOESM1_ESM.doc (193 kb)
Supplementary material 1 (DOC 193 kb)

References

  1. 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(2), 141–8. Doi: 10.3354/dao060141 CrossRefPubMedGoogle Scholar
  2. Bradford, D. F. (1991). Mass mortality and extinction in a high-elevation population of Rana muscosa. Journal of Herpetology, 25(2), 174–177.CrossRefGoogle Scholar
  3. Briggs, C. J., Knapp, RA, Vredenburg, VT. (2010). Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences of the United States of America, 107(21), 9695–9700. Doi: 10.1073/pnas.0912886107 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Catalina Island and Chamber of Commerce Visitors Bureau (2012) Monthly Visitor ReportGoogle Scholar
  5. Champely S (2015) pwr: Basic Functions for Power Analysis. R package version 1.1-2. http://CRAN.R-project.org/package=pwr
  6. Cheng, T. L., Rovito, S. M., Wake, D. B., & Vredenburg, V. T. (2011). Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America, 108(23), 9502–9507. Doi: 10.1073/pnas.1105538108 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Dorai-Raj S (2014) binom: Binomial Confidence Intervals for Several Parameterizations. R package version 1.1-1. http://CRAN.R-project.org/package=binom
  8. 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(1), 2–9. Doi: 10.1016/j.fbr.2007.02.002 CrossRefGoogle Scholar
  9. Fisher, M. C., Garner, T. W. J., & Walker, S. F. (2009). Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology, 63, 291–310. Doi: 10.1146/annurev.micro.091208.073435 CrossRefPubMedGoogle Scholar
  10. Fisher, M. C., Henk, D. A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S. L., & Gurr, S. J. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature, 484(7393), 186–94. Doi:  10.1038/nature10947 CrossRefPubMedGoogle Scholar
  11. Gray MJ, Brunner JL, Earl JE, Ariel E (2015) Design and analysis of ranavirus studies: surveillance and assessing risk. In: Ranaviruses, Springer International Publishing, pp 209–240Google Scholar
  12. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25(15), 1965–1978. Doi: 10.1002/joc.1276 CrossRefGoogle Scholar
  13. Huss, M., Huntley, L., Vredenburg, V., Johns, J., & Green, S. (2013). Prevalence of Batrachochytrium dendrobatidis in 120 archived specimens of Lithobates catesbeianus (American bullfrog) collected in California, 1924-2007. EcoHealth, 10(4), 339–343. Doi: 10.1007/s10393-013-0895-6 CrossRefPubMedGoogle Scholar
  14. Johnson, M. L., & Speare, R. (2003). Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases 9(8), 1–4.CrossRefGoogle Scholar
  15. Kolby, J. E., Ramirez, S. D., Berger, L., Richards-Hrdlicka, K. L., Jocque, M., & Skerratt, L. F. (2015). Terrestrial dispersal and potential environmental transmission of the amphibian chytrid fungus (Batrachochytrium dendrobatidis). Plos One, 10(4), e0125386. Doi: 10.1371/journal.pone.0125386 CrossRefPubMedPubMedCentralGoogle Scholar
  16. National Parks Conservation Association (2010) Alcatraz Island Challenges and Highlights. State of the Parks ProgramGoogle Scholar
  17. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, Fisher MC et al. (2013) Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PloS One 8(2):e56802. Doi: 10.1371/journal.pone.0056802 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Padgett-Flohr, G. E., & Hopkins, R. L. (2009). Batrachochytrium dendrobatidis, a novel pathogen approaching endemism in central California. Diseases of Aquatic Organisms, 83(1), 1–9. Doi: 10.3354/dao02003 CrossRefPubMedGoogle Scholar
  19. Phillips S, Dudík M, Schapire R (2004) A maximum entropy approach to species distribution modeling. Proceedings of the Twenty-First International Conference on Machine Learning 62:655–662. doi: 10.1145/1015330.1015412 Google Scholar
  20. Picco, A. M., & Collins, J. P. (2008). Amphibian commerce as a likely source of pathogen pollution. Conservation Biology , 22(6), 1582–9. Doi: 10.1111/j.1523-1739.2008.01025.x CrossRefPubMedGoogle Scholar
  21. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
  22. Richards-Hrdlicka, K. L. (2012). Extracting the amphibian chytrid fungus from formalin-fixed specimens. Methods in Ecology and Evolution3(5), 842–849CrossRefGoogle Scholar
  23. Rödder D., Kielgast, J., Bielby, J., Schmidtlein, S., Bosch, J., Garner, T. W. J., Lötters, S., et al. (2009). Global amphibian extinction risk assessment for the panzootic chytrid fungus. Diversity, 1(1), 52–66. Doi: 10.3390/d1010052 CrossRefGoogle Scholar
  24. Rodriguez, D., Becker, C. G., Pupin, N. C., Haddad, C. F. B., & Zamudio, K. R. (2014). Long-term endemism of two highly divergent lineages of the amphibian-killing fungus in the Atlantic Forest of Brazil. Molecular Ecology, 23(4), 774–787. Doi: 10.1111/mec.12615 CrossRefPubMedGoogle Scholar
  25. Schloegel, L. M., Toledo, L. F., Longcore, J. E., Greenspan, S. E., Vieira, C. A., Lee, M., James, T. Y, et al. (2012). Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology, 21(21), 5162–5177. Doi: 10.1111/j.1365-294X.2012.05710.x CrossRefPubMedGoogle Scholar
  26. Skerratt, L. F., Berger, L., Speare, R., Cashins, S., McDonald, K. R., Phillott, A. D., Kenyon, N et al. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth, 4(2), 125–134. Doi: 10.1007/s10393-007-0093-5 CrossRefGoogle Scholar
  27. Stockwell, M. P., Clulow, J., & Mahony, M. J. (2015a). Evidence of a salt refuge: chytrid infection loads are suppressed in hosts exposed to salt. Oecologia, 177(3), 901-910.CrossRefPubMedGoogle Scholar
  28. Stockwell, M. P., Storrie, L. J., Pollard, C. J., Clulow, J., & Mahony, M. J. (2015b). Effects of pond salinization on survival rate of amphibian hosts infected with the chytrid fungus. Conservation Biology, 29(2), 391-399.CrossRefPubMedGoogle Scholar
  29. Talley, B. L., Muletz, C. R., Vredenburg, V. T., Fleischer, R. C., & Lips, K. R. (2015). A century of Batrachochytrium dendrobatidis in Illinois amphibians (1888–1989). Biological Conservation, 182, 254–261. Doi:  10.1016/j.biocon.2014.12.007 CrossRefGoogle Scholar
  30. Une, Y., Kadekaru, S., Tamukai, K., Goka, K., & Kuroki, T. (2008). First report of spontaneous chytridiomycosis in frogs in Asia. Diseases of Aquatic Organisms, 82(2), 157–160. Doi: 10.3354/dao02006 CrossRefPubMedGoogle Scholar
  31. U.S. Census Bureau (2010) General population and housing characteristics. http://factfinder.census.gov. Accessed May 8 2015
  32. Van Rooij, P., Martel, A., Nerz, J., Voitel, S., Van Immerseel, F., Haesebrouck, F., & Pasmans, F. (2011). Detection of Batrachochytrium dendrobatidis in Mexican bolitoglossine salamanders using an optimal sampling protocol. EcoHealth, 8(2), 237–243. Doi: 10.1007/s10393-011-0704-z CrossRefPubMedGoogle Scholar
  33. Vredenburg, V. T., Felt, S. A., Morgan, E. C., McNally, S. V. G., Wilson, S., & Green, S. L. (2013). Prevalence of Batrachochytrium dendrobatidis in Xenopus collected in Africa (1871-2000) and in California (2001-2010). PLoS One, 8(5), e63791. Doi: 10.1371/journal.pone.0063791 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 United States of America, 107(21), 9689–94. Doi: 10.1073/pnas.0914111107 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 United States of America, 105, 11466–11473. Doi: 10.1073/pnas.0801921105 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Yap, T. A., Koo, M. S., Ambrose, R. F., Wake, D. B., & Vredenburg, V. T. (2015). Averting a North American biodiversity crisis. Science, 349(6247), 481–482. Doi: 10.1126/science.aab1052 CrossRefPubMedGoogle Scholar

Copyright information

© International Association for Ecology and Health 2015

Authors and Affiliations

  • Tiffany A. Yap
    • 1
    • 2
    • 3
  • Lauren Gillespie
    • 3
  • Silas Ellison
    • 3
  • Sandra V. Flechas
    • 4
  • Michelle S. Koo
    • 2
  • Ari E. Martinez
    • 3
  • Vance T. Vredenburg
    • 2
    • 3
    Email author
  1. 1.Institute of the Environment and SustainabilityUniversity of CaliforniaLos AngelesUSA
  2. 2.Museum of Vertebrate ZoologyUniversity of CaliforniaBerkeleyUSA
  3. 3.Department of BiologySan Francisco State UniversitySan FranciscoUSA
  4. 4.Department of Biological SciencesUniversidad de los AndesBogotáColombia

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