Advertisement

EcoHealth

, Volume 14, Issue 1, pp 155–161 | Cite as

Recent Emergence of a Chytrid Fungal Pathogen in California Cascades Frogs (Rana cascadae)

  • Marina E. De León
  • Vance T. Vredenburg
  • Jonah Piovia-ScottEmail author
Original Contribution

Abstract

The pathogenic fungus Batrachochytrium dendrobatidis (Bd) has been associated with global amphibian declines, but it is often difficult to discern the relative importance of Bd as a causal agent in declines that have already occurred. Retrospective analyses of museum specimens have allowed researchers to associate the timing of Bd arrival with the timing of past amphibian declines. Cascades frogs (Rana cascadae) have experienced dramatic declines in northern California, but it is not clear whether the onset of these declines corresponds to the arrival of Bd. We used quantitative real-time PCR assays of samples collected from museum specimens to determine historical Bd prevalence in the northern California range of Cascades frogs. We detected Bd in 13 of 364 (3.5%) Cascades frog specimens collected between 1907 and 2003, with the first positive result from 1978. A Bayesian analysis suggested that Bd arrived in the region between 1973 and 1978, which corresponds well with the first observations of declines in the 1980s.

Keywords

chytridiomycosis museum specimen quantitative PCR Klamath Mountains Cascade Mountains 

Notes

Acknowledgements

This project was supported by a grant from the United States Fish and Wildlife Service Contaminants Branch to JPS and grants from the National Science Foundation to VV (DEB-11202283 and IOS-1258133). We thank Janet Foley for providing access to her laboratory, Ben Phillips for providing advice on statistical analyses, and Karen Pope for providing comments on a draft of the manuscript; Colleen Kamoroff helped assemble the list of samples, Laurence Cyril Henson helped create the map, and David Tran helped with computing.

References

  1. 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 Sciences of the United States of America 95:9031-9036. doi: 10.1073/pnas.95.15.9031 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Boyle DG, Boyle DB, Olsen V, Morgan JAT, and 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. doi: 10.3354/dao060141 CrossRefPubMedGoogle Scholar
  3. Briggs CJ, Knapp RA, and 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 107:9695-9700. doi: 10.1073/pnas.0912886107 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cheng TL, Rovito SM, Wake DB, and 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 Sciences 108:9502-9507. doi: 10.1073/pnas.1105538108 CrossRefGoogle Scholar
  5. Davidson C (2004) Declining downwind: Amphibian population declines in California and historical pesticide use. Ecological Applications 14:1892-1902. doi: 10.1890/03-5224 CrossRefGoogle Scholar
  6. Davidson C, Stanley K, and Simonich SM (2012) Contaminant residues and declines of the Cascades frog (Rana cascadae) in the California Cascades, USA. Environ Toxicol Chem 31:1895-1902. doi: 10.1002/etc.1902 CrossRefPubMedGoogle Scholar
  7. Fellers GM, and Drost CA (1993) Disappearance of the Cascades frog Rana cascadae at the southern end of its range, California, USA. Biological Conservation 65:177-181. doi: 10.1016/0006-3207(93)90447-9 CrossRefGoogle Scholar
  8. Fellers GM, Pope KL, Stead JE, Koo MS, and Welsh HH (2008) Turning population trend monitoring into active conservation: Can we save the Cascades frog (Rana Cascadae) in the Lassen region of California? Herpetological Conservation and Biology 3:28-39.Google Scholar
  9. Garcia TS, Romansic JM, and Blaustein AR (2006) Survival of three species of anuran metamorphs exposed to UV-B radiation and the pathogenic fungus Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 72:163-169. doi: 10.3354/dao072163 CrossRefPubMedGoogle Scholar
  10. Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S, Cunningham AA, et al. (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters 2:455-459. doi: 10.1098/rsbl.2006.0494 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Heyer WR, Donnelly MA, McDiarmid RW, Hayek LC, and Foster M (1994). Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithsonian Institution Press, Washington, DC.Google Scholar
  12. Huss M, Huntley L, Vredenburg V, Johns J, and Green S (2013) Prevalence of Batrachochytrium dendrobatidis in 120 archived specimens of Lithobates catesbeianus (American bullfrog) collected in California, 1924-2007. Ecohealth 10:339-343. doi: 10.1007/s10393-013-0895-6 CrossRefPubMedGoogle Scholar
  13. 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. doi: 10.3354/dao073175 CrossRefPubMedGoogle Scholar
  14. 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 Sciences of the United States of America 103:3165-3170. doi: 10.1073/pnas.0506889103 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Lips KR, Diffendorfer J, Mendelson JR, and Sears MW (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. Plos Biology 6:e72. doi: 10.1371/journal.pbio.0060072 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Padgett-Flohr GE, and Hopkins RL (2009) Batrachochytrium dendrobatidis, a novel pathogen approaching endemism in central California. Diseases of Aquatic Organisms 83:1-9. doi: 10.3354/dao02003 CrossRefPubMedGoogle Scholar
  17. Phillips BL, and Puschendorf R (2013) Do pathogens become more virulent as they spread? Evidence from the amphibian declines in Central America. Proceedings of the Royal Society B: Biological Sciences 280:20131290. doi: 10.1098/rspb.2013.1290 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Piovia-Scott J, Pope K, Worth SJ, Rosenblum EB, Poorten TJ, Refsnider J, et al. (2015) Correlates of virulence in a frog-killing fungal pathogen: evidence from a California amphibian decline. ISME J 9:1570-1578. doi: 10.1038/ismej.2014.241 CrossRefPubMedGoogle Scholar
  19. Piovia-Scott J, Pope KL, Lawler SP, Cole EM, and Foley JE (2011) Factors related to the distribution and prevalence of the fungal pathogen Batrachochytrium dendrobatidis in Rana cascadae and other amphibians in the Klamath Mountains. Biological Conservation 144:2913-2921. doi: 10.1016/j.biocon.2011.08.008 CrossRefGoogle Scholar
  20. Pope KL (2008) Assessing changes in amphibian population dynamics following experimental manipulations of introduced fish. Conservation Biology 22:1572-1581. doi: 10.1111/j.1523-1739.2008.00998.x CrossRefPubMedGoogle Scholar
  21. Pope KL, Brown C, Hayes M, Green G, and Macfarlane D (2014). Cascades Frog Conservation Assessment. Pacific Southwest Research Station, United States Forest Service, Albany, California.CrossRefGoogle Scholar
  22. R Development Core Team (2015) R: A language and environment for statistical computing. https://cran.r-project.org/.
  23. Rachowicz LJ, Hero J-M, Alford RA, Taylor JW, Morgan JAT, Vredenburg VT, et al. (2005) The Novel and Endemic Pathogen Hypotheses: Competing Explanations for the Origin of Emerging Infectious Diseases of Wildlife. Conservation Biology 19:1441-1448. doi: 10.1111/j.1523-1739.2005.00255.x CrossRefGoogle Scholar
  24. Retallick RWR, Miera V, Richards KL, Field KJ, and Collins JP (2006) A non-lethal technique for detecting the chytrid fungus Batrachochytrium dendrobatidis on tadpoles. Diseases of Aquatic Organisms 72:77-85. doi: 10.3354/dao072077 CrossRefPubMedGoogle Scholar
  25. Schloegel LM, Picco AM, Kilpatrick AM, Davies AJ, Hyatt AD, and Daszak P (2009) Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biological Conservation 142:1420-1426. doi: 10.1016/j.biocon.2009.02.007 CrossRefGoogle Scholar
  26. Schloegel LM, Toledo LF, Longcore JE, Greenspan SE, Vieira CA, Lee M, et al. (2012) Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology 21:5162-5177. doi: 10.1111/j.1365-294X.2012.05710.x CrossRefPubMedGoogle Scholar
  27. Sette CM, Vredenburg VT, and Zink AG (2015) Reconstructing historical and contemporary disease dynamics: A case study using the California slender salamander. Biological Conservation 192:20-29. doi: 10.1016/j.biocon.2015.08.039 CrossRefGoogle Scholar
  28. Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, et al. (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 4:125-134. doi: 10.1007/s10393-007-0093-5 CrossRefGoogle Scholar
  29. Talley BL, Muletz CR, Vredenburg VT, Fleischer RC, and Lips KR (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. Vredenburg VT, Felt SA, Morgan EC, McNally SVG, Wilson S, and Green SL (2013) Prevalence of Batrachochytrium dendrobatidis in Xenopus Collected in Africa (1871-2000) and in California (2001-2010). PLoS ONE 8:e63791. doi: 10.1371/journal.pone.0063791 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Vredenburg VT, Knapp RA, Tunstall TS, and Briggs CJ (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 107:9689-9694. doi: 10.1073/pnas.0914111107 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Wake DB, and 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 Sciences of the United States of America 105:11466-11473. doi: 10.1073/pnas.0801921105 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Weldon C, du Preez LH, Hyatt AD, Muller R, and Speare R (2004) Origin of the amphibian chytrid fungus. Emerging Infectious Diseases 10:2100-2105. doi: 10.3201/eid1012.030804 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Welsh HH, Pope KL, Boiano D (2006) Sub-alpine amphibian distributions related to species palatability to non-native salmonids in the Klamath mountains of northern California. Diversity and Distributions 12:298-309. doi: 10.1111/j.1366-9516.2006.00254.x CrossRefGoogle Scholar
  35. Yap TA, Gillespie L, Ellison S, Flechas SV, Koo MS, Martinez AE, et al. (2016) Invasion of the fungal pathogen Batrachochytrium dendrobatidis on California islands. Ecohealth 13:145-150. doi: 10.1007/s10393-015-1071-y CrossRefPubMedGoogle Scholar

Copyright information

© International Association for Ecology and Health 2016

Authors and Affiliations

  • Marina E. De León
    • 1
  • Vance T. Vredenburg
    • 2
  • Jonah Piovia-Scott
    • 3
    Email author
  1. 1.Department of BiologyCalifornia State Polytechnic University, PomonaPomonaUSA
  2. 2.Department of BiologySan Francisco State UniversitySan FranciscoUSA
  3. 3.School of Biological SciencesWashington State UniversityVancouverUSA

Personalised recommendations