Skip to main content
Log in

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

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Davidson C (2004) Declining downwind: Amphibian population declines in California and historical pesticide use. Ecological Applications 14:1892-1902. doi:10.1890/03-5224

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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.

    Book  Google Scholar 

  • R Development Core Team (2015) R: A language and environment for statistical computing. https://cran.r-project.org/.

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonah Piovia-Scott.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

De León, M.E., Vredenburg, V.T. & Piovia-Scott, J. Recent Emergence of a Chytrid Fungal Pathogen in California Cascades Frogs (Rana cascadae). EcoHealth 14, 155–161 (2017). https://doi.org/10.1007/s10393-016-1201-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-016-1201-1

Keywords

Navigation