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EcoHealth

, Volume 14, Issue 2, pp 285–295 | Cite as

Batrachochytrium dendrobatidis and the Decline and Survival of the Relict Leopard Frog

  • Jef R. JaegerEmail author
  • Anthony W. Waddle
  • Rebeca Rivera
  • D. Tyler Harrison
  • Silas Ellison
  • Matthew J. Forrest
  • Vance T. Vredenburg
  • Frank van Breukelen
Original Contribution

Abstract

Epizootic disease caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) is a major driver of amphibian declines, yet many amphibians declined before the pathogen was described. The Relict Leopard Frog, Rana onca (=Lithobates onca), was nearly extinct, with the exception of populations within a few geothermal springs. Growth of Bd, however, is limited by high water temperature, and geothermal springs may have provided refuge during outbreaks of chytridiomycosis. We conducted field surveys and laboratory experiments to assess the susceptibility of R. onca to Bd. In the field, we found Bd at one of the two areas where remnant populations of R. onca still occur, but not in the other. In the laboratory, we infected juvenile frogs from these two areas with two hypervirulent Bd isolates associated with declines in other ranid species. In our experiments, these Bd isolates did not affect survivorship of R. onca and most infections (64%) were cleared by the end of the experiments. We propose that R. onca either has inherent resistance to Bd or has recently evolved such resistance. These results may be important for conservation efforts aimed at establishing new populations of R. onca across a landscape where Bd exists. Resistance, however, varies among life stages, and we also did not assess Bd from the local environment. We caution that the resistance we observed for young frogs under laboratory conditions may not translate to the situation for R. onca in the wild.

Keywords

Rana onca Lithobates onca Batrachochytrium dendrobatidis Chytridiomycosis Environmental refuge 

Notes

Acknowledgements

We recognize the field assistance of: Joe Barnes, Milind Bunyan, Lindsay Chiquoine, Alejandra Cortes, Alex Jones, Paul van Els, Simon Madill, Marc Maynard, Amelia Savage, Crystal Shanley, David Syzdek, and Carla Wise, among others. Laboratory efforts were assisted by: Alejandra Cortes, Bella Dressel, Sotodeh Ebrahimi, Megan Hickman, Greg Munson, and Stephanie Rosen. We thank Jonah Piovia-Scott and Joy Worth for graciously sharing isolates of the fungal pathogen. We thank Amelia Savage, Mark Slaughter, and Jon Sjöberg for their efforts in gaining support for this research. Funding was provided by the Bureau of Land Management and Nevada Department of Wildlife (NDOW) under agreements with the University of Nevada, Las Vegas (UNLV), as well as from NSF IOS-1258133 to VTV. Members of the Relict Leopard Frog Conservation Team reviewed research proposals. Protocols involving live animals were approved by the Institutional Animal Care and Use Committee at UNLV, and authorized by NDOW and Arizona Game and Fish Department.

References

  1. Boyle DG, Boyle DB, Olsen V, Morgan JAT, 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.CrossRefPubMedGoogle Scholar
  2. Bradford DF, Jaeger JR, Jennings RD (2004) Population status and distribution of a decimated amphibian, the relict leopard frog (Rana onca). Southwestern Naturalist 49:218–228.CrossRefGoogle Scholar
  3. Brem F, Mendelson III JR, Lips KR (2007) Field-sampling protocol for Batrachochytrium dendrobatidis from living amphibians, using alcohol preserved swabs. Version 1.0. http://www.amphibians.org. Conservation International, Arlington, Virginia, USA
  4. Brem FMR, Parris MJ, Padgett-Flohr GE (2013) Re-isolating Batrachochytrium dendrobatidis from an amphibian host increases pathogenicity in a subsequent exposure. PLoS ONE 8:e61260. doi: 10.1371/journal.pone.0061260 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Briggs CJ, Knapp RA, Vredenburg VT (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceeding of the National Academy of Sciences 107:9695–9700. doi: 10.1073/pnas.0912886107 CrossRefGoogle Scholar
  6. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H (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 95:9031–9036.CrossRefGoogle Scholar
  7. Cheng TL, Rovito S, Wake DB, Vredenburg VT (2011) Coincident mass extinction of neotropical amphibians with the emergence of the fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences 108:9502–9507. doi: 10.1073/pnas.1105538108 CrossRefGoogle Scholar
  8. Daszak P, Strieby A, Cunningham AA, Longcore JE, Brown CC, Porter D (2004) Experimental evidence that the Bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetological Journal 14:201–207.Google Scholar
  9. Ebert D (1998) Experimental evolution of parasites. Science 282:1432–1436.CrossRefPubMedGoogle Scholar
  10. Ellison AR, Tunstall T, DiRenzo GV, Hughey MC, Rebollar EA, Belden LK, Harris RN, Ibáñez R, Lips KR, Zamudio KR (2015) More than skin deep: functional genomic basis for resistance to amphibian chytridiomycosis. Genome Biology and Evolution 7:286–298. doi: 10.1093/gbe/evu285 CrossRefGoogle Scholar
  11. Forrest MJ, Schlaepfer MA (2011) Nothing a hot bath won’t cure: infection rates of amphibian chytrid fungus correlate negatively with water temperature under natural field settings. PLoS ONE 6:e28444. doi: 10.1371/journal.pone.0028444 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Forrest MJ, Edwards MS, Rivera R, Sjöberg JC, Jaeger JR (2015) High Prevalence and Seasonal Persistence of Amphibian Chytrid Fungus Infections in the Desert-dwelling Amargosa Toad, Anaxyrus nelsoni. Herpetological Conservation Biology 10:917–925.Google Scholar
  13. Jaeger JR, Riddle BR, Jennings RD, Bradford DF (2001) Rediscovering Rana onca: Evidence for phylogenetically distinct leopard frogs from the border region of Nevada, Utah, and Arizona. Copeia 2001(2):339–354.CrossRefGoogle Scholar
  14. James TY, Toledo LF, Rödder D, da Silva Leite D, Belasen AM, Betancourt-Román CM, Jenkinson TS, et al. (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. doi: 10.1002/ece3.1672 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Kirshtein JD, Anderson CW, Wood JS, Longcore JE, Voytek MA (2007). Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. Diseases of Aquatic Organisms 77:11–15. doi: 10.3354/dao01831 CrossRefPubMedGoogle Scholar
  16. Langhammer PF, Lips KR, Burrowes PA, Tunstall T, Palmer CM, Collins JP (2013) A fungal pathogen of amphibians, Batrachochytrium dendrobatidis, attenuates in pathogenicity with in vitro passages. PLoS ONE 8:e77630. doi: 10.1371/journal.pone.0077630 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Lips KR (1998) Decline of a tropical montane amphibian fauna. Conservation Biology 12:106–117. doi: 10.1111/j.1523-1739.1998.96359.x CrossRefGoogle Scholar
  18. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Carey C, Livo L, Pessier AP, Collins JP (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences. 103:3165–3170. doi: 10.1073/pnas.0506889103 CrossRefGoogle Scholar
  19. Longo AV, Rodriguez D, Leite DS, Toledo LF, Mendoza, Almeralla CM, Burrow PA, Zamudio KR (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 CrossRefPubMedPubMedCentralGoogle Scholar
  20. McMahon TA, Sears BF, Venesky MD, Bessler SM, Brown JM, Deutsch K, Halstead NT, et al. (2014) Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 551:224–227. doi: 10.1038/nature13491 CrossRefGoogle Scholar
  21. Oláh-Hemmings V, Jaeger JR, Sredl MJ, Schlaepfer MA, Jennings RD, Drost CA, Bradford DF, Riddle BR (2010) Phylogeography of declining relict and lowland leopard frogs in the desert Southwest of North America. Journal of Zoology 280:343–354. doi: 10.1111/j.1469-7998.2009.00667.x CrossRefGoogle Scholar
  22. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15.CrossRefPubMedGoogle Scholar
  23. Piovia-Scott J, Pope K, Worth SJ, Rosenblum EB, Poorten T, Refsnider J, Rollins-Smith LA, et al. (2014) Correlates of virulence in a frog-killing fungal pathogen: evidence from a California amphibian decline. ISME Journal 9:1570–1578. doi: 10.1038/ismej.2014.241 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Puschendorf R, Carnaval AC, VanDerWal J, Zumbado-Ulate H, Chaves G, Bolanos F, Alford RA (2009) Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica. Diversity and Distributions 15:401–408. doi: 10.1111/j.1472-4642.2008.00548.x CrossRefGoogle Scholar
  25. Reeder NMM, Pessier AP, Vredenburg VT (2012) A reservoir species for the emerging amphibian pathogen Batrachochytrium dendrobatidis thrives in a landscape decimated by disease. PLoS ONE 7:e33567. doi: 10.1371/journal.pone.0033567 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Refsnider JM, Poorten TJ, Langhammer PF, Burrowes PA, Rosenblum EB (2015) Genomic correlates of virulence attenuation in the deadly amphibian chytrid fungus, Batrachochytrium dendrobatidis. Genes, Genomes, Genetics 5:2291–2298. doi: 10.1534/g3.115.021808 Google Scholar
  27. Richmond JQ, Savage AE, Zamudio KR, Rosenblum EB (2009) Toward immunogenetic studies of amphibian chytridiomycosis: linking innate and acquired immunity. BioScience 59:311–320. doi: 10.1525/bio.2009.59.4.9 CrossRefGoogle Scholar
  28. RLFCT—Relict Leopard Frog Conservation Team (2016) Conservation agreement and conservation assessment and strategy for the Relict Leopard Frog (Rana onca [=Lithobates Onca]). http://www.ndow.org/uploadedFiles/ndoworg/Content/Our_Agency/Divisions/Fisheries/Relict-Leopard-Frog-Conservation-Agreement.pdf
  29. Rollins-Smith LA, Ramsey JP, Pask JD, Reinert LK, Woodhams DC (2011) Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integrated and Comparative Biology 51:552–562. doi: 10.1093/icb/icr095 CrossRefGoogle Scholar
  30. Rosenblum EB, James TY, Zamudio KR, Poorten TJ, Ilut D, Rodriguez D, Eastman JM, et al. (2013) Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proceedings of the National Academy of Sciences 110:9385–9390. doi: 10.1073/pnas.1300130110 CrossRefGoogle Scholar
  31. Savage AE, Becker CG, Zamudio KR (2015) Linking genetic and environmental factors in amphibian disease risk. Evolutionary Applications 8:560–572. doi: 10.1111/eva.1226 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Savage AE, Zamudio KR (2011) MHC genotypes associated with resistance to a frog-killing fungus. Proceeding National Academy Sciences. 108:16705–16710. doi: 10.1073/pnas.1106893108 CrossRefGoogle Scholar
  33. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786. doi: 10.1126/science.1103538 CrossRefPubMedGoogle Scholar
  34. Voyles J, Johnson LR, Briggs CJ, Cashins SD, Alford RA, Berger L, Skerratt LF, et al. (2014) Experimental evolution alters the rate and temporal pattern of population growth in Batrachochytrium dendrobatidis, a lethal fungal pathogen of amphibians. Ecology and Evolution 4:3633–3641. doi: 10.1002/ece3.1199 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences 107:9689–9694. doi: 10.1073/pnas.0914111107 CrossRefGoogle Scholar
  36. Wake DB, 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 105:11466–11473.CrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2017

Authors and Affiliations

  • Jef R. Jaeger
    • 1
    Email author
  • Anthony W. Waddle
    • 1
  • Rebeca Rivera
    • 1
  • D. Tyler Harrison
    • 1
  • Silas Ellison
    • 2
  • Matthew J. Forrest
    • 3
  • Vance T. Vredenburg
    • 2
  • Frank van Breukelen
    • 1
  1. 1.School of Life SciencesUniversity of Nevada, Las VegasLas VegasUSA
  2. 2.Department of BiologySan Francisco State UniversitySan FranciscoUSA
  3. 3.Scripps Institution of OceanographyLa JollaUSA

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