EcoHealth

, Volume 10, Issue 2, pp 166–171 | Cite as

Experimental Evidence for American Bullfrog (Lithobates catesbeianus) Susceptibility to Chytrid Fungus (Batrachochytrium dendrobatidis)

  • Stephanie S. Gervasi
  • Jenny Urbina
  • Jessica Hua
  • Tara Chestnut
  • Rick A. Relyea
  • Andrew R. Blaustein
Short Communication

Abstract

The emerging fungal pathogen, Batrachochytrium dendrobatidis (Bd), has been associated with global amphibian population declines and extinctions. American bullfrogs (Lithobates catesbeianus) are widely reported to be a tolerant host and a carrier of Bd that spreads the pathogen to less tolerant hosts. Here, we examined whether bullfrogs raised from eggs to metamorphosis in outdoor mesocosms were susceptible to Bd. We experimentally exposed metamorphic juveniles to Bd in the laboratory and compared mortality rates of pathogen-exposed animals to controls (non-exposed) in two separate experiments; one using a Bd strain isolated from a Western toad and another using a strain isolated from an American bullfrog. We wanted to examine whether metamorphic bullfrogs were susceptible to either of these strains. We show that bullfrogs were susceptible to one strain of Bd and not the other. In both experiments, infection load detected in the skin decreased over time, suggesting that metamorphic bullfrogs from some populations may be inefficient long-term carriers of Bd.

Keywords

chytrid tolerance rana boreas resistance vector 

Supplementary material

10393_2013_832_MOESM1_ESM.doc (30 kb)
Supplementary material 1 (DOC 30 kb)

References

  1. Bai C, Liu X, Fisher MC, Garner TWJ, and Li Y (2012) Global and endemic Asian lineages of the emerging pathogenic fungus Batrachochytrium dendrobatidis widely infect amphibians in China. Diversity and Distributions 18:307-318CrossRefGoogle Scholar
  2. Bancroft B, Han BA, Searle CL, Biga LM, Olson DH, Kats LB, Lawler JJ, Blaustein AR (2011) Species-level correlates of susceptibility to the pathogenic amphibian fungus Batrachochytrium dendrobatidis in the United States. Biodiversity and Conservation 20: 1911-1920CrossRefGoogle Scholar
  3. 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 of the United States of America 95:9031-9036PubMedCrossRefGoogle Scholar
  4. Best A, Webb S, Antonovics J, Boots M (2012) Local transmission processes and disease driven host extinctions. Theoretical Ecology 5: 211-217CrossRefGoogle Scholar
  5. Blaustein AR, Romansic JM, Scheessele EA, Han BA, Pessier AP, Longcore JE (2005) Interspecific Variation in Susceptibility of Frog Tadpoles to the Pathogenic Fungus Batrachochytrium dendrobatidis. Conservation Biology 19: 1460-1468CrossRefGoogle Scholar
  6. Blaustein AR, Han BA, Relyea RA, Johnson PTJ, Buck JC, Gervasi SS, Kats LB (2011) The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses Annals of the New York Academy of Sciences 1223:108-119PubMedCrossRefGoogle Scholar
  7. 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: 141-148PubMedCrossRefGoogle Scholar
  8. Briggs CJ, Knapp RA, Vredenburg VT (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Acadamy of Sciences 107: 9695-9700CrossRefGoogle Scholar
  9. Brutyn M, D’Herde K, Dhaenens M, Van Rooij P, Verbrugghe E, Hyatt AD, Croubels S, Deforce D, Ducatelle R, Haesebrouck F, Martel A, Pasmans F (2012) Batrachochytrium dendrobatidis zoospore secretions rapidly disturb intercellular junctions in frog skin. Fungal Genetics Biology 49: 830-837CrossRefGoogle Scholar
  10. Crawford AJ, Lips KR and Bermingham E (2010) Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Acadamy of Science USA 107: 13777-13782CrossRefGoogle Scholar
  11. Daszak P, Strieby A, Cunningham AA, Longcore JE, Brown CC, Porter D (2004) Experimentalevidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetological Journal 14 201-207Google Scholar
  12. Farrer RA, Weinert LA, Bielby J, Garner TWJ, Balloux F, Clare F, Bosch J, Cunningham AA, Welcon C, duPreez LH, Anderson L, Kosakovsky Pond SL, Shahar-Golan R, Henk D, Fisher MC (2011) Multiple emergences of genetically diverse amphibian-infecting chytrids include a globally hypervirulent recombinant lineage. Proceedings of the National Academy of Sciences 108:18732-18736CrossRefGoogle Scholar
  13. Fisher MC, Bosch J, Yin, Stead DA, Walker J, Selway L, Brown AJP, Walker LA, Gow NAR, Stajich JE, Garner TWJ (2009) Proteomic and phenotypica profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Molecular Ecology 18: 415-429PubMedCrossRefGoogle Scholar
  14. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, and Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484: 186-194PubMedCrossRefGoogle Scholar
  15. Gahl MK, Longcore JE, and Houlahan JE (2012) Varying responses of northeastern North American amphibians to the chytrid pathogen Batrachochytrium dendrobatidis. Conservation Biology 26:135-141PubMedCrossRefGoogle Scholar
  16. Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S, Cunningham AA, Fisher MC (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters 2:455-459PubMedCrossRefGoogle Scholar
  17. Gervasi SS, Gondhalekar C, Olson DH, Blaustein AR (2013) Host identity matters in the amphibian-Batrachochytrium dendrobatidis system: fine-scale patterns of variation in responses to a multi-host pathogen. PLoS ONE 8:e54490PubMedCrossRefGoogle Scholar
  18. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190Google Scholar
  19. Greenspan SE, Longcore JE Calhoun AJK (2012) Host invasion by Batrachochytrium dencrobatidis: fungal and epidermal ultrastructure in model anurans. Diseases of Aquatic Organisms 100: 201-210PubMedCrossRefGoogle Scholar
  20. Hanselmann R, Rodriguez A, Lampo M, Fajardo-Ramos L, Aguirre AA, Kilpatrick AM, Rodriguez JP, Daszak P (2004) Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela. Biological Conservation 120:115-119CrossRefGoogle Scholar
  21. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993PubMedCrossRefGoogle Scholar
  22. Kats LB, and Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Diversity and Distributions 9:99-110CrossRefGoogle Scholar
  23. Keesing F, Holt RD, and Ostfeld RS (2006) Effects of species diversity on disease risk. Ecology Letters 9:485-498PubMedCrossRefGoogle Scholar
  24. Keesing F, Belden LK, Daszak P, Dobson A, Harvel CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647-652PubMedCrossRefGoogle Scholar
  25. Lips KR (1998) Decline of a tropical montane fauna. Conservation Biology 12:106-117CrossRefGoogle Scholar
  26. Lips KR, Reeve JD, Witters LR (2003) Ecological traits predicting amphibian population declines in Central America. Conservation Biology 17:1078-1088CrossRefGoogle Scholar
  27. Liu X, Rohr JR, Li Y (2013) Climate, vegetation, introduced host and trade shape a global wildlife pandemic. Proceedings of the Royal Society B: Biological Sciences 280: 20122506PubMedCrossRefGoogle Scholar
  28. McCallum ML (2012) Disease and the dynamics of extinction. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 2828-2839CrossRefGoogle Scholar
  29. McMahon TA, Brannelly LA, Chatfield MWH, Johnson PTJ, Joseph MB, McKenzie VJ, Richards-Zawacki CL, Venesky MD, Rohr JR(2013) The chytrid fungus, Batrachochytrium dendrobatidis, has non-amphibian hosts and releases chemicals that cause pathology in the absence of infection. Proceedings of the National Academy of Sciences of the United States of America 110: 210-215PubMedCrossRefGoogle Scholar
  30. Morgan JAT, Vredenburg VT, Rachowicz LJ, Knapp RA, Stice MJ, Tunstall T, Bingham RE, Parker JM, Longcore JE, Moritz C, Briggs CJ, Taylor JW (2007) Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America 104:13845-13850PubMedCrossRefGoogle Scholar
  31. Raberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B 364: 37-49CrossRefGoogle Scholar
  32. Read AF, Graham AL, Raberg L (2008) Animal defenses against infectious agents: is damage control more important than pathogen control? PLoS Biol 6: 2638-2641CrossRefGoogle Scholar
  33. Reeder NMM, Pessier AP, and Vredenburg VT (2012) A reservoir species for the emerging amphibian pathogen Batrachochytrium dendrobatidis thrives in a landscape decimated by disease. PLoS ONE 7:e33567PubMedCrossRefGoogle Scholar
  34. Rodriguez-Serna M, Flores-Nava A, Olvera-Novoa MA, and Carmona-Osalde C (1996) Growth and production of bullfrog Rana catesbeiana Shaw, 1802, at three stocking densities in a vertical intensive cultrue system. Aquacultural Engineering 15:233-242CrossRefGoogle Scholar
  35. Rohr JR, Raffel TR (2010) Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Sciences of the United States of America 107: 8269-8274PubMedCrossRefGoogle Scholar
  36. Rohr JR, Raffel TR, Hall CA (2010) Developmental variation in resistance and tolerance in a multi-host—parasite system. Functional Ecology 24: 1110-1121CrossRefGoogle Scholar
  37. Rosenblum EB, Stajich JE, Maddox N, Eisen MB. 2008. Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America105:17034-17039PubMedCrossRefGoogle Scholar
  38. Rosenblum, E.B., Poorten,T.J., Joneson, S. & Settles, M. (2012) Substrate-specific gene expression in Batrachochytrium dendrobatidis, the chytrid fungus of amphibians.PLoS ONE 7, e49924PubMedCrossRefGoogle Scholar
  39. Savage AE and Zamudio KR (2011) MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Acadamy of Sciences 108:16705-16710CrossRefGoogle Scholar
  40. Schloegel LM, Toledo LF, Longcore JE, Greenspan SE, Vieira CA, Lee M, Zhao S, Wangen C, Ferreira CM, Hipolito M, Davies AJ, Cuomo CA, Daszak P, James TY (2012) Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology 21:5162-5177PubMedCrossRefGoogle Scholar
  41. Searle CL, Gervasi SS, Hua J, Hammond JI, Relyea RA, Olson DH, Blaustein AR (2011) Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conservation Biology 25:965-974PubMedCrossRefGoogle Scholar
  42. Skerratt L, Berger L, Speare R, Cashins S, McDonald K, Phillott A, Hines HB, Kenyon N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125-134CrossRefGoogle Scholar
  43. Telfer S, Brown K (2012) The effects of invasion on parasite dynamics and communities. Functional Ecology 26: 1288-1299CrossRefGoogle Scholar
  44. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, Cook D, Webb R, Alford RA, Skerratt LF, Speare R (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326: 582-585PubMedCrossRefGoogle Scholar
  45. 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 of the United States of America 107: 9689-9694PubMedCrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2013

Authors and Affiliations

  • Stephanie S. Gervasi
    • 1
  • Jenny Urbina
    • 2
  • Jessica Hua
    • 3
  • Tara Chestnut
    • 2
  • Rick A. Relyea
    • 3
  • Andrew R. Blaustein
    • 1
    • 2
  1. 1.Department of ZoologyOregon State UniversityCorvallisUSA
  2. 2.Environmental Sciences ProgramOregon State UniversityCorvallisUSA
  3. 3.Department of Biological SciencesUniversity of PittsburghPittsburghUSA

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