, Volume 16, Issue 1, pp 141–150 | Cite as

Field Diagnostics and Seasonality of Ophidiomyces ophiodiicola in Wild Snake Populations

  • Jennifer M. McKenzie
  • Steven J. PriceEmail author
  • J. Leo Fleckenstein
  • Andrea N. Drayer
  • Grant M. Connette
  • Elizabeth Bohuski
  • Jeffrey M. Lorch
Original Contribution


Snake fungal disease (SFD) is an emerging disease caused by the fungal pathogen, Ophidiomyces ophiodiicola. Clinical signs of SFD include dermal lesions, including regional and local edema, crusts, and ulcers. Snake fungal disease is widespread in the Eastern United States, yet there are limited data on how clinical signs of SFD compare with laboratory diagnostics. We compared two sampling methods for O. ophiodiicola, scale clip collection and swabbing, to evaluate whether collection method impacted the results of polymerase chain reaction (PCR). In addition, we evaluated the use of clinical signs to predict the presence of O. ophiodiicola across seasons, snake habitat affiliation (aquatic or terrestrial) and study sites. We found no significant difference in PCR results between sampling methods. Clinical signs were a strong predictor of O. ophiodiicola presence in spring and summer seasons. Snakes occupying terrestrial environments had a lower overall probability of testing positive for O. ophiodiicola compared to snakes occupying aquatic environments. Although our study indicates that both clinical signs of SFD and prevalence of O. ophiodiicola vary seasonally and based on habitat preferences of the host, our analysis suggests that clinical signs can serve as a reliable indicator of O. ophiodiicola presence, especially during spring and summer.


Clinical signs Fungal pathogens PCR Reptiles Snake fungal disease 



Funding for this project was provided by the Department of Forestry and Natural Resources at the University of Kentucky, the McIntire-Stennis Cooperative Forestry Research Program (#1001968), the Chicago Herpetological Society, Kentucky Academy of Sciences, the Wildlife Society-Kentucky Chapter, University of Kentucky’s Eller and Billings Student Research Award, American Society of Ichthyologists and Herpetologists’ Helen T. and Frederick M. Gaige Award, the Kentucky Society of Natural History Student Research Award, the National Geographic Society, and the US Geological Survey. We thank Mickey Agha, Phillip Arant, Jeb Ayres, Sara Beth Freytag, Jake Hutton, Michaela Lambert, Thomas Maigret, Jonathan Matthews, Mason Murphy, and Christian Oldham for assistance in the field. The use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.


  1. Allender MC, Deslik M, Wylie S, Phillips C, Wylie DB, Maddox C, Delaney MA, Kinsel M (2011) Chrysosporium sp. infection in Eastern Massasauga rattlesnakes. Emerging Infectious Diseases 17:2383–2384CrossRefPubMedCentralGoogle Scholar
  2. Allender MC, Raudabaugh DB, Gleason FH, Miller AN (2015) The natural history, ecology, and epidemiology of Ophidiomyces ophiodiicola and its potential impact on free-ranging snake populations. Fungal Ecology 17:187–196CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1–48CrossRefGoogle Scholar
  4. 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 95:9031–9036CrossRefGoogle Scholar
  5. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Ward B (2008) Bat white-nose syndrome: an emerging fungal pathogen? Science 323:227CrossRefGoogle Scholar
  6. Bohuski E, Lorch JM, Griffin KM, Blehert DS (2015) TaqMan real-time polymerase chain reaction for detection of Ophidiomyces ophiodiicola, the fungus associated with snake fungal disease. BMC Veterinary Research 11:1–10CrossRefGoogle Scholar
  7. Burbrink FT, Lorch JM, Lips KR (2017) Host susceptibility to snake fungal disease is highly dispersed across phylogenetic and functional trait space. Science Advances 3:e1701387CrossRefPubMedCentralGoogle Scholar
  8. Burnham KP, Anderson DR (2002) Model Selection and Inference—A Practical Information-Theoretic Approach, New York, NY: SpringerGoogle Scholar
  9. Clark RW, Marchand MN, Clifford BJ, Stechert R, Stephens S (2011) Decline of an isolated timber rattlesnake (Crotalus horridus) population: interactions between climate change, disease, and loss of genetic diversity. Biological Conservation 144:886–891CrossRefGoogle Scholar
  10. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194CrossRefGoogle Scholar
  11. Franklinos LH, Lorch JM, Bohuski E, Fernandez JR, Wright ON, Fitzpatrick L, Petrovan S, Durrant C, Linton C, Baláž V, Cunningham AA (2017) Emerging fungal pathogen Ophidiomyces ophiodiicola in wild European snakes. Scientific Reports 7:3844–3850CrossRefPubMedCentralGoogle Scholar
  12. Guthrie AL, Knowles S, Ballmann AE, Lorch JM (2016) Detection of snake fungal disease due to Ophidiomyces ophiodiicola in Virginia, USA. Journal of Wildlife Diseases 52:57–69CrossRefGoogle Scholar
  13. Hileman ET, Allender MC, Bradke DR, Faust LJ, Moore JA, Ravesi MJ, Tetzlaff SJ (2018) Estimation of Ophidiomyces prevalence to evaluate snake fungal disease risk. The Journal of Wildilfe Management 82(1):173–181CrossRefGoogle Scholar
  14. Kriger KM, Hero JM (2007) Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. Journal of Zoology 271:352–359Google Scholar
  15. Lorch JM, Knowles S, Lankton JS, Michell K, Edwards JL, Kapfer JM, Staffen RA, Wild ER, Schmidt KZ, Ballmann AE, Blodgett D, Farrell TM, Glorioso BM, Last LA, Price SJ, Schuler KL, Smith CE, Wellehan JFX. Jr, Blehert DS (2016) Snake fungal disease: an emerging threat to wild snakes. Philosophical Transactions of the Royal Society B: Biological Sciences 371:20150457CrossRefGoogle Scholar
  16. Lorch JM, Lankton J, Werner K, Falendysz EA, McCurley K, Blehert DS (2015) Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease. mBio 6:1–9Google Scholar
  17. Martel A, Spitzen-van der Sluijs A, Blooi M, Bert W, Ducatelle R, Fisher MC, Woeltjes A, Bosman W, Chiers K, Bossuyt F, Pasmans F (2013) Batrachochytrium salamandrivorans sp. nov. causes chytridiomicosis in amphibians. Proceedings of the National Academy of Sciences of the United States of America 110(38):15325–15329Google Scholar
  18. Mazerolle JM (2016) AICcmodavg: Model Selection and Multimodel Inference Based on (Q)AIC(c). R Package Version 2.0-4. Accessed 25 Feb 2017
  19. McCoy, CM, Lind CM, Farrell TM (2017) Environmental and physiological correlates of the severity of clinical signs of snake fungal disease in a population of pigmy rattlesnakes, Sistrurus miliarius. Conservation Physiology 5:1–10CrossRefGoogle Scholar
  20. Nelson RJ, Demas GE (1996) Seasonal changes in immune function. The Quarterly Review of Biology 71:511–548CrossRefGoogle Scholar
  21. Oldham C, Fleckenstein JL, Boys W, Price SJ (2016) Enhancing ecological investigations of snakes with passive integrated transponder (PIT) telemetry. Herpetological Review 47:385–388Google Scholar
  22. Paré JA, Sigler L, Rypien KL, Gibas CC (2003) Survey for the Chrysosporium anamorph of Nanizziopsis vriesii on the skin of healthy captive squamate reptiles and notes on theis cutaneous fungal mycobiota. Journal of Herpethological Medical Surgery 13:10–15CrossRefGoogle Scholar
  23. R Core Team (2016) R: A Language and Environment for Statistical Computing, Vienna: R Foundation for Statistical ComputingGoogle Scholar
  24. Sigler L, Hambleton S, Pare JA (2013) Molecular characterization of reptile pathogens currently known as members of the Chrysosporium anamorph of Nannizziopsis vriesii complex and relationship with some human-associated isolates. Journal of Clinical Microbiology 51:3338–3357CrossRefPubMedCentralGoogle Scholar
  25. Stokes GD, Dunson WA (1982) Permeability and channel structure of reptilian skin. American Journal of Physiology 242(6):F681-F689Google Scholar
  26. Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Fourth Edition, New York: SpringerCrossRefGoogle Scholar

Copyright information

© EcoHealth Alliance 2018

Authors and Affiliations

  • Jennifer M. McKenzie
    • 1
  • Steven J. Price
    • 1
    Email author
  • J. Leo Fleckenstein
    • 1
  • Andrea N. Drayer
    • 1
  • Grant M. Connette
    • 2
  • Elizabeth Bohuski
    • 3
  • Jeffrey M. Lorch
    • 3
  1. 1.Department of Forestry and Natural ResourcesUniversity of KentuckyLexingtonUSA
  2. 2.Conservation Ecology CenterSmithsonian Conservation Biology InstituteFront RoyalUSA
  3. 3.U.S. Geological Survey - National Wildlife Health CenterMadisonUSA

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