The Influence of Temperature on Chytridiomycosis In Vivo
Chytridiomycosis, an amphibian disease caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), is an ideal system for studying the influence of temperature on host–pathogen relationships because both host and pathogen are ectothermic. Studies of Bd in culture suggest that optimal growth occurs between 17 and 23°C, and death of the fungus occurs above 29 or below 0°C. Amphibian immune systems, however, are also temperature dependent and often more effective at higher temperatures. We therefore hypothesized that pathogen load, probability of infection and mortality in Bd-exposed frogs would peak at a lower temperature than that at which Bd grows best in vitro. To test this, we conducted a study where Bd- and sham-exposed Northern cricket frogs (Acris crepitans) were incubated at six temperatures between 11 and 26°C. While probability of infection did not differ across temperatures, pathogen load and mortality were inversely related to temperature. Survival of infected hosts was greatest between 20 and 26°C, temperatures where Bd grows well in culture. These results demonstrate that the conditions under which a pathogen grows best in culture do not necessarily reflect patterns of pathogenicity, an important consideration for predicting the threat of this and other wildlife pathogens.
Keywordsamphibian Batrachochytrium dendrobatidis ecophysiology fungal pathogen in vitro thermal
The authors thank David Heins, Sunshine Van Bael and Warren Porter for feedback on earlier drafts. Thanks also to Gina Zwicky, Megan Exnicios, Tammy Vo, Xander Rose, Megan McWilliams, and Ian Buchta who assisted with animal husbandry and data collection and Mary Neligh who assisted with database design. This work was funded by grants from the National Science Foundation (Award No. 1649443) and Louisiana Board of Regents (Award No. LEQSF (2011-14)-RD-A-26) to CLRZ. Permission to collect A. crepitans was provided by the Louisiana Department of Wildlife and Fisheries (Permit Nos. WL-Research-2012-06 and LNHP-14-060). This study and its methods were approved by the Institutional Animal Care and Use Committees (IACUC) at Tulane University (Protocol Nos. 0391 – 0391R2).
- Butler MW, Stahlschmidt ZR, Ardia DR, Davies S, Davis J, Guillette LJ, Johnson N, McCormick SD, McGraw KJ, DeNardo DF (2013) Thermal sensitivity of immune function: Evidence against a generalist-specialist trade-off among endothermic and ectothermic vertebrates. The American Naturalist 181:761–774CrossRefPubMedGoogle Scholar
- Chaturvedi V, Springer DJ, Behr MJ, Ramani R, Li X, Peck MK, Ren P, Bopp DJ, Wood B, Samsonoff WA, Butchkoski CM, Hicks AC, Stone WB, Rudd RJ, Chaturvedi S (2010) Morphological and molecular characterizations of psychrophilic fungus Geomyces destructans from New York bats with white nose syndrome (WNS). PLoS ONE 5:e19783Google Scholar
- Kwon-Chung KJ, Bennett JE (1992) Medical Mycology, Philadelphia: Lea & FebigerGoogle Scholar
- Langwig KE, Frick WF, Reynolds R, Parise KL, Drees KP, Hoyt JR, Cheng TL, Kinz TH, Foster JT, Kilpatrick AM (2015) Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proceedings of the Royal Society of London, Series B 282:2014–2335Google Scholar
- Martel A, Spitzen-van der Sluijs A, Blooi M, Bert W, Ducatelle R, Fisher MC, Pasmans F (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences of the United States of America 110:15325–15329CrossRefPubMedPubMedCentralGoogle Scholar
- Menardo F, Praz CR, Wyder S, Roi B-D, Bourras S, Matsumae H, McNally KE, Parlange F, Riba A, Roffler S, Schaefer LK, Shimizu KK, Valenti L, Zbinden H, Wicker T, Keller B (2016) Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nature Genetics 48:201–205CrossRefPubMedGoogle Scholar
- Murray KA, Retallick RWR, Puschendorf R, Skerratt LF, Rosauer D, McCallum HI, Berger L, Speare R, VanDerWal J (2010) Assessing spatial patterns of disease risk to biodiversity: implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis. Journal of Applied Ecology 48:163–173CrossRefGoogle Scholar
- Raffel TR, Romansic JM, Halstead, NT, McMahon TA, Venesky MD, Rohr JR (2013) Disease and thermal acclimation in a more variable and unpredictable climate. Nature Climate Change 2:1–6Google Scholar
- Rollins-Smith LA, Woodhams DC (2012) Amphibian immunity: staying in tune with the environment. In: Ecoimmunology, Demas GE, Nelson RJ (editors), Oxford, UK: Oxford University Press, pp 92–143Google Scholar
- Voyles J, Johnson LR, Briggs CJ, Cashins SD, Alford RA, Berger L, Rosenblum EB (2012) Temperature alters reproductive life history patterns in Batrachochytrium dendrobatidis, a lethal pathogen associated with the global loss of amphibians. Ecology and Evolution 2:2241–2249CrossRefPubMedPubMedCentralGoogle Scholar
- Zippel K, Tabaka C (2008) Amphibian chytridiomycosis in captive Acris crepitans blanchardi (Blanchard’s cricket frog) collected from Ohio, Missouri, and Michigan, USA. Herpetological Review 39:192–193Google Scholar