EcoHealth

, Volume 14, Issue 4, pp 762–770 | Cite as

The Influence of Temperature on Chytridiomycosis In Vivo

  • Julia M. Sonn
  • Scott Berman
  • Corinne L. Richards-Zawacki
Original Contribution

Abstract

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.

Keywords

amphibian Batrachochytrium dendrobatidis ecophysiology fungal pathogen in vitro thermal 

Notes

Acknowledgements

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).

Supplementary material

10393_2017_1269_MOESM1_ESM.docx (43 kb)
Supplementary material 1 (DOCX 43 kb)

References

  1. Andre SE, Parker J, Briggs CJ (2008) Effect of temperature on host response to Batrachochytrium dendrobatidis infection in the mountain yellow-legged frog (Rana muscosa). Journal of Wildlife Diseases 44(3):716–720CrossRefPubMedGoogle Scholar
  2. 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 60:141–148CrossRefPubMedGoogle Scholar
  3. Bradley GA, Rosen PC, Sredl MJ, Jones TR, Longcore, JE (2002) Chytridiomycosis in native Arizona frogs. Journal of Wildlife Diseases 38:206–212CrossRefPubMedGoogle Scholar
  4. Bustamante HM, Livo, LJ, Carey C (2010) Effects of temperature and hydric environment on survival of the Panamanian golden frog infected with a pathogenic chytrid fungus. Integrative Zoology 5(2):143–153CrossRefPubMedGoogle Scholar
  5. 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
  6. Carey C (2000) Infectious disease and worldwide declines of amphibian populations, with comments on emerging diseases in coral reef organisms and in humans. Environmental Health Perspectives 108:143–150PubMedPubMedCentralGoogle Scholar
  7. Carey C, Alexander MA (2003) Climate change and amphibian declines: is there a link? Diversity and Distributions 9:111–121CrossRefGoogle Scholar
  8. Casadevall A (2005) Fungal virulence, vertebrate endotherm, and dinosaur extinction: is there a connection? Fungal Genetics and Biology 42:98–106CrossRefPubMedGoogle Scholar
  9. 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
  10. Chatfield MWH, Richards-Zawacki CL (2011) Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs. Diseases of Aquatic Organisms 94:235–238CrossRefPubMedGoogle Scholar
  11. Cohen JM, Venesky MD, Sauer EL, Civitello DJ, McMahon TA, Roznik EA, Rohr JR (2017) The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease. Ecology Letters 20:184–193CrossRefPubMedGoogle Scholar
  12. Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time and host. Annual Review of Microbiology 63:291–310CrossRefPubMedGoogle Scholar
  13. 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 484:186–194CrossRefPubMedGoogle Scholar
  14. Furst MA, McMahon DP, Osborne JL, Paxton RJ, Brown, MJF (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–6CrossRefPubMedPubMedCentralGoogle Scholar
  15. Grunwald NJ, Goss EM, Press CM (2008) Phytophthora ramorum: A pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals. Molecular Plant Pathology 9:729–740CrossRefPubMedGoogle Scholar
  16. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162CrossRefPubMedGoogle Scholar
  17. Jakob EM, Marshall SD, Uetz GW (2011) Estimating fitness : a comparison of body condition indices estimating fitness. Oikos 77:61–67CrossRefGoogle Scholar
  18. Kwon-Chung KJ, Bennett JE (1992) Medical Mycology, Philadelphia: Lea & FebigerGoogle Scholar
  19. 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
  20. Leach CM (1967) Interaction of near-ultraviolet light and temperature on sporulation of the fungi Alternaria, Cercosporella, Fusarium, Helmonthosporium and Stemphylium. Canadian Journal of Botany 45:1999–2016CrossRefGoogle Scholar
  21. Lehtinen RM, Skinner AA (2006) The enigmatic decline of Blanchard’s cricket frog (Acris crepitans blanchardi): a test of the habitat acidification hypothesis. Copeia 2006:159–167CrossRefGoogle Scholar
  22. Lips KR, Diffendorfer J, Mendelson JR, Sears MW (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biology 6:e72CrossRefPubMedPubMedCentralGoogle Scholar
  23. Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227CrossRefGoogle Scholar
  24. Longcore JR, Longcore JE, Pessier AP, Halteman WA (2007) Chytridiomycosis widespread in anurans of northeastern United States. Journal of Wildlife Management 71:435–444CrossRefGoogle Scholar
  25. Maniero GD, Carey C (1997) Changes in selected aspects of immune function in the leopard frog, Rana pipiens, associated with exposure to cold. Journal of Comparative Physiology B 167:256–263CrossRefGoogle Scholar
  26. 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
  27. 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
  28. Murphy PJ, St-Hilaire S, Corn PS (2011) Temperature, hydric environment, and prior pathogen exposure alter the experimental severity of chytridiomycosis in boreal toads. Diseases of Aquatic Organisms 95:31–42CrossRefPubMedGoogle Scholar
  29. 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
  30. Murray KA, Skerratt LF (2012) Predicting wild hosts for amphibian chytridiomycosis: integrating host life-history traits with pathogen environmental requirements. Human and Ecological Risk Assessment 18:200e224CrossRefGoogle Scholar
  31. Muths E, Corn PS, Pessier AP, Green DE (2003) Evidence for disease related amphibian decline in Colorado. Biological Conservation 110:357–365CrossRefGoogle Scholar
  32. Ouellet M, Mikaelian I, Pauli BD, Rodrigue J, Green DM (2005) Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology 19:1431–1440CrossRefGoogle Scholar
  33. Pearl CA, Bull EL, Green DE, Bowerman J, Adams MJ, Hyatt A, Wente WH (2007) Occurrence of the amphibian pathogen Batrachochytrium dendrobatidis in the Pacific Northwest. Journal of Herpetology 41:145–149CrossRefGoogle Scholar
  34. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15CrossRefPubMedGoogle Scholar
  35. 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: proposing climatic refuges as a conservation tool. Diversity and Distributions 15:401–408CrossRefGoogle Scholar
  36. Rachowicz LJ, Knapp RA, Morgan JAT, Stice MJ, Vredenburg VT, Parker JM, Briggs CJ (2006) Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87:1671–1683CrossRefPubMedGoogle Scholar
  37. Raffel TR, Rohr JR, Kiesecker JM, Hudson PJ (2006) Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology 20:819–828CrossRefGoogle Scholar
  38. 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
  39. Retallick RWR, Miera V (2007) Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection. Diseases of Aquatic Organisms 75:201–207CrossRefPubMedGoogle Scholar
  40. Rödder D, Kielgast J, Bielby J, Schmidtlein S, Bosch J, Garner TWJ, Lötters S. (2009) Global amphibian extinction risk assessment for the panzootic chytrid fungus. Diversity 1:52–66CrossRefGoogle Scholar
  41. 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
  42. Ron S (2005) Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica 37:209–221CrossRefGoogle Scholar
  43. Rothermel BB, Walls SC, Mitchell JC, Dodd KC, Irwin LK, Green DE, Vazquez VM, Petranka JW, Stevenson DJ (2008) Widespread occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in the southeastern USA. Diseases of Aquatic Organisms 82:3–18CrossRefPubMedGoogle Scholar
  44. Smith GR, Todd A, Rettig JE, Nelson F (2003) Microhabitat selection by northern cricket frogs (Acris crepitans) along a West-Central Missouri Creek: field and experimental observations. Journal of Herpetology 37:383–385CrossRefGoogle Scholar
  45. Thomas MB, Jenkins NE (1997) Effects of temperature on growth of Metarhizium flavoviride and virulence to the variegated grasshopper, Zonocerus variegatus. Mycological Research 101:1469–1474CrossRefGoogle Scholar
  46. Voyles J, Berger L, Young S, Speare R, Webb R, Warner J, Rudd D, Campbell R, Skerratt LF (2007) Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Diseases of Aquatic Organisms 77:113–8CrossRefPubMedGoogle Scholar
  47. 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
  48. 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 of the United States of America 105:11466–11473CrossRefPubMedPubMedCentralGoogle Scholar
  49. Woodhams DC, Alford RA, Briggs CJ, Johnson M, Rollins-Smith LA (2008) Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology 89:1627–1639CrossRefPubMedGoogle Scholar
  50. 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

Copyright information

© EcoHealth Alliance 2017

Authors and Affiliations

  • Julia M. Sonn
    • 1
  • Scott Berman
    • 1
  • Corinne L. Richards-Zawacki
    • 1
    • 2
  1. 1.Department of Ecology and Evolutionary BiologyTulane UniversityNew OrleansUSA
  2. 2.Department of Biological SciencesUniversity of PittsburghPittsburghUSA

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