Skip to main content

Advertisement

Log in

The Influence of Temperature on Chytridiomycosis In Vivo

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • 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):716–720

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bradley GA, Rosen PC, Sredl MJ, Jones TR, Longcore, JE (2002) Chytridiomycosis in native Arizona frogs. Journal of Wildlife Diseases 38:206–212

    Article  PubMed  Google Scholar 

  • 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):143–153

    Article  PubMed  Google Scholar 

  • 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 181:761–774

    Article  PubMed  Google Scholar 

  • 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 108:143–150

    PubMed  PubMed Central  Google Scholar 

  • Carey C, Alexander MA (2003) Climate change and amphibian declines: is there a link? Diversity and Distributions 9:111–121

    Article  Google Scholar 

  • Casadevall A (2005) Fungal virulence, vertebrate endotherm, and dinosaur extinction: is there a connection? Fungal Genetics and Biology 42:98–106

    Article  PubMed  Google 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:e19783

    Google Scholar 

  • Chatfield MWH, Richards-Zawacki CL (2011) Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs. Diseases of Aquatic Organisms 94:235–238

    Article  PubMed  Google Scholar 

  • 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 20:184–193

    Article  PubMed  Google Scholar 

  • Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time and host. Annual Review of Microbiology 63:291–310

    Article  CAS  PubMed  Google Scholar 

  • 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 484:186–194

    Article  CAS  PubMed  Google Scholar 

  • Furst MA, McMahon DP, Osborne JL, Paxton RJ, Brown, MJF (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:729–740

    Article  PubMed  Google Scholar 

  • 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 296:2158–2162

    Article  CAS  PubMed  Google Scholar 

  • Jakob EM, Marshall SD, Uetz GW (2011) Estimating fitness : a comparison of body condition indices estimating fitness. Oikos 77:61–67

    Article  Google Scholar 

  • Kwon-Chung KJ, Bennett JE (1992) Medical Mycology, Philadelphia: Lea & Febiger

    Google 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 282:2014–2335

    Google Scholar 

  • 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 45:1999–2016

    Article  Google Scholar 

  • Lehtinen RM, Skinner AA (2006) The enigmatic decline of Blanchard’s cricket frog (Acris crepitans blanchardi): a test of the habitat acidification hypothesis. Copeia 2006:159–167

    Article  Google Scholar 

  • 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:e72

    Article  PubMed  PubMed Central  Google Scholar 

  • Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227

    Article  Google Scholar 

  • Longcore JR, Longcore JE, Pessier AP, Halteman WA (2007) Chytridiomycosis widespread in anurans of northeastern United States. Journal of Wildlife Management 71:435–444

    Article  Google Scholar 

  • 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 167:256–263

    Article  CAS  Google 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 110:15325–15329

    Article  CAS  PubMed  PubMed Central  Google 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 48:201–205

    Article  CAS  PubMed  Google Scholar 

  • 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 95:31–42

    Article  PubMed  Google 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 48:163–173

    Article  Google Scholar 

  • 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 18:200e224

    Article  CAS  Google Scholar 

  • Muths E, Corn PS, Pessier AP, Green DE (2003) Evidence for disease related amphibian decline in Colorado. Biological Conservation 110:357–365

    Article  Google Scholar 

  • Ouellet M, Mikaelian I, Pauli BD, Rodrigue J, Green DM (2005) Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology 19:1431–1440

    Article  Google Scholar 

  • 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 41:145–149

    Article  Google Scholar 

  • Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15

    Article  PubMed  Google Scholar 

  • 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 15:401–408

    Article  Google Scholar 

  • 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 87:1671–1683

    Article  PubMed  Google Scholar 

  • Raffel TR, Rohr JR, Kiesecker JM, Hudson PJ (2006) Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology 20:819–828

    Article  Google 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 2:1–6

    Google Scholar 

  • 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 75:201–207

    Article  PubMed  Google Scholar 

  • 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 1:52–66

    Article  Google 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 92–143

    Google Scholar 

  • Ron S (2005) Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica 37:209–221

    Article  Google Scholar 

  • 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 82:3–18

    Article  PubMed  Google Scholar 

  • 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 37:383–385

    Article  Google Scholar 

  • Thomas MB, Jenkins NE (1997) Effects of temperature on growth of Metarhizium flavoviride and virulence to the variegated grasshopper, Zonocerus variegatus. Mycological Research 101:1469–1474

    Article  Google Scholar 

  • 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 77:113–8

    Article  CAS  PubMed  Google 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 2:2241–2249

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 105:11466–11473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 89:1627–1639

    Article  PubMed  Google 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 39:192–193

    Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julia M. Sonn.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 43 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sonn, J.M., Berman, S. & Richards-Zawacki, C.L. The Influence of Temperature on Chytridiomycosis In Vivo. EcoHealth 14, 762–770 (2017). https://doi.org/10.1007/s10393-017-1269-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-017-1269-2

Keywords

Navigation