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Published in: EcoHealth 4/2017

01-12-2017 | Original Contribution

The Influence of Temperature on Chytridiomycosis In Vivo

Authors: Julia M. Sonn, Scott Berman, Corinne L. Richards-Zawacki

Published in: EcoHealth | Issue 4/2017

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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.
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Literature
go back to reference 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):716–720CrossRefPubMed 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):716–720CrossRefPubMed
go back to reference 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 60:141–148CrossRefPubMed 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 60:141–148CrossRefPubMed
go back to reference Bradley GA, Rosen PC, Sredl MJ, Jones TR, Longcore, JE (2002) Chytridiomycosis in native Arizona frogs. Journal of Wildlife Diseases 38:206–212CrossRefPubMed Bradley GA, Rosen PC, Sredl MJ, Jones TR, Longcore, JE (2002) Chytridiomycosis in native Arizona frogs. Journal of Wildlife Diseases 38:206–212CrossRefPubMed
go back to reference 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):143–153CrossRefPubMed 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):143–153CrossRefPubMed
go back to reference 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 181:761–774CrossRefPubMed 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 181:761–774CrossRefPubMed
go back to reference 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 108:143–150PubMedPubMedCentral 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 108:143–150PubMedPubMedCentral
go back to reference Carey C, Alexander MA (2003) Climate change and amphibian declines: is there a link? Diversity and Distributions 9:111–121CrossRef Carey C, Alexander MA (2003) Climate change and amphibian declines: is there a link? Diversity and Distributions 9:111–121CrossRef
go back to reference Casadevall A (2005) Fungal virulence, vertebrate endotherm, and dinosaur extinction: is there a connection? Fungal Genetics and Biology 42:98–106CrossRefPubMed Casadevall A (2005) Fungal virulence, vertebrate endotherm, and dinosaur extinction: is there a connection? Fungal Genetics and Biology 42:98–106CrossRefPubMed
go back to reference 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 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
go back to reference Chatfield MWH, Richards-Zawacki CL (2011) Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs. Diseases of Aquatic Organisms 94:235–238CrossRefPubMed Chatfield MWH, Richards-Zawacki CL (2011) Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs. Diseases of Aquatic Organisms 94:235–238CrossRefPubMed
go back to reference 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 20:184–193CrossRefPubMed 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 20:184–193CrossRefPubMed
go back to reference Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time and host. Annual Review of Microbiology 63:291–310CrossRefPubMed Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time and host. Annual Review of Microbiology 63:291–310CrossRefPubMed
go back to reference 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 484:186–194CrossRefPubMed 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 484:186–194CrossRefPubMed
go back to reference Furst MA, McMahon DP, Osborne JL, Paxton RJ, Brown, MJF (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–6CrossRefPubMedPubMedCentral Furst MA, McMahon DP, Osborne JL, Paxton RJ, Brown, MJF (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–6CrossRefPubMedPubMedCentral
go back to reference 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 9:729–740CrossRefPubMed 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 9:729–740CrossRefPubMed
go back to reference 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 296:2158–2162CrossRefPubMed 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 296:2158–2162CrossRefPubMed
go back to reference Jakob EM, Marshall SD, Uetz GW (2011) Estimating fitness : a comparison of body condition indices estimating fitness. Oikos 77:61–67CrossRef Jakob EM, Marshall SD, Uetz GW (2011) Estimating fitness : a comparison of body condition indices estimating fitness. Oikos 77:61–67CrossRef
go back to reference Kwon-Chung KJ, Bennett JE (1992) Medical Mycology, Philadelphia: Lea & Febiger Kwon-Chung KJ, Bennett JE (1992) Medical Mycology, Philadelphia: Lea & Febiger
go back to reference 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 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
go back to reference 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 45:1999–2016CrossRef 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 45:1999–2016CrossRef
go back to reference Lehtinen RM, Skinner AA (2006) The enigmatic decline of Blanchard’s cricket frog (Acris crepitans blanchardi): a test of the habitat acidification hypothesis. Copeia 2006:159–167CrossRef Lehtinen RM, Skinner AA (2006) The enigmatic decline of Blanchard’s cricket frog (Acris crepitans blanchardi): a test of the habitat acidification hypothesis. Copeia 2006:159–167CrossRef
go back to reference 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:e72CrossRefPubMedPubMedCentral 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:e72CrossRefPubMedPubMedCentral
go back to reference Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227CrossRef Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227CrossRef
go back to reference Longcore JR, Longcore JE, Pessier AP, Halteman WA (2007) Chytridiomycosis widespread in anurans of northeastern United States. Journal of Wildlife Management 71:435–444CrossRef Longcore JR, Longcore JE, Pessier AP, Halteman WA (2007) Chytridiomycosis widespread in anurans of northeastern United States. Journal of Wildlife Management 71:435–444CrossRef
go back to reference 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 167:256–263CrossRef 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 167:256–263CrossRef
go back to reference 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 110:15325–15329CrossRefPubMedPubMedCentral 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 110:15325–15329CrossRefPubMedPubMedCentral
go back to reference 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 48:201–205CrossRefPubMed 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 48:201–205CrossRefPubMed
go back to reference 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 95:31–42CrossRefPubMed 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 95:31–42CrossRefPubMed
go back to reference 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 48:163–173CrossRef 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 48:163–173CrossRef
go back to reference 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 18:200e224CrossRef 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 18:200e224CrossRef
go back to reference Muths E, Corn PS, Pessier AP, Green DE (2003) Evidence for disease related amphibian decline in Colorado. Biological Conservation 110:357–365CrossRef Muths E, Corn PS, Pessier AP, Green DE (2003) Evidence for disease related amphibian decline in Colorado. Biological Conservation 110:357–365CrossRef
go back to reference Ouellet M, Mikaelian I, Pauli BD, Rodrigue J, Green DM (2005) Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology 19:1431–1440CrossRef Ouellet M, Mikaelian I, Pauli BD, Rodrigue J, Green DM (2005) Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology 19:1431–1440CrossRef
go back to reference 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 41:145–149CrossRef 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 41:145–149CrossRef
go back to reference Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15CrossRefPubMed Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15CrossRefPubMed
go back to reference 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 15:401–408CrossRef 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 15:401–408CrossRef
go back to reference 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 87:1671–1683CrossRefPubMed 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 87:1671–1683CrossRefPubMed
go back to reference Raffel TR, Rohr JR, Kiesecker JM, Hudson PJ (2006) Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology 20:819–828CrossRef Raffel TR, Rohr JR, Kiesecker JM, Hudson PJ (2006) Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology 20:819–828CrossRef
go back to reference 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 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
go back to reference 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 75:201–207CrossRefPubMed 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 75:201–207CrossRefPubMed
go back to reference 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 1:52–66CrossRef 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 1:52–66CrossRef
go back to reference 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 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
go back to reference Ron S (2005) Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica 37:209–221CrossRef Ron S (2005) Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica 37:209–221CrossRef
go back to reference 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 82:3–18CrossRefPubMed 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 82:3–18CrossRefPubMed
go back to reference 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 37:383–385CrossRef 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 37:383–385CrossRef
go back to reference Thomas MB, Jenkins NE (1997) Effects of temperature on growth of Metarhizium flavoviride and virulence to the variegated grasshopper, Zonocerus variegatus. Mycological Research 101:1469–1474CrossRef Thomas MB, Jenkins NE (1997) Effects of temperature on growth of Metarhizium flavoviride and virulence to the variegated grasshopper, Zonocerus variegatus. Mycological Research 101:1469–1474CrossRef
go back to reference 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 77:113–8CrossRefPubMed 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 77:113–8CrossRefPubMed
go back to reference 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 2:2241–2249CrossRefPubMedPubMedCentral 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 2:2241–2249CrossRefPubMedPubMedCentral
go back to reference 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 105:11466–11473CrossRefPubMedPubMedCentral 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 105:11466–11473CrossRefPubMedPubMedCentral
go back to reference 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 89:1627–1639CrossRefPubMed 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 89:1627–1639CrossRefPubMed
go back to reference 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 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
Metadata
Title
The Influence of Temperature on Chytridiomycosis In Vivo
Authors
Julia M. Sonn
Scott Berman
Corinne L. Richards-Zawacki
Publication date
01-12-2017
Publisher
Springer US
Published in
EcoHealth / Issue 4/2017
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-017-1269-2

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