Skip to main content Accessibility help
×
Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-05T04:20:48.620Z Has data issue: false hasContentIssue false

Chapter Eighteen - When chytrid fungus invades: integrating theory and data to understand disease-induced amphibian declines

from Part III - Understanding wildlife disease ecology at the community and landscape level

Published online by Cambridge University Press:  28 October 2019

Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
Get access

Summary

Amphibian populations are experiencing declines globally, many of which are driven by the fungal pathogen Batrachochytrium dendrobatidis (Bd), but different species of amphibians, as well as divergent populations of the same species, can show drastically different responses to Bd invasion. We answer three questions: what are the potential trajectories of amphibian host populations following Bd invasion; how are each of these trajectories influenced by the transmission dynamics and load dynamics governing an amphibian–Bd system; and) how do ecological, evolutionary, and environmental factors affect both Bd transmission and load dynamics, which influence the amphibian hosts’ population levels? We build a general framework that identifies eight population-level trajectories that amphibian populations can take upon Bd invasion that are a result of five different branch points. Each of these branch points is affected by either the transmission dynamics or the load dynamics underlying the system. Integrating relevant disease ecology theory and empirical data, this framework can be used to guide context-dependent management strategies for amphibian populations infected with Bd.

Type
Chapter
Information
Wildlife Disease Ecology
Linking Theory to Data and Application
, pp. 511 - 543
Publisher: Cambridge University Press
Print publication year: 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

References

Bielby, J., Fisher, M.C., Clare, F.C., Rosa, G.M. & Garner, T.W.J. (2015) Host species vary in infection probability, sub-lethal effects, and costs of immune response when exposed to an amphibian parasite. Scientific Reports, 5, 18.Google Scholar
Briggs, C.J., Vredenburg, V.T.,Knapp, R.A. & Rachowicz, L.J. (2005) Investigating the population-level effects of chytridiomycosis: an emerging infectious disease of amphibians. Ecology, 86, 31493159.CrossRefGoogle Scholar
Hanlon, S.M., Lynch, K.J., Kerby, J. & Parris, M.J. (2015) Batrachochytrium dendrobatidis exposure effects on foraging efficiencies and body size in anuran tadpoles. Diseases of Aquatic Organisms, 112, 237242.Google Scholar
Jani, A.J., Knapp, R.A. & Briggs, C.J. (2017) Epidemic and endemic pathogen dynamics correspond to distinct host population microbiomes at a landscape scale. Proceedings of the Royal Society of London B, 284, 20170944.Google Scholar
Kilpatrick, A.M., Briggs, C.J. & Daszak, P. (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends in Ecology and Evolution, 25, 109118.CrossRefGoogle ScholarPubMed
Knapp, R.A. & Matthews, K.R. (2000) Non-native mountain fish introductions and the decline of the mountain yellow-legged frog from within protected areas. Conservation Biology, 14, 428438.Google Scholar
Knapp, R.A., Fellers, G.M., Kleeman, P.M., et al. (2016) Large-scale recovery of an endangered amphibian despite ongoing exposure to multiple stressors. Proceedings of the National Academy of Sciences of the United States of America, 113, 11,88911,894.Google Scholar
Longcore, J.E., Pessier, A.P. &Nichols, D.K. (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia, 91, 219227.CrossRefGoogle Scholar
Voyles, J., Berger, L., Young, S., et al. (2007) Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Diseases of Aquatic Organisms, 77, 113118.Google Scholar
Voyles, J., Young, S., Berger, L., et al. (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science, 326, 58.CrossRefGoogle ScholarPubMed
Vredenburg, V.T., Knapp, R.A., Tunstall, T.S. & Briggs, C.J. (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences of the United States of America, 107, 96899694.CrossRefGoogle ScholarPubMed

References

Boyle, D.G., Boyle, D.B., Olsen, V., Morgan, J.A.T. & Hyatt, A.D. (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms, 60, 141148.CrossRefGoogle ScholarPubMed
Briggs, C.J., Knapp, R.A. & Vredenburg, V.T. (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences of the United States of America, 107, 96959700.Google Scholar
Easterling, M.R., Ellner, S.P. & Dixon, P.M. (2000) Size-specific sensitivity: applying a new structured population model. Ecology, 81, 694708.Google Scholar
Jani, A.J., Knapp, R.A. & Briggs, C.J. (2017) Epidemic and endemic pathogen dynamics correspond to distinct host population microbiomes at a landscape scale. Proceedings of the Royal Society of London B, 284, 20170944.Google Scholar
Wilber, M.Q., Knapp, R.A., Toothman, M. & Briggs, C.J. (2017) Resistance, tolerance and environmental transmission dynamics determine host extinction risk in a load-dependent amphibian disease. Ecology Letters, 30, 11691181.Google Scholar
Wilber, M.Q., Langwig, K.E., Kilpatrick, A.M., McCallum, H.I. & Briggs, C.J. (2016) Integral projection models for host–parasite systems with an application to amphibian chytrid fungus. Methods in Ecology and Evolution, 7, 11821194.CrossRefGoogle ScholarPubMed
Woodhams, D.C., Alford, R.A., Briggs, C.J., Johnson, M. & Rollins-Smith, L.A. (2008) Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology, 89, 16271639.Google Scholar

References

Briggs, C.J., Knapp, R.A. & Vredenburg, V.T. (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences of the United States of America, 107, 96959700.CrossRefGoogle ScholarPubMed
Wilber, M.Q., Knapp, R.A., Toothman, M. & Briggs, C.J. (2017) Resistance, tolerance and environmental transmission dynamics determine host extinction risk in a load-dependent amphibian disease. Ecology Letters, 30, 11691181.Google Scholar

References

Adams, A.J., Kupferberg, S.J., Wilber, M.Q., et al. (2017) Extreme drought, host density, sex, and bullfrogs influence fungal pathogen infection in a declining lotic amphibian. Ecosphere, 8(3), e01740.CrossRefGoogle Scholar
Allen, L.J.S. (2015) Stochastic Population and Epidemic Models: Persistence and Extinction. London: Springer International Publishing.CrossRefGoogle Scholar
Altwegg, R. & Reyer, H.-U. (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution, 57, 872882.Google Scholar
Anderson, R.M. & May, R.M. (1979) Population biology of infectious diseases: Part I. Nature, 280, 361367.CrossRefGoogle ScholarPubMed
Anderson, R.M. & May, R.M. (1981) The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London B, 291, 451524.Google Scholar
Anderson, R.M. & May, R.M. (1991) Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press.Google Scholar
Becker, C.G., Greenspan, S.E., Tracy, K.E., et al. (2017) Variation in phenotype and virulence among enzootic and panzootic amphibian chytrid lineages. Fungal Ecology, 26, 4550.Google Scholar
Begon, M., Bennett, M., Bowers, R.G., et al. (2002) A clarification of transmission terms in host–microparasite models: numbers, densities and areas. Epidemiology and Infection, 129, 147153.CrossRefGoogle ScholarPubMed
Bletz, M.C., Rosa, G.M., Andreone, F., et al. (2015) Widespread presence of the pathogenic fungus Batrachochytrium dendrobatidis in wild amphibian communities in Madagascar. Scientific Reports, 5, 110.Google Scholar
Boots, M., Best, A., Miller, M.R. & White, A. (2009) The role of ecological feedbacks in the evolution of host defence: what does theory tell us? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 364, 2736.CrossRefGoogle ScholarPubMed
Bosch, J., Martínez-Solano, I. & García-París, M. (2001) Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biological Conservation, 97, 331337.Google Scholar
Briggs, C.J., Knapp, R.A. & Vredenburg, V.T. (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences of the United States of America, 107, 96959700.Google Scholar
Briggs, C.J., Vredenburg, V.T., Knapp, R.A. & Rachowicz, L.J. (2005) Investigating the population-level effects of chytridiomycosis: an emerging infectious disease of amphibians. Ecology, 86, 31493159.Google Scholar
Chestnut, T., Anderson, C., Popa, R., et al. (2014) Heterogeneous occupancy and density estimates of the pathogenic fungus Batrachochytrium dendrobatidis in waters of North America. PLoS ONE, 9, e106790.CrossRefGoogle ScholarPubMed
Clare, F.C., Halder, J.B., Daniel, O., et al. (2016) Climate forcing of an emerging pathogenic fungus across a montane multi-host community. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 371, 20150454.Google Scholar
Cohen, J.M., Venesky, M.D., Sauer, E.L., et al. (2017) The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease. Ecology Letters, 20, 184193.Google Scholar
Combes, C. (2000) Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago, IL: The University of Chicago Press.Google Scholar
Courtois, E.A., Loyau, A., Bourgoin, M. & Schmeller, D.S. (2017) Initiation of Batrachochytrium dendrobatidis infection in the absence of physical contact with infected hosts – a field study in a high altitude lake. Oikos, 126, 843851.CrossRefGoogle Scholar
Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2003) Infectious disease and amphibian population declines. Diversity and Distributions, 9, 141150.Google Scholar
De Castro, F. & Bolker, B. (2005) Mechanisms of disease-induced extinction. Ecology Letters, 8, 117126.Google Scholar
Diekmann, O. & Heesterbeek, J.A.P. (2000) Mathematical Epidemiology of Infectious Disease: Model Building, Interpretation, and Analysis. New York, NY: John Wiley & Sons.Google Scholar
DiRenzo, G.V., Langhammer, P.F., Zamudio, K.R. & Lips, K.R. (2014) Fungal infection intensity and zoospore output of Atelopus zeteki, a potential acute chytrid supershedder. PLoS ONE, 9, e93356.Google Scholar
Doddington, B.J., Bosch, J., Oliver, J.A., et al. (2013) Context-dependent amphibian host population response to an invading pathogen. Ecology, 94, 17951804.Google Scholar
Drawert, B., Griesemer, M., Petzold, L.R. & Briggs, C.J. (2017) Using stochastic epidemiological models to evaluate conservation strategies for endangered amphibians. Journal of The Royal Society Interface, 14, 20170480.Google Scholar
Ellison, A.R., Tunstall, T., Direnzo, G.V., et al. (2015) More than skin deep: functional genomic basis for resistance to amphibian chytridiomycosis. Genome Biology and Evolution, 7, 286298.Google Scholar
Farrer, R.A., Weinert, L.A., Bielby, J., et al. (2011) Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proceedings of the National Academy of Sciences of the United States of America, 108, 18,73218,736.CrossRefGoogle ScholarPubMed
Fisher, M.C., Bosch, J., Yin, Z., et al. (2009) Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Molecular Ecology, 18, 415429.Google Scholar
Fisher, M.C., Henk, D.A., Briggs, C.J., et al. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature, 484, 186194.Google Scholar
Garmyn, A.,Rooij, P. van, Pasmans, F., et al. (2012) Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLoS ONE, 7, e35038.Google Scholar
Garner, T.W.J., Walker, S., Bosch, J., et al. (2009) Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos, 118, 783791.CrossRefGoogle Scholar
Godfray, H.C.J., Briggs, C.J., Barlow, N.D., et al. (1999) A model of insect–pathogen dynamics in which a pathogenic bacterium can also reproduce saprophytically. Proceedings of the Royal Society of London B, 266, 233240.Google Scholar
Hagman, M. & Alford, R.A. (2015) Patterns of Batrachochytrium dendrobatidis transmission between tadpoles in a high-elevation rainforest stream in tropical Australia. Diseases of Aquatic Organisms, 115, 213221.CrossRefGoogle Scholar
Hanlon, S.M., Lynch, K.J., Kerby, J. & Parris, M.J. (2015) Batrachochytrium dendrobatidis exposure effects on foraging efficiencies and body size in anuran tadpoles. Diseases of Aquatic Organisms, 112, 237242.CrossRefGoogle ScholarPubMed
Jani, A.J., Knapp, R.A. & Briggs, C.J. (2017) Epidemic and endemic pathogen dynamics correspond to distinct host population microbiomes at a landscape scale. Proceedings of the Royal Society of London B, 284, 20170944.Google Scholar
Johnson, M.L. & Speare, R. (2003) Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases, 9, 922925.Google Scholar
Johnson, M.L. & Speare, R. (2005) Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Diseases of Aquatic Organisms, 65, 181186.Google Scholar
Kilburn, V., Ibáñez, R. & Green, D. (2011) Reptiles as potential vectors and hosts of the amphibian pathogen Batrachochytrium dendrobatidis in Panama. Diseases of Aquatic Organisms, 97, 127134.Google Scholar
Kilpatrick, A.M., Briggs, C.J. & Daszak, P. (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends in Ecology and Evolution, 25, 109118.Google Scholar
Knapp, R.A., Fellers, G.M., Kleeman, P.M., et al. (2016) Large-scale recovery of an endangered amphibian despite ongoing exposure to multiple stressors. Proceedings of the National Academy of Sciences of the United States of America, 113, 11,88911,894.Google Scholar
Kolby, J.E., Ramirez, S.D., Berger, L., et al. (2015) Terrestrial dispersal and potential environmental transmission of the amphibian chytrid fungus (Batrachochytrium dendrobatidis). PLoS ONE, 10, e0125386.Google Scholar
Lande, R., Engen, S. & Saether, B.-E. (2003) Stochastic Population Dynamics in Ecology and Conservation. Oxford: Oxford University Press.CrossRefGoogle Scholar
Langhammer, P.F., Lips, K.R., Burrowes, P.A., et al. (2013) A fungal pathogen of amphibians, Batrachochytrium dendrobatidis, attenuates in pathogenicity with in vitro passages. PLoS ONE, 8, e77630.Google Scholar
Langwig, K.E., Voyles, J., Wilber, M.Q., et al. (2015) Context-dependent conservation responses to emerging wildlife diseases. Frontiers in Ecology and the Environment, 13, 195202.Google Scholar
Laurance, W.F., McDonald, K.R. & Speare, R. (1996) Epidemic disease and the catastrophic decline of Australian rain forest frogs. Conservation Biology, 10, 406413.CrossRefGoogle Scholar
Liew, N., Mazon Moya, M.J., Wierzbicki, C.J., et al. (2017) Chytrid fungus infection in zebrafish demonstrates that the pathogen can parasitize non-amphibian vertebrate hosts. Nature Communications, 8, 15048.Google Scholar
Lloyd-Smith, J.O., Cross, P.C., Briggs, C.J., et al. (2005) Should we expect population thresholds for wildlife disease? Trends in Ecology and Evolution, 20, 511519.Google Scholar
Longcore, J.E., Pessier, A.P. & Nichols, D.K. (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia, 91, 219227.Google Scholar
Maniero, G.D. & 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, 256263.Google Scholar
Marca, E.L., Lips, K.R., Lötters, S., et al. (2005) Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica, 37, 190201.Google Scholar
McCallum, H. (2012) Disease and the dynamics of extinction. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 367, 28282839.Google Scholar
McCallum, H., Barlow, N. & Hone, J. (2001) How should pathogen transmission be modelled? Trends in Ecology and Evolution, 16, 295300.CrossRefGoogle ScholarPubMed
McCallum, H., Jones, M., Hawkins, C., et al. (2009) Transmission dynamics of Tasmanian devil facial tumor disease may lead to disease-induced extinction. Ecology, 90, 33793392.CrossRefGoogle ScholarPubMed
McMahon, T.A., Brannelly, L.A., Chatfield, M.W.H., et al. (2013) Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. Proceedings of the National Academy of Sciences of the United States of America, 110, 210215.Google Scholar
McMahon, T.A., Sears, B.F., Venesky, M.D., et al. (2014) Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature, 511, 224227.Google Scholar
Medzhitov, R., Schneider, D.S. & Soares, M.P. (2012) Disease tolerance as a defense strategy. Science, 335, 936941.Google Scholar
Perez, R., Richards-Zawacki, C.L., Krohn, A.R., et al. (2014) Field surveys in Western Panama indicate populations of Atelopus varius frogs are persisting in regions where Batrachochytrium dendrobatidis is now enzootic. Amphibian and Reptile Conservation, 8, 3035.Google Scholar
Piotrowski, J.S., Annis, S.L. & Longcore, J.E. (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia, 96, 915.Google Scholar
Rachowicz, L.J. & Briggs, C.J. (2007) Quantifying the disease transmission function: effects of density on Batrachochytrium dendrobatidis transmission in the mountain yellow-legged frog Rana muscosa. The Journal of Animal Ecology, 76, 711721.CrossRefGoogle ScholarPubMed
Raffel, T.R., Halstead, N.T., McMahon, T.A., Davis, A.K. & Rohr, J.R. (2015) Temperature variability and moisture synergistically interact to exacerbate an epizootic disease. Proceedings of the Royal Society of London B, 282, 20142039.Google Scholar
Raffel, T.R., Rohr, J.R., Kiesecker, J.M. & Hudson, P.J. (2006) Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology, 20, 819828.CrossRefGoogle Scholar
Raffel, T.R., Romansic, J.M., Halstead, N.T., et al. (2012) Disease and thermal acclimation in a more variable and unpredictable climate. Nature Climate Change, 3, 146151.Google Scholar
Råberg, L., Graham, A.L. & Read, A.F. (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364, 3749.Google Scholar
Reeder, N.M.M., Pessier, A.P. & Vredenburg, V.T. (2012) A reservoir species for the emerging amphibian pathogen Batrachochytrium dendrobatidis thrives in a landscape decimated by disease. PLoS ONE, 7, e33567.Google Scholar
Refsnider, J.M., Poorten, T.J., Langhammer, P.F., Burrowes, P.A. & Rosenblum, E.B. (2015) Genomic correlates of virulence attenuation in the deadly amphibian chytrid fungus, Batrachochytrium dendrobatidis. G3: Genes|Genomes|Genetics, 5, 22912298.Google Scholar
Retallick, R.W.R., McCallum, H. & Speare, R. (2004) Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biology, 2, e351.Google Scholar
Retallick, R.W.R. & Miera, V. (2007) Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection. Diseases of Aquatic Organisms, 75, 201207.Google Scholar
Rosenblum, E.B., James, T.Y., Zamudio, K.R., et al. (2013) Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proceedings of the National Academy of Sciences of the United States of America, 110, 93859390.Google Scholar
Savage, A.E., Becker, C.G. & Zamudio, K.R. (2015) Linking genetic and environmental factors in amphibian disease risk. Evolutionary Applications, 8, 560572.Google Scholar
Savage, A.E. & Zamudio, K.R. (2011) MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences of the United States of America, 108, 16,70516,710.Google Scholar
Savage, A.E. & Zamudio, K.R. (2016) Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations. Proceedings of the Royal Society of London B, 283, 20153115.Google Scholar
Scheele, B.C., Guarino, F., Osborne, W., et al. (2014) Decline and re-expansion of an amphibian with high prevalence of chytrid fungus. Biological Conservation, 170, 8691.Google Scholar
Scheele, B.C., Skerratt, L.F., Grogan, L.F., et al. (2017) After the epidemic: ongoing declines, stabilizations and recoveries in amphibians afflicted by chytridiomycosis. Biological Conservation, 206, 3746.Google Scholar
Schmeller, D.S., Blooi, M., Martel, A., et al. (2014) Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Current Biology, 24, 176180.Google Scholar
Semlitsch, R.D. (1990) Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Canadian Journal of Zoology, 68, 10271030.Google Scholar
Skerratt, L.F., Berger, L., Speare, R., et al. (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth, 4, 125134.Google Scholar
Smith, D.C. (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology, 68, 344350.Google Scholar
Stockwell, M.P., Bower, D.S., Clulow, J. & Mahony, M.J. (2016) The role of non-declining amphibian species as alternative hosts for Batrachochytrium dendrobatidis in an amphibian community. Wildlife Research, 43, 341347.Google Scholar
Stockwell, M.P., Clulow, J. & Mahony, M.J. (2010) Host species determines whether infection load increases beyond disease-causing thresholds following exposure to the amphibian chytrid fungus. Animal Conservation, 13, 6271.Google Scholar
Stuart, S.N., Chanson, J.S., Cox, N.A., et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science, 306, 17831786.Google Scholar
Venesky, M.D., Liu, X., Sauer, E.L. & Rohr, J.R. (2013) Linking manipulative experiments to field data to test the dilution effect. Journal of Animal Ecology, 83, 557565.CrossRefGoogle ScholarPubMed
Voyles, J., Young, S., Berger, L., et al. (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science, 326, 58.Google Scholar
Vredenburg, V.T., Knapp, R.A., Tunstall, T.S. & Briggs, C.J. (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences of the United States of America, 107, 96899694.Google Scholar
Wilber, M.Q., Knapp, R.A., Toothman, M. & Briggs, C.J. (2017) Resistance, tolerance and environmental transmission dynamics determine host extinction risk in a load-dependent amphibian disease. Ecology Letters, 30, 11691181.CrossRefGoogle Scholar
Wilber, M.Q., Langwig, K.E., Kilpatrick, A.M., McCallum, H.I. & Briggs, C.J. (2016) Integral projection models for host–parasite systems with an application to amphibian chytrid fungus. Methods in Ecology and Evolution, 7, 11821194.Google Scholar
Woodhams, D.C., Alford, R.A., Briggs, C.J., Johnson, M. & Rollins-Smith, L.A. (2008) Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology, 89, 16271639.Google Scholar
Woodhams, D.C., Bosch, J., Briggs, C.J., et al. (2011) Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Frontiers in Zoology, 8, 8.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×