Assessing spatial patterns of disease risk to biodiversity: Implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis

1. Emerging infectious diseases can have serious consequences for wildlife populations, ecosystem structure and biodiversity. Predicting the spatial patterns and potential impacts of diseases in free-ranging wildlife are therefore important for planning, prioritizing and implementing research and management actions. 2. We developed spatial models of environmental suitability (ES) for infection with the pathogen Batrachochytrium dendrobatidis, which causes the most significant disease affecting vertebrate biodiversity on record, amphibian chytridiomycosis. We applied relatively newly developed methods for modelling ES (Maxent) to the first comprehensive, continent-wide data base (comprising >10000 observations) on the occurrence of infection with this pathogen and employed novel methodologies to deal with common but rarely addressed sources of model uncertainty. 3. We used ES to (i) predict the minimum potential geographic distribution of infection with B. dendrobatidis in Australia and (ii) test the hypothesis that ES for B. dendrobatidis should help explain patterns of amphibian decline given its theoretical and empirical link with organism abundance (intensity of infection), a known determinant of disease severity. 4. We show that (i) infection with B. dendrobatidis has probably reached its broad geographic limits in Australia under current climatic conditions but that smaller areas of invasion potential remain, (ii) areas of high predicted ES for B. dendrobatidis accurately reflect areas where population declines due to severe chytridiomycosis have occurred and (iii) that a host-specific metric of ES for B. dendrobatidis (ES for Bdspecies) is the strongest predictor of decline in Australian amphibians at a continental scale yet discovered. 5. Synthesis and applications. Our results provide quantitative information that helps to explain both the spatial distribution and potential effects (risk) of amphibian infection with B. dendrobatidis at the population level. Given scarce conservation resources, our results can be used immediately in Australia and our methods applied elsewhere to prioritize species, regions and actions in the struggle to limit further biodiversity loss.

[1]  D. Rosauer,et al.  Integrating species traits with extrinsic threats: closing the gap between predicting and preventing species declines , 2011, Proceedings of the Royal Society B: Biological Sciences.

[2]  M. Driessen,et al.  Distribution and risk factors for spread of amphibian chytrid fungus Batrachochytrium dendrobatidis in the Tasmanian Wilderness World Heritage Area, Australia. , 2010, Diseases of aquatic organisms.

[3]  R. Speare,et al.  Minimising exposure of amphibians to pathogens during field studies. , 2010, Diseases of aquatic organisms.

[4]  Paul Stephen Corn,et al.  Effects of Amphibian Chytrid Fungus on Individual Survival Probability in Wild Boreal Toads , 2010, Conservation biology : the journal of the Society for Conservation Biology.

[5]  Cheryl J. Briggs,et al.  Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians , 2010, Proceedings of the National Academy of Sciences.

[6]  D. Driscoll,et al.  The distribution and host range of the pandemic disease chytridiomycosis in Australia, spanning surveys from 1956–2007 , 2010 .

[7]  David Reinitz,et al.  Using occupancy models to understand the distribution of an amphibian pathogen, Batrachochytrium dendrobatidis. , 2010, Ecological applications : a publication of the Ecological Society of America.

[8]  T. Kuroki,et al.  Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan , 2009, Molecular ecology.

[9]  R. Speare,et al.  Impact and Dynamics of Disease in Species Threatened by the Amphibian Chytrid Fungus, Batrachochytrium dendrobatidis , 2009, Conservation biology : the journal of the Society for Conservation Biology.

[10]  Jeremy VanDerWal,et al.  Abundance and the Environmental Niche: Environmental Suitability Estimated from Niche Models Predicts the Upper Limit of Local Abundance , 2009, The American Naturalist.

[11]  R. Alford,et al.  Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: proposing climatic refuges as a conservation tool , 2009 .

[12]  W. Thuiller,et al.  Comparing niche- and process-based models to reduce prediction uncertainty in species range shifts under climate change. , 2009, Ecology.

[13]  M. Fisher,et al.  Rapid Global Expansion of the Fungal Disease Chytridiomycosis into Declining and Healthy Amphibian Populations , 2009, PLoS pathogens.

[14]  M. Kearney,et al.  Mechanistic niche modelling: combining physiological and spatial data to predict species' ranges. , 2009, Ecology letters.

[15]  C. Graham,et al.  Selecting pseudo-absence data for presence-only distribution modeling: How far should you stray from what you know? , 2009 .

[16]  J. Stajich,et al.  Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence , 2009, Molecular ecology.

[17]  Steven J. Phillips,et al.  Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. , 2009, Ecological applications : a publication of the Ecological Society of America.

[18]  L. Skerratt,et al.  Chytridiomycosis in frogs of Mount Gede Pangrango, Indonesia. , 2008, Diseases of aquatic organisms.

[19]  Peter J. Hudson,et al.  Evaluating the links between climate, disease spread, and amphibian declines , 2008, Proceedings of the National Academy of Sciences.

[20]  G. Rossi,et al.  Toward improved species niche modelling: Arnica montana in the Alps as a case study , 2008 .

[21]  A. Peterson,et al.  Effects of sample size on the performance of species distribution models , 2008 .

[22]  D. Wake,et al.  Are we in the midst of the sixth mass extinction? A view from the world of amphibians , 2008, Proceedings of the National Academy of Sciences.

[23]  Richard Speare,et al.  Survey protocol for detecting chytridiomycosis in all Australian frog populations. , 2008, Diseases of aquatic organisms.

[24]  N. Cooper,et al.  Predicting susceptibility to future declines in the world's frogs , 2008 .

[25]  D. Pilliod,et al.  Distribution and environmental limitations of an amphibian pathogen in the Rocky Mountains, USA , 2008 .

[26]  R. Alford,et al.  Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. , 2008, Ecology.

[27]  Robert R Parmenter,et al.  The spread of invasive species and infectious disease as drivers of ecosystem change , 2008 .

[28]  J. Mendelson,et al.  Riding the Wave: Reconciling the Roles of Disease and Climate Change in Amphibian Declines , 2008, PLoS biology.

[29]  Kate E. Jones,et al.  Global trends in emerging infectious diseases , 2008, Nature.

[30]  Miroslav Dudík,et al.  Maximum Entropy Density Estimation with Generalized Regularization and an Application to Species Distribution Modeling , 2007, J. Mach. Learn. Res..

[31]  L. Gibson,et al.  Dealing with uncertain absences in habitat modelling: a case study of a rare ground‐dwelling parrot , 2007 .

[32]  M. Fisher,et al.  Environmental detection of Batrachochytrium dendrobatidis in a temperate climate. , 2007, Diseases of aquatic organisms.

[33]  R. Speare,et al.  Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. , 2007, Diseases of aquatic organisms.

[34]  C. Moritz,et al.  Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis , 2007, Proceedings of the National Academy of Sciences.

[35]  S. Andelman,et al.  Conserving Biodiversity Efficiently: What to Do, Where, and When , 2007, PLoS biology.

[36]  M. Voytek,et al.  Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. , 2007, Diseases of aquatic organisms.

[37]  A. Townsend Peterson,et al.  The influence of spatial errors in species occurrence data used in distribution models , 2007 .

[38]  A. Townsend Peterson,et al.  Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent , 2007 .

[39]  Wilfried Thuiller,et al.  Prediction and validation of the potential global distribution of a problematic alien invasive species — the American bullfrog , 2007 .

[40]  Richard Speare,et al.  Spread of Chytridiomycosis Has Caused the Rapid Global Decline and Extinction of Frogs , 2007, EcoHealth.

[41]  D. Rosauer,et al.  An assessment of endemism and species richness patterns in the Australian Anura , 2007 .

[42]  J. P. Collins,et al.  Amphibian Conservation Action Plan. Proceedings IUCN/SSC Amphibian Conservation Summit 2005. , 2007 .

[43]  R. D. Moore,et al.  Amphibian Conservation Action Plan , 2007 .

[44]  M. Araújo,et al.  Five (or so) challenges for species distribution modelling , 2006 .

[45]  R. Pearson,et al.  Predicting species distributions from small numbers of occurrence records: A test case using cryptic geckos in Madagascar , 2006 .

[46]  J. Hero,et al.  Large‐scale seasonal variation in the prevalence and severity of chytridiomycosis , 2006 .

[47]  Mark S. Boyce,et al.  Modelling distribution and abundance with presence‐only data , 2006 .

[48]  A. Lehmann,et al.  Using Niche‐Based Models to Improve the Sampling of Rare Species , 2006, Conservation biology : the journal of the Society for Conservation Biology.

[49]  A. Townsend Peterson,et al.  Novel methods improve prediction of species' distributions from occurrence data , 2006 .

[50]  R. Alford,et al.  Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Robert P. Anderson,et al.  Maximum entropy modeling of species geographic distributions , 2006 .

[52]  R. Alford,et al.  Experimental Exposures of Boreal Toads (Bufo boreas) to a Pathogenic Chytrid Fungus (Batrachochytrium dendrobatidis) , 2006, EcoHealth.

[53]  Jane Elith,et al.  Fauna habitat modelling and mapping: A review and case study in the Lower Hunter Central Coast region of NSW , 2005 .

[54]  R. Alford,et al.  Ecology of Chytridiomycosis in Rainforest Stream Frog Assemblages of Tropical Queensland , 2005 .

[55]  R. Alford,et al.  The Novel and Endemic Pathogen Hypotheses: Competing Explanations for the Origin of Emerging Infectious Diseases of Wildlife , 2005 .

[56]  W. Thuiller,et al.  Predicting species distribution: offering more than simple habitat models. , 2005, Ecology letters.

[57]  B. Murray,et al.  Life-history and ecological correlates of decline and extinction in the endemic Australian frog fauna , 2005 .

[58]  S. Ron.  Predicting the Distribution of the Amphibian Pathogen Batrachochytrium dendrobatidis in the New World 1 , 2005 .

[59]  B. Young,et al.  Status and Trends of Amphibian Declines and Extinctions Worldwide , 2004, Science.

[60]  C. Williams,et al.  Effect of season and temperature on mortality in amphibians due to chytridiomycosis. , 2004, Australian veterinary journal.

[61]  J. Piotrowski,et al.  Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. , 2004, Mycologia.

[62]  R. Speare,et al.  Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. , 2003, Diseases of aquatic organisms.

[63]  R. Speare,et al.  Survival of Batrachochytrium dendrobatidis in Water: Quarantine and Disease Control Implications , 2003, Emerging infectious diseases.

[64]  R. Alford,et al.  Emerging disease of amphibians cured by elevated body temperature. , 2003, Diseases of aquatic organisms.

[65]  R. Vilgalys,et al.  Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone , 2003, Molecular ecology.

[66]  J Teuffert,et al.  Analysis of sampling strategies to substantiate freedom from disease in large areas. , 2002, Preventive veterinary medicine.

[67]  L. Berger.  Diseases in Australian frogs , 2001 .

[68]  P. Daszak,et al.  Emerging infectious diseases of wildlife--threats to biodiversity and human health. , 2000, Science.

[69]  J. Longcore,et al.  BATRACHOCHYTRIUM DENDROBATIDIS GEN. ET SP. NOV., A CHYTRID PATHOGENIC TO AMPHIBIANS , 1999 .

[70]  D E Green,et al.  Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[71]  John Bell,et al.  A review of methods for the assessment of prediction errors in conservation presence/absence models , 1997, Environmental Conservation.

[72]  Koepsell Td,et al.  Sampling for detection of infection or disease in animal populations. , 1986 .