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

Journal of Applied Ecology

Volumn 48, Issue 1, 2011, Pages 163-173

  Murray, Kris A ^a   Retallick, Richard W R ^b   Puschendorf, Robert ^c   Skerratt, Lee F ^c   Rosauer, Dan ^d,e   McCallum, Hamish I ^f   Berger, Lee ^c   Speare, Rick ^c   VanDerWal, Jeremy ^c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GHD PTY LTD   (Australia)

^c JAMES COOK UNIVERSITY   (Australia)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e Centre for Plant Biodiversity Research   (Australia)

^f GRIFFITH UNIVERSITY   (Australia)

Author keywords

Amphibian declines; Bioclimatic modelling; Chytrid fungus; Chytridiomycosis; Infectious disease; Maxent; Species distribution model

Indexed keywords

ABUNDANCE; AMPHIBIAN; BIODIVERSITY; BIOLOGICAL INVASION; CONSERVATION MANAGEMENT; DATABASE; DISEASE CONTROL; ECOSYSTEM STRUCTURE; FUNGAL DISEASE; FUNGUS; HYPOTHESIS TESTING; INFECTIOUS DISEASE; NUMERICAL MODEL; POPULATION DECLINE; RISK ASSESSMENT; SPATIAL ANALYSIS; WILDLIFE MANAGEMENT;

AUSTRALIA;

AMPHIBIA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; VERTEBRATA;

EID: 78650937583     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/j.1365-2664.2010.01890.x     Document Type: Article

References (78)

1. Adams, M.J., Chelgren, N.D., Reinitz, D., Cole, R.A., Rachowicz, L.J., Galvan, S., McCreary, B., Pearl, C.A., Bailey, L.L., Bettaso, J., Bull, E.L. & Leu, M. (2010) Using occupancy models to understand the distribution of an amphibian pathogen, Batrachochytrium dendrobatidis. Ecological Applications, 20, 289-302.
2. Araujo, M.B. & Guisan, A. (2006) Five (or so) challenges for species distribution modelling. Journal of Biogeography, 33, 1677-1688.
3. Berger, L. (2001) Diseases in Australian frogs. PhD, James Cook University, Townsville.
4. Berger, L., Speare, R., Daszak, P., Green, D.E., Cunningham, A.A., Goggin, C.L., Slocombe, R., Ragan, M.A., Hyatt, A.D., McDonald, K.R., Hines, H.B., Lips, K.R., Marantelli, G. & Parkes, H. (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America, 95, 9031-9036.
5. Berger, L., Speare, R., Hines, H.B., Marantelli, G., Hyatt, A.D., McDonald, K.R., Skerratt, L.F., Olsen, V., Clarke, J.M., Gillespie, G., Mahony, M., Sheppard, N., Williams, C. & Tyler, M.J. (2004) Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Australian Veterinary Journal, 82, 434-439.
6. Bielby, J., Cooper, N., Cunningham, A., Garner, T. & Purvis, A. (2008) Predicting susceptibility to future declines in the world's frogs. Conservation Letters, 1, 82-90.
7. Briggs, C., 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, 9695-9700.
8. Carey, C., Bruzgul, J.E., Livo, L.J., Walling, M.L., Kuehl, K.A., Dixon, B.F., Pessier, A.P., Alford, R.A. & Rogers, K.B. (2006) Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth, 3, 5-21.
9. Crowl, T.A., Crist, T.O., Parmenter, R.R., Belovsky, G. & Lugo, A.E. (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Frontiers in Ecology and the Environment, 6, 238-246.
10. Daszak, P., Cunningham, A. & Hyatt, A. (2000) Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science, 287, 443-449.
11. Digiacomo, R.F. & Koepsell, T.D. (1986) Sampling for detection of infection or disease in animal populations. Journal of the American Veterinary Medical Association, 189, 22-23.
12. Dudik, M., Phillips, S.J. & Schapire, R.E. (2007) Maximum entropy density estimation with generalized regularization and an application to species distribution modeling. Journal of Machine Learning Research, 8, 1217-1260.
13. Elith, J., Graham, C.H., Anderson, R.P., Dudik, M., Ferrier, S., Guisan, A., Hijmans, R.J., Huettmann, F., Leathwick, J.R., Lehmann, A., Li, J., Lohmann, L.G., Loiselle, B.A., Manion, G., Moritz, C., Nakamura, M., Nakazawa, Y., Overton, J.M., Peterson, A.T., Phillips, S.J., Richardson, K., Scachetti-Pereira, R., Schapire, R.E., Soberon, J., Williams, S., Wisz, M.S. & Zimmermann, N.E. (2006) Novel methods improve prediction of species' distributions from occurrence data. Ecography, 29, 129-151.
14. Ficetola, G.F., Thuiller, W. & Miaud, C. (2007) Prediction and validation of the potential global distribution of a problematic alien invasive species - the American bullfrog. Diversity and Distributions, 13, 476-485.
15. Fielding, A.H. & Bell, J.F. (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation, 24, 38-49.
16. Fisher, M.C., Bosch, J., Yin, Z., Stead, D.A., Walker, J., Selway, L., Brown, A.J.P., Walker, L.A., Gow, N.A.R., Stajich, J.E. & Garner, T.W.J. (2009) Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Molecular Ecology, 18, 415-429.
17. Gascon, C., Collins, J.P., Moore, R.D., Church, D.R., McKay, J.E. & Mendelson, J.R. III (eds) (2007) Amphibian Conservation Action Plan: Proceedings: IUCN/SSC Amphibian Conservation Summit 2005. The World Conservation Union (IUCN), Gland, Switzerland.
18. Gibson, L., Barrett, B. & Burbidge, A. (2007) Dealing with uncertain absences in habitat modelling: a case study of a rare ground-dwelling parrot. Diversity and Distributions, 13, 704-713.
19. Goka, K., Yokoyama, J., Une, Y., Kuroki, T., Suzuki, K., Nakahara, M., Kobayashi, A., Inaba, S., Mizutani, T. & Hyatt, A.D. (2009) Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Molecular Ecology, 18, 4757-4774.
20. Graham, C.H., Elith, J., Hijmans, R.J., Guisan, A., Peterson, A.T., Loiselle, B.A. & Group, N.P.S.W. (2008) The influence of spatial errors in species occurrence data used in distribution models. Journal of Applied Ecology, 45, 239-247.
21. Guisan, A. & Thuiller, W. (2005) Predicting species distribution: offering more than simple habitat models. Ecology Letters, 8, 993-1009.
22. Guisan, A., Broennimann, O., Engler, R., Vust, M., Yoccoz, N.G., Lehmann, A. & Zimmermann, N.E. (2006) Using niche-based models to improve the sampling of rare species. Conservation Biology, 20, 501-511.
23. Hines, H., Mahony, M. & McDonald, K. (1999) An assessment of frog declines in wet subtropical Australia. Declines and Disappearances of Australian Frogs (eds A. Campbell), pp. 44-63. Environment Australia, Canberra.
24. IUCN (2008) The IUCN red list of threatened species. IUCN., accessed July 2008.
25. James, T.Y., Litvintseva, A.P., Vilgalys, R., Morgan, J.A.T., Taylor, J.W., Fisher, M.C., Berger, L., Weldon, C., du Preez, L. & Longcore, J.E. (2009) Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathogens, 5, e1000458.
26. Johnson, M.L. & Speare, R. (2003) Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases, 9, 922-925.
27. Johnson, M.L., Berger, L., Philips, L. & Speare, R. (2003) Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms, 57, 255-260.
28. Jones, K.E., Patel, N.G., Levy, M.A., Storeygard, A., Balk, D., Gittleman, J.L. & Daszak, P. (2008) Global trends in emerging infectious diseases. Nature, 451, 990-994.
29. Kearney, M. & Porter, W. (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species' ranges. Ecology Letters, 12, 334-350.
30. Kirshtein, J.D., Anderson, C.W., Wood, J.S., Longcore, J.E. & Voytek, M.A. (2007) Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. Diseases of Aquatic Organisms, 77, 11-15.
31. Kriger, K.M. & Hero, J.M. (2007) Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. Journal of Zoology, 271, 352-359.
32. Kusrini, M.D., Skerratt, L.F., Garland, S., Berger, L. & Endarwin, W. (2008) Chytridiomycosis in frogs of Mount Gede Pangrango, Indonesia. Diseases of Aquatic Organisms, 82, 187-194.
33. Lips, K.R., Brem, F., Brenes, R., Reeve, J.D., Alford, R.A., Voyles, J., Carey, C., Livo, L., Pessier, A.P. & Collins, J.P. (2006) Emerging infectious disease and the loss of biodiversity in a neotropical amphibian community. Proceedings of the National Academy of Sciences of the United States of America, 103, 3165-3170.
34. Lips, K.R., Diffendorfer, J., Mendelson, J.R. & Sears, M.W. (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biology, 6, e72.
35. Longcore, J.E., Pessier, A.P. & Nichols, D.K. (1999) Batrachochytrium dendrobatidis gen et sp nov, a chytrid pathogenic to amphibians. Mycologia, 91, 219-227.
36. McDonald, K. & Alford, R. (1999) A review of declining frogs in Northern Queensland. Declines and Disappearances of Australian Frogs (eds A. Campbell), pp. 9-22. Environment Australia, Canberra.
37. Morehouse, E.A., James, T.Y., Ganley, A.R.D., Vilgalys, R., Berger, L., Murphy, P.J. & Longcore, J.E. (2003) Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Molecular Ecology, 12, 395-403.
38. Morgan, J.A.T., Vredenburg, V.T., Rachowicz, L.J., Knapp, R.A., Stice, M.J., Tunstall, T., Bingham, R.E., Parker, J.M., Longcore, J.E., Moritz, C., Briggs, C.J. & Taylor, J.W. (2007) Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America, 104, 13845-13850.
39. Morin, X. & Thuiller, W. (2009) Comparing niche- and process-based models to reduce prediction uncertainty in species range shifts under climate change. Ecology, 90, 1301-1313.
40. Murray, B.R. & Hose, G.C. (2005) Life-history and ecological correlates of decline and extinction in the endemic Australian frog fauna. Austral Ecology, 30, 564-571.
41. Murray, K.A., Skerratt, L.F., Speare, R. & McCallum, H. (2009) Impact and dynamics of disease in species threatened by the amphibian chytrid fungus, Batrachochytrium dendrobatidis. Conservation Biology, 23, 1242-1252.
42. Murray, K.A., Retallick, R., McDonald, K., Mendez, D., Aplin, K., Kirkpatrick, P. et al. (2010) The distribution and host range of the pandemic disease chytridiomycosis in Australia spanning surveys from 1956 to 2007. Ecology, 91, 1557.
43. Murray, K.A., Rosauer, D., McCallum, H. & Skerratt, L.F. (in press) Integrating species traits with extrinsic threats: closing the gap between predicting and preventing species declines. Proceedings of the Royal Society B-Biological Sciences.
44. Muths, E., Pilliod, D.S. & Livo, L.J. (2008) Distribution and environmental limitations of an amphibian pathogen in the Rocky Mountains, USA. Biological Conservation, 141, 1484-1492.
45. Olson, D. & Ronnenberg, K. (2008) Global Bd Mapping Project: Update - 17 January 2008. Available from (accessed January 2008). USDA Forest Service, Pacific Northwest Research Station, Corvallis, Oregon.
46. Osborne, W., Hunter, D. & Hollis, G. (1999) Population declines and range contraction in Australian alpine frogs. Declines and Disappearances of Australian Frogs (eds A. Campbell), pp. 145-157. Environment Australia, Canberra.
47. Parolo, G., Rossi, G. & Ferrarini, A. (2008) Toward improved species niche modelling: Arnica montana in the Alps as a case study. Journal of Applied Ecology, 45, 1410-1418.
48. Pauza, M., Driessen, M. & Skerratt, L.F. (2010) Distribution and risk factors for spread of amphibian chytrid fungus Batrachochytrium dendrobatidis in the Tasmanian Wilderness World Heritage Area, Australia. Diseases of Aquatic Organisms, published online September 23 2010, 1-7.
49. Pearce, J.L. & Boyce, M.S. (2006) Modelling distribution and abundance with presence-only data. Journal of Applied Ecology, 43, 405-412.
50. Pearson, R.G., Raxworthy, C.J., Nakamura, M. & Peterson, A.T. (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. Journal of Biogeography, 34, 102-117.
51. Peterson, A.T., Papes, M. & Eaton, M. (2007) Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent. Ecography, 30, 550-560.
52. Phillips, S.J., Anderson, R.P. & Schapire, R.E. (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190, 231-259.
53. Phillips, S.J., Dudik, M., Elith, J., Graham, C.H., Lehmann, A., Leathwick, J. & Ferrier, S. (2009) Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. Ecological Applications, 19, 181-197.
54. Phillott, A.D., Speare, R., Hines, H.B., Meyer, E., Skerratt, L.F., McDonald, K.R., Cashins, S.D., Mendez, D. & Berger, L. (2010) Minimising exposure of amphibians to pathogens during field studies. Diseases of Aquatic Organisms, in press. doi.
55. Pilliod, D.S., Muths, E., Scherer, R.D., Bartelt, P.E., Corn, P.S., Hossack, B.R., Lambert, B.A., McCaffery, R. & Gaughan, C. (2010) Effects of amphibian chytrid fungus on individual survival probability in wild boreal toads. Conservation Biology, 24, 1259-1267.
56. Piotrowski, J.S., Annis, S.L. & Longcore, J.E. (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia, 96, 9-15.
57. Puschendorf, R., Carnaval, A.C., VanDerWal, J., Zumbado-Ulate, H., Chaves, G., Bolanos, F. & Alford, R.A. (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.
58. Rachowicz, L.J., Hero, J.M., Alford, R.A., Taylor, J.W., Morgan, J.A.T., Vredenburg, V.T., Collins, J.P. & Briggs, C.J. (2005) The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conservation Biology, 19, 1441-1448.
59. Rohr, J.R., Raffel, T.R., Romansic, J.M., McCallum, H. & Hudson, P.J. (2008) Evaluating the links between climate, disease spread, and amphibian declines. Proceedings of the National Academy of Sciences of the United States of America, 105, 17436-17441.
60. Ron, S.R. (2005) Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica, 37, 209-221.
61. Skerratt, L.F., Berger, L., Speare, R., Cashins, S., McDonald, K.R., Phillott, A.D., Hines, H.B. & Kenyon, N. (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth, 4, 125-134.
62. Skerratt, L.F., Berger, L., Hines, H.B., McDonald, K.R., Mendez, D. & Speare, R. (2008) Survey protocol for detecting chytridiomycosis in all Australian frog populations. Diseases of Aquatic Organisms, 80, 85-94.
63. Slatyer, C., Rosauer, D. & Lemckert, F. (2007) An assessment of endemism and species richness patterns in the Australian Anura. Journal of Biogeography, 34, 583-596.
64. Speare, R. & Berger, L. (2000) Global Distribution of Chytridiomycosis in Amphibians. Amphibian Diseases Research Group, Townsville., accessed July 2007.
65. Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L. & Waller, R.W. (2004) Status and trends of amphibian declines and extinctions worldwide. Science, 306, 1783-1786.
66. VanDerWal, J., Shoo, L.P., Graham, C. & William, S.E. (2009a) Selecting pseudo-absence data for presence-only distribution modeling: how far should you stray from what you know? Ecological Modelling, 220, 589-594.
67. VanDerWal, J., Shoo, L.P., Johnson, C.N. & Williams, S.E. (2009b) Abundance and the environmental niche: environmental suitability estimated from niche models predicts the upper limit of local abundance. American Naturalist, 174, 282-291.
68. Voyles, J., Berger, L., Young, S., Speare, R., Webb, R., Warner, J., Rudd, D., Campbell, R. & Skerratt, L.F. (2007) Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Diseases of Aquatic Organisms, 77, 113-118.
69. Wake, D.B. & Vredenburg, V.T. (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.
70. Walker, S.F., Salas, M.B., Jenkins, D., Garner, T.W.J., Cunningham, A.A., Hyatt, A.D., Bosch, J. & Fisher, M.C. (2007) Environmental detection of Batrachochytrium dendrobatidis in a temperate climate. Diseases of Aquatic Organisms, 77, 105-112.
71. Wilson, K.A., Underwood, E.C., Morrison, S.A., Klausmeyer, K.R., Murdoch, W.W., Reyers, B., Wardell-Johnson, G., Marquet, P.A., Rundel, P.W., McBride, M.F., Pressey, R.L., Bode, M., Hoekstra, J.M., Andelman, S., Looker, M., Rondinini, C., Kareiva, P., Shaw, M.R. & Possingham, H.P. (2007) Conserving biodiversity efficiently: what to do, where, and when. PLoS Biology, 5, 1850-1861.
72. Wintle, B.A., Elith, J. & Potts, J.M. (2005) Fauna habitat modelling and mapping: a review and case study in the Lower Hunter Central Coast region of NSW. Austral Ecology, 30, 719-738.
73. Wisz, M.S., Hijmans, R.J., Li, J., Peterson, A.T., Graham, C.H., Guisan, A. & NCEAS (2008) Effects of sample size on the performance of species distribution models. Diversity and Distributions, 14, 763-773.
74. Woodhams, D.C. & Alford, R.A. (2005) Ecology of chytridiomycosis in rainforest stream frog assemblages of tropical Queensland. Conservation Biology, 19, 1449-1459.
75. Woodhams, D.C., Alford, R.A. & Marantelli, G. (2003) Emerging disease of amphibians cured by elevated body temperature. Diseases of Aquatic Organisms, 55, 65-67.
76. 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, 1627-1639.
77. World Organisation for Animal Health (2008) Aquatic Animal Code 2008. World Organisation for Animal Health, Paris. Available from (accessed July 2008).
78. Ziller, M., Selhorst, T., Teuffert, J., Kramer, M. & Schluter, H. (2002) Analysis of sampling strategies to substantiate freedom from disease in large areas. Preventive Veterinary Medicine, 52, 333-343.