Ecophysiology meets conservation: Understanding the role of disease in amphibian population declines

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1596, 2012, Pages 1688-1707

  Blaustein, Andrew R ^a   Gervasi, Stephanie S ^a   Johnson, Pieter T J ^b   Hoverman, Jason T ^b   Belden, Lisa K ^c   Bradley, Paul W ^a   Xie, Gisselle Y ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Amphibians; Batrachochytrium; Biodiversity; Pathogens; Ranavirus; Trematodes

Indexed keywords

ADAPTATION; AMPHIBIAN; ANNELID; BIODIVERSITY; CLIMATE CHANGE; CONSERVATION MANAGEMENT; DISEASE PREVALENCE; ECOLOGICAL MODELING; ECOPHYSIOLOGY; FUNGAL DISEASE; HOST-PATHOGEN INTERACTION; INFECTIOUS DISEASE; LIFE HISTORY TRAIT; PHYSIOLOGICAL RESPONSE; POPULATION DECLINE; VIRAL DISEASE;

AMPHIBIA; BATRACHOCHYTRIUM; RANAVIRUS; TREMATODA;

EID: 84860684082     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0011     Document Type: Review

References (246)

1. 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. (doi:10.1038/nature06536)
2. Harvell, C. D. et al. 1999 Emerging marine diseasesclimate links and anthropogenic factors. Science 285, 1505-1510. (doi:10.1126/science.285.5433.1505)
3. Deem, S. L., Karesh, W. B. & Weisman, W. 2001 Putting theory into practice: wildlife health in conservation. Conserv. Biol. 15, 1224-1233. (doi:10.1046/j.1523-1739.2001.00336.x)
4. Daszak, P. & Cunningham, A. A. 2002 Emerging infectious diseases a key role for conservation medicine. In Conservation medicine ecological health in practice (eds A. A. Aguirre, R. S. Ostfeld, G. M. Tabor, C. House & M. C. Pearl), pp. 40-61. Oxford, UK: Oxford University Press.
5. Anderson, P. K., Cunningham, A. A., Patel, N. G., Morales, F. J., Epstein, P. R. & Daszak, P. 2004 Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535-544. (doi:10.1016/j.tree.2004.07.021)
6. Smith, K. F., Acevedo-Whitehouse, K. & Penderson, A. B. 2009 The role of infectious disease in biological conservation. Anim. Conserv. 12, 1-12. (doi:10.1111/j.1469-1795.2008.00228.x)
7. Keesing, F. et al. 2010 Impact of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647-652. (doi:10.1038/nature09575)
8. Daszak, P., Cunningham, A. A. & Hyatt, A. D. 2000 Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287, 443-449. (doi:10.1126/science.287.5452.443)
9. Horwitz, P. & Wilcox, B. A. 2005 Parasites, ecosystems and sustainability: an ecological and complex systems perspective. Inter. J. Parasitol. 35, 725-732. (doi:10.1016/j.ijpara.2005.03.002)
10. Eviner, V. T. & Likens, G. E. 2008 Effects of pathogens on terrestrial ecosystem function. In Infectious disease ecology: effects of ecosystems on disease and of disease on ecosystems (eds R. S. Ostfeld, F. Keesing & V. T. Eviner), pp. 260-284. Princeton, NJ: Princeton University Press.
11. Hudson, P.J., Dobson, A. P. & Lafferty, K. D. 2006 Is a healthy ecosystem one that is rich in parasites? Trends Ecol. Evol. 21, 381-385. (doi:10.1016/j.tree.2006.04.007)
12. Lafferty, K. D. 2008 Effects of disease on community interactions and food webs. In Infectious disease ecology: the effects of ecosystems on disease and of disease on ecosystems (eds R. Ostfeld, F. Keesing & V. T. Eviner), pp. 205-222. Princeton, NJ: Princeton University Press.
13. Hatcher, M. J., Dick, J. T. A. & Dunn, A. M. In press. Diverse effects of parasites in ecosystems. Front. Ecol. Evol.
14. Blaustein, A. R., Walls, S. C., Bancroft, B. A., Lawler, J. J., Searle, C. L. & Gervasi, S. S. 2010 Direct and indirect effects of climate change on amphibian populations. Diversity 2, 281-313. (doi:10.3390/d2020281)
15. Houlahan, J. E., Findlay, C. S., Schmidt, B. R., Meyer, A. H. & Kuzmin, S. L. 2000 Quantitative evidence for global amphibian population declines. Nature 404, 752-755. (doi:10.1038/35008052)
16. Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S. L., Fischmann, D. L. & Waller, R. W. 2004 Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783-1786. (doi:10.1126/science.1103538)
17. Lannoo, M. 2005 Amphibian declines: the conservation status of United States species. Berkeley, CA: USA University California Press.
18. Bielby, J., Cooper, N., Cunningham, A. A., Garner, T. W. J. & Purvis, A. 2008 Predicting susceptibility to rapid declines in the world's frogs. Conserv. Lett. 1, 82-90. (doi:10.1111/j.1755-263X.2008.00015.x)
19. McCallum, M. L. 2007 Amphibian decline or extinction? Current declines dwarf background extinction rate. J. Herpetol. 41, 483-491. (doi:10.1670/0022-1511(2007)41[483:ADOECD]2.0.CO;2)
20. Wake, D. B. & Vredenburg, V. T. 2008 Are we in the midst of the sixth mass extinction? A review from the world of amphibians. Proc. Natl Acad. Sci. USA 105, 11466-11473.
21. Blaustein, A. R., Han, B., Relyea, R. A., Johnson, P. T. J., Buck, J. C., Gervasi, S. S. & Kats, L. B. 2011 The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses. Ann. NY Acad. Sci. 1223, 108-119. (doi:10.1111/j.1749-6632.2010.05909.x)
22. Prudhoe, S. & Bray, R. A. 1982 Platyhelminth parasites of the Amphibia. Oxford, UK: Oxford University Press.
23. Densmore, C. & Green, D. 2007 Diseases of amphibians. ILAR J. 48, 235-254.
24. Klaphake, E. 2009 Bacterial and parasitic diseases of amphibians. Vet. Clin. N. Am. Exotic 12, 597-608. (doi:10.1016/j.cvex.2009.06.005)
25. Daszak, P. A., Cunningham, A. & Hyatt, A. D. 2003 Infectious disease and amphibian population declines. Divers. Distrib. 9, 141-150. (doi:10.1046/j.1472-4642.2003.00016.x)
26. 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. (doi:10.1007/s10393-007-0093-5)
27. Rodder, D. et al. 2009 Global amphibian extinction risk assessment for the panzootic chytrid fungus. Diversity 1, 52-66. (doi:10.3390/d1010052)
28. Blaustein, A. R. & Kiesecker, J. M. 2002 Complexity in conservation: lessons from the global decline of amphibian populations. Ecol. Lett. 5, 597-608. (doi:10.1046/j.1461-0248.2002.00352.x)
29. Mendelson III, J. R. et al. 2006 Confronting amphibian declines and extinctions. Science 313, 48. (doi:10.1126/science.1128396)
30. Kilpatrick, A. M., Briggs, C. J. & Daszak, P. 2010 The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends. Ecol. Evol. 25, 109-118. (doi:10.1016/j.tree.2009.07.011)
31. Hudson, P. J. & Greenman, J. V. 1998 Competition mediated by parasites: biological and theoretical progress. Trends Ecol. Evol. 13, 387-390. (doi:10.1016/S0169-5347(98)01475-X)
32. Keesing, F., Holt, R. D. & Ostfeld, R. S. 2006 Effects of species diversity on disease risk. Ecol. Lett. 9, 485-498. (doi:10.1111/j.1461-0248.2006.00885.x)
33. Ostfeld, R., Keesing, F. & Eviner, V. T. 2008 Infectious disease ecology: the effects of ecosystems on disease and of disease on ecosystems. Princeton, NJ: Princeton University Press.
34. Johnson, P. T. J., Dobson, A., Lafferty, K. D., Marcogliese, D. J., Memmott, J., Orlofske, S. A., Poulin, R. & Thieltges, D. W. 2010 When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol. Evol. 25, 362-371. (doi:10.1016/j.tree.2010.01.005)
35. Tracy, C. R. & Turner, J. S. 1982 What is physiological ecology? Bull. Ecol. Soc. Am. 63, 340-347.
36. Ricklefs, R. E. & Wikelski, M. 2002 The physiology/lifehistory nexus. Trends Ecol. Evol. 17, 462-468. (doi:10.1016/S0169-5347(02)02578-8)
37. Raberg, L., Sim, D. & Read, A. F. 2007 Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318, 812-814. (doi:10.1126/science.1148526)
38. Raberg, L., Graham, A. L. & Read, A. F. 2009 Decomposing health: tolerance and resistance to parasites in animals. Phil. Trans. R. Soc. B 364, 37-49. (doi:10.1098/rstb.2008.0184)
39. Read, A. F., Graham, A. L. & Raberg, L. 2008 Animal defenses against infectious agents: is damage control more important than pathogen control. PLoS Biol. 6, 2638-2641.
40. Hart, B. L. 1994 Behavioral defense against parasitesinteraction with parasite invasiveness. Parasitology 109, S139-S151. (doi:10.1017/S0031182000085140)
41. Schmid-Hempel, P. & Ebert, D. 2003 On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 18, 27-32. (doi:10.1016/S0169-5347(02)00013-7)
42. Hasselquist, D. 2007 Comparative immunoecology in birds: hypotheses and tests. J. Ornithol. 148, S571-S582. (doi:10.1007/s10336-007-0201-x)
43. Rohr, J. R., Raffel, T. R. & Hall, C. A. 2010 Developmental variation in resistance and tolerance in a multihost-parasite system. Funct. Ecol. 24, 1110-1121. (doi:10.1111/j.1365-2435.2010.01709.x)
44. Johnson, P. T. J., Kellermanns, E. & Bowerman, J. 2011 Critical windows of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance. Funct. Ecol. 25, 726-734. (doi:10.1111/j.1365-2435.2010.01830.x)
45. Komar, N., Langevin, S., Hinten, S., Nemeth, N., Edwards, E., Hettler, D., Davis, B., Bowen, R. & Bunning, M. 2003 Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg. Infect. Dis. 9, 311-322.
46. Martin, L. B., Weil, Z. M. & Nelson, R. J. 2007 Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88, 2516-2528. (doi:10.1890/07-0060.1)
47. Hoverman, J. T., Gray, M. J., Haislip, N. A. & Miller, D. L. 2011 Phylogeny and ecology impact amphibian susceptibility to ranaviruses. EcoHealth 8, 301-319. (doi:10.1007/s10393-011-0717-7).
48. Kiesecker, J. M., Blaustein, A. R. & Belden, L. K. 2001 Complex causes of amphibian population declines. Nature 410, 681-684. (doi:10.1038/35070552)
49. Kiesecker, J. M. 2002 Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature. Proc. Natl Acad. Sci. USA 99, 9900-9904. (doi:10.1073/pnas.152098899)
50. Forson, D. D. & Storfer, A. 2006 Atrazine increases ranavirus susceptibility in the tiger salamander, Ambystoma tigrinum. Ecol. Appl. 16, 2325-2332. (doi:10.1890/1051-0761(2006)016[2325:AIRSIT]2.0.CO;2)
51. Rohr, J. R. et al. 2008 Agrochemicals increase trematode infections in a declining amphibian species. Nature 455, 1235-1239. (doi:10.1038/nature07281)
52. Bancroft, B. A., Baker, N. J. & Blaustein, A. R. 2008 A meta-analysis of the effects of ultraviolet B radiation and its synergistic interactions with pH, contaminants, and disease on amphibian survival. Conserv. Biol. 22, 987-996. (doi:10.1111/j.1523-1739.2008.00966.x)
53. Garner, T. W. J., Perkins, M. W., Govindarajulu, P., Segile, D., Walker, S., Cunningham, A. A. & Fisher, M. C. 2006 The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biol. Lett. 2, 455-459. (doi:10.1098/rsbl.2006.0494)
54. Harvell, C. D., Mitchell, C., Ward, J., Altizer, S., Dobson, A., Ostfeld, R. & Samuel, M. 2002 Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158-2162. (doi:10.1126/science.1063699)
55. Williams, T., Barbosa-Solomieu, V. & Chinchar, G. D. 2005 A decade of advances in iridovirus research. In Advances in virus research, vol. 65 (eds K. Maramorosch & A. Shatkin), pp. 173-248. New York, NY: Academic Press.
56. Gray, M. J., Miller, D. L. & Hoverman, J. T. 2009 Ecology and pathology of amphibian ranaviruses. Dis. Aquat. Org. 87, 243-266. (doi:10.3354/dao02138)
57. Chinchar, G. D., Essbauer, S., He, J. G., Hyatt, A., Miyazaki, T., Seligy, V. & Williams, T. 2005 Iridoviridae. In Virus taxonomy: 8th report of the Int. committee on the taxonomy of viruses (eds C. M. Fauguet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball), pp. 163-175. London, UK: Elsevier.
58. Cunningham, A. A., Langton, T. E. S., Bennett, P. M., Lewin, J. F., Drury, S. E. N., Gough, R. E. & MacGregor, S. K. 1996 Pathological and microbiological findings from incidents of unusual mortality of the common frog (Rana temporaria). Phil. Trans. R. Soc. Lond. B 351, 1539-1557. (doi:10.1098/rstb.1996.0140)
59. Bollinger, T. K., Mao, J. H., Schock, D., Brigham, R. M. & Chinchar, V. G. 1999 Pathology, isolation, and preliminary molecular characterization of a novel iridovirus from tiger salamanders in Saskatchewan. J. Wildl. Dis. 35, 413-429.
60. Green, D. E., Converse, K. A. & Schrader, A. K. 2002 Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996-2001. Ann. NY Acad. Sci. 969, 323-339. (doi:10.1111/j.1749-6632.2002.tb04400.x)
61. Carey, C., Pessier, A. P. & Peace, A. D. 2003 Pathogens, infectious disease, and immune defenses. In Amphibian conservation (ed. R. D. Semlitsch), pp. 127-136. Washington, DC: Smithsonian Institute.
62. Converse, K. A. & Green, D. E. 2005 Diseases of tadpoles. In Wildlife diseases: landscape epidemiology, spatial distribution and utilization of remote sensing technology (eds S. K. Majumdar, J. E. Huffman, F. J. Brenner & A. I. Panah), pp. 72-88. Easton, PA: Penn. Acad. Science.
63. Greer, A. L., Berrill, M. & Wilson, P. J. 2005 Five amphibian mortality events associated with ranavirus infection in south central Ontario, Canada. Dis. Aquat. Org. 67, 9-14. (doi:10.3354/dao067009)
64. Jancovich, J. K., Davidson, E. W., Parameswaran, N., Mao, J., Chinchar, V. G., Collins, J. P., Jacobs, B. L. & Storfer, A. 2005 Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. Mol. Ecol. 14, 213-224. (doi:10.1111/j.1365-294X.2004.02387.x)
65. Fox, S. F., Greer, A. L., Torres-Cervantes, R. & Collins, J. P. 2006 First case of ranavirus-associated morbidity and mortality in natural populations of the South American frog Atelognathus patagonicus. Dis. Aquat. Org. 72, 87-92. (doi:10.3354/dao072087)
66. Ariel, E., Kielgast, J., Svart, H. E., Larsen, K., Tapiovaara, H., Jensen, B. B. & Holopainen, R. 2009 Ranavirus in wild edible frogs Pelophylax kl. esculentus in Denmark. Dis. Aquat. Org. 85, 7-14. (doi:10.3354/dao02060)
67. Balseiro, A., Dalton, K. P., del Cerro, A., Marquez, I., Cunningham, A. A., Parra, F., Prieto, J. M. & Casais, R. 2009 Pathology, isolation and molecular characterisation of a ranavirus from the common midwife toad Alytes obstetricans on the Iberian Peninsula. Dis. Aquat. Org. 84, 95-104. (doi:10.3354/dao02032)
68. Une, Y., Nakajima, K., Taharaguchi, S., Ogihara, K. & Murakami, M. 2009 Ranavirus infection outbreak in the Salamander (Hynobius Nebulosus) in Japan. J. Comp. Pathol. 141, 310-310. (doi:10.1016/j.jcpa.2009.08.133)
69. Gantress, J., Maniero, G. D., Cohen, N. & Robert, J. 2003 Development and characterization of a model system to study amphibian immune responses to iridoviruses. Virology 311, 254-262. (doi:10.1016/S0042-6822(03)00151-X)
70. Harp, E. M. & Petranka, J. W. 2006 Ranavirus in wood frogs (Rana sylvatica): potential sources of transmission within and between ponds. J. Wildl. Dis. 42, 307-318.
71. Brunner, J. L., Schock, D. M. & Collins, J. P. 2007 Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Dis. Aquat. Org. 77, 87-95. (doi:10.3354/dao01845)
72. Daszak, P., Berger, L., Cunningham, A. A., Hyatt, A. D., Green, D. E. & Speare, R. 1999 Emerging infectious diseases and amphibian population declines. Emerg. Infect. Dis. 5, 735-748. (doi:10.3201/eid0506.990601)
73. Brunner, J. L., Schock, D. M., Davidson, E. W. & Collins, J. P. 2004 Intraspecific reservoirs: complex life history and the persistence of a lethal ranavirus. Ecology 85, 560-566. (doi:10.1890/02-0374)
74. Bancroft, B. A., Han, A. A., Searle, C. L., Biga, L. M., Olson, D. H., Kats, L. B., Lawler, J. J. & Blaustein, A. R. 2011 Species-level correlates of susceptibility to the pathogenic amphibian fungus Batrachochytrium dendrobatidis in the United States. Biodivers. Conserv. 20, 1911-1920. (doi:10.1007/s10531-011-0066-4)
75. Haislip, N. A., Gray, M. J., Hoverman, J. T. & Miller, D. L. 2011 Development and disease: how susceptibility to an emerging pathogen changes through anuran development. PLoS ONE 6, e22307.
76. Warne, R. W., Crespi, E. J. & Brunner, J. L. 2011 Escape from the pond: stress and developmental responses to ranavirus infection in wood frog tadpoles. Funct. Ecol. 25, 139-146. (doi:10.1111/j.1365-2435.2010.01793.x)
77. Rojas, S., Richards, K., Jancovich, J. K. & Davidson, E. W. 2005 Influence of temperature on Ranavirus infection in larval salamanders Ambystoma tigrinum. Dis. Aquat. Org. 63, 95-100. (doi:10.3354/dao063095)
78. Maniero, G. D. & Carey, C. 1997 Changes in selected aspects of immune function in the leopard frog, Rana pipiens, associated with exposure to cold. J. Comp. Physiol. B 167, 256-263. (doi:10.1007/s003600050072)
79. Gray, M. J., Miller, D. L., Schmutzer, A. C. & Baldwin, C. A. 2007 Frog virus 3 prevalence in tadpole populations inhabiting cattle-access and non-access wetlands in Tennessee, USA. Dis. Aquat. Org. 77, 97-103. (doi:10.3354/dao01837)
80. Esch, G. W., Barger, M. A. & Fellis, K. J. 2002 The transmission of digenetic trematodes: style, elegance, complexity. ICB 42, 304-312.
81. Goater, C. P. & Vandenbos, R. E. 1997 Effects of larval history and lungworm infection on the growth and survival of juvenile wood frogs (Rana sylvatica). Herpetologica 53, 331-338.
82. Yoder, H. R., Coggins, J. R. & Reinbold, J. C. 2001 Helminth parasites of the green frog (Rana clamitans) from southeastern Wisconsin, USA. Comp. Parasitol. 68, 269-272.
83. King, K. C., McLaughlin, J. D., Boily, M. & Marcogliese, D. J. 2010 Effects of agricultural landscape and pesticides on parasitism in native bullfrogs. Biol. Conserv. 143, 302-310. (doi:10.1016/j.biocon.2009.10.011)
84. Smyth, J. D. & Smyth, M. M. 1980 Frogs as host -parasite systems I: an introduction to parasitology through the parasites of Rana temporaria, R. esculenta and R. pipiens. London, UK: Macmillan Press.
85. Sutherland, D. R. 2005 Parasites of North American frogs. In Amphibian declines: the conservation status of United States species (ed. M. J. Lannoo), pp. 109-123. Berkley, CA: University of California Press.
86. Blaustein, A. R. & Johnson, P. T. 2003 The complexity of deformed amphibians. Front. Ecol. Environ. 1, 87-94. (doi:10.1890/1540-9295(2003)001[0087:TCO DA]2.0.CO;2)
87. Johnson, P. T. J., Sutherland, D. R., Kinsella, J. M. & Lunde, K. B. 2004 Review of the trematode genus Ribeiroia (Psilostomidae): ecology, life history, and pathogenesis with special emphasis on the amphibian malformation problem. Adv. Parasitol. 57, 191-253. (doi:10.1016/S0065-308X(04)57003-3)
88. Johnson, P. T. J. & McKenzie, V. J. 2008 Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in North America. In The Biology of echinostomes (eds B. Fried & R. Toledo). New York, NY: Springer.
89. Rohr, J. R., Raffel, T. R. & Sessions, S. K. 2009 Digenetic trematodes and their relationship to amphibian declines and deformities. In Amphibian biology, vol. 8. Amphibian decline: diseases, parasites, maladies, and pollution (eds H. Heatwole & J. W. Wilkinson), pp. 3067-3088. Chipping Norton, Australia: Surrey Beatty & Sons.
90. Johnson, P. T. J., Reeves, M. K., Krest, S. K. & Pinkney, A. E. 2010 A decade of deformities: advances in our understanding of amphibian malformations and their implications. In Ecotoxicology of amphibians and reptiles, 2nd edn (eds D. W. Sparling, G. Linder, C. Bishop & S. K. Krest), pp. 511-536. Pensacola, FL: SETAC Press.
91. Johnson, P. T. J., Rohr, J. R., Hoverman, J. T., Kellermanns, E., Bowerman, J. & Lunde, K. B. 2012 Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecol. Lett. 15, 235-242. (doi:10.1111/j.1461-0248.2011.01730.x)
92. Sessions, S. K. & Ruth, S. B. 1990 Explanation of naturally-occurring supernumerary limbs in amphibians. J. Exp. Zool. 254, 38-47. (doi:10.1002/jez.1402540107)
93. Johnson, P. T. J., Lunde, K. B., Ritchie, E. G. & Launer, A. E. 1999 The effect of trematode infection on amphibian limb development and survivorship. Science 284, 802-804. (doi:10.1126/science.284.5415.802)
94. Johnson, P. T. J., Lunde, K. B., Ritchie, E. G., Reaser, J. K. & Launer, A. E. 2001 Morphological abnormality patterns in a California amphibian community. Herpetologica 57, 336-352.
95. Johnson, P. T. J. et al. 2002 Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecol. Monogr. 72, 151-168. (doi:10.1890/0012-9615(2002)072[0151:PROILT]2.0.CO;2)
96. Sessions, S. K., Franssen, R. A. & Horner, V. L. 1999 Morphological clues from multilegged frogs: are retinoids to blame. Science 284, 800-802. (doi:10.1126/science.284.5415.800)
97. Schotthoefer, A. M., Koehler, A. V., Meteyer, C. U. & Cole, R. A. 2003 Influence of Ribeiroia ondatrae (Trematoda: Digenea) infection on limb development and survival of northern leopard frogs (Rana pipiens): effects of host stage and parasite-exposure level. Can. J. Zool. 81, 1144-1153. (doi:10.1139/z03-099)
98. Goodman, B. A. & Johnson, P. T. J. 2011 Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan. PLoS ONE 6, 5-10. (doi:10.1371/journal.pone.0020193)
99. Fried, B., Frazer, B. A. & Reddy, A. 1997 Chemoattraction and penetration of Echinostoma trivolvis and E. caproni cercariae in the presence of Biomphalaria glabrata, Helisoma trivolvis, and Lymnaea elodes dialysate. Parasitol. Res. 83, 193-197. (doi:10.1007/s004360050231)
100. Beasley, V. R. et al. 2005 Risk factors and the decline of the cricket frog, Acris crepitans: evidence for the involvement of herbicides, parasitism, and habitat modifications. In Amphibian declines: the conservation status of United States species (ed. M. J. Lannoo), pp. 75-87. Chicago, IL: University of Chicago Press.
101. Holland, M. P., Skelly, D. K., Kashgarian, M., Bolden, S. R., Harrison, L. M. & Cappello, M. 2007 Echinostome infection in green frogs (Rana clamitans) is stage and age dependent. J. Zool. 271, 455-462. (doi:10.1111/j.1469-7998.2006.00229.x)
102. Koprivnikar, J., Baker, R. L. & Forbes, M. R. 2006 Environmental factors influencing trematode prevalence in grey tree frog (Hyla versicolor) tadpoles in southern Ontario. J. Parasitol. 92, 997-1001. (doi:10.1645/GE-771R.1)
103. Daly, E. W. & Johnson, P. T. J. 2011 Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission. Oecologia 165, 1043-1050. (doi:10.1007/s00442-010-1778-y)
104. Belden, L. K. & Kiesecker, J. M. 2005 Glucocorticosteroid hormone treatment of larval treefrogs increases infection by Alaria sp. trematode cercariae. J. Parasitol. 91, 686-688. (doi:10.1645/GE-397R)
105. Todd, B. D. 2007 Parasites lost? An overlooked hypothesis for the evolution of alternative reproductive strategies in amphibians. Am. Nat. 170, 793-799. (doi:10.1086/521958)
106. Chase, J. M. 2003 Experimental evidence for alternative stable equilibria in a benthic pond food web. Ecol. Lett. 6, 733-741. (doi:10.1046/j.1461-0248.2003.00482.x)
107. Johnson, P. J. & Lunde, K. B. 2005 Parasite infection and limb malformations: a growing problem in amphibian conservation. In Amphibian declines: the conservation status of United States species (ed. M. Lannoo), pp. 124-138. Berkeley, CA: University of California Press.
108. Johnson, P. T. J., Chase, J. M., Dosch, K. L., Hartson, R. B., Gross, J. A., Larson, D. J., Sutherland, D. R. & Carpenter, S. R. 2007 Aquatic eutrophication promotes pathogenic infection in amphibians. Proc. Natl Acad. Sci. USA 104, 15781-15786.
109. McKenzie, V. J. & Townsend, A. R. 2007 Parasitic and infectious disease responses to a changing nitrogen cycle. EcoHealth 4, 384-396. (doi:10.1007/s10393-007-0131-3)
110. Johnson, P. T. J. & Carpenter, S. R. 2008 Influence of eutrophication on disease in aquatic ecosystems: patterns, processes, and predictions. In Infectious disease ecology: effects of ecosystems on disease and of disease on ecosystems (eds R. Ostfeld & F. Keesing), pp. 71-99. Princeton, NJ: Princeton University Press.
111. King, K. C., Mclaughlin, J. D., Gendron, A. D., Pauli, B. D., Giroux, I., Rondeau, B., Boily, M., Juneau, P. & Marcogliese, D. J. 2007 Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens) in southern Quebec. Can. Parasitol. 134, 2063-2080.
112. Hartson, R. B., Orlofske, S. A., Keller, V., Dillon Jr, R. T. & Johnson, P. T. J. Submitted. Land use and wetland spatial position jointly determine amphibian parasite communities.
113. Schotthoefer, A. M., Labak, K. M. & Beasley, V. R. 2007 Ribeiroia ondatrae cercariae are consumed by aquatic invertebrate predators. J. Parasitol. 93, 1240-1243. (doi:10.1645/GE1129R.1)
114. Thieltges, D. W., Jensen, K. T. & Poulin, R. 2008 The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407-426.
115. Johnson, P. T. J., Hartson, R. B., Larson, D. J. & Sutherland, D. R. 2008 Diversity and disease: community structure drives parasite transmission and host fitness. Ecol. Lett. 11, 1017-1026. (doi:10.1111/j.1461-0248.2008.01212.x)
116. Fisher, M. C., Garner, T. W. J. & Walker, S. F. 2009 Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time and host. Annu. Rev. Microbiol. 63, 291-310. (doi:10.1146/annurev.micro.091208.073435)
117. Piotrowski, J. S., Annis, S. L. & Longcore, J. E. 2004 Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96, 9-15. (doi:10.2307/3761981)
118. 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. (doi:10.2307/3761366)
119. 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. (doi:10.1890/06-1842.1)
120. Berger, L. et al. 1998 Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl Acad. Sci. USA. 95, 9031-9036. (doi:10.1073/pnas.95.15.9031)
121. Savage, A. E., Sredl, M. J. & Zamudio, K. R. 2011 Disease dynamics vary spatially and temporally in a North American amphibian. Biol. Conserv. 144, 1910-1915. (doi:10.1016/j.biocon.2011.03.018)
122. Johnson, M. L. & Speare, R. 2005 Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Dis. Aquat. Org. 65, 181-186. (doi:10.3354/dao065181)
123. Ortiz-Santaliestra, M. E., Fisher, M. C., Fernandez-Beaskoetzea, S., Fernandez-Beneitez, M. J. & Bosch, J. 2011 Ambient ultraviolet B radiation and prevalence of infection by Batrachochytrium dendrobatidis in two amphibian species. Conserv. Biol. 25, 975-982.
124. Johnson, M. L., Berger, L., Philips, L. & Speare, R. 2003 Fungicidal effects of chemical disinfectants, UV light, dessication and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Dis. Aquat. Org. 57, 255-260. (doi:10.3354/dao057255)
125. Webb, R., Mendez, D., Berger, L. & Speare, R. 2007 Additional disinfectants effective against the amphibian chytrid fungus Batrachochytrium dendrobatidis. Dis. Aquat. Org. 74, 13-16. (doi:10.3354/dao074013)
126. Di Rosa, I., Simoncelli, F., Fagotti, A. & Pascolini, R. 2007 Ecology: the proximate cause of frog declines. Nature 447, E4-E5. (doi:10.1038/nature05941)
127. Daszak, P., Strieby, A., Cunningham, A. A., Longcore, J. E., Brown, C. C. & Porter, D. 2004 Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetol. J. 14, 201-208.
128. Blaustein, A. R., Romansic, J. M., Scheessele, E. A., Han, B. A., Pessier, A. P. & Longcore, J. E. 2005 Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conserv. Biol. 19, 1460-1468. (doi:10.1111/j.1523-1739.2005.00195.x)
129. 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.(doi:10.1007/s10393-005-0006-4)
130. Garcia, T. S., Romansic, J. M. & Blaustein, A. R. 2006 Survival of three species of anuran metamorphs exposed to UV-B radiation and the pathogenic fungus Batrachochytrium dendrobatidis. Dis. Aquat. Org. 72, 163-169. (doi:10.3354/dao072163)
131. Searle, C. L., Gervasi, S.S., Hua, J., Hammond, J. I., Relyea, R. A., Olson, D. H. & Blaustein, A. R. 2011 Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conserv. Biol. 25, 965-974. (doi:10.1111/j.1523-1739.2011.01708.x)
132. Ron, S. R. 2005 Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropic 37, 209-221. (doi:10.1111/j.1744-7429.2005.00028.x)
133. Lips, K. R., Reeve, J. D. & Witters, L. R. 2003 Ecological traits predicting amphibian population declines in Central America. Conserv. Biol. 17, 1078-1088. (doi:10.1046/j.1523-1739.2003.01623.x)
134. Moss, A. S., Reddy, N. S., Dortaj, I. M. & Francisco, M. J. 2008 Chemotaxis of the amphibian pathogen Batrachochytrium dendrobatidis and its response to a variety of attractants. Mycologia 100, 1-5. (doi:10.3852/mycologia.100.1.1)
135. Venesky, M. D. & Parris, M. J. 2009 Effects of Batrachochytrium dendrobatidis infection on larval foraging performance. ICB 49, E176-E176.
136. Venesky, M. D., Parris, M. J. & Storfer, A. 2010 Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. Ecohealth 6, 565-575. (doi:10.1007/s10393-009-0272-7)
137. 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. Dis. Aquat. Org. 77, 113-118. (doi:10.3354/dao01838)
138. Voyles, J. et al. 2009 Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326, 582-585. (doi:10.1126/science.1176765)
139. Rosenblum, E. B., Stajich, J. E., Maddox, N. & Eisen, M. B. 2008 Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proc. Natl Acad. Sci. USA 105, 17034-17039.
140. Briggs, C. J., Knapp, R. A. & Vredenburg, V. T. 2010 Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl Acad. Sci. USA 107, 9695-9700. (doi:10.1073/pnas.0912886107)
141. Rollins-Smith, L. A. 1998 Metamorphosis and the amphibian immune system. Immunol. Rev. 166, 221-230. (doi:10.1111/j.1600-065X.1998.tb01265.x)
142. Russell, D. M., Goldberg, C. S., Waits, L. P. & Rosenblum, E. B. 2010 Batrachochytrium dendrobatidis infection dynamics in the Columbia spotted frog Rana luteiventris in north Idaho, USA. Dis. Aquat. Org. 92, 223-230. (doi:10.3354/dao02286)
143. Voyles, J., Rosenblum, E.B. & Berger, L. 2011 Interactions between Batrachochytrium dendrobatidis and its amphibian hosts: a review of pathogenesis and immunity. Microbes Infect. 13, 25-32. (doi:10.1016/j.micinf.2010.09.015)
144. Vredenburg, V. T., Knapp, R. A., Tunstall, T. S. & Briggs, C. J. 2010 Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc. Natl Acad. Sci. USA 107, 9689-9694. (doi:10.1073/pnas.0914111107)
145. Richmond, J. Q., Savage, A. E., Zamudio, K. R. & Rosenblum, E. B. 2009 Toward immunogenetic studies of amphibian chytridiomycosis: linking innate and acquired immunity. Bioscience 54, 311-320. (doi:10.1525/bio.2009.59.4.9)
146. Rollins-Smith, L. A., Carey, C., Longcore, J., Doersam, J. K., Boutte, A., Bruzgal, J. E. & Conlon, J. M. 2002 Activity of antimicrobial skin peptides from ranid frogs against Batrachochytrium dendrobatidis, the chytrid fungus associated with global amphibian declines. Dev. Comp. Immunol. 26, 471-479. (doi:10.1016/S0145-305X(01)00088-X)
147. Rollins-Smith, L. A. & Conlon, J. M. 2005 Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Dev. Comp. Immunol. 29, 589-598. (doi:10.1016/j.dci.2004.11.004)
148. Woodhams, D. C., Rollins-Smith, L. A., Carey, C., Reinert, L., Tyler, M. J. & Alford, R. A. 2006 Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia 146, 531-540. (doi:10.1007/s00442-005-0228-8)
149. Rollins-Smith, L. A., Ramsey, J. P., Reinert, J. K., Woodhams, D. C., Livo, L. J. & Carey, C. 2009 Immune defenses of Xenopus laevis against Batrachochytrium dendrobatidis. Front. Biosci. S1, 68-91.
150. Nichols, D. K., Lamirande, E. W., Pessier, A. P. & Longcore, J. E. 2001 Experimental transmission of cutaneous chytridiomycosis in dendrobatid frogs. J. Wildl. Dis. 37, 1-11.
151. Berger, L., Speare, R. & Skerratt, L. F. 2005 Distribution of Batrachochytrium dendrobatidis and pathology in the skin of green tree frogs Litorria caerulea with severe chytridiomycosis. Dis. Aquat. Org. 68, 65-70. (doi:10.3354/dao068065)
152. Ribas, L. et al. 2009 Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS ONE 4, e8408. (doi:10.1371/journal.pone.0008408)
153. Blatteis, C. M. & Sehic, E. 1997 Fever: how may circulating pyrogens signal the brain? News Physiol. Sci. 12, 1-9.
154. Richards-Zawacki, C. L. 2009 Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proc. R. Soc. B 277, 519-528. (doi:10.1098/rspb.2009.1656)
155. Geiger, C. C., Kupfer, E., Schar, S., Wolf, S. & Schmidt, B. R. 2011 Elevated temperature clears chytrid fungus infections from tadpoles of the midwife toad, Alytes obstetricans. Amphibia-Reptilia 32, 276-280. (doi:10.1163/017353711X556970)
156. Weinstein, S. 2009 An aquatic disease on a terrestrial salamander: individual and population level effects of the amphibian chytrid fungus, Batrachochytrium dendrobatidis, on Batrachoseps attenuatus (Plethodontidae). Copeia 4, 653-660. (doi:10.1643/CH-08-180)
157. Retallick, R. W. R. & Miera, V. 2007 Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection. Dis. Aquat. Org. 75, 201-207. (doi:10.3354/dao075201)
158. Han, B. A., Bradley, P. W. & Blaustein, A. R. 2008 Ancient behaviors of larval amphibians in response to an emergent fungal pathogen, Batrochochytrium dendrobatidis. Behav. Ecol. Sociobiol. 63, 241-250. (doi:10.1007/s00265-008-0655-8)
159. Harris, R. N., James, T. Y., Lauer, A., Simon, M. A. & Patel, A. 2006 Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3, 53-56. (doi:10.1007/s10393-005-0009-1)
160. Brucker, R. M., Harris, R. N., Schwantes, C. R., Gallaher, T. N., Flaherty, D. C., Lam, B. A. & Minbiole, K. P. C. 2008 Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J Chem. Ecol. 34, 1422-1429. (doi:10.1007/s10886-008-9555-7)
161. Lam, B. A., Walton, D. B. & Harris, R. N. 2011 Motile zoospores of Batrachochytrium dendrobatidis move away from antifungal metabolites produced by amphibian skin bacteria. Ecohealth 8, 36-45. (doi:10.1007/s10393-011-0689-7)
162. Bettin, C. & Greven, H. 1986 Bacteria on the skin of Salamandra salamandra (L) (Amphibia, Urodela) with notes on their possible significance. Zool. Anz. 216, 267-270.
163. Barra, D., Simmaco, M. & Boman, H. G. 1998 Gene-encoded peptide antibiotics and innate immunity. Do 'animalcules' have defence budgets. FEBS Lett. 430, 130-134.
164. Austin Jr, R. M. 2000 Cutaneous microbial flora and antibiosis in Plethodon ventralis. In The biology of plethodontid salamanders (eds R. C. Bruce, R. G. Jaegar & L. D. Houck), pp. 451-462. New York, NY: Kluwer Academic/Plenum Publishers.
165. Culp, C. E., Falkinham, J. O. & Belden, L. K. 2007 Identification of the natural bacterial microflora on the skin of eastern newts, bullfrog tadpoles and redback salamanders. Herpetologica 63, 66-71. (doi:10.1655/0018-0831(2007)63[66:IOTNBM]2.0.CO;2)
166. Lauer, A., Simon, M. A., Banning, J. L., Andre, E., Duncan, K. & Harris, R. N. 2007 Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 2007, 630-640. (doi:10.1643/0045-8511(2007)2007[630:CCBFTE]2.0.CO;2)
167. Lauer, A., Simon, M. A., Banning, J. L., Lam, B. A. & Harris, R. N. 2008 Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders. ISME J. 2, 145-157. (doi:10.1038/ismej.2007.110)
168. Brucker, R. M., Baylor, C. M., Walters, R. L., Lauer, A., Harris, R. N. & Minbiole, K.P.C. 2008 The identification of 2,4-diacetylphloroglucinol as an antifungal metabolite produced by cutaneous bacteria of the salamander Plethodon cinereus. J. Chem. Ecol. 34, 39-43. (doi:10.1007/s10886-007-9352-8)
169. Harris, R. N. et al. 2009 Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J. 3, 818-824. (doi:10.1038/ismej.2009.27)
170. Harris, R. N., Lauer, A., Simon, M. A., Banning, J. L. & Alford, R. A. 2009 Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. Dis. Aquat. Org. 83, 11-16. (doi:10.3354/dao02004)
171. Becker, M. H. & Harris, R. N. 2010 Cutaneous bacteria of the redback salamander prevent morbidity associated with a lethal disease. PLoS ONE 5, e10957.
172. McKenzie, V. J., Bowers, R. M., Fierer, N., Knight, R. & Lauber, C. L. 2012 Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. ISME J. 6, 588-596.
173. Boman, H. G. 2000 Innate immunity and the normal microflora. Immunol. Rev. 173, 5-16. (doi:10.1034/j.1600-065X.2000.917301.x)
174. Conlon, J. M. 2011 The contribution of skin antimicrobial peptides to the system of innate immunity in anurans. Cell Tissue Res. 343, 201-212. (doi:10.1007/s00441-010-1014-4)
175. Rosenblum, E. B., Stajich, J. E., Maddox, N. & Eisen, M. B. 2008 Global gene expression profile for life stages of the deadly amphibian pathogen Batcahochytrium dendrobatidis. Proc. Natl Acad. Sci. USA 105, 17034-17039.
176. Rosenblum, E. B., Fisher, M. C., James, T. Y., Stajich, J. E., Longcore, J. E., Gentry, L. R. & Poorten, T. J. 2009 A molecular perspective: biology of the emerging pathogen Batrachochytrium dendrobatidis. Dis. Aquat. Org. 92, 131-147. (doi:10.3354/dao02179)
177. Beldomenico, P.M. & Begon, M. 2009 Disease spread, susceptibility and infection intensity: vicious circles. Trends Ecol. Evol. 25, 21-27. (doi:10.1016/j.tree.2009.06.015)
178. Sodhi, N. S., Bickford, D., Diesmos, A. C., Lee, T. M., Koh, L. P., Brook, B. W., Sekercioglu, C. H. & Bradshaw, C. J. A. 2008 Measuring the meltdown: drivers of global amphibian extinction and decline. PLoS ONE 3, e1636. (doi:10.1371/journal.pone.0001636)
179. Haydon, D. T., Cleaveland, S., Taylor, L. H. & Laurenson, M. K. 2002 Identifying reservoirs of infection: a conceptual and practical challenge. Emerg. Infect. Dis. 8, 1468-1473. (doi:10.3201/eid0812.010317)
180. Hanselmann, R., Rodrigues, A., Lampo, M., Fajardo-Ramos, L., Aguirre, A. A., Kilpatrick, A. M., Rodriguez, J. P. & Daszak, P. 2004 Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela. Biol. Conserv. 120, 115-119. (doi:10.1016/j.biocon.2004.02.013)
181. Rachowicz, L. J. & Vredenburg, V. T. 2004 Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Dis. Aquat. Org. 61, 75-83. (doi:10.3354/dao061075)
182. Parris, M. J. & Beaudoin, J. G. 2004 Chytridiomycosis impacts predator-prey interactions in larval amphibian communities. Oecologia 140, 626-632. (doi:10.1007/s00442-004-1631-2)
183. Parris, M. J. & Cornelius, T. O. 2004 Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85, 3385-3395. (doi:10.1890/04-0383)
184. Rowley, J. J. L. & Alford, R. A. 2007 Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. Dis. Aquat. Org. 77, 1-9. (doi:10.3354/dao01830)
185. Searle, C., Biga, L., Spatafora, J. & Blaustein, A. R. 2011 A dilution effect in the emerging amphibian pathogen, Batrachochytrium dendrobatidis. Proc. Natl Acad. Sci USA 16322-16326. (doi:10.1073/pnas.1108490108)
186. Connelly, S., Pringle, M. C., Bixby, R. J., Brenes, R., Whiles, M. R., Lips, M. R., Kilham, S. & Huryn, A. D. 2008 Changes in stream primary producer communities resulting from large-scale catastrophic amphibian declines: can small-scale experiments predict effects of tadpole loss? Ecosystems 11, 1262-1276. (doi:10.1007/s10021-008-9191-7)
187. Carey, C., Cohen, N. & Rollins-Smith, L. 1999 Amphibian declines: an immunological perspective. Dev. Comp. Immunol. 23, 459-472. (doi:10.1016/S0145-305X(99)00028-2)
188. Power, A. G. & Mitchell, C. E. 2004 Pathogen spillover in disease epidemics. Am. Nat. 164, S79-S89. (doi:10. 1086/424610)
189. Sapolsky, R. M. 1993 Neuroendocrinology of the stress-response. In Behavioral endocrinology (eds J. B. Becker & S. M. Breedlove & D. Crews), pp. 287-324. Cambridge, MA: MIT Press.
190. Denver, R. J. 1998 Hormonal correlates of environmentally induced metamorphosis in the western spadefoot toad, Scaphiopus hammondii. Gen. Comp. Endorcr. 110, 326-336. (doi:10.1006/gcen.1998.7082)
191. Denver, R. J., Mirhadi, N. & Phillips, M. 1998 Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology 79, 1859-1872.
192. Fraker, M. E. et al. 2009 Characterization of an alarm pheromone secreted by amphibian tadpoles that induces behavioral inhibition and suppression of the neuroendocrine stress axis. Horm. Behav. 55, 520-529. (doi:10.1016/j.yhbeh.2009.01.007)
193. Hossie, T. J., Ferland-Raymond, B., Burness, G. & Murray, D. L. 2010 Morphological and behavioural responses of frog tadpoles to perceived predation risk: a possible role for corticosterone mediation. Ecoscience 17, 100-108. (doi:10.2980/17-1-3312)
194. Gendron, A. D., Bishop, C. A., Fortin, R. & Hontela, A. 1997 In vivo testing of the functional integrity of the corticosterone-producing axis in mudpuppy (Amphibia) exposed to chlorinated hydrocarbons in the wild. Environ. Toxicol. Chem. 16, 194-170.
195. Hopkins, W. A., Mendonca, M. T. & Congdon, J. D. 1997 Increased circulating levels of testosterone and corticosterone in southern toads, Bufo terrestris, exposed to coal combustion waste. Gen. Comp. Endocr. 108, 237-246. (doi:10.1006/gcen.1997.6969)
196. Larson, D. L., McDonald, S., Fivizzani, A. J., Newton, W. E. & Hamilton, S. J. 1998 Effects of the herbicide atrazine on Ambystoma tigrinum metamorphosis: duration, larval growth, and hormonal response. Physiol. Zool. 71, 671-679.
197. Peterson, J. D., Peterson, V. A. & Mendonca, M. T. 2009 Exposure to coal combustion residues during metamorphosis elevates corticosterone content and adversely affects oral morphology, growth, and development in Rana sphenocephala. Comp. Biochem. Phys. C 149, 36-39.
198. Janin, A., Lena, J. P. & Joly, P. 2011 Beyond occurrence: body condition and stress hormone as integrative indicators of habitat availability and fragmentation in the common toad. Biol. Conserv. 144, 1008-1016. (doi:10.1016/j.biocon.2010.12.009)
199. Norris, D. O., Donahue, S., Dores, R. M., Lee, J. K., Maldonado, T. A., Ruth, T. & Woodling, J. D. 1999 Impaired adrenocorical response to stress in brown trout, Salmo trutta, living in metal-contaminated waters of the Eagle River, Colorado. Gen. Comp. Endocr. 113, 1-8. (doi:10.1006/gcen.1998.7177)
200. Cyr, N. E. & Romero, L. M. 2007 Chronic stress in free-living European starlings reduces corticosterone concentrations and reproductive success. Gen. Comp. Endocr. 151, 82-89. (doi:10.1016/j.ygcen. 2006.12.003)
201. Maule, A. G. & VanderKooi, S. P. 1999 Stress-induced immune-endocrine interactions. In Stress physiology in animals (ed. P. H. M. Balm), pp. 205-245. Sheffield, UK: Sheffield Academic Press.
202. Ottaviani, E. & Franceschi, C. 1996 The neuroimmunology of stress from invertebrates to man. Prog. Neurobiol. 48, 421-440. (doi:10.1016/0301-0082(95)00049-6)
203. Mastorakos, G., Bamberger, C. & Chrousos, G. P. 1999 Neuroendocrine regulation of the immune process. In Cytokines: stress and immunity (eds N. P. Plotnikoff, R. E. Faith, A. J. Murgo & R. A. Good), pp. 17-37. Boca Raton, CA: CRC Press.
204. Tournefier, A. 1982 Corticosteroid action on lymphocyte subpopulations and humoral immune responses of axolotl (urodele amphibian). Immunology 46, 155-162.
205. Wilckens, T. & De Rijk, R. 1997 Glucocorticoids and immune function: unknown dimensions and new frontiers. Immunol. Today 18, 418-424. (doi:10.1016/S0167-5699(97)01111-0)
206. McEwen, B. S. et al. 1997 The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res. Rev. 23, 79-133. (doi:10.1016/S0165-0173(96)00012-4)
207. Coutinho, A. E. & Chapman, K. E. 2011 The anti-inflammatory and immunosuppressive effects of glucocorticoids, recent developments and mechanistic insights. Mol. Cell. Endocrinol. 335, 2-13. (doi:10.1016/j.mce.2010.04.005)
208. Pederson, A. B. & Babayan, S. A. 2011 Wild immunology. Mol. Ecol. 20, 872-880. (doi:10.1111/j.1365-294X.2010.04938.x)
209. Hayes, T. B. 1997 Steroids as potential modulators of thyroid hormone activity in anuran metamorphosis. Am. Zool. 37, 185-194.
210. Glennemeier, K. A. & Denver, R. J. 2002 Role for corticoids in mediating the response of Rana pipiens tadpoles to intraspecific competition. J. Exp. Zool. 292, 32-40. (doi:10.1002/jez.1140)
211. Belden, L. K., Rubbo, M. J., Wingfield, J. C. & Kiesecker, J. M. 2007 Searching for the physiological mechanism of density-dependence: does corticosterone regulate tadpole responses to density? Physiol. Biochem. Zool. 80, 444-451. (doi:10.1086/518375)
212. Davis, A. K., Maney, D. L. & Maerz, J. C. 2008 The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct. Ecol. 22, 760-772. (doi:10.1111/j.1365-2435.2008.01467.x)
213. Davis, A. K. & Maerz, J. C. 2008 Comparison of hematological stress indicators in recently captured and captive paedomorphic Mole Salamanders, Ambystoma talpoideum. Copeia 2008, 613-617. (doi:10.1643/CP-07-133)
214. Davis, A. K. & Maerz, J. C. 2009 Effects of larval density on hematological stress indices in Salamanders. J. Exp. Zool. A 311A, 697-704. (doi:10.1002/jez.557)
215. McMenamin, S. K., Hadley, E. A. & Wright, C. K. 2008 Climatic change and wetland desiccation cause amphibian decline in Yellowstone National Park. Proc. Natl Acad. Sci. USA 105, 16988-16993. (doi:10.1073/pnas.0809090105)
216. Burdon, J. & Elmqvist, T. 1996 Selective sieves in the epidemiology of Melampsora lini. Plant Pathol. 45, 933-943. (doi:10.1111/j.1365-3059.1996.tb02904.x)
217. Dwyer, G. & Elkinton, J. S. 1993 Using simple models to predict virus epizootics in gypsy moth populations. J. Anim. Ecol. 62, 1-11. (doi:10.2307/5477)
218. Schindler, D. W. 1997 Widespread effects of climatic warming on freshwater ecosystems in North America. Hydrol. Process. 11, 1043-1067. (doi:10.1002/(SICI)1099-1085 (19970630)11:8,1043::AID-HYP517.3.0.CO;2-5)
219. IPCC. 2008 Climate change and water. In Technical Paper of the Intergovernmental Panel on Climate Change (eds B. C. Bates, Z. W. Kundzewicz, S. Wu, J. P. Palutikof), Geneva, Switzerland: Secretariat.
220. Kriger, K. M. 2009 Lack of evidence for the drought-linked chytridiomycosis hypothesis. J. Wildl. Dis. 45, 537-541.
221. Burrowes, P. A., Joglar, R. L. & Green, D. L. 2004 Potential causes for amphibian declines in Puerto Rico. Herpetologica 60, 141-154. (doi:10.1655/03-50)
222. Lampo, M., Rodríguez-Contreras, A., La Marca, E. & Daszak, P. 2006 A chytridiomycosis epidemic and a severe dry season precede the disappearance of Atelopus species from the Venezuelan Andes. Herpetol. J. 16, 395-402.
223. Seimon, T. A. et al. 2007 Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Glob. Change Biol. 13, 288-299. (doi:10.1111/j.1365-2486. 2006.01278.x)
224. Kupferberg, S. J., Catenazzi, A., Lunde, K., Lind, A. J., Palen, W. J. 2009 Parasitic Copepod (Lernaea cyprinacea) outbreaks in foothill yellow-legged Frogs (Rana boylii) linked to unusually warm summers and amphibian malformations in Northern California. Copeia 2009, 529-537. (doi:10.1643/CH-08-011)
225. Pounds, A. et al. 2006 Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161-167. (doi:10.1038/nature04246)
226. Bosch, J., Carrascal, L. M., Duran, L., Walker, S. & Fisher, M. C. 2006 Climate change and outbreaks of amphibian chytridiomycosis in a montane area of Central Spain; is there a link? Proc. R. Soc. B 274, 253-260. (doi:10.1098/rspb.2006.3713)
227. D'Amen, M. & Bombi, P. 2009 Global warming and biodiversity: evidence of climate-linked amphibian declines in Italy. Biol. Conserv. 142, 3060-3067. (doi:10.1016/j.biocon.2009.08.004)
228. Drew, A., Allen, E. J. & Allen, L. J. S. 2006 Analysis of climatic and geographic factors affecting the presence of chytridiomycosis in Australia. Dis. Aquat. Org. 68, 245-250. (doi:10.3354/dao068245)
229. 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 Biol. 6, 441-454.
230. Parmesan, C. & Singer, M. C. 2008 Amphibian extinctions: disease not the whole story. Plos Biol. 28 March 2008. (doi:10.1371/journal.pbio.0060072#r2213)
231. 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. Proc. Natl Acad. Sci. USA 105, 17436-17441. (doi:10. 1073/pnas.0806368105)
232. Daszak, P., Scott, D. E., Kilpatrick, A. M., Faggioni, C., Gibbons, J. W. & Porter, D. 2005 Amphibian population declines at Savannah River Site are linked to climate, not chytridiomycosis. Ecology 86, 3232-3237. (doi:10.1890/05-0598)
233. Van Sluys, M. & Hero, J.-M. 2009 How does Chytrid infection vary among habitats? The case of Litoria wilcoxii (Anura, Hylidae) in SE Queensland, Australia. EcoHealth 6, 576-583. (doi:10.1007/s10393-010-0278-1)
234. Muths, E., Pilliod, D. S. & Livo, L. J. 2008 Distribution and environmental limitations of an amphibian pathogen in the Rocky Mountains, USA. Biol. Conserv. 141, 1484-1492. (doi:10.1016/j.biocon. 2008.03.011)
235. Raffel, T. R., Michel, P. J., Sites, E. W. & Rohr, J. R. 2010 What drives Chytrid infections in newt populations? Associations with substrate, temperature, and shade. EcoHealth 7, 526-536. (doi:10.1007/s10393010-0358-2)
236. Rohr, J. R., Halstead, N. T. & Raffel, T. R. 2011 Modelling the future distribution of the amphibian chytrid fungus: the influence of climate and human-associated factors. J. Appl. Ecol. 48, 174-176. (doi:10.1111/j. 1365-2664.2010.01891.x)
237. Paull, S. H. & Johnson, P. T. J. In press. Predicting the synergies between climate change and infectious disease. In Conserving wildlife populations in a changing climate (eds J. Brodie, E. Post & D. Doak). Chicago, IL: University of Chicago Press.
238. Lawler, J. J., White, D., Neilson, R. P. & Blaustein, A. R. 2006 Predicting climate-induced range shifts: model differences and model reliability. Global Change Biol. 12, 1568-1584. (doi:10.1111/j.1365-2486.2006. 01191.x)
239. Poulin, R. 2006 Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parisitology 132, 143-151. (doi:10.1017/S0031182005008693)
240. Paull, S. H. & Johnson, P. T. J. 2011 High temperature enhances host pathology in a snail-trematode system: possible consequences of climate change for the emergence of disease. Freshw. Biol. 56, 767-778. (doi:10. 1111/j.1365-2427.2010.02547.x)
241. Tracy, C. R. et al. 2006 The importance of physiological ecology in conservation biology. Integr. Compar. Biol. 46, 1191-1205. (doi:10.1093/icb/icl054)
242. Carey, C. 2005 How physiological methods and concepts can be useful in conservation biology. Integr comp. Biol. 45, 4-11. (doi:10.1093/icb/45.1.4)
243. Cronin, J. P., Welsh, M. E., Dekkers, M. G., Abercrombie, S. T. & Mitchell, C. E. 2010 Host physiological phenotype explains pathogen reservoir potential. Ecol. Lett. 13, 1221-1232. (doi:10.1111/j.1461-0248.2010. 01513.x)
244. Zuk, M. & Stoehr, A. M. 2002 Immune defense and host life history. Am. Nat. 160, S9-S22. (doi:10.1086/342131)
245. Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. 2005 Superspreading and the effect of individual variation on disease emergence. Nature 438, 355-359. (doi:10.1038/nature04153)
246. Seebacher, F. & Franklin, C. E. 2012 Determining environmental causes of biological effects: the need for a mechanistic physiological dimension in conservation biology. Phil. Trans. R. Soc. B 367, 1607-1614. (doi:10.1098/rstb.2012.0036)