History and recent progress on chytridiomycosis in amphibians

Fungal Ecology

Volumn 19, Issue , 2016, Pages 89-99

  Berger, Lee ^a   Roberts, Alexandra A ^a   Voyles, Jamie ^b   Longcore, Joyce E ^c   Murray, Kris A ^d   Skerratt, Lee F ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b UNIVERSITY OF NEVADA   (United States)

^c UNIVERSITY OF MAINE   (United States)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

B. salamandrivorans; Batrachochytrium dendrobatidis; Chytridiomycosis; Conservation; Emerging infectious disease; Extinction; Population decline; Wildlife

Indexed keywords

EID: 84949033648     PISSN: 17545048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funeco.2015.09.007     Document Type: Article

References (140)

1. Alexopoulos C.J., Mims C.W., Blackwell M. Introductory Mycology 1996, John Wiley & Sons, Inc, New York.
2. Alford R.A., Richards S.J. Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 1999, 30:133-165.
3. Allender M.C., Raudabaugh D.B., Gleason F.H., Miller A.N. The natural history, ecology, and epidemiology of Ophidiomyces ophiodiicola and its potential impact on free-ranging snake populations. Fungal Ecol. 2015, 17:187-196.
4. Aziz M.-N.B., Skerratt L.F., McCallum H. Dynamics of chytridiomycosis in a Tasmanian frog community. Herpetological Review 2011, 42:53-57.
5. Bai C., Liu X., Fisher M.C., Garner T.W.J., Li Y. Global and endemic Asian lineages of the emerging pathogenic fungus Batrachochytrium dendrobatidis widely infect amphibians in China. Diversity and Distributions 2012, 18:307-318.
6. Baitchman E.J., Pessier A.P. Pathogenesis, diagnosis, and treatment of amphibian chytridiomycosis. Veterinary Clinics of North America: Exotic Animal Practice 2013, 16:669-685.
7. Bataille A., Fong J.J., Cha M., Wogan G.O., Baek H.J., Lee H., Min M.S., Waldman B. Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. Molecular Ecology 2013, 22:4196-4209.
8. Bataille A., Cashins S.D., Grogan L., Skerratt L.F., Hunter D., McFadden M., Scheele B., Brannelly L.A., Macris A., Harlow P.S., Bell S., Berger L., Waldman B. Susceptibility of amphibians to chytridiomycosis is associated with MHC class II conformation. Proceedings of the Royal Society B 2015, 20143127. 10.1098/rspb.2014.3127.
9. Berger L., Hyatt A., Speare R., Longcore J.E. Lifecycle stages of Batrachochytrium dendrobatidis, the amphibian chytrid. Diseases of Aquatic Organisms 2005, 68:51-63.
10. Berger L., Marantelli G., Skerratt L.F., Speare R. Virulence of the amphibian chytrid fungus Batrachochytium dendrobatidis varies with the strain. Diseases of Aquatic Organisms 2005, 68:47-50.
11. Berger L., Longcore J.E., Speare R., Hyatt A., Skerratt L.F. Fungal diseases in amphibians. Amphibian Decline: Disease, Parasites, Maladies, and Pollution 2009, vol. 8:2986-3052. Surrey Beatty and Sons, NSW. H. Heatwole, J.W. Wilkinson (Eds.).
12. 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. 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 1998, 95:9031-9036.
13. Berger L., Speare R., Hyatt A.D. Chytrid fungi and amphibian declines: overview, implications and future directions. Declines and Disappearances of Australian Frogs 1999, 23-33. Environment Australia, Canberra, Avail at:. http://www.environment.gov.au/biodiversity/threatened/publications/declines-and-disappearances-australian-frogs, A. Campbell (Ed.).
14. Berger L., Speare R., Hines H., 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. Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Australian Veterinary Journal 2004, 82:31-36.
15. Berger L., Speare R., Pessier A., Voyles J., Skerratt L.F. Treatment of chytridiomycosis requires urgent clinical trials. Diseases of Aquatic Organisms 2010, 92:165-174.
16. Bielby J., Cooper N., Cunningham A.A., Garner T.W.J., Purvis A. Predicting susceptibility to future declines in the world's frogs. Conservation Letters 2008, 1:82-90.
17. Bletz M.C., Loudon A.H., Beckerm M.H., Bell S.C., Woodhams D.C., Minbiole K.P.C., Harris R.N. Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecology Letters 2013, 16:807-820.
18. Bletz M.C., Rosa G.M., Andreone F., Courtois E.A., Schmeller D.S., Rabibisoa N.H.C., Rabemananjara F.C.E., Raharivololoniaina L., Vences M., Weldon C., Edmonds D., Raxworthy C.J., Harris R.N., Fisher M.C., Crottini A. Widespread presence of the pathogenic fungus Batrachochytrium dendrobatidis in wild amphibian communities in Madagascar. Scientific Reports 2015, 5:8633. 10.1038/srep08633.
19. Blooi M., Pasmans F., Longcore J.E., Spitzen-van der Sluijs A., Vercammen F., Martel A. Duplex real-time PCR for rapid simultaneous detection of Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans in amphibian samples. Journal of Clinical Microbiology 2013, 51:4173-4177.
20. Brannelly L.A., Chatfield M.W.H., Richards-Zawacki C.L. Field and laboratory studies of the susceptibility of the green treefrog (Hyla cinerea) to Batrachochytrium dendrobatidis infection. PLoS One 2012, 7:e38473.
21. Brannelly L.A., Hunter D.A., Skerratt L.F., Scheele B.C., Lenger D., McFadden M.S., Harlow P.S., Berger L. Chytrid infection and post-release fitness in the reintroduction of an endangered alpine tree frog. Animal Conservation 2015, 10.1111/acv.12230.
22. Brannelly L.A., McMahon T.A., Hinton M., Lenger D., Richards-Zawacki C.L. Batrachochytrium dendrobatidis in natural and farmed Louisiana crayfish populations: prevalence and implications. Diseases of Aquatic Organisms 2015, 112:229-235.
23. Brem F.M., Parris M.J., Padgett-Flohr G.E. Re-isolating Batrachochytrium dendrobatidis from an amphibian host increases pathogenicity in a subsequent exposure. PLoS One 2013, 8:e61260.
24. Brutyn M., D'Herde K., Dhaenens M., Van Rooij P., Verbrugghe E., Hyatt A.D., Croubels S., Deforce D., Ducatelle R., Haesebrouk F., Martel A., Pasmans F. Batrachochytrium dendrobatidis zoospore secretions rapidly disturb intercellular junctions in frog skin. Fungal Genetics and Biology 2012, 49:830-837.
25. Buck J.C., Truong L., Blaustein A.R. Predation by zooplankton on Batrachochytrium dendrobatidis: biological control of the deadly amphibian chytrid fungus?. Biodiversity and Conservation 2011, 20:3549-3553.
26. Carey C., Bruzgul J.E., Livo L.J., Walling M.L., Kuehl K.A., Dixon B.F., Pessier A.P., Alford R.A., Rodgers K.B. Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 2006, 3:5-21.
27. Cashins S., Grogan L., McFadden M., Hunter D., Harlow P., Berger L., Skerratt L. Prior infection does not improve survival against the amphibian disease chytridiomycosis. PLoS One 2013, 8:e56747.
28. Connolly J.H. A review of mucormycosis in the platypus (Ornithorhynchus anatinus). Australian Journal of Zoology 2009, 57:235-244.
29. Dahanukar N., Krutha K., Paingankar M.S., Padhye A.D., Modak N., Molur S. Endemic asian chytrid strain infection in threatened and endemic anurans of the northern Western ghats, India. PloS One 2013, 8:e77528. 10.1371/journal.pone.0077528.
30. Ellison A.R., Savage A.E., DiRenzo G.V., Langhammer P., Lips K.R., Zamudio K.R. Fighting a losing battle: vigorous immune response countered by pathogen suppression of host defenses in the chytridiomycosis-susceptible frog Atelopus zeteki. G3: Genes, Genomes, Genetics 2014, 4:1275-1289.
31. Ellison A.R., Tunstall T., DiRenzo G.V., Hughey M.C., Rebollar E.A., Belden L.K., Harris R.N., Ibáñez R., Lips K.R., Zamudio K.R. More than skin deep: functional genomic basis for resistance to amphibian chytridiomycosis. Genome Biology and Evolution 2014, 7:286-298.
32. Eskew E.A., Todd B.D. Parallels in amphibian and bat declines from pathogenic fungi. Emerging Infectious Diseases 2013, 10.3201/eid1903.120707.
33. Farrer R.A., Henk D.A., Garner T.W., Balloux F., Woodhams D.C., Fisher M.C. Chromosomal copy number variation, selection and uneven rates of recombination reveal cryptic genome diversity linked to pathogenicity. PLoS Genetics 2013, 9:e1003703.
34. Farrer R.A., Weinert L.A., Bielby J., Garner T.W., Balloux F., Clare F., Bosch J., Cunningham A.A., Weldon C., du Preez L.H., Anderson L., Pond S.L., Shahar-Golan R., Henk D.A., Fisher M.C. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proceeding of the National Academy of Sciences of the United States of America 2011, 108:18732-18736.
35. Fites J.S., Ramsey J.P., Holden W.M., Collier S.P., Sutherland D.M., Reinert L.K., Gayek A.S., Dermody T.S., Aune T.M., Oswald-Richter K., Rollins-Smith L.A. The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science 2013, 342:366-369.
36. Fites J.S., Reinert L.K., Chappell T.M., Rollins-Smith L.A. Inhibition of local immune responses by the frog-killing fungus Batrachochytrium dendrobatidis. Infection and Immunity 2014, 82:4698-4706.
37. 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. Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Molecular Ecology 2009, 18:415-429.
38. Fisher M.C., Henk D.A., Briggs C.J., Brownstein J.S., Madoff L.C., McCraw S.L., Gurr S.J. Emerging fungal threats to animal, plant and ecosystem health. Nature 2012, 484:186-194.
39. Fisher M.C., Garner T.W.J., Walker S.F. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology 2009, 63:291-310.
40. Gahl M.K., Longcore J.E., Houlahan J.E. Varying responses of northeastern north American amphibians to the chytrid pathogen Batrachochytrium dendrobatidis. Conservation Biology 2011, 26:135-141.
41. Garland S., James T.Y., Blair D., Berger L., Skerratt L.F. Polymorphic repetitive loci of the amphibian pathogen Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 2011, 97:1-9.
42. Garmyn A., Van Rooij P., Pasmans F., Hellebuyck T., Van Den Broeck W., Haesebrouck F., Martel A. Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLoS One 2012, 7:e35038.
43. Goka K., Yokoyama J., Une Y., Kuroki T., Suzuki K., Nakahara M., Kobayashi A., Inaba S., Mizutani T., Hyatt A.D. Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Molecular Ecology 2009, 18:4757-4774.
44. Gower D.J., Doherty-Bone T., Loader S.P., Wilkinson M., Kouete M.T., Tapley B., Orton F., Daniel O.Z., Wynne F., Flach E., Müller H., Menegon M., Stephen I., Browne R.K., Fisher M.C., Cunningham A.A., Garner T.W. Batrachochytrium dendrobatidis infection and lethal chytridiomycosis in caecilian amphibians (Gymnophiona). EcoHealth 2013, 2013:173-183.
45. Greenspan S.E., Longcore J.E., Calhoun A.J.K. Host invasion by Batrachochytrium dendrobatidis: fungal and epidermal ultrastructure in model anurans. Diseases of Aquatic Organisms 2012, 100:201-210.
46. Grogan L.F., Berger L., Rose K., Grillo V., Cashins S.D., Skerratt L.F. Surveillance for emerging biodiversity diseases of wildlife. PLoS Pathogens 2014, 10:e1004015.
47. Heard G.W., Scroggie M.P., Clemann N., Ramsey D.S.L. Wetland characteristics influence disease risk for a threatened amphibian. Ecological Applications 2014, 24:650-662.
48. Hyman O.J., Collins J.P. Evaluation of a filtration-based method for detecting Batrachochytrium dendrobatidis in natural bodies of water. Diseases of Aquatic Organisms 2012, 97:185-195.
49. Johnson M.L., Berger L., Phillips L., Speare R. Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid, Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 2003, 57:255-260.
50. Kilpatrick A.M., Briggs C., Daszak P. The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends in Ecology and Evolution 2010, 25:109-118.
51. Johnson M.L., Speare R. Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases 2003, 9:922-925.
52. Kilburn V.L., Ibáñez R., Green D.M. Reptiles as potential vectors and hosts of the amphibian pathogen Batrachochytrium dendrobatidis in Panama. Diseases of Aquatic Organisms 2011, 97:127-134.
53. Kirshtein J.D., Anderson C.W., Wood J., Longcore J.E., Voytek M.A. Quantitative PCR detection of Batachochtrium dendrobatidis DNA from sediments and water. Diseases of Aquatic Organisms 2007, 77:11-15.
54. Kolby J.E., Smith K.M., Berger L., Karesh W.B., Preston A., Pessier A.P., Skerratt L.F. First evidence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) and ranavirus in Hong Kong amphibian trade. PLoS One 2014, 9:e90750.
55. Kolby J.E., Smith K.M., Ramirez S.D., Rabemananjara F., Pessier A.P., Brunner J.L., Goldberg C.S., Berger L., Skerratt L.F. Rapid response to evaluate the presence of amphibian chytrid fungus Batrachochytrium dendrobatidis and ranavirus in wild amphibian populations in Madagascar. PLoS One 2015, 10:e0125330.
56. Kriger K.M., Hero J.M. Large scale seasonal variation in the prevalence and severity of chytridiomycosis. Journal of Zoology 2007, 271:352-359.
57. Kriger K.M., Hero J.-M. The chytrid fungus Batrachochytrium dendrobatidis is non-randomly distributed across amphibian breeding habitats. Diversity and Distributions 2007, 13:781-788.
58. Langhammer P.F., Lips K.R., Burrowes P.A., Tunstall T., Palmer C.M., Collins J.P. A fungal pathogen of amphibians, Batrachochytrium dendrobatidis, attenuates in pathogenicity with in vitro passages. PLoS One 2013, 8:e77630.
59. Langwig K.E., Voyles J., Wilber M.Q., Frick W.F., Murray K.A., Bolker B.M., Collins J.P., Cheng T.L., Fisher M.C., Hoyt J.R., Lindner D.L., McCallum H.I., Puschendorf R., Rosenblum E.B., Toothman M., Willis C.K.R., Briggs C.J., Kilpatrick A.M. Context-dependent conservation responses to emerging wildlife diseases. Frontiers in Ecology and the Environment 2015, 13:195-202.
60. Laurance W.F., McDonald K.R., Speare R. Epidemic disease and the catastrophic decline of Australian rain forest frogs. Conservation Biology 1996, 10:406-413.
61. Letcher P.M., Powell M.J., Churchill P.F., Chambers J.G. Ultrastructural and molecular phylogenetic delineation of a new order, the Rhizophydiales (Chytridiomycota). Mycological Research 2006, 110:898-915.
62. Letcher P.M., Powell M.J. Kappamyces, a new genus in the Chytridiales (Chytridiomycota). Nova Hedwigia 2005, 80:115-133.
63. 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. 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 2006, 103:3165-3170.
64. Liu X., Rohr J.R., Li Y. Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic. Proceedings of the Royal Society B: Biological Sciences 2013, 280. 10.1098/rspb.2012.2506.
65. Longcore J.E., Pessier A.P., Nichols D.K. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 1999, 91:219-227.
66. Longcore J.E., Letcher P.M., James T.Y. Homolaphlyctis polyrhiza gen. et sp. nov., a species in the Rhizophydiales (Chytridiomycetes) with multiple rhizoidal axes. Mycotaxon 2011, 118:433-440.
67. Longcore J.E. Rhizophydium brooksianum sp. nov., a multipored chytrid from soil. Mycologia 2004, 96:162-171.
68. Marantelli G., Berger L., Speare R., Keegan L. Distribution of the amphibian chytrid Batrachochytrium dendrobatidis and keratin during tadpole development. Pacific Conservation Biology 2004, 10:173-179.
69. Marcum R.D., St-Hilaire S., Murphy P.J., Rodnick K.J. Effects of Batrachochytrium dendrobatidis infection on ion concentrations in the boreal toad Anaxyrus (Bufo) boreas boreas. Diseases of Aquatic Organisms 2010, 91:17-21.
70. Martel A., Spitzen-van der Sluijs A., Blooi M., Bert W., Ducatelle R., Fisher M.C., Woeltjes A., Bosman W., Chiers K., Bossuyt F., Pasmans F. Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences of the United States of America 2013, 110:15325-15329.
71. Martel A., Blooi M., Adriaensen C., Van Rooij P., Beukema W., 22 others Recent introduction of chytrid fungus endangers Western Palearctic salamanders. Science 2014, 346:630-631.
72. McDonald K., Alford R. A review of declining frogs in northern Queensland. Declines and Disappearances of Australian Frogs 1999, 14-22. Environment Australia, Canberra. A. Campbell (Ed.).
73. McDonald K.R., Mendez D., Muller R., Freeman A.B., Speare R. Decline in the prevalence of chytridiomycosis in frog populations in north Queensland, Australia. Pacific Conservation Biology 2005, 2005:114-120.
74. McMahon T.A., Brannelly L.A., Chatfield M.W., Johnson P.T., Joseph M.B., McKenzie V.J., Richards-Zawacki C.L., Venesky M.D., Rohr J.R. 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 2013, 110:210-215.
75. McMahon T.A., Sears B.F., Venesky M.D., Bessler S.M., Brown J.M., Deutsch K., 11 others Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 2014, 511:224-227.
76. Minnis A.M., Lindner D.L. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biology 2013, 117:638-649.
77. Moss A.S., Carty N., San Francisco M.J. Identification and partial characterization of an elastolytic protease in the amphibian pathogen Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 2010, 92:149-158.
78. Murray K.A., Retallick R.W.R., Puschendorf R., Skerratt L.F., Rosauer D., McCallum H., Berger L., Speare R., VanDerWal J. Assessing spatial patterns of disease risk to biodiversity: implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis. Journal of Applied Ecology 2011, 48:163-173.
79. Murray K., Retallick R., McDonald K.R., Mendez D., Aplin K., Kirkpatrick P., Berger L., Hunter D., Hines H.B., Campbell R., Pauza M., Driessen M., Speare R., Richards S.J., Mahony M., Freeman A., Phillott A.D., Hero J.-M., Driscoll D., Puschendorf R., Skerratt L.F. The distribution and host range of the pandemic disease chytridiomycosis in Australia spanning surveys from 1956 to 2007. Ecology 2010, 91:1557.
80. Murray K.A., Rosauer D., McCallum H., Skerratt L.F. Integrating species traits with extrinsic threats: closing the gap between predicting and preventing species declines. Proceedings of the Royal Society B: Biological Sciences 2011, 278:1515-1523.
81. Murray K.A., Skerratt L.F., Garland S., Kriticos D., McCallum H. Whether the weather drives patterns of endemic amphibian chytridiomycosis: A pathogen proliferation approach. PLoS One 2013, 8:e61061.
82. Murray K.A., Skerratt L.F. Predicting wild hosts for amphibian chytridiomycosis: integrating host life-history traits with pathogen environmental requirements. Human and Ecological Risk Assessment 2012, 18:200-224.
83. Murray K.A., Skerratt L.F., Speare R., McCallum H. Impact and dynamics of disease in species threatened by the amphibian chytrid fungus, Batrachochytrium dendrobatidis. Conservation Biology 2009, 23:1242-1252.
84. Muths E., Scherer R.D., Pilliod D.S. Compensatory effects of recruitment and survival when amphibian populations are perturbed by disease. Journal of Applied Ecology 2011, 48:873-879.
85. Newell D.A., Goldingay R.L., Brooks L.O. Population recovery following decline in an endangered stream-breeding frog (Mixophyes fleayi) from subtropical Australia. PloS One 2013, 8:e58559.
86. Ocock J.F., Rowley J.J., Penman T.D., Rayner T.S., Kingsford R.T. Amphibian chytrid prevalence in an amphibian community in arid Australia. EcoHealth 2013, 10:77-81.
87. Olson D.H., Aanensen D.M., Ronnenberg K.L., Powell C.I., Walker S.F., Bielby J., Garner T.W.J., Weaver G., the Bd Mapping Group, Fisher M.C. Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS One 2013, 8:e56802.
88. Penner J., Adum G.B., McElroy M.T., Doherty-Bone T., Hirschfeld M., 14 others West Africa - a safe haven for frogs? A sub-continental assessment of the chytrid fungus (Batrachochytrium dendrobatidis). PLoS One 2013, 8:e56236.
89. Pessier A.P., Nichols D.K., Longcore J.E., Fuller M.S. Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). Journal of Veterinary Diagnostic Investigations 1999, 11:194-199.
90. Phillott A.D., Grogan L.F., Cashins S.D., McDonald K.R., Berger L., Skerratt L.F. Chytridiomycosis and seasonal mortality of tropical stream-associated frogs 15 years after introduction of Batrachochytrium dendrobatidis. Conservation Biology 2013, 27:1058-1068.
91. Pilliod D.S., Muths E., Scherer R.D., Bartelt P.E., Corn P.S., Hossack B.R., Lambert B.A., McCaffery R., Gaughan C. Effects of amphibian chytrid fungus on individual survival probability in wild boreal toads. Conservation Biology 2010, 24:1259-1267.
92. Piotrowski J.S., Annis S.L., Longcore J.E. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 2004, 96:9-15.
93. Piovia-Scott J., Pope K., Joy Worth S., Rosenblum E.B., Poorten T.J., Refsnider J., Rollins-Smith L.A., Reinert L.K., Wells H.J., Rejmanek D., Lawler S., Foley J. Correlates of virulence in a frog-killing fungal pathogen: evidence from a California amphibian decline. The ISME Journal 2014, 10.1038/ismej.2014.241.
94. Puschendorf R., Hoskin C.J., Cashins S.D., McDonald K., Skerratt L.F., Vanderwal J., Alford R.A. Environmental refuge from disease-driven amphibian decines. Conservation Biology 2011, 25:956-964.
95. Puschendorf R., Carnaval A.C., VanDerWal J., Zumbado-Ulate H., Chaves G., Bolanos F., Alford R.A. Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: proposing climatic refuges as a conservation tool. Diversity and Distributions 2009, 15:401-408.
96. Ramsey J.P., Reinert L.K., Harper L.K., Woodhams D.C., Rollins-Smith L.A. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infection and Immunity 2010, 78:3981-3992.
97. Robert V.A., Casadevall A. Vertebrate endothermy restricts most fungi as potential pathogens. Infectious Diseases 2009, 2009:1623-1626.
98. Rödder D., Kielgast J., Lötters S. Future potential distribution of the emerging amphibian chytrid fungus under anthropogenic climate change. Diseases of Aquatic Organisms 2010, 92:201-207.
99. Rodriguez D., Becker C.G., Pupin N.C., Haddad C.F.B., Zamudio K.R. Long-term endemism of two highly divergent lineages of the amphibian-killing fungus in the Atlantic Forest of Brazil. Molecular Ecology 2013, 23:774-787.
100. Rollins-Smith L., Ramsey J.P., Pask J.D., Reinert L.K., Woodhams D.C. Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integrated and Comparative Biology 2011, 51:552-562.
101. Rosenblum E.B., Fisher M.C., James T.Y., Stajich J.E., Longcore J.E., Gentry L.R., Poorten T.J. A molecular perspective: biology of the emerging pathogen Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 2009, 10.3354/dao02179.
102. Rosenblum E.B., James K.R., Zamudio T.J., Poorten D., Ilut D., 15 others Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proceeding of the National Academy of Sciences of the United States of America 2013, 110:9385-9398.
103. Rosenblum E.B., Poorten T.J., Joneson S., Settles M. Substrate-specific gene expression in Batrachochytrium dendrobatidis, the chytrid pathogen of amphibians. PLoS One 2012, 7:e49924.
104. Rosenblum E.B., Stajich J.E., Maddox N., Eisen M.B. Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proceeding of the National Academy of Sciences of the United States of America 2008, 105:17034-17039.
105. Rowley J.J.L., Alford R.A. Hot bodies protect amphibians against chytrid infection in nature. Scientific Reports 2013, 3:1515.
106. Savage A.E., Sredl M.J., Zamudio K.R. Disease dynamics vary spatially and temporally in a North American amphibian. Biological Conservation 2011, 144:1910-1915.
107. Savage A.E., Zamudio K.R. MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:16705-16710.
108. Scheele B.C., Guarino F., Osborne W., Hunter D.A., Skerratt L.F., Driscoll D.A. Decline and re-expansion of an amphibian despite high prevalence of chytrid fungus. Biological Conservation 2014, 170:86-91.
109. Scheele B.C., Hunter D.A., Grogan L.F., Berger L., Kolby J.E., McFadden M.S., Marantelli G., Skerratt L.F., Driscoll D.A. Interventions for reducing extinction risk in disease-threatened amphibians. Conservation Biology 2014, 28:1195-1205.
110. Scheele B.C., Hunter D., Skerratt L.F., Brannelly L., Driscoll D.A. Low impact of chytridiomycosis on frog recruitment enables persistence in refuges despite high adult mortality. Biological Conservation 2015, 182:36-43.
111. Schloegel L.M., Toledo L.F., Longcore J.E., Greenspan S.E., Vieira C.A., Lee M., Zhao S., Wangen C., Ferreira C.M., Hipolito M., Davies A.J., Cuomo C.A., Daszak P., James T.Y. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology 2012, 10.1111/j.1365-294X.2012.05710.x.
112. Schmeller D.S., Blooi M., Martel A., Garner T.W.J., Fisher M.C., Azemar F., Clare F.C., Leclerc C., Jäger L., Guevara-Nieto M., Loyau A., Pasmans F. Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Current Biology 2014, 24:176-180.
113. Scott M.E. The impact of infection and disease on animal populations: implications for conservation biology. Conservation Biology 1988, 2:40-56.
114. Skerratt L.F., Berger L., Clemann N., Hunter D.A., Marantelli G., Newell D.A., Philips A., McFadden M., Hines H.B., Scheele B.C., Brannelly L.A., Speare R., Cashins S.D., Versteegen S., West M. Priorities for management of chytridiomycosis in Australia: saving frogs from extinction. Wildlife Research 2015, (accepted for publication).
115. Skerratt L.F., Berger L., Hines H.B., McDonald K.R., Mendez D., Speare R. Survey protocol for detecting chytridiomycosis in all Australian frog populations. Diseases of Aquatic Organisms 2008, 80:85-94.
116. Skerratt L.F., Berger L., Speare R., Cashins S., McDonald K., Phillott A., Hines H., Kenyon N. The spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 2007, 4:125-134.
117. Skerratt L.F., McDonald K.R., Hines H.B., Berger L., Mendez D., Phillott A., Cashins S.D., Murray K.A., Speare R. Validation of the mapping protocol for Batrachochytrium dendrobatidis in Queensland, Australia. Diseases of Aquatic Organisms 2010, 92:117-129.
118. Skerratt L.F., Mendez D., McDonald K.R., Garland S., Livingstone J., Berger L., Speare R. Validation of diagnostic tests in wildlife: the case of chytridiomycosis in wild amphibians. Journal of Herpetology 2011, 45:444-450.
119. Spitzen-Van Der Sluijs A., Martel A., Hallmann C.A., Bosman W., Garner T.W.J., Van Rooij P., Jooris R., Haesebrouck F., Pasmans F. Environmental determinants of recent endemism of Batrachochytrium dendrobatidis infections in amphibian assemblages in the absence of disease outbreaks: environmental determinants promote Bd endemism. Conservation Biology 2014, 28. 10.1111/cobi.12281.
120. Stevenson L.A., Alford R.A., Bell S.C., Roznik E.A., Berger L., Pike D.A. Variation in thermal performance of a widespread pathogen, the amphibian chytrid fungus Batrachochytrium dendrobatidis. PLoS One 2013, 8:e73830.
121. Stockwell M.P., Bower D.S., Bainbridge L., Clulow J., Mahony M.J. Island provides a pathogen refuge within climatically suitable area. Biodiversity and Conservation 2015, 10.1007/s10531-015-0946-0.
122. Stockwell M.P., Clulow J., Mahony M.J. Evidence of a salt refuge: chytrid infection loads are suppressed in hosts exposed to salt. Oecologia 2015, 177:901-910.
123. Stuart S.N., Chanson J.S., Cox N.A., Young B.E., Rodrigues A.S.L., Fischman D.L., Waller R.W. Status and trends of amphibian declines and extinctions worldwide. Science 2004, 306:1783-1786.
124. Swei A., Rowley J.J.L., Rödder D., Diesmos M.L.L., Diesmos A.C., 28 others Is chytridiomycosis an emerging infectious disease in Asia?. PLoS One 2011, 6:e23179.
125. Symonds E.P., Trott D.J., Bird P.S., Mills P. Growth characteristics and enzyme activity in Batrachochytrium dendrobatidis isolates. Mycopathologia 2008, 166:143-147.
126. Talley B.L., Muletz C.R., Vredenburg V.T., Fleischer R.C., Lips K.R. A century of Batrachochytrium dendrobatidis in Illinois amphibians (1888-1989). Biological Conservation 2015, 182:254-261. 10.1016/j.biocon.2014.12.007.
127. Tarrant J., Cilliers D., du Preez L.H., Weldon C. Spatial assessment of amphibian chytrid fungus (Batrachochytrium dendrobatidis) in South Africa confirms endemic and widespread infection. PLoS One 2013, 8:e69591.
128. Tompkins D.M., Carver S., Jones M.E., Krkošek M., Skerratt L.F. Emerging infectious diseases of wildlife: a critical perspective. Trends in Parasitology 2015, 10.1016/j.pt.2015.01.007.
129. Voyles J., Johnson L.R., Briggs C.J., Cashins S.D., Alford R.A., Berger L., Skerratt L.F., Speare R., Rosenblum E.B. Experimental evolution alters the rate and temporal pattern of population growth in Batrachochytrium dendrobatidis, a lethal fungal pathogen of amphibians. Ecology and Evolution 2014, 4:3633-3641.
130. Voyles J., Johnson L.R., Briggs C.J., Cashins S.D., Alford R.A., Berger L., Skerratt L.F., Speare R., Rosenblum E.B. Temperature alters reproductive life history patterns in Batrachochytrium dendrobatidis, a lethal pathogen associated with the global loss of amphibians. Ecology and Evolution 2012, 2:2241-2249.
131. Voyles J., Kilpatrick A.M., Collins J.P., Fisher M.C., Frick W.F., McCallum H., Willis C.K., Blehert D.S., Murray K.A., Puschendorf R., Rosenblum E.B., Bolker B.M., Cheng T.L., Langwig K.E., Lindner D.L., Toothman M., Wilber M.Q., Briggs C.J. Moving beyond too little, too late: managing emerging infectious diseases in wild populations requires international policy and partnerships. Ecohealth 2014, 10.1007/s10393-014-0980-5.
132. Voyles J., Rosenblum E.B., Berger L. Interactions between Batrachochytrium dendrobatidis and its amphibian hosts: a review of pathogenesis and immunity. Microbes and Infection 2011, 13:25-32.
133. Voyles J., Young S., Berger L., Campbell C., Voyles W.F., Dinudom A., Cook D., Webb R., Alford R.A., Skerratt L.F., Speare R. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 2009, 326:582-585.
134. Vredenburg V.T., Knapp R.A., Tunstall T.S., Briggs C.J. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:9689-9694.
135. Walker S.F., Baldi Salas M., Jenkins D., Garner T.W.J., Cunningham A.A., Hyatt A.D., Bosch J., Fisher M.C. Environmental detection of Batrachochytrium dendrobatidis in a temperate climate. Diseases of Aquatic Organisms 2007, 77:105-112.
136. Weldon C., du Preez L.H., Hyatt A.D., Muller R., Speare R. Origin of the amphibian chytrid fungus. Emerging Infectious Diseases 2004, 10.3201/eid1012.030804.
137. Woodhams D.C., Alford R.A., Marantelli G. Emerging disease of amphibians cured by elevated body temperature. Diseases of Aquatic Organisms 2003, 55:65-67.
138. Woodhams D.C., Bosch J., Briggs C.J., Cashins S., Davis L.R., Lauer A., Muths E., Puschendorf R., Schmidt B.R., Sheafor B. Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Frontiers in Zoology 2011, 8:1-24.
139. Yap T.A., Koo M., Ambrose R.F., Wake D.B., Vredenburg V.T. Averting a North American biodiversity crisis. Science 2015, 349:481-482.
140. Young S., Whitehorn P., Berger L., Skerratt L.F., Speare R., Garland S.H., Webb R.J. Defects in host immune function in tree frogs with chronic chytridiomycosis. PLoS One 2014, 9:1-16.