Interventions for Reducing Extinction Risk in Chytridiomycosis-Threatened Amphibians

Conservation Biology

Volumn 28, Issue 5, 2014, Pages 1195-1205

  Scheele, Ben C ^a,b   Hunter, David A ^b   Grogan, Laura F ^c   Berger, Lee ^c   Kolby, Jon E ^c,d   Mcfadden, Michael S ^e   Marantelli, Gerry ^f   Skerratt, Lee F ^c   Driscoll, Don A ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b OFFICE OF ENVIRONMENT AND HERITAGE   (Australia)

^c JAMES COOK UNIVERSITY   (Australia)

^d IUCN SSC Amphibian Specialist Group Regional Co Chair (Honduras)   (Australia)

^e TARONGA CONSERVATION SOCIETY AUSTRALIA   (Australia)

^f Amphibian Research Centre   (Australia)

Author keywords

Amphibian decline; Batrachochytrium dendrobatidis; Chytrid; Disease management; Emerging infectious disease; Frog; Wildlife management

Indexed keywords

AMPHIBIA; ANURA; BATRACHOCHYTRIUM DENDROBATIDIS;

AMPHIBIA; ANIMAL; BIODIVERSITY; CHYTRIDIOMYCETES; ENDANGERED SPECIES; ENVIRONMENTAL PROTECTION; EPIDEMIC; GENETICS; MICROBIOLOGY; MYCOSES; PHYSIOLOGY; RISK ASSESSMENT; SPECIES EXTINCTION; VETERINARY;

AMPHIBIANS; ANIMALS; BIODIVERSITY; CHYTRIDIOMYCOTA; CONSERVATION OF NATURAL RESOURCES; DISEASE OUTBREAKS; ENDANGERED SPECIES; EXTINCTION, BIOLOGICAL; MYCOSES; RISK ASSESSMENT;

EID: 84907948723     PISSN: 08888892     EISSN: 15231739     Source Type: Journal    
DOI: 10.1111/cobi.12322     Document Type: Article

References (73)

1. Araki, H., B. Cooper, and M. S. Blouin 2007. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100-103.
2. Australian Government Department of the Environment and Heritage. 2006. Threat abatement plan: infection of amphibians with chytrid fungus resulting in chytridiomycosis. Canberra, Australia. Available from http://www.environment.gov.au/system/files/resources/8d01e983-3619-4d83-9b5a-6f9fb4d34e3b/files/chytrid-report.pdf (accessed December 2013).
3. Baitchman, E. J., and A. P. Pessier 2013. Pathogenesis, diagnosis, and treatment of amphibian chytridiomycosis. Veterinary Clinics of North America: Exotic Animal Practice 16:669-685.
4. Beiswenger, R. E. 1977. Diel patterns of aggregative behavior in tadpoles of Bufo americanus, in relation to light and temperature. Ecology 58:98-108.
5. Berger, L., et al. 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.
6. Berger, L., and L. Skerratt 2012. Disease strategy chytridiomycosis (infection with Batrachochytrium dendrobatidis) Version 1, 2012. Department of Sustainability, Environment, Water, Populations and Communities, Public Affairs, Canberra, Australia. Available from http://www.environment.gov.au/system/files/resources/387d3e66-3cdc-4676-8fed-759328277da4/files/chytrid-fungus-manual.pdf(accessed January 2014).
7. Bletz, M. C., A. H. Loudon, M. H. Becker, S. C. Bell, D. C. Woodhams, K. P. C. Minbiole, and R. N. Harris 2013. Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecology Letters 16:807-820.
8. Bowerman, J., C. Rombough, S. R. Weinstock, and G. E. Padgett-Flohr 2010. Terbinafine hydrochloride in ethanol effectively clears Batrachochytrium dendrobatidis in amphibians. Journal of Herpetological Medicine and Surgery 20:24-28.
9. Boyles, J. G., and C. K. R. Willis 2010. Could localized warm areas inside cold caves reduce mortality of hibernating bats affected by white-nose syndrome? Frontiers in Ecology and the Environment 8:92-98.
10. Briggs, C. J., R. A. Knapp, and V. T. Vredenburg 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.
11. Cashins, S. D., L. F. Grogan, M. McFadden, D. Hunter, P. S. Harlow, L. Berger, and L. F. Skerratt 2013. Prior infection does not improve survival against the amphibian disease chytridiomycosis. PLoS One 8. DOI:10.1371/journal.pone.0056747.
12. Chatfield, M., and C. Richards-Zawacki 2011. Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs. Diseases of Aquatic Organisms 94:235-238.
13. Daskin, J. H., R. A. Alford, and R. Puschendorf 2011. Short-term exposure to warm microhabitats could explain amphibian persistence with Batrachochytrium dendrobatidis. PLoS One 6. DOI: 10.1371/journal.pone.0026215.
14. Daszak, P., A. A. Cunningham, and A. D. Hyatt 2000. Wildlife ecology - emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287:443-449.
15. DPIPWE. 2010. Tasmanian Chytrid Management Plan. Department of Primary Industries, Parks, Water and Environment, Tasmania, Australia. Available from http://www.dpiw.tas.gov.au/inter, nsf/Attachments/LJEM-8887K5/$FILE/Tasmanian%20Frog%20Management%20Plan.pdf (accessed January 2014).
16. Fisher, M. C., D. A. Henk, C. J. Briggs, J. S. Brownstein, L. C. Madoff, S. L. McCraw, and S. J. Gurr 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186-194.
17. Forrest, M. J., and M. A. Schlaepfer 2011. Nothing a hot bath won't cure: infection rates of amphibian chytrid fungus correlate negatively with water temperature under natural field settings. PLoS One 6. DOI: 10.1371/journal.pone.0028444.
18. Frankham, R., J. D. Ballou, M. D. Eldridge, R. C. Lacy, K. Ralls, M. R. Dudash, and C. B. Fenster 2011. Predicting the probability of outbreeding depression. Conservation Biology 25:465-475.
19. Freidenburg, L. K., and D. K. Skelly 2004. Microgeographical variation in thermal preference by an amphibian. Ecology Letters 7:369-373.
20. Geiger, C. C., E. Kupfer, S. Schar, S. Wolf, and B. R. Schmidt 2011. Elevated temperature clears chytrid fungus infections from tadpoles of the midwife toad, Alytes obstetricans. Amphibia-Reptilia 32:276-280.
21. Geiger, C. C., and B. R. Schmidt 2013. Laboratory tests of antifungal agents to treat tadpoles against the pathogen Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 103:191-197.
22. Hanlon, S. M., J. L. Kerby, and M. J. Parris 2012. Unlikely remedy: fungicide clears infection from pathogenic fungus in larval southern leopard frogs (Lithobates sphenocephalus). PLoS One 7. DOI: 10.1371/journal.pone.0043573.
23. Heard, G. W., M. P. Scroggie, N. Clemann, and D. S. L. Ramsey 2013. Wetland characteristics influence disease risk for a threatened amphibian. Ecological Applications. DOI:10.1890/1813-0389.1891.
24. Hoegh-Guldberg, O., L. Hughes, S. McIntyre, D. B. Lindenmayer, C. Parmesan, H. P. Possingham, and C. D. Thomas 2008. Assisted colonization and rapid climate change. Science 321:345-346.
25. Hunter, D. A., R. Speare, G. Marantelli, D. Mendez, R. Pietsch, and W. Osborne 2010. Presence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in threatened corroboree frog populations in the Australian Alps. Diseases of Aquatic Organisms 92:209-216.
26. Johnson, M. L., L. Berger, L. Philips, and R. Speare 2003. Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 57:255-260.
27. Joseph, M. B., J. R. Mihaljevic, A. L. Arellano, J. G. Kueneman, D. L. Preston, P. C. Cross, and P. T. Johnson 2013. Taming wildlife disease: bridging the gap between science and management. Journal of Applied Ecology 50:702-712.
28. Kolby, J. E., G. E. Padgett-Flohr, and R. Field 2010. Amphibian chytrid fungus Batrachochytrium dendrobatidis in Cusuco National Park, Honduras. Diseases of Aquatic Organisms 92:245-251.
29. Kouba, A. J., et al. 2013. Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade. Biological Conservation 164:10-21.
30. Lesbarreres, D., M. S. Fowler, A. Pagano, and T. Lode 2010. Recovery of anuran community diversity following habitat replacement. Journal of Applied Ecology 47:148-156.
31. Loudon, A. H., D. C. Woodhams, L. W. Parfrey, H. Archer, R. Knight, V. McKenzie, and R. N. Harris 2013. Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). The ISME Journal. DOI:10.1038/ismej.2013.1200.
32. Martel, A., et al. 2011. Developing a safe antifungal treatment protocol to eliminate Batrachochytrium dendrobatidis from amphibians. Medical Mycology 49:143-149.
33. McCallum, H. 2012. Disease and the dynamics of extinction. Philosophical Transactions of the Royal Society B-Biological Sciences 367:2828-2839.
34. McLachlan, J. S., J. J. Hellmann, and M. W. Schwartz 2007. A framework for debate of assisted migration in an era of climate change. Conservation Biology 21:297-302.
35. McMahon, T. A., J. M. Romansic, and J. R. Rohr 2013. Non-monotonic and monotonic effects of pesticides on the pathogenic fungus Batrachochytrium dendrobatidis in culture and on tadpoles. Environmental Science & Technology 47:7958-7964.
36. Mendelson, J. R., et al. 2006. Biodiversity - confronting amphibian declines and extinctions. Science 313:48-48.
37. Muletz, C. R., J. M. Myers, R. J. Domangue, J. B. Herrick, and R. N. Harris 2012. Soil bioaugmentation with amphibian cutaneous bacteria protects amphibian hosts from infection by Batrachochytrium dendrobatidis. Biological Conservation 152:119-126.
38. Murphy, P. J., S. St-Hilaire, and P. S. Corn 2011. Temperature, hydric environment, and prior pathogen exposure alter the experimental severity of chytridiomycosis in boreal toads. Diseases of Aquatic Organisms 95:31-42.
39. Murray, K. A., D. Rosauer, H. McCallum, and L. F. Skerratt 2011. Integrating species traits with extrinsic threats: closing the gap between predicting and preventing species declines. Proceedings of the Royal Society B-Biological Sciences 278:1515-1523.
40. Murray, K. A., L. F. Skerratt, S. Garland, D. Kriticos, and H. McCallum 2013. Whether the weather drives patterns of endemic amphibian chytridiomycosis: a pathogen proliferation approach. PLoS One 8. DOI:10.1371/journal.pone.0061061.
41. Murray, K. A., L. F. Skerratt, R. Speare, and H. McCallum 2009. Impact and dynamics of disease in species threatened by the amphibian chytrid fungus, Batrachochytrium dendrobatidis. Conservation Biology 23:1242-1252.
42. Muths, E., R. D. Scherer, and D. S. Pilliod 2011. Compensatory effects of recruitment and survival when amphibian populations are perturbed by disease. Journal of Applied Ecology 48:873-879.
43. Newell, D. A., R. L. Goldingay, and L. O. Brooks 2013. Population recovery following decline in an endangered stream-breeding frog (Mixophyes fleayi) from subtropical Australia. PloS One 8. DOI: 10.1371/journal.pone.0058559.
44. Olson, D. H., D. M. Aanensen, K. L. Ronnenberg, C. I. Powell, S. F. Walker, J. Bielby, T. W. Garner, G. Weaver, and M. C. Fisher 2013. Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PloS One 8. DOI: 10.1371/journal.pone.0056802.
45. Phillott, A. D., L. F. Grogan, S. D. Cashins, K. R. McDonald, L. Berger, and L. F. Skerratt 2013. Chytridiomycosis and seasonal mortality of tropical stream-associated frogs 15 years after introduction of Batrachochytrium dendrobatidis. Conservation Biology 27:1058-1068.
46. Piotrowski, J. S., S. L. Annis, and J. E. Longcore 2004. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9-15.
47. Puschendorf, R., A. C. Carnaval, J. VanDerWal, H. Zumbado-Ulate, G. Chaves, F. Bolanos, and R. A. Alford 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.
48. Puschendorf, R., L. Hodgson, R. A. Alford, L. F. Skerratt, and J. VanDerWal 2013. Underestimated ranges and overlooked refuges from amphibian chytridiomycosis. Diversity and Distributions 19:1313-1321.
49. Puschendorf, R., C. J. Hoskin, S. D. Cashins, K. McDonald, L. F. Skerratt, J. VanDerWal, and R. A. Alford 2011. Environmental refuge from disease-driven amphibian extinction. Conservation Biology 25:956-964.
50. Raffel, T. R., P. J. Michel, E. W. Sites, and J. R. Rohr 2010. What drives chytrid infections in newt populations? Associations with substrate, temperature, and shade. EcoHealth 7:526-536.
51. Richards-Zawacki, C. L. 2010. Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proceedings of the Royal Society B-Biological Sciences 277:519-528.
52. Rohr, J. R., T. R. Raffel, A. R. Blaustein, P. T. Johnson, S. H. Paull, and S. Young 2013. Using physiology to understand climate-driven changes in disease and their implications for conservation. Conservation Physiology 1. DOI:10.1093/conphys/cot1022.
53. Rowley, J. J. L., and R. A. Alford 2013. Hot bodies protect amphibians against chytrid infection in nature. Scientific Reports 3. DOI:10.1038/srep01515.
54. Savage, A. E., M. J. Sredl, and K. R. Zamudio 2011. Disease dynamics vary spatially and temporally in a North American amphibian. Biological Conservation 144:1910-1915.
55. Savage, A. E., and K. R. Zamudio 2011. MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences of the United States of America 108:16705-16710.
56. Shoo, L. P., et al. 2011. Engineering a future for amphibians under climate change. Journal of Applied Ecology 48:487-492.
57. Skerratt, L. F., L. Berger, H. B. Hines, K. R. McDonald, D. Mendez, and R. Speare 2008. Survey protocol for detecting chytridiomycosis in all Australian frog populations. Diseases of Aquatic Organisms 80:85-94.
58. Skerratt, L. F., L. Berger, R. Speare, S. Cashins, K. R. McDonald, A. D. Phillott, H. B. Hines, and N. Kenyon 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 4:125-134.
59. Stevenson, L. A., R. A. Alford, S. C. Bell, E. A. Roznik, L. Berger, and D. A. Pike 2013. Variation in thermal performance of a widespread pathogen, the amphibian chytrid fungus Batrachochytrium dendrobatidis. PLoS One 8. DOI:10.1371/journal.pone.0073830.
60. Stockwell, M. P., J. Clulow, and M. J. Mahony 2012. Sodium chloride inhibits the growth and infective capacity of the amphibian chytrid fungus and increases host survival rates. PLoS One 7. DOI: 10.1371/journal.pone.0036942.
61. Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A. S. L. Rodrigues, D. L. Fischman, and R. W. Waller 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786.
62. Tobler, U., A. Borgula, and B. R. Schmidt 2012. Populations of a susceptible amphibian species can grow despite the presence of a pathogenic chytrid fungus. PLoS One 7. DOI:10.1371/journal.pone.0034667.
63. Venesky, M. D., J. R. Mendelson, B. F. Sears, P. Stiling, and J. R. Rohr 2012. Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation. Conservation Biology 26:586-592.
64. Venesky, M. D., T. R. Raffel, T. A. McMahon, and J. R. Rohr 2013. Confronting inconsistencies in the amphibian-chytridiomycosis system: implications for disease management. Biological Reviews. DOI: 10.1111/brv.12064.
65. Vredenburg, V. T. 2004. Reversing introduced species effects: experimental removal of introduced fish leads to rapid recovery of a declining frog. Proceedings of the National Academy of Sciences of the United States of America 101:7646-7650.
66. Vredenburg, V. T., R. A. Knapp, T. S. Tunstall, and C. J. Briggs 2010. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences of the United States of America 107:9689-9694.
67. Whiles, M. R., et al. 2006. The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Frontiers in Ecology and the Environment 4:27-34.
68. Wobeser, G. 2002. Disease management strategies for wildlife. Revue Scientifique et Technique de l'Office International des Epizooties 21:159-178.
69. Wobeser, G. 2007. Disease in wild animals: investigation and management. Springer, Berlin.
70. Woodhams, D. C., et al. 2011. Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Frontiers in Zoology 8. DOI:10.1186/1742-9994-1188-1188.
71. Woodhams, D. C., C. C. Geiger, L. K. Reinert, L. A. Rollins-Smith, B. Lam, R. N. Harris, C. J. Briggs, V. T. Vredenburg, and J. Voyles 2012. Treatment of amphibians infected with chytrid fungus: learning from failed trials with itraconazole, antimicrobial peptides, bacteria, and heat therapy. Diseases of Aquatic Organisms 98:11.
72. Young, S., R. Speare, L. Berger, and L. F. Skerratt 2012. Chloramphenicol with fluid and electrolyte therapy cures terminally ill green tree frogs (Litoria caerulea) with chytridiomycosis. Journal of Zoo and Wildlife Medicine 43:330-337.
73. Zippel, K., K. Johnson, R. Gagliardo, R. Gibson, M. McFadden, R. Browne, C. Martinez, and E. Townsend 2011. The amphibian ark: A global community for ex situ conservation of amphibians. Herpetological Conservation and Biology 6:340-352.