Mitigating amphibian chytridiomycoses in nature

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 371, Issue 1709, 2016, Pages

  Garner, Trenton W J ^a,b   Schmidt, Benedikt R ^c,d   Martel, An ^e   Pasmans, Frank ^e   Muths, Erin ^f   Cunningham, Andrew A ^a   Weldon, Che ^b   Fisher, Matthew C ^g   Bosch, Jaime ^h  

^a INSTITUTE OF ZOOLOGY   (United Kingdom)

^b NORTH WEST UNIVERSITY   (South Africa)

^c KARCH Switzerland   (Switzerland)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e GHENT UNIVERSITY   (Belgium)

^f U S GEOLOGICAL SURVEY   (United States)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

^h MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

Chytridiomycosis; Conservation strategy; Mitigation

Indexed keywords

AMPHIBIAN; CONSERVATION STATUS; DISEASE CONTROL; DISEASE INCIDENCE; DISEASE VECTOR; INFECTIOUS DISEASE; MOVEMENT; PATHOGEN; POPULATION DECLINE; SPECIES CONSERVATION;

AMPHIBIA; FUNGI;

AMPHIBIA; ANIMAL; CHYTRIDIOMYCETES; MICROBIOLOGY; MYCOSIS; PHYSIOLOGY; VETERINARY;

AMPHIBIANS; ANIMALS; CHYTRIDIOMYCOTA; MYCOSES;

EID: 84992453320     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2016.0207     Document Type: Article

References (91)

1. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ. 2012 Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194. (doi:10.1038/nature10947)
2. 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)
3. Martel A et al. 2014 Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346, 630–631. (doi:10.1126/science.1258268)
4. Woodhams DC et al. 2011 Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Front. Zool. 8, 8. (doi:10.1186/1742-9994-8-8)
5. Scheele BC, Hunter DA, Skerratt LF, Brannelly LA, Driscoll DA. 2015 Low impact of chytridiomycosis on frog recruitment enables persistence in refuges despite high adult mortality. Biol. Conserv. 182, 36–43. (doi:10.1016/j.biocon.2014.11.032)
6. Skerratt LF et al. 2016 Priorities for management of chytridiomycosis in Australia: saving frogs from extinction. Wildl. Res. 43, 105–120. (doi:10.1071/WR15071)
7. Converse SJ, Bailey LL, Mosher BA, Funk WC, Gerner BD, Muths E. 2016 A model to inform management actions as a response to chytridiomycosis-associated decline. Ecohealth. (doi:10.1007/s10393-016-1117-9)
8. Grant EHC, Zipkin EF, Nichols JD, Campbell JP. 2013 A strategy for monitoring and managing declines in an amphibian community. Conserv. Biol. 27, 1245–1253. (doi:10.1111/cobi.12137)
9. Langwig KE et al. 2015 Context-dependent conservation responses to emerging wildlife diseases. Front. Ecol. Environ. 13, 195–202. (doi:10.1890/140241)
10. Gray MJ et al. 2015 Batrachochytrium salamandrivorans: the North American response and a call for action. PLoS Pathog. 11, e1005251. (doi:10.1371/journal.ppat.1005251)
11. Walker SF et al. 2008 Invasive pathogens threaten species recovery programs. Curr. Biol. 18, R853–R854. (doi:10.1016/j.cub.2008.07.033)
12. Weldon C, Fisher MC. 2011 The effect of trademediated spread of amphibian chytrid on amphibian conservation. In Fungal diseases: an emerging challenge to human, animal, and plant health (ed. IOM (Institute of Medicine)), pp. 355–367. Washington, DC: The National Academies Press.
13. Wombwell E, Garner TWJ, Cunningham AA, Quest R, Pritchard S, Rowcliffe JM, Griffiths R. 2016 Detection of Batrachochytrium dendrobatidis in amphibians imported into the UK for the pet trade. Ecohealth. (doi:10.1007/s10393-016-1138-4)
14. Schloegel LM, Daszak P, Cunningham AA, Speare R, Hill B. 2010 Two amphibian diseases, chytridiomycosis and ranaviral disease, are now globally notifiable to the World Organization for Animal Health (OIE): an assessment. Dis. Aquat. Organ. 92, 101–108. (doi:10.3354/dao02140)
15. Scheele BC, Hunter DA, Grogan LF, Berger L, Kolby JE, McFadden MS, Marantelli G, Skerratt LF, Driscoll DA. 2014 Interventions for reducing extinction risk in chytridiomycosis-threatened amphibians. Conserv. Biol. 28, 1195–1205. (doi:10.1111/cobi.12322)
16. Smith RK, Sutherland WJ. 2014 Amphibian conservation: global evidence for the effects of interventions. Exeter, UK: Pelagic Publishing.
17. Hudson MA et al. 2016 In-situ itraconazole treatment improves survival rate during an amphibian chytridiomycosis epidemic. Biol. Conserv. 195, 37–45. (doi:10.1016/j.biocon.2015.12.041)
18. Olson DH et al. 2013 Mapping the Global Emergence of Batrachochytrium dendrobatidis, the Amphibian Chytrid Fungus. PLoS ONE 8, e56802. (doi:10.1371/journal.pone.0056802)
19. Weldon C, du Preez LH, Hyat AD, Muller R, Speare R. 2004 Origin of the amphibian chytrid fungus. Emerg. Infect. Dis. 10, 2100–2105. (doi:10.3201/eid1012.030804)
20. Farrer RA et al. 2011 Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc. Natl Acad. Sci. USA 108, 18 732–18 736. (doi:10.1073/pnas.1111915108)
21. Bottrill MC et al. 2008 Is conservation triage just smart decision making? Trends Ecol. Evol. 23, 649–654. (doi:10.1016/j.tree.2008.07.007)
22. Muths E, Fisher RN. 2016 An alternative framework for responding to the amphibian crisis. Oryx. (doi:10.1017/S0030605315001131)
23. Doddington BJ, Bosch J, Oliver JA, Grassly NC, Garcia G, Schmidt BR, Garner TWJ, Fisher MC. 2013 Context-dependent amphibian host population response to an invading pathogen. Ecology 94, 1795–1804. (doi:10.1890/12-1270.1)
24. Grant EHC et al. 2015 Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States—developing research, monitoring, and management strategies. U.S. Geological Survey Open-File Report 2015–1233, p. 16. See http://dx.doi.org/10.3133/ofr20151233.
25. Vredenburg VT, Briggs CJ, Harris RN. 2011 Host pathogen dynamics of amphibian chytridiomycosis: the role of the skin microbiome in health and disease. In Fungal diseases: an emerging threat to human, animal, and plant health (eds L Olson, E Choffnes, D Relman, L Pray), pp. 342–355. Washington, DC: National Academy Press.
26. Muths E, Bailey LL, Watry MK. 2014 Animal reintroductions: an innovative assessment of survival. Biol. Conserv. 172, 200–208. (doi:10.1016/j.biocon.2014.02.034)
27. Bosch J, Sanchez-Tomè, Fernàndez-Loras A, Oliver JA, Fisher MC, Garner TWJ. 2015 Successful elimination of a lethal wildlife infectious disease in nature. Biol. Lett. 11, 20150874. (doi:10.1098/rsbl.2015.0874)
28. Fellers GM, Bradford DF, Pratt D, Wood LL. 2007 Demise of repatriated populations of mountain yellow-legged frogs (Rana muscosa) in the Sierra Nevada of California. Herpetol. Conserv. Biol. 2, 5–21.
29. Rija AA, Khatibu FH, Kohi EM, Muheto R. 2011 Status and reintroduction of the Kihansi spray toad Nectophrynoides asperginis in Kihansi gorge: challenges and opportunities. In Proc. of the 7th TAWIRI Scientific Conference, pp. 11–20.
30. Brannelly LA, Hunter DA, Skerratt LF, Scheele BC, Lenger D, McFadden MS, Harlow PS, Berger L. 2016 Chytrid infection and post-release fitness in the reintroduction of an endangered alpine tree frog. Anim. Conserv. 19, 153–162. (doi:10.1111/acv.12230)
31. Bosch J, Carrascal LM, Duràn L, Walker S, Fisher MC. 2007 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)
32. IUCN/SSC. 2013 Guidelines for reintroductions and other conservation translocations. Version 1.0. Gland, Switzerland: IUCN Species Survival Commission, viiiiþ57 pp.
33. Harris RN, James TY, Lauer A, Simon MA, 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)
34. Kueneman JG, Woodhams DC, Van Treuren W, Archer HM, Knight R, McKenzie VJ. 2016 Inhibitory bacteria reduce fungi on early life stages of endangered Colorado boreal toads (Anaxyrus boreas). ISME J. 10, 934–944. (doi:10.1038/ismej.2015.168)
35. Bletz MC, Loudon AH, Becker MH, Bell SC, Woodhams DC, Minbiole KPC, Harris RN. 2013 Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecol. Lett. 16, 807–820. (doi:10.1111/ele.12099)
36. Woodhams DC, Bletz M, Kueneman J, McKenzie V. 2016 Managing amphibian disease with skin microbiota. Trends Microbiol. 24, 161–164. (doi:10.1016/j.tim.2015.12.010)
37. Robyn J, Rasschaert G, Messens W, Pasmans F, Heyndrickx M. 2012 Screening for lactic acid bacteria capable of inhibiting Campylobacter jejuni in in vitro simulations of the broiler chicken caecal environment. Beneficial Microbes 3, 299–308. (doi:10.3920/BM2012.0021)
38. Robyn J, Rasschaert G, Hermans D, Pasmans F, Heyndrickx M. 2013 In vivo broiler experiments to assess anti-Campylobacter jejuni activity of a live Enterococcus faecalis strain. Poultry Sci. 92, 265–271. (doi:10.3382/ps.2012-02712)
39. Daskin JH, Alford RA. 2012 Context-dependent symbioses and their potential roles in wildlife diseases. Proc. R. Soc. B 279, 1457–1465. (doi:10.1098/rspb.2011.2276)
40. Woodhams DC et al. 2014 Interacting symbionts and immunity in the Amphibian skin mucosome predict disease risk and probiotic effectiveness. PLoS ONE 9, e96375. (doi:10.1371/journal.pone.0096375)
41. Antwis RE, Preziosi RF, Harrison XA, Garner TWJ. 2015 Amphibian symbiotic bacteria do not show a universal ability to inhibit growth of the global panzootic lineage of Batrachochytrium dendrobatidis. Appl. Environ. Microbiol. 81, 3706–3711. (doi:10.1128/AEM.00010-15)
42. Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S. 2002 Agricultural sustainability and intensive production practices. Nature 418, 671–677. (doi:10.1038/nature01014)
43. Hanlon SM, Parris MJ. 2014 The interactive effects of chytrid fungus, pesticides, and exposure timing on gray treefrog (Hyla versicolor) larvae. Environ. Toxicol. Chem. 33, 216–222. (doi:10.1002/etc.2419)
44. Hanlon SM, Lynch KJ, Kerby JL, Parris MJ. 2015 The effects of a fungicide and chytrid fungus on anuran larvae in aquatic mesocosms. Environ. Sci. Pollut. Res. 22, 12929–12940. (doi:10.1007/s11356-015-4566-8)
45. Dayan FE, Cantrell CL, Duke SO. 2009 Natural products in crop protection. Bioorg. Med. Chem. 17, 4022–4034. (doi:10.1016/j.bmc.2009.01.046)
46. Stearns SC. 2012 Evolutionary medicine: its scope, interest and potential. Proc. R. Soc. B 279, 4305–4321. (doi:10.1098/rspb.2012.1326)
47. Farrer RA, Henk DA, Garner TWJ, Balloux F, Woodhams DC, Fisher MC. 2013 Chromosomal copy number variation, selection and uneven rates of recombination reveal cryptic genome diversity linked to pathogenicity. PLoS Genet. 9, e1003703. (doi:10.1371/journal.pgen.1003703)
48. Holloman DW. 2015 Fungicide resistance: 40 years on and still a major problem. In Fungicide resistance in plant pathogens (eds H Ishii, DW Holloman), pp. 3–11. New York, NY: Springer.
49. Savage AE, Zamudio KR. 2016 Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations. Proc. R. Soc. B 283, 20153115. (doi:10.1098/rspb.2015.3115)
50. Brannelly LA, Hunter DA, Skerratt LF, Scheele BC, Lenger D, McFadden MS, Harlow PS, Berger L. 2016 Chytrid infection and post-release fitness in the reintroduction of an endangered alpine tree frog. Anim. Conserv. 19, 153–162. (doi:10.1111/acv.12230)
51. Kilpatrick AM. 2006 Facilitating the evolution of resistance to avian malaria in Hawaiian birds. Biol. Conserv. 128, 475–485. (doi:10.1016/j.biocon.2005.10.014)
52. Venesky MD, Mendelson III JR, Sears BF, Stiling P, Rohr JR. 2012 Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation. Conserv. Biol. 26, 586–592. (doi:10.1111/j.1523-1739.2012.01854.x)
53. Edholm E-S, Goyos A, Taran J, Andino FDJ, Ohta Y, Robert J. 2014 Unusual evolutionary conservation and further species-specific adaptations of a large family of nonclassical MHC class Ib genes across different degrees of genome ploidy in the amphibian subfamily Xenopodinae. Immunogenetics 66, 411–426. (doi:10.1007/s00251-014-0774-5)
54. Robert J, Edholm ES. 2014 A prominent role for invariant T cells in the amphibian Xenopus laevis tadpoles. Immunogenetics 66, 513–523. (doi:10.1007/s00251-014-0781-6)
55. Savage AE, Kiemnec-Tyburczy KM, Ellison AR, Fliescher RC, Zamudio KR. 2014 Conservation and divergence in the frog immunome: pyrosequencing and de novo assembly of immune tissue transcriptomes. Gene 542, 98–108. (doi:10.1016/j.gene.2014.03.051)
56. Raffel TR, Romansic JM, Halstead NT, McMahon TA, Venesky MD, Rohr JR. 2012 Disease and thermal acclimation in a more variable and unpredictable climate. Nat. Clim. Change 3, 146–151. (doi:10.1038/nclimate1659)
57. 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)
58. Garner TWJ, Rowcliffe JM, Fisher MC. 2011 Climate change, chytridiomycosis or condition: an experimental test of amphibian survival. Glob. Change Biol. 17, 667–675. (doi:10.1111/j.1365-2486.2010.02272.x)
59. Clare FC et al. 2016 Climate forcing of an emerging pathogenic fungus across a montane multi-host community. Phil. Trans. R. Soc. B 371, 20150454. (doi:10.1098/rstb.2015.0454)
60. Cho SW, Kim S, Kim JM, Kim JS. 2013 Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 230–232. (doi:10.1038/nbt.2507)
61. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013 RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol. 31, 233–239. (doi:10.1038/nbt.2508)
62. Johnson JA, Altwegg R, Evans DM, Ewen JG, Gordon IJ, Pettorelli N, Young JK. 2016 Is there a future for genome-editing technologies in conservation? Anim. Conserv. 19, 97–101. (doi:10.1111/acv.12273)
63. Rollins-Smith LA, Ramsey JP, Reinert LK, Woodhams DC, Livo LJ, Carey C. 2009 Immune defenses of Xenopus laevis against Batrachochytrium dendrobatidis. Front. Biosci. S1, 68–91. (doi:10.2741/s8)
64. Stice MJ, Briggs CJ. 2010 Immunization is ineffective at preventing infection and mortality due to the amphibian chytrid fungus Batrachochytrium dendrobatidis. J. Wildl. Dis. 46, 70–77. (doi:10.7589/0090-3558-46.1.70)
65. McMahon TA et al. 2014 Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 511, 224–227. (doi:10.1038/nature13491)
66. Andino FDJ, Chen G, Li Z, Grayfer L, Robert J. 2012 Susceptibility of Xenopus laevis tadpoles to infection by the ranavirus Frog-Virus 3 correlates with a reduced and delayed innate immune response in comparison with adult frogs. Virology 432, 435–443. (doi:10.1016/j.virol.2012.07.001)
67. Geiger CC, Schmidt BR. 2013 Laboratory tests of antifungal agents to treat tadpoles against the pathogen Batrachochytrium dendrobatidis. Dis. Aquat. Organ. 103, 191–197. (doi:10.3354/dao02576)
68. Hels T, Nachman G. 2002 Simulating viability of a spadefoot toad Pelobates fuscus metapopulation in a landscape fragmented by a road. Ecography 25, 730–744. (doi:10.1034/j.1600-0587.2002.250609.x)
69. Conroy SDS, Brook BW. 2003 Demographic sensitivity and persistence of the threatened whiteand orange-bellied frogs of Western Australia. Popul. Ecol. 45, 105–114. (doi:10.1007/s10144-003-0145-9)
70. Di Minin E, Griffiths RA. 2011 Viability analysis of a threatened amphibian population: modelling the past, present and future. Ecography 34, 162–169. (doi:10.1111/j.1600-0587.2010.06263.x)
71. Spellberg B. 2011 Vaccines for invasive fungal infections. F1000 Med Rep 3, 13. (doi:10.3410/M3-13)
72. Cassone A, Casadevall A. 2012 Recent progress in vaccines against fungal diseases. Curr. Opin. Microbiol. 15, 427–433. (doi:10.1016/j.mib.2012.04.004)
73. Mignon B, Tabart J, Baldo A, Mathy A, Losson B, Vermout S. 2008 Immunization and dermatophytes. Curr. Opin. Infect. Dis. 21, 134–140. (doi:10.1097/QCO.0b013e3282f55de6)
74. Blooi M, Martel A, Vercammen F, Haesebrouck F, Pasmans F. 2015 Treatment of urodelans based on temperature dependent infection dynamics of Batrachochytrium salamandrivorans. Sci. Rep. 5, 8037. (doi:10.1038/srep08037)
75. Spitzen-van der Sluijs A, Martel A, Hallmann C, Bosman W, Garner TWJ, Van Rooij P, Jooris R, Haesebrouck F, Pasmans F. 2014 Environmental determinants of recent endemism of Batrachochytrium dendrobatidis infections in amphibian assemblages in the absence of disease outbreaks. Conserv. Biol. 28, 1302–1311. (doi:10.1111/cobi.12281)
76. Puschendorf R, Hodgson L, Alford RA, Skerratt LF, VanDerWal J. 2013 Underestimated ranges and overlooked refuges from amphibian chytridiomycosis. Diver. Distrib. 19, 1313–1321. (doi:10.1111/ddi.12091)
77. Walker SF et al. 2010 Factors driving pathogenicity versus prevalence of the amphibian pathogen Batrachochytrium dendrobatidis and chytridiomycosis in Iberia. Ecol. Lett. 13, 372–382. (doi:10.1111/j.1461-0248.2009.01434.x)
78. Denton JS, Hitchings SP, Beebee TJC, Gent A. 1997 A recovery program for the natterjack toad (Bufo calamita) in Britain. Conserv. Biol. 11, 1329–1338. (doi:10.1046/j.1523-1739.1997.96318.x)
79. Schmeller DS et al. 2014 Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Curr. Biol. 24, 176–180. (doi:10.1016/j.cub.2013.11.032)
80. Roznik EA, Sapsford DA, Pike L, Schwarzkopf L, Alford RA. 2015 Natural disturbance reduces disease risk in endangered rainforest frog populations. Sci. Rep. 5, 13472. (doi:10.1038/srep13472)
81. Stockwell MP, Storrie LJ, Pollard CJ, Clulow J, Mahoney MJ. 2015 Effects of pond salinization on survival rate of amphibian hosts infected with the chytrid fungus. Conserv. Biol. 29, 391–399. (doi:10.1111/cobi.12402)
82. Mitchell KM, Churcher TS, Garner TWJ, Fisher MC. 2008 Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction. Proc. R. Soc. B 275, 329–334. (doi:10.1098/rspb.2007.1356)
83. Briggs CJ, Knapp RA, Vredenburg VT. 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)
84. Muths E, Scherer RD, Pilliod DS. 2011 Compensatory effects of recruitment and survival when amphibian populations are perturbed by disease. J. Appl. Ecol. 48, 873–879. (doi:10.1111/j.1365-2664.2011.02005.x)
85. Lebreton J-D. 2005 Dynamical and statistical models for exploited populations. Aust. N. Z. J. Stat. 47, 49–63. (doi:10.1111/j.1467-842X.2005.00371.x)
86. Martin TG et al. 2012 Acting fast helps avoid extinction. Conserv. Lett. 5, 274–280. (doi:10.1111/j.1755-263X.2012.00239.x)
87. Kendall WL. 2001 Using models to facilitate complex decisions. In Modeling in natural resource management: valid development, interpretation and application (eds TM Shenk, AB Franklin), pp. 147–170. Washington, DC: Island Press.
88. Martin J, Runge MC, Nichols JD, Lubow BC, Kendall WL. 2009 Structured decision making as a conceptual framework to identify thresholds for conservation and management. Ecol. Appl. 19, 1079–1090. (doi:10.1890/08-0255.1)
89. Canessa S, Guillera-Arroita G, Lahoz-Monfort JJ, Southwell DM, Armstrong DP, Chadès I, Lacy RC, Converse SJ. 2015 When do we need more data? A primer on calculating the value of information for applied ecologists. Methods Ecol. Evol. 6, 1219–1228. (doi:10.1111/2041-210X.12423)
90. Nichols JD, Johnson FA, Williams BK, Boomer SG. 2015 On formally integrating science and policy: walking the walk. J. Appl. Ecol. 52, 539–543. (doi:10.1111/1365-2664.12406)
91. Sarkar S, David FM. 2012 Conservation biology: ethical foundations. Nat. Educ. Knowledge 3, 3.