In-situ itraconazole treatment improves survival rate during an amphibian chytridiomycosis epidemic

Biological Conservation

Volumn 195, Issue , 2016, Pages 37-45

  Hudson, Michael A ^a,b,c   Young, Richard P ^c,d   Lopez, Javier ^e   Martin, Lloyd ^f   Fenton, Calvin ^f   McCrea, Rachel ^b   Griffiths, Richard A ^b   Adams, Sarah Louise ^c   Gray, Gerard ^f   Garcia, Gerardo ^e   Cunningham, Andrew A ^a  

^a INSTITUTE OF ZOOLOGY   (United Kingdom)

^b UNIVERSITY OF KENT   (United Kingdom)

^c DURRELL WILDLIFE CONSERVATION TRUST   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e CHESTER ZOO   (United Kingdom)

^f Montserrat Department of the Environment   (Montserrat)

Author keywords

Amphibian declines; Antifungal; Batrachochytrium dendrobatidis; Chytridiomycosis; In situ treatment; Itraconazole

Indexed keywords

AMPHIBIAN; DISEASE TREATMENT; DRUG; FUNGICIDE; MARK-RECAPTURE METHOD; POPULATION MODELING; SPECIES CONSERVATION; SURVIVAL;

AMPHIBIA; ANIMALIA; ANURA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; LEPTODACTYLUS FALLAX;

EID: 84953410275     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2015.12.041     Document Type: Article

References (74)

1. Amphibian Conservation Summit Amphibian conservation action plan, Washington DC See:. http://www.globalamphibians.org/acap_5fsummit_5fdeclaration.pdf.
2. Baitchman E.J., Pessier A.P. Pathogenesis, diagnosis, and treatment of amphibian chytridiomycosis. Vet. Clin. North Am. Exot. Anim. Pract. 2013, 16:669-685.
3. Barbour A.B., Ponciano J.M., Lorenzen K. Apparent survival estimation from continuous mark-recapture/resighting data. Methods Ecol. Evol. 2013, 4:846-853.
4. Berger L., Skerrat L. Disease Strategy Chytridiomycosis (Infection with Batrachochytrium dendrobatidis) Version 1 2012, Department of Sustainability, Environment, Water, Populations and Communities, Public Affairs, Canberra, Australia.
5. Bielby J., Cooper N., Cunningham A.A., Garner T.W.J., Purvis A. Predicting susceptibility to future declines in the world's frogs. Conserv. Lett. 2008, 1:82-90.
6. Bletz M., et al. Widespread presence of the pathogenic fungus Batrachochytrium dendrobatidis in wild amphibian communities in Madagascar. Sci. Rep. 2015, 5:8633. 10.1038/srep08633.
7. Blomquist S.M., Zydlewski J.D., Hunter M.L. Efficacy of PIT tags for tracking the terrestrial anurans Rana pipiens and Rana sylvatica. Herpetol. Rev. 2008, 39:174-179.
8. Bosch J., Sanchez-Tomé E., Fernández-Loras A., Oliver J.A., Fisher M.C., Garner T.W.J. Successful elimination of a lethal wildlife infectious disease in nature. Biol. Lett. 2015, 10.1098/rsbl.2015.0874.
9. Boyle D.G., Boyle D.B., Olsen V., Morgan J.A.T., Hyatt A.D. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time TaqMan PCR assay. Dis. Aquat. Org. 2004, 60:141-148.
10. Brannelly L.A. Reduced itraconazole concentration and durations are successful in treating Batrachochytrium dendrobatidis infection in amphibians. J. Vis. Exp. 2014, 85.
11. Brannelly L.A., Richards-Zawacki C.L., Pessier A.P. Clinical trials with itraconazole as a treatment for chytrid fungal infections in amphibians. Dis. Aquat. Org. 2012, 101:95-104.
12. Brannelly L.A., Skerrat L.F., Berger L. Treatment trial of clinically ill corroboree frogs with chytridiomycosis with two triazole antifungals and electrolyte therapy. Vet. Res. Commun. 2015, 39:179-187.
13. Briggs C.J., Knapp R.A., Vredenberg V.T. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9695-9700.
14. Burnham K.P. A theory for combined analysis of ring recovery and recapture data. Marked Individuals in Bird Population Studies 1993, 199-213. Birkhauser Verlag, Basel. J.-D. Lebreton, P. North (Eds.).
15. Burnham K.P., Anderson D.R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2002, Springer-Verlag, New York.
16. Cashins S.D., Grogan L.F., McFadden M., Hunter M., Harlow P.S., Berger L., Skerrat L.F. Prior infection does not improve survival against the amphibian diseases chytridiomycosis. PLoS One 2013, 10.1371/journal.pone.0056747.
17. Caughley G. Directions in conservation biology. J. Anim. Ecol. 1994, 63:215-244.
18. Choquet R., Lebreton J.-D., Giminez O., Reboulet A.-M., Pradel R. U-CARE: utilities for performing goodness of fit tests and manipulating CApture-REcapture data. Ecography 2009, 32:1071-1074. (Version 2.3).
19. Daszak P., Berger L., Cunningham A.A., Hyatt A.D., Green D.E., Speare R. Emerging infectious diseases and amphibian population declines. Emerg. Infect. Dis. 1999, 5:735-748.
20. Daszak P., Cunningham A.A., Hyatt A.D. Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 2000, 287:443-449.
21. Dawson J., Patel F., Griffiths R., Young R. Assessing the global zoo response to the amphibian crisis through 20-year trends in captive collections. Conserv. Biol. 2015, 10.1111/cobi.12563.
22. Fa J., Hedges B., Ibéné B., Breuil M., Powell R., Magin C. Leptodactylus fallax. The IUCN Red List of Threatened Species. Version 2014.3 2010, (. Downloaded 10 March 2015).
23. Fites J.S., et al. The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science 2013, 342:366-369.
24. Fong G.A., Viña Dávila N., López-Iborra G.M. Amphibian hotspots and conservation priorities in eastern Cuba identified by species distribution modelling. Biotropica 2015, 47:119-127.
25. Forzan M., Gunn H., Scott P. Chytridiomycosis in an aquarium collection of frogs: diagnosis, treatment, and control. J. Zoo Wildl. Med. 2008, 39:406-411.
26. Garcia G., Cunningham A.A., Horton D.L., Garner T.W.J., Hyatt A., Hengstberger S., Lopez J., Orgrodowczyk A., Fenton C., Fa J.E. Mountain chickens Leptodactylus fallax and sympatric amphibians appear to be disease free on Montserrat. Oryx 2007, 41:398-401.
27. Garner T.W.J., Garcia G., Carroll B., Fisher M.C. Using itraconazole to clear Batrachochytrium dendrobatidis infection, and subsequent depigmentation of Alytes muletensis tadpoles. Dis. Aquat. Org. 2009, 83:257-260.
28. Amphibian Conservation Action Plan 2007, IUCN/SSC Amphibian Specialist Group. Gland, Switzerland and Cambridge, UK. C. Gascon, J.P. Collins, R.D. Moore, D.R. Church, J.E. McKay, J.R. Mendelson (Eds.).
29. Georoff T.A., Moore R.P., Rodriguez C., Pessier A.P., Newton A.L., McAloose D., Calle P.P. Efficacy of treatment and long-term follow-up of Batrachochytrium dendrobatidis PCR-positive anurans following itraconazole bath treatment. J. Zoo Wildl. Med. 2013, 44:395-403.
30. Gerland S., Baker A., Phillott A.D., Skerratt L. BSA reduces inhibition of a TaqMan assay for the detection of Batrachochytrium dendrobatidis. Dis. Aquat. Org. 2010, 92:113-116.
31. Harding G., Griffiths R.A., Pavajeau L. Developments in amphibian captive breeding and reintroduction programs. Conserv. Biol. 2015, 10.1111/cobi.12612.
32. Hardy B.M., Pope K.L., Piovia-Scott J., Brown R.N., Foley J.E. Itraconazole treatment reduces Batrachochytrium dendrobatidis prevalence and increases overwinter field survival in juvenile cascades frogs. Dis. Aquat. Org. 2015, 112:243-250.
33. Holden W.M., Ebert A.R., Canning P.F., Rollins-Smith L.A. Evaluation of amphotericin B and chloramphenicol as alternative drugs for treatment of chytridiomycosis and their impacts on innate skin defences. Appl. Environ. Microbiol. 2014, 80:4034-4041.
34. Hyatt A.D., et al. Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis. Aquat. Org. 2007, 75:175-192.
35. Jenelle C.S., Cooch E.G., Conroy M.J., Senar J.C. State specific detection probabilities and disease prevalence. Ecol. Appl. 2007, 17:154-167.
36. Johnson M.L., Speare R. Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerg. Infect. Dis. 2003, 9:922-925.
37. Johnson M.L., Speare R. Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Dis. Aquat. Org. 2005, 65:181-186.
38. Jones M.E.B., Paddock D., Bender L., Allen J.L., Schrenzel M.S., Pessier A.P. Treatment of chytridiomycosis with reduced-dose itraconazole. Dis. Aquat. Org. 2012, 99:243-249.
39. Joseph M.B., Mihaljevic J.R., Arellano A.L., Kueneman J.G., Preston D.L., Cross P.C., Johnson P.T. Taming wildlife disease: bridging the gap between science and management. J. Appl. Ecol. 2013, 50:702-712.
40. Kanafani Z.A., Perfect J.R. Resistance to antifungal agents: mechanisms and clinical impact. Clin. Infect. Dis. 2008, 46:120-128.
41. Kriger K.M., Hero J.-M. Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. J. Zool. 2006, 271:352-359.
42. Lebreton J.D., Burnham K.P., Clobert J., Anderson D.R. Modelling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol. Monogr. 1992, 62:67-118.
43. Lebreton J.D., Nichols J.D., Barker R.J., Pradel R., Spendelow J.A. Modelling individual animal histories with multistate capture-recapture models. Advances in Ecological Research 2009, vol. 41:87-173. Burlington Academic Press. H. Caswell (Ed.).
44. 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. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:3165-3170.
45. Longo A.V., Burrowes P.A., Joglar R.L. Seasonality of Batrachochytrium dendrobatidis infection in direct-developing frogs suggests a mechanism for persistence. Dis. Aquat. Org. 2010, 92:253-260.
46. Lucaks P.M., Thompson W.L., Kendall W.L., Gould W.R., Doherty P.F., Burnham K.P., Anderson D.R. Concerns regarding a call for pluralism of information theory and hypothesis testing. J. Appl. Ecol. 2007, 44(2):456-460.
47. Magin C. Dominica's frogs are croaking. Oryx 2003, 37:406.
48. Marano N., Arguin P.M., Pappaioanou M. Impact of globalization and animal trade on infectious disease ecology. Emerg. Infect. Dis. 2007, 13:1807-1809.
49. A Species Action Plan for the Montserrat Mountain Chicken Leptodactylus fallax 2007, Department of Environment, Montserrat, (Available from: http://www.durrell.org/library/document/montserrat_mountain_chicken_action_plan.pdf). L. Martin, M.N. Morton, G.M. Hilton, R.P. Young, G. Garcia, A.A. Cunningham, A. James, G. Gray, S. Mendes (Eds.).
50. McMahon T.A., et al. Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 2014, 511:224-227.
51. Mendelson J.R., et al. Confronting amphibian declines and extinctions. Science 2006, 313:48.
52. Mitchell K.M., Churcher T.S., Garner T.W.J., Fisher M.C. Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction. Proc. R. Soc. B Biol. Sci. 2008, 275:329-334.
53. Morens D.M., Fauci A.S. Emerging infectious diseases: threats to human health and global stability. PLoS Pathog. 2013, 9.
54. Mountain Chicken Recovery Programme Long-Term Recovery Strategy for the Critically Endangered Mountain Chicken 2014-2034 2014, Mountain Chicken Recovery Programme.
55. Murray K.A., Skerrat L.F., Speare R., McCallum H. Impact and dynamics of disease in species threatened by the amphibian chytrid fungus, Batrachochytrium dendrobatidis. Conserv. Biol. 2009, 23:1242-1252.
56. Nichols D.K., Lamirande E.W. Treatment of cutaneous chytridiomycosis in blue and yellow poison dart frogs (Dendrobates tinctorius). Proceedings: Getting the Jump on Amphibian Disease 2000, 51. James Cook University, Cairns. R. Speare (Ed.).
57. NOAH (National Office of Animal Health) NOAH compendium of animal medicines: Itrafungol 10mg/ml oral solution: contra-indications, warnings etc Available at, (Accessed 20/06/2015). http://www.noahcompendium.co.uk/.
58. A Manual for Control of Infectious Diseases in Amphibian Survival Assurance Colonies and Reintroduction Programs 2010, IUCN/SSC Conservation Breeding Specialist Group, Apple Valley, MN. A.P. Pessier, J.R. Mendelson (Eds.).
59. Phillot 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 15years after introduction of Batrachochytrium dendrobatidis. Conserv. Biol. 2013, 27:1058-1068.
60. Retallick R.W.R., McCallum H., Speare R. Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biol. 2004, 2:1965-1971.
61. Scheele B.C., Hunter D.A., Grogan L.F., Berger L., Kolby J.E., McFadden M.S., Marantelli G., Skerratt L., Driscoll D.A. Interventions for reducing extinction risk in chytridiomycosis-threatened amphibians. Conserv. Biol. 2014, 28:1195-1205.
62. Skerrat L.F., Berger L., Speare R., Cashins S., McDonald K.R., Phillot A.D., Hines H.B., Kenyon N. Spread of chytridiomycosis has caused the rapid global declines and extinction of frogs. EcoHealth 2007, 4:125-134.
63. Stice M.J., Briggs C.J. Immunization is infective against preventing infection and mortality due to the amphibian fungus Batrachochytrium dendrobatidis. J. Wildl. Dis. 2010, 46:70-77.
64. Stuart S.N., Hoffmann M., Chanson J.S., Cox N.A., Berridge R.J., Ramani P., Young B.E. Threatened Amphibians of the World 2008, Lynx Edicions, Barcelona, Spain; IUCN, Gland, Switzerland; and Conservation International, Arlington, Virginia, USA.
65. Tamukai K., Une Y., Tominaga A., Suzuki K., Goka K. Treatment of spontaneous chytridiomycosis in captive amphibians using itraconazole. J. Vet. Med. Sci. 2011, 73:155-159.
66. Venesky M.D., Raffel T.R., McMahon T.A., Rohr J.R. Confronting inconsistencies in the amphibian-chytridiomycosis system: implications for disease management. Biol. Rev. 2014, 89:477-483.
67. Vredenburg V.T., Knapp R.A., Tunstall T.S., Briggs C.J. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9689-9694.
68. Whiles M.R., et al. The effects of amphibian population declines on the structure and function of neotropical stream ecosystems. Front. Ecol. Environ. 2006, 4:27-34.
69. White G.C., Burnham K.P. Program MARK: survival estimation from populations of marked animals. Bird Study 1999, 46:120-139.
70. Wobeser G. Disease management strategies for wildlife. Rev. Sci. Tech. 2002, 21:159-178.
71. Woodhams D.C., et al. Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Front. Zool. 2011, 8. 10.1186/1742-9994-8-8.
72. Woodhams D.C., Geiger C.C., Reinert L.K., Rollins-Smith L.A., Lam B., Harris R.N., Briggs C.J., Vredenburg V.T., Voyles J. Treatment of amphibians infected with chytrid fungus: learning from failed treatments with itraconazole, anti-microbial peptides, bacteria, and heat therapy. Dis. Aquat. Org. 2012, 98:11-25.
73. A biodiversity assessment of the Centre Hills, Montserrat. Durrell Conservation Monograph No. 1 2008, Durrell Wildlife Conservation Trust, Jersey, Channel Islands. R.P. Young (Ed.).
74. Zippel K., Johnson K., Gagliardo R., Gibson R., McFadden M., Browne R., Martinez C., Townsend E. The amphibian ark: a global community for ex-situ conservation of amphibians. Herpetol. Conserv. Biol. 2011, 6:340-352.