Qualitative risk analysis of introducing batrachochytrium dendrobatidis to the UK through the importation of live amphibians

Diseases of Aquatic Organisms

Volumn 98, Issue 2, 2012, Pages 95-112

  Peel, Alison J ^a   Hartley, Matt ^b   Cunningham, Andrew A ^a  

^a INSTITUTE OF ZOOLOGY   (United Kingdom)

^b Food and Rural Affairs   (United Kingdom)

Author keywords

Amphibian trade; Chytridiomycosis; Emerging infectious disease; Risk assessment

Indexed keywords

AMPHIBIAN; DISEASE CONTROL; DISEASE INCIDENCE; DISEASE SPREAD; ENVIRONMENTAL RISK; EXTINCTION; FUNGAL DISEASE; GUIDELINE; IMPORT; INFECTIOUS DISEASE; INTRODUCED SPECIES; NATIVE SPECIES; PATHOGEN; POPULATION DECLINE; QUALITATIVE ANALYSIS; RISK ASSESSMENT; SURVIVAL;

UNITED KINGDOM;

AMPHIBIA; ANIMALIA; BATRACHOCHYTRIUM DENDROBATIDIS;

AMPHIBIA; ANIMAL; ANIMAL DISEASE; ARTICLE; CHYTRIDIOMYCETES; COMMERCIAL PHENOMENA; MICROBIOLOGY; MYCOSIS; PHYSIOLOGY; RISK FACTOR; UNITED KINGDOM;

AMPHIBIANS; ANIMALS; CHYTRIDIOMYCOTA; COMMERCE; GREAT BRITAIN; MYCOSES; RISK FACTORS;

EID: 84861674554     PISSN: 01775103     EISSN: 16161580     Source Type: Journal    
DOI: 10.3354/dao02424     Document Type: Article

References (79)

1. Anderson RM, May RM, Joysey K, Mollison D and others (1986) The invasion, persistence and spread of infectious diseases within animal and plant communities. Philos Trans R Soc Lond B Biol Sci 314: 533-570
2. Aplin K, Kirkpatrick P (2000) Chytridiomycosis in southwest Australia: historical sampling documents the date of introduction, rates of spread and seasonal epidemiology, and sheds new light on chytrid ecology. In: Speare R et al. (eds) Getting the jump! on amphibian disease. Conference and Workshop Compendium, 26-30 August 2000, Cairns, p 24 (Abstract). Available at www.jcu.edu. au/school/phtm/PHTM/frogs/GJKirk.htm
3. Bai C, Garner TWJ, Li Y (2010) First evidence of Batrachochytrium dendrobatidis in China: discovery of chytri-diomycosis in introduced American bullfrogs and native amphibians in the Yunnan Province, China. EcoHealth 7: 127-134
4. Baker RHA, Black R, Copp GH, Haysom KA and others (2008) The UK risk assessment scheme for all non-native species. In: Rabitsch W, Essl F, Klingenstein F (eds) Biological invasions-from ecology to conservation. Neobiota 7: 46-57
5. Baker RHA, Copp G, Hulme P, Thomas M, Black R, Hayson K (2005) UK non-native organism risk assessment scheme user manual, version 3.3. Department for Environment, Food, and Rural Affairs, London. Available at https://secure. fera.defra.gov.uk/nonnativespecies/download Document.cfm?id=158 (accessed 14 April 2011)
6. Banks C, McCracken H, Natrass A (2002) Captive management and pathology of sharp snouted dayfrogs, Taudac-tylus acutirostris, at Melbourne and Taronga zoos. In: Frogs in the community. Proc Brisbane Symp Queensland Frog Society. Queensland Frog Society, Brisbane, p 94-102
7. Berger L, Speare R, Daszak P, Green D and others (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 (Pubitemid 28350609)
8. Berger L, Marantelli G, Skerratt LF, Speare R (2005) Virulence of the amphibian chytrid fungus Batrachochytrium dendrobatidis varies with the strain. Dis Aquat Org 68: 47-50 (Pubitemid 43161979)
9. Bielby J, Cooper N, Cunningham AA, Garner TWJ, Purvis A (2008) Predicting susceptibility to future declines in the world's frogs. Conserv Lett 1: 82-90
10. Bosch J, Martinez-Solano I (2006) Chytrid fungus infection related to unusual mortalities of Salamandra salamandra and Bufo bufo in the Penalara Natural Park, Spain. Oryx 40: 84-89
11. Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Org 60: 141-148 (Pubitemid 39588268)
12. Bradley GA, Rosen PC, Sredl MJ, Jones TR, Longcore JE (2002) Chytridiomycosis in native Arizona frogs. J Wildl Dis 38: 206-212 (Pubitemid 135692490)
13. Burrowes P, Joglar R, Green D (2004) Potential causes for amphibian declines in Puerto Rico. Herpetologica 60: 141-154 (Pubitemid 38641494)
14. Covello VT, Merkhofer M (1993) Risk assessment methods: approaches for assessing health and environmental risks. Plenum Publishing, New York, NY
15. Cunningham AA (1996) Disease risks of wildlife translocations. Conserv Biol 10: 349-353
16. Cunningham AA, Garner TWJ, Aguilar-Sanchez V, Banks B and others (2005) Emergence of amphibian chytridio-mycosis in Britain. Vet Rec 157: 386-387
17. Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R (1999) Emerging infectious diseases and amphi-bian population declines. Emerg Infect Dis 5: 735-748 (Pubitemid 30022457)
18. Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9: 141-150 (Pubitemid 36317431)
19. Daszak P, Strieby A, Cunningham AA, Longcore JE, Brown 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: 201-207 (Pubitemid 39645550)
20. DEFRA (Department for Environment Food and Rural Affairs) (2011a) Frogs' legs for human consumption (BAL IIN 3A). DEFRA, London. Available at www.defra. gov. uk/foodfarm/animaltrade/inports/iins/frog/bal3a.htm (accessed 14 April 2011)
21. DEFRA (Department for Environment Food and Rural Affairs) (2011b) Personal import rules database. DEFRA, London. http://importdetails.defra.gov.uk (accessed 16 June 2011)
22. DEH (Department of the Environment and Heritage) (2005) Threat abatement plan: infection of amphibians with chytrid fungus resulting in chytridiomycosis. Background document. DEH, Canberra. Available at www. environment. gov.au/biodiversity/threatened/publications/tap/pubs/chytrid-background.pdf (accessed 29 June 2009)
23. Drew A, Allen EJ, Allen LJS (2006) Analysis of climatic and geographic factors affecting the presence of chytridio-mycosis in Australia. Dis Aquat Org 68: 245-250
24. FAO (Food and Agriculture Organization) (2011) Cultured aquatic species information programme: Rana catesbei-ana. UN FAO, Rome. Available at www. fao. org/fi/website/FIRetrieve Action. do? dom= culture species & xml = Rana-catesbeiana.xml (accessed 29 June 2009)
25. Fisher MC, Garner TWJ (2007) The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphi-bian species. Fungal Biol Rev 21: 2-9 (Pubitemid 46946867)
26. Fisher MC, Garner TWJ, Walker S (2009a) Global emergence of Batrachochytrium dendrobatidis and amphi-bian chytridiomycosis in space, time, and host. Annu Rev Microbiol 63: 291-310
27. Fisher MC, Bosch J, Yin Z, Stead DA and others (2009b) Proteomic and phenotypic profiling of the amphibian patho-gen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Mol Ecol 18: 415-429
28. Garner TWJ, Perkins M, Govindarajulu P, Seglie D, Walker S, Cunningham AA, Fisher MC (2006) The emerging patho gen Batrachochytrium dendrobatidis globally in-fects introduced populations of the North American bullfrog, Rana catesbeiana. Biol Lett 2: 455-459 (Pubitemid 44387387)
29. Garner TWJ, Walker S, Bosch J, Leech S, RowcliffeMJ, Cunningham AA, Fisher MC (2009a) Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118: 783-791
30. Garner TWJ, Stephen I, Wombwell E, Fisher MC (2009b) The amphibian trade: bans or best practice? EcoHealth 6: 148-151 & author reply, p 152
31. Gleason FH, Letcher PM, McGee PA (2008) Freeze tolerance of soil chytrids from temperate climates in Australia. Mycol Res 112: 976-982
32. Goka K, Yokoyama J, Une Y, Kuroki T and others (2009) Amphibian chytridiomycosis in Japan: distribution, haplo types and possible route of entry into Japan. Mol Ecol 18: 4757-4774
33. Holsbeek G, Mergeay J, Hotz H, Plötner J, Volckaert F, De Meester L (2008) A cryptic invasion within an invasion and widespread introgression in the European water frog complex: consequences of uncontrolled commercial trade and weak international legislation. Mol Ecol 17: 5023-5035
34. Holsbeek G, Mergeay J, Volckaert F, De Meester L (2010) Genetic detection of multiple exotic water frog species in Belgium illustrates the need for monitoring and immediate action. Biol Invasions 12: 1459-1463
35. Hyatt AD, Boyle DG, Olsen V, Boyle DB and others (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis Aquat Org 73: 175-192
36. IUCN (International Union for Conservation of Nature) (2011) IUCN red list of threatened species. Available at www.iucnredlist.org (accessed 16 September 2010)
37. James TY, Litvintseva AP, Vilgalys R, Morgan JAT and others (2009) Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy am phi-bian populations. PLoS Pathog 5: e1000458
38. Johnson ML, Speare R (2003) Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerg Infect Dis 9: 922-925 (Pubitemid 36944510)
39. Johnson ML, Berger L, Philips L, Speare R (2003) Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Org 57: 255-260 (Pubitemid 38908533)
40. Kielgast J, Rödder D, Veith M, Lotters S (2010) Widespread occurrence of the amphibian chytrid fungus in Kenya. Anim Conserv 13:36-43
41. Kilpatrick AM, Briggs CJ, Daszak P (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol 25: 109-118
42. Kriger KM, Hero JM (2007) The chytrid fungus Batrachochytrium dendrobatidis is non-randomly distributed across amphibian breeding habitats. Divers Distrib 13: 781-788 (Pubitemid 47622027)
43. Kriger KM, Hero JM (2009) Chytridiomycosis, amphibian extinctions, and lessons for the prevention of future panzootics. EcoHealth 6: 6-10
44. Kriger KM, Hero JM, Ashton KJ (2006a) Cost efficiency in the detection of chytridiomycosis using PCR assay. Dis Aquat Org 71: 149-154 (Pubitemid 44284752)
45. Kriger KM, Hines HB, Hyatt AD, Boyle DG, Hero JM(2006b) Techniques for detecting chytridiomycosis in wild frogs: comparing histology with real-time Taqman PCR. Dis Aquat Org 71: 141-148 (Pubitemid 44284751)
46. Kriger KM, Ashton K, Hines HB, Hero JM (2007) On the biolo gical relevance of a single Batrachochytrium dendrobatidis zoospore: a reply to Smith (2007). Dis Aquat Org 73: 257-260
47. Laurance W, McDonald K, Speare R (1996) Epidemic disease and the catastrophic decline of Australian rain forest frogs. Conserv Biol 10: 406-413
48. Lips KR, Brem F, Brenes R, Reeve J and others (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci USA 103: 3165-3170 (Pubitemid 43346442)
49. Lips KR, Diffendorfer J, Mendelson JR, Sears MW (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biol 6: e72
50. Longcore JE, Pessier A, Nichols D (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91: 219-227 (Pubitemid 29157942)
51. Lötters S, Kielgast J, Bielby J, Schmidtlein S, Bosch J (2009) The link between rapid enigmatic amphibian decline and the globally emerging chytrid fungus. EcoHealth 6: 358-372
52. Marantelli G, Hobbs R (2000) Disease vectors and the community: from lost frogs to frog friendly gardens-How do we help frogs while containing disease spread? In: Speare R et al. (eds) Getting the jump! on amphibian disease. Conference and Workshop Compendium, 26-30 August 2000, Cairns p 49 (Abstract). Available at www. jcu.edu.au/school/phtm/PHTM/frogs/GJHobbs.htm
53. Mendelson JR III, Lips KR, Gagliardo RW, Rabb GB and others (2006) Confronting amphibian declines and ex-tinctions. Science 313: 48
54. Nichols DK, Lamirande EW, Pessier AP, Longcore JE (2001) Experimental transmission of cutaneous chytridiomy-cosis in dendrobatid frogs. J Wildl Dis 37: 1-11 (Pubitemid 33614753)
55. OIE (Office International des Epizooties) (2006) Report of the meeting of the OIE Aquatic Animal Health Standards Commission. OIE, Paris
56. OIE (Office International des Epizooties) (2010a) Aqua tic animal health code. OIE, Paris. Available at www. oie. int/en/in ternational-standard-setting/ aquatic-code/accessonline/(accessed 16 June 2011)
57. OIE (Office International des Epizooties) (2010b) Handbook on import risk analysis for animals and animal products, Vol 1. Introduction and qualitative risk analyses, 2nd edn. OIE, Paris
58. Picco AM, Collins JP (2008) Amphibian commerce as a likely source of pathogen pollution. Conserv Biol 22: 1582-1589
59. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96: 9-15 (Pubitemid 38300150)
60. Rachowicz L, Hero JM, Alford R, Taylor J and others (2005) The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conserv Biol 19: 1441-1448 (Pubitemid 41718148)
61. Raverty S, Reynolds T (2001) Cutaneous chytridiomycosis in dwarf aquatic frogs (Hymenochirus boettgeri) originating from southeast Asia and in a western toad (Bufo boreas) from northeastern British Columbia. Can Vet J 42: 385-386 (Pubitemid 33611577)
62. Reed K, Ruth G, Meyer J, Shukla S (2000) Chlamydia pneumoniae infection in a breeding colony of African clawed frogs (Xenopus tropicalis). Emerg Infect Dis 6:196-199 (Pubitemid 30226901)
63. Retallick RWR, 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 (Pubitemid 46910369)
64. Ron S (2005) Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica 37: 209-221 (Pubitemid 40802324)
65. Rowley JJL, Chan SKF, Tang WS, Speare R and others (2007) Survey for the amphibian chytrid Batrachochy-trium dendrobatidis in Hong Kong in native amphibians and in the international amphibian trade. Dis Aquat Org 78: 87-95 (Pubitemid 351547564)
66. Schlaepfer M, Hoover C, Dodd C Jr (2005) Challenges in evaluating the impact of the trade in amphibians and reptiles on wild populations. Bioscience 55: 256-264 (Pubitemid 40383775)
67. Schloegel LM, Picco A, Kilpatrick A, Davies A, Hyatt A, Daszak P (2009) Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biol Conserv 142: 1420-1426
68. 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 Org 92: 101-108
69. Skerratt L, Berger L, Speare R, Cashins S and others (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4: 125-134 (Pubitemid 47038075)
70. Smith KG (2007) Use of quantitative PCR assay for amphi-bian chytrid detection: comment on Kriger et al. (2006a,b). Dis Aquat Org 73: 253-255
71. Speare R, Core Working Group of Getting the Jump on Amphibian Disease (2001) Nomination for listing of amphibian chytridiomycosis as a key threatening process under the Environment Protection and Biodiversity Conservation Act 1999. In: Speare et al. (eds) Developing management strategies to control amphibian diseases: decreasing the risks due to communicable diseases. School of Public Health and Tropical Medicine, James Cook University, Townsville, p 186-208
72. Spitzen-van der Sluijs AM, Zollinger R (2010) Risk assessment on the American bullfrog and the fungus Batra-chochytrium dendrobatidis. Stichting RAVON, Nijmegen
73. St-Hilaire S, ThrushM, Tatarian T, Prasad A, Peeler E (2009) Tool for estimating the risk of anthropogenic spread of Batrachochytrium denrobatidis between water bodies. EcoHealth 6: 16-19
74. Thrush MA, Murray AG, Brun E, Wallace S, Peeler E (2011) The application of risk and disease modelling to emerging freshwater diseases in wild aquatic animals. Freshw Biol 56: 658-675
75. UK National Ecosystem Assessment (2011) UK National Ecosystem Assessment: synthesis of key findings. UN Environment Programme, World Conservation Moni-toring Centre, Cambridge. Available at http://archive. defra.gov.uk/ environment/natural/documents/UKNEA-SynthesisReport.pdf (accessed 9 June 2011)
76. Walker SF, Salas MB, Jenkins D, Garner TWJ and others (2007) Environmental detection of Batrachochytrium dendrobatidis in a temperate climate. Dis Aquat Org 77: 105-112 (Pubitemid 351547072)
77. Walker SF, Bosch J, James TY, Litvintseva AP and others (2008) Invasive pathogens threaten species recovery programs. Curr Biol 18: R853-R854
78. Walker SF, Bosch J, Gomez V, Garner TWJ and others (2010) Factors driving pathogenicity vs. prevalence of amphibian panzootic chytridiomycosis in Iberia. Ecol Lett 13: 372-382
79. Weldon C, du Preez L, Hyatt A, Muller R, Speare R (2004) Origin of the amphibian chytrid fungus. Emerg Infect Dis 10:2100-2105 (Pubitemid 39587332)