Biological Invasions

, Volume 15, Issue 6, pp 1273–1286 | Cite as

A risk assessment for managing non-native parasites

  • Chris F. Williams
  • J. Robert Britton
  • James F. Turnbull
Original Paper

Abstract

The spread of non-native parasites with the movement of animals is a primary cause of disease emergence worldwide. Such introductions can threaten native biodiversity, hinder conservation efforts and limit the socio-economic development of natural resources. Evaluating the threats from alien parasites can represent a considerable challenge, due to the limited information that often accompanies their introduction. We present a comprehensive modular risk assessment scheme that supports the management of non-native fish parasites in their pre- and post-introduction phases. This scheme addresses some of the shortcomings of current risk analysis, including the risk management of non-notifiable pathogens and impact assessment of parasites following establishment. An initial procedure for hazard identification promotes a rapid assessment of disease risk and prompt imposition of management measures. This is followed by a longer-term assessment of impact that accommodates available and emerging knowledge on the pathogen and its distribution. Consideration is given to ecological and economic consequences of disease at the host, population and fishery levels. Each module provides an easily interpreted output that underpins management responses, ranging from monitoring parasite distribution to their attempted eradication. A final module ensures clear communication of disease risk to relevant stakeholders, using the other modules as a framework. Outputs of this risk assessment will inform the prioritisation of available resources and provides a scientifically robust foundation on which to base practical and proportionate management measures to protect native environments. The scheme presented here was specifically developed for freshwater fisheries in England and Wales, but may be modified for use globally and for the non-native parasite fauna of other taxa.

Keywords

Risk assessment Parasite Disease Non-native Fisheries 

References

  1. Adjei ELL, Barnes A, Lester RJG (1986) A method for estimating possible parasite-related host mortality, illustrated using data from Callitetrarhynchus gracilis (Cestoda: Trypanorhyncha) in lizardfish (Saurida spp.). Parasitology 92:227–243CrossRefGoogle Scholar
  2. Alston S, Lewis JW (1994) The ergasilid parasites (Copepoda: Poecilostomatoida) of British freshwater fish. In: Pike AW, Lewis JW (eds) Parasitic diseases of fish. Samara, Dyfed, pp 171–189Google Scholar
  3. Anderson MC, Adams H, Hope B, Powell M (2004) Risk assessment for invasive species. Risk Anal 42:787–795CrossRefGoogle Scholar
  4. Auld BA, Tisdell CA (1986) Impact assessment of biological invasions. In: Groves RH, Burdon JJ (eds) Ecology of biological invasions. Cambridge University Press, Cambridge, pp 79–88Google Scholar
  5. Baker RHA, Black R, Copp GH et al (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, Berlin, pp 46–57Google Scholar
  6. Bakke TA, Cable J, Harris PD (2007) The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Adv Parasit 64:161–376CrossRefGoogle Scholar
  7. Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fisher 10:131–165CrossRefGoogle Scholar
  8. Bartley DM (2004) Precautionary approach to the introduction and transfer of aquatic species. FAO Technical Report. http://www.fao.org/docrep/003/w1238E/W1238E08.htm. Accessed 1 December 2011
  9. Bartley DM, Subasinghe RP (1996) Historical aspects of international movement of living aquatic species. Revue Scientifique et Technique, International Office de Epizootics 15:387–400Google Scholar
  10. Beyer K, Kochanowska D, Longshaw M, Feist SW, Gozlan RE (2005) A potential role for invasive sunbleak in the further dissemination of non-native parasites. J Fish Biol 67:1730–1733CrossRefGoogle Scholar
  11. Blanc G (1997) Introduction of pathogens in European aquatic ecosystems: attempt of evaluation and realities. B Fr Peche Piscic 344:37–56Google Scholar
  12. Boxshall GA, Frear PA (1990) Tracheliastes maculatus (Kollar, 1836) (Crustacea: Lernaeopodidae) a new species for Britain. J Fish Biol 37:489–491CrossRefGoogle Scholar
  13. Britton JR, Cucherousset J, Davies GD, Godard M, Copp GH (2010) Non-native fishes and climate change: predicting species responses to warming temperatures in a temperate region. Freshw Biol 55:1130–1141CrossRefGoogle Scholar
  14. Britton JR, Copp GH, Vilizzi L, Braizer M, Davies GD (2011a) A modular assessment tool for managing introduced fishes according to risks of species and their populations, and impacts of management actions. Biol Invasions. doi:10.1007/s10530-011-9967-0
  15. Britton JR, Gozlan RE, Copp GH (2011b) Managing non-native fish in the environment. Fish Fish. doi:10.1111/j.1467-2979.2010.00390.x
  16. Britton JR, Pegg J, Williams C (2011c) Pathological and ecological host consequences of infection by an introduced fish parasite. PLoS ONE 6:e26365PubMedCrossRefGoogle Scholar
  17. Bullock JM, Hodder SJ, Manchester SJ, Stevenson MJ (1996) Review of information, policy and legislation on species translocation: a report commissioned by the Joint Nature Conservation Committee as a background for future policy formulation. JNCC Report No 261, 295 ppGoogle Scholar
  18. Carlton JT (2002) Bioinvasion ecology: assessing invasion impact and scale. In: Leppakoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, Dordrecht, pp 7–19Google Scholar
  19. CBD (2001) Invasive alien species: report on existing international procedures, criteria and capacity for assessing risk from invasive alien species. Convention on Biological Diversity. Subsidiary Body on Scientific, Technical and Technological Advice, Sixth Meeting, Montreal, 12–16 March 2001Google Scholar
  20. Ciruna KA, Meyerson LA, Gutierrez A (2004) The ecological and socio-economic impacts of invasive alien species in inland water ecosystems. Report to the conservation on biological diversity on behalf of the global invasive species programme, Washington, p 34Google Scholar
  21. Copp GH, Garthwaite R, Gozlan RE (2005) Risk identification and assessment of non-native freshwater fishes: concepts and perspectives on protocols for the UK. UK Science Series Technical Report 129, Cefas Lowestoft, p 32Google Scholar
  22. Copp GH, Britton JR, Jeney G et al (2008) Risk assessment protocols and decision making tools for use of alien species in aquaculture and stock enhancement. http://www.cefas.co.uk/media/437410/impasse_44142_d3-2.pdf. Accessed 1 Dec 2011
  23. Copp GH, Vilizzi L, Mumford J, Fenwick GV, Godard MJ, Gozlan RE (2009) Calibration of FISK, an invasive screening tool for non-native freshwater fishes. Risk Anal 29:457–467PubMedCrossRefGoogle Scholar
  24. Covello VT, Merkhofer MW (1993) Risk assessment methods: approaches for assessing health and environmental risks. Plenum, New YorkGoogle Scholar
  25. Cunningham AA, Daszak P, Rodriguez JP (2003) Pathogen pollution: defining a parasitological threat to biodiversity conservation. J Parasitol 89:78–83Google Scholar
  26. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449PubMedCrossRefGoogle Scholar
  27. Davies C, Shelley J, Harding P, McLean I, Gardiner R, Peirson G (2004) Freshwater fishes in Britain: the species and their distribution. Colchester, Harley Books, 176 ppGoogle Scholar
  28. Defra (2003) Review of non-native species policy. Report of the Working Group. Defra, London. http://www.Defra.gov.uk/wildlifecountryside/resprog/findings/non-native/report.pdf. Accessed 1 June 2010
  29. Defra (2005) UK non-native organism risk assessment scheme user manual. http://www.Defra.gov.uk. Accessed 1 Dec 2011
  30. Dunn AM, Torchin ME, Hatcher MJ, Kotanen PM, Blumenthal DM, Byers JE, Coon CAC, Frankel VM, Holt RD, Hufbauer RA, Kanarek AR, Schierenbeck A, Wolfe LM, Perkins SE (2012) Indirect effects of parasites in invasions. Functional Ecol. doi:10.1111/j.1365-2435.2012.02041.x
  31. Environment Agency (2004) Our nation’s fisheries, the migratory and freshwater fisheries of England and Wales—a snapshot. Environment Agency, Bristol, p 51. http://www.environment-agency.gov.uk/research/library/publications/38069.aspx
  32. EPPO (1997) Guidelines on pest risk assessment—pest risk assessment scheme. EPPO Bull 27:281–305CrossRefGoogle Scholar
  33. EPPO (2000) EPPO standards: pest risk analysis. EPPO PM 5:1–4Google Scholar
  34. European Food Safety Authority (2008) Risk assessment. Appendix 1 EFSA J 736:75–122Google Scholar
  35. FAO (1996) Precautionary approach to capture fisheries and species introductions. FAO Technical Guidelines for Responsible Fisheries 2. FAO, RomeGoogle Scholar
  36. Fenton A, Brockhurst MA (2008) The role of specialist parasites in structuring host communities. Ecol Res 23:795–804CrossRefGoogle Scholar
  37. Fevre EM, Bronsvoort BMDC, Hamilton KA, Cleaveland S (2006) Animal movements and the spread of infectious diseases. Trends Microbiol 14:125–131PubMedCrossRefGoogle Scholar
  38. Finnoff D, Shogrena JF, Leung B, Lodge D (2007) Take a risk: preferring prevention over control of biological invaders. Ecol Econ 62:216–222CrossRefGoogle Scholar
  39. Gaughan DJ (2002) Disease-translocation across geographic boundaries must be recognized as a risk even in the absence of disease identification: the case with Australian Sardinops. Rev Fish Biol Fisher 11:113–123CrossRefGoogle Scholar
  40. Gozlan RE, St-Hilaire S, Feist SW, Martin P, Kent ML (2005) Disease threat to European fish. Nature 435:1046PubMedCrossRefGoogle Scholar
  41. Gozlan RE, Peeler EJ, Longshaw M, St-Hilaire S, Feist SW (2006) Effect of microbial pathogens on the diversity of aquatic populations, notably in Europe. Microbes Infect 8:1358–1364PubMedCrossRefGoogle Scholar
  42. Gozlan RE, Whipps CM, Andreou D, Arkush KD (2009) Identification of a rosette-like agent as Sphaerothecum destruens, a multi-host fish pathogen. Int J Parasitol 39:1055–1058PubMedCrossRefGoogle Scholar
  43. Gussev AV, Strizhak OI (1972) A new species of Pellucidhaptor (Monogenea) from Europe. Parazitologia 6:555–557Google Scholar
  44. Harris P (2003) Pellucidhaptor pricei—an initial appraisal of its biology, pathogenicity and potential environmental impact. Environment Agency, BristolGoogle Scholar
  45. Hedrick RP (1998) Relationships of the host, pathogen and environment: implications for diseases of cultured and wild fish populations. Dis Aquat Organ 10:107–111Google Scholar
  46. Hewitt CL, Hayes KR (2002) Risk assessment of marine biological invasions. In: Leppakoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, Dordrecht, pp 456–466Google Scholar
  47. Hewlett NR, Snow J, Britton JR (2009) The role of management practises in fish mortality incidents in recreational lake fisheries in England and Wales. Fish Manag Ecol 16:248–254CrossRefGoogle Scholar
  48. Hickley P, Chare S (2004) Fisheries for non-native species in England and Wales. Angling or the environment? Fish Manag Ecol 11:203–212CrossRefGoogle Scholar
  49. Hockley FA, Williams CF, Reading AJ, Cable J (2011) First record of Onchocleidus dispar in the British Isles: a monogenean parasite of pumpkinseed, Lepomis gibbosus. Dis Aquat Organ 97:65–73PubMedCrossRefGoogle Scholar
  50. Hoffman GL (1999) Parasites of North American freshwater fishes. 2nd edn. Comstock Publishing, London, 539 ppGoogle Scholar
  51. Hudson PJ, Dobson AP (1991) The direct and indirect effects of the caecal nematode Trichostrongylus tenuis on red grouse. In: Loyle JE, Zuk M (eds) Bird-parasite interactions. Ecology, evolution and behaviour. Oxford University Press, Oxford, pp 49–68Google Scholar
  52. Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (2001) The ecology of wildlife diseases. Oxford University Press, OxfordGoogle Scholar
  53. Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18CrossRefGoogle Scholar
  54. Johnson BO, Jensen AJ (1991) The Gyrodactylus story in Norway. Aquaculture 98:289–302CrossRefGoogle Scholar
  55. Johnson PTJ, Paull SH (2011) The ecology and emergence of diseases in fresh waters. Freshw Biol 56:638–657CrossRefGoogle Scholar
  56. Kennedy CR (1993) Introductions, spread and colonization of new localities by fish helminth and crustacean parasites in the British Isles; a perspective and appraisal. J Fish Biol 43:287–301CrossRefGoogle Scholar
  57. Kennedy CR (1994) The ecology of introductions. In: Pike AW, Lewis JW (eds) Parasitic diseases of fish. Samara, Dyfed, pp 189–208Google Scholar
  58. Kirk RS (2003) The impact of Anguillicola crassus on European eels. Fish Manag Ecol 10:385–394CrossRefGoogle Scholar
  59. Kolar CS, Lodge DM (2002) Ecological predictions and risk assessment for alien fishes in North America. Science 298:1233–1236PubMedCrossRefGoogle Scholar
  60. Leprieur F, Brosse S, García-Berthou E, Oberdorff T, Olden JD, Townsend CR (2009) Scientific uncertainty and the assessment of risks posed by non-native freshwater fishes. Fish Fish 10:88–97CrossRefGoogle Scholar
  61. Lilley JH, Cerenius L, Söderhäll K (1997) RAPD evidence for the origin of crayfish plague outbreaks in Britain. Aquaculture 157:181–185CrossRefGoogle Scholar
  62. Mack RN, Simberloff D, Lonsdale WM, Evand H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  63. Mortensen S, Korsnes K, Bergh Ø (2006) “Eyes wide shut” a critical view of aquaculture health management and risk factors in the real world. Bull Eur Assn Fish P 26:2–6Google Scholar
  64. Moyle PB (1999) Effects of invading species on freshwater and estuarine ecosystems. In: Sandeland T (ed) Invasive species and biodiversity management. Kluwer, Dordrecht, pp 177–191CrossRefGoogle Scholar
  65. Müller-Graf C et al (2007) Risk assessment in animal welfare—EFSA approach. AATEX 14(Special Issue):789–794Google Scholar
  66. OIE (Office International des Epizooties) (2009) Aquatic animal health code 2009. www.oie.int/eng/normes/fcode/en_sommaire.htm. Accessed 1 Oct 2010
  67. Paisley LG, Karlsen E, Jarp J, Mo TA (1999) A Monte Carlo simulation model for assessing the risk of introduction of Gyrodactylus salaris to the Tana River, Norway. Dis Aquat Organ 37:145–152PubMedCrossRefGoogle Scholar
  68. Peeler EJ, Feist SW (2011) Human intervention in freshwater ecosystems drives disease emergence. Freshwater Biol 56:705–716CrossRefGoogle Scholar
  69. Peeler EJ, Thrush MA (2004) Qualitative analysis of the risk of introducing Gyrodactylus salaris into the United Kingdom. Dis Aquat Organ 62:103–113PubMedCrossRefGoogle Scholar
  70. Peeler E, Thrush M (2005) Planning for exotic notifiable fish disease outbreaks. Trout News 40:14–16Google Scholar
  71. Peeler E, Murray AG, Thebault A, Brun E, Thrush MA, Giovaninni A (2006a) Risk assessment and predictive modelling—a review of their application in aquatic animal health. DIPNET. http://www.dipnet.info. Accessed 1 Oct 2011
  72. Peeler E, Thrush M, Paisley L, Rodgers C (2006b) An assessment of the risk of spreading the fish parasite Gyrodactylus salaris to uninfected territories in the European Union with the movement of live Atlantic salmon (Salmo salar) from coastal waters. Aquaculture 258:187–197CrossRefGoogle Scholar
  73. Peeler EJ, Oidtmann BC, Midtlyng PJ, Miossec L, Gozlan RE (2010) Non-native aquatic animals have driven disease emergence in Europe. Biol Invasions 13:1291–1303CrossRefGoogle Scholar
  74. Perkins SE, Altizer S, Bjornstad O, Burdon JJ, Clay K et al (2008) Invasion biology and parasitic infections. In: Ostfeld RS, Keesing F, Eviner VT (eds) Infectious disease ecology—effects of ecosystems on disease and of disease on ecosystems. Princeton University Press, Princeton, pp 347–367Google Scholar
  75. Pheloung PC (2001) Weed risk assessment for plant introductions to Australia. In: Groves RH, Panetta FD, Virtue JG (eds) Weed risk assessment. CSIRO, Australia, pp 83–93Google Scholar
  76. Pheloung PC, Williams PA, Halloy SR (1999) A weed risk assessment model for use as a biosecurity tool evaluating plant introductions. J Environ Manag 57:239–251CrossRefGoogle Scholar
  77. Poulin R, Paterson RA, Townsend CR, Tompkins DM, Kelly DW (2011) Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshw Biol 56:676–688CrossRefGoogle Scholar
  78. Ricciardi A (2003) Predicting the impacts of an introduced species from its invasion history: an empirical approach applied to zebra mussel invasion. Freshw Biol 48:972–981CrossRefGoogle Scholar
  79. Ruesink JL, Parker IM, Groom MJ, Kareiva PM (1995) Reducing the risks of nonindigenous species introductions—guilty until proven innocent. Bioscience 45:465–477CrossRefGoogle Scholar
  80. Simberloff D (2006) Risk assessments, blacklists, and white lists for introduced species: are predications good enough to be useful? Agric Res Eco Rev 35:1–10Google Scholar
  81. Simpson D, Mawle GW (2001) Survey of rod licence holders. R&D Project W2-057, Environment Agency, Bristol, 100 ppGoogle Scholar
  82. Sinderman CJ (1987) Effects of parasites on fish populations: practical considerations. Int J Parasitol 17:371–382CrossRefGoogle Scholar
  83. Stokes KE, O’Neill KP, Montgomery WI, Dick JTA et al (2006) The importance of stakeholder engagement in invasive species management: a cross-jurisdictional perspective in Ireland. Biodivers Conserv 15:2829–2852CrossRefGoogle Scholar
  84. Taraschewski H (2006) Hosts and parasites as aliens. J Helmin 80:99–128CrossRefGoogle Scholar
  85. Thrush MA, Peeler E (2006) Stochastic simulation of live salmonid movement in England and Wales to predict potential spread of exotic pathogens. Dis Aquat Organ 72:115–123PubMedCrossRefGoogle Scholar
  86. Thrush MA, Murray AG, Brun E, Wallace S, Peeler EJ (2011) The application of risk and disease modelling to emerging freshwater diseases in wild aquatic animals. Freshw Biol 56:658–675CrossRefGoogle Scholar
  87. Tompkins DM, Dunn AM, Smith MJ, Telfer S (2010) Wildlife diseases: from individuals to ecosystems. J Anim Ecol. doi:10.1111/j.1365-2656.2010.01742.x
  88. Villeneuve F, Copp GH, Fox MG, Stakenas S (2005) Interpopulation variation in growth and life-history traits of the introduced sunfish, pumpkinseed Lepomis gibbosus, in southern England. J Appl Ichthyol 21:275–281CrossRefGoogle Scholar
  89. Way K (2004) Koi herpes virus—a threat to wild carp. Trout News 38:32–34Google Scholar
  90. Whittington RJ, Chong R (2007) Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Prev Vet Med 81:92–116PubMedCrossRefGoogle Scholar
  91. Williams JE, Williams CD (2004) Oversimplified habitats and oversimplified solutions in our search for sustainable freshwater fisheries. Sustainable Management of North American Fisheries-American Fisheries Society Symposium 43, pp 67–89Google Scholar
  92. Woolhouse MEJ, Taylor LH, Haydon DT (2001) Population biology of multihost pathogens. Science 292:1109–1112PubMedCrossRefGoogle Scholar
  93. Yeomans WE, Chubb JC, Sweeting RA (1997) Khawia sinensis (Cestoda: Caryophyllidea)—an indicator of legislative failure to protect freshwater habitats in British Isles? J Fish Biol 51:880–885Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Chris F. Williams
    • 1
  • J. Robert Britton
    • 2
  • James F. Turnbull
    • 3
  1. 1.Environment Agency, Bromholme LaneHuntingdonUK
  2. 2.Centre for Conservation Ecology and Environmental Sciences, School of Applied SciencesBournemouth UniversityPooleUK
  3. 3.Institute of AquacultureUniversity of StirlingStirlingScotland, UK

Personalised recommendations