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.
Similar content being viewed by others
References
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 92:227–243
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 171–189
Anderson MC, Adams H, Hope B, Powell M (2004) Risk assessment for invasive species. Risk Anal 42:787–795
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 79–88
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 46–57
Bakke TA, Cable J, Harris PD (2007) The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Adv Parasit 64:161–376
Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fisher 10:131–165
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
Bartley DM, Subasinghe RP (1996) Historical aspects of international movement of living aquatic species. Revue Scientifique et Technique, International Office de Epizootics 15:387–400
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 67:1730–1733
Blanc G (1997) Introduction of pathogens in European aquatic ecosystems: attempt of evaluation and realities. B Fr Peche Piscic 344:37–56
Boxshall GA, Frear PA (1990) Tracheliastes maculatus (Kollar, 1836) (Crustacea: Lernaeopodidae) a new species for Britain. J Fish Biol 37:489–491
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 55:1130–1141
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
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
Britton JR, Pegg J, Williams C (2011c) Pathological and ecological host consequences of infection by an introduced fish parasite. PLoS ONE 6:e26365
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 pp
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 7–19
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 2001
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 34
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 32
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
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 29:457–467
Covello VT, Merkhofer MW (1993) Risk assessment methods: approaches for assessing health and environmental risks. Plenum, New York
Cunningham AA, Daszak P, Rodriguez JP (2003) Pathogen pollution: defining a parasitological threat to biodiversity conservation. J Parasitol 89:78–83
Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449
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 pp
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
Defra (2005) UK non-native organism risk assessment scheme user manual. http://www.Defra.gov.uk. Accessed 1 Dec 2011
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
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
EPPO (1997) Guidelines on pest risk assessment—pest risk assessment scheme. EPPO Bull 27:281–305
EPPO (2000) EPPO standards: pest risk analysis. EPPO PM 5:1–4
European Food Safety Authority (2008) Risk assessment. Appendix 1 EFSA J 736:75–122
FAO (1996) Precautionary approach to capture fisheries and species introductions. FAO Technical Guidelines for Responsible Fisheries 2. FAO, Rome
Fenton A, Brockhurst MA (2008) The role of specialist parasites in structuring host communities. Ecol Res 23:795–804
Fevre EM, Bronsvoort BMDC, Hamilton KA, Cleaveland S (2006) Animal movements and the spread of infectious diseases. Trends Microbiol 14:125–131
Finnoff D, Shogrena JF, Leung B, Lodge D (2007) Take a risk: preferring prevention over control of biological invaders. Ecol Econ 62:216–222
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 11:113–123
Gozlan RE, St-Hilaire S, Feist SW, Martin P, Kent ML (2005) Disease threat to European fish. Nature 435:1046
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 8:1358–1364
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 39:1055–1058
Gussev AV, Strizhak OI (1972) A new species of Pellucidhaptor (Monogenea) from Europe. Parazitologia 6:555–557
Harris P (2003) Pellucidhaptor pricei—an initial appraisal of its biology, pathogenicity and potential environmental impact. Environment Agency, Bristol
Hedrick RP (1998) Relationships of the host, pathogen and environment: implications for diseases of cultured and wild fish populations. Dis Aquat Organ 10:107–111
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 456–466
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 16:248–254
Hickley P, Chare S (2004) Fisheries for non-native species in England and Wales. Angling or the environment? Fish Manag Ecol 11:203–212
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 97:65–73
Hoffman GL (1999) Parasites of North American freshwater fishes. 2nd edn. Comstock Publishing, London, 539 pp
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 49–68
Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (2001) The ecology of wildlife diseases. Oxford University Press, Oxford
Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18
Johnson BO, Jensen AJ (1991) The Gyrodactylus story in Norway. Aquaculture 98:289–302
Johnson PTJ, Paull SH (2011) The ecology and emergence of diseases in fresh waters. Freshw Biol 56:638–657
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 43:287–301
Kennedy CR (1994) The ecology of introductions. In: Pike AW, Lewis JW (eds) Parasitic diseases of fish. Samara, Dyfed, pp 189–208
Kirk RS (2003) The impact of Anguillicola crassus on European eels. Fish Manag Ecol 10:385–394
Kolar CS, Lodge DM (2002) Ecological predictions and risk assessment for alien fishes in North America. Science 298:1233–1236
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 10:88–97
Lilley JH, Cerenius L, Söderhäll K (1997) RAPD evidence for the origin of crayfish plague outbreaks in Britain. Aquaculture 157:181–185
Mack RN, Simberloff D, Lonsdale WM, Evand H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
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 26:2–6
Moyle PB (1999) Effects of invading species on freshwater and estuarine ecosystems. In: Sandeland T (ed) Invasive species and biodiversity management. Kluwer, Dordrecht, pp 177–191
Müller-Graf C et al (2007) Risk assessment in animal welfare—EFSA approach. AATEX 14(Special Issue):789–794
OIE (Office International des Epizooties) (2009) Aquatic animal health code 2009. www.oie.int/eng/normes/fcode/en_sommaire.htm. Accessed 1 Oct 2010
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 37:145–152
Peeler EJ, Feist SW (2011) Human intervention in freshwater ecosystems drives disease emergence. Freshwater Biol 56:705–716
Peeler EJ, Thrush MA (2004) Qualitative analysis of the risk of introducing Gyrodactylus salaris into the United Kingdom. Dis Aquat Organ 62:103–113
Peeler E, Thrush M (2005) Planning for exotic notifiable fish disease outbreaks. Trout News 40:14–16
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
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 258:187–197
Peeler EJ, Oidtmann BC, Midtlyng PJ, Miossec L, Gozlan RE (2010) Non-native aquatic animals have driven disease emergence in Europe. Biol Invasions 13:1291–1303
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 347–367
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 83–93
Pheloung PC, Williams PA, Halloy SR (1999) A weed risk assessment model for use as a biosecurity tool evaluating plant introductions. J Environ Manag 57:239–251
Poulin R, Paterson RA, Townsend CR, Tompkins DM, Kelly DW (2011) Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshw Biol 56:676–688
Ricciardi A (2003) Predicting the impacts of an introduced species from its invasion history: an empirical approach applied to zebra mussel invasion. Freshw Biol 48:972–981
Ruesink JL, Parker IM, Groom MJ, Kareiva PM (1995) Reducing the risks of nonindigenous species introductions—guilty until proven innocent. Bioscience 45:465–477
Simberloff D (2006) Risk assessments, blacklists, and white lists for introduced species: are predications good enough to be useful? Agric Res Eco Rev 35:1–10
Simpson D, Mawle GW (2001) Survey of rod licence holders. R&D Project W2-057, Environment Agency, Bristol, 100 pp
Sinderman CJ (1987) Effects of parasites on fish populations: practical considerations. Int J Parasitol 17:371–382
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 15:2829–2852
Taraschewski H (2006) Hosts and parasites as aliens. J Helmin 80:99–128
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 72:115–123
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 56:658–675
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
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 21:275–281
Way K (2004) Koi herpes virus—a threat to wild carp. Trout News 38:32–34
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 81:92–116
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 67–89
Woolhouse MEJ, Taylor LH, Haydon DT (2001) Population biology of multihost pathogens. Science 292:1109–1112
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 51:880–885
Acknowledgments
The authors acknowledge the Environment Agency for funding this work. Particular thanks to Phil Hickley, Nigel Hewlett and Amy Reading of Fisheries Technical Services, Brampton, for advice on fish movement regulations, non-native species management and fish disease monitoring in England and Wales. Thanks also to Dr. Christine Müller-Graf of the Federal Institute of Risk Assessment, Berlin and Dr. Stephen Feist, Cefas, Weymouth for early comments on this risk assessment process. Also to Drs Andy Shinn (University of Stirling), Philip Harris (Natural History Museum, Oslo), and Joanne Cable (University of Cardiff), for providing expert opinion on the monogenean parasites used in the trial risk assessments.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Williams, C.F., Britton, J.R. & Turnbull, J.F. A risk assessment for managing non-native parasites. Biol Invasions 15, 1273–1286 (2013). https://doi.org/10.1007/s10530-012-0364-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-012-0364-0