Parasite transmission between captive and wild fish is mediated by spatial, abiotic, biotic, and management factors. More effective population management and conservation strategies can result from multivariable assessments of factors associated with spatial dynamics of parasite spillover.
Our study characterised spatial patterns of sea lice (Lepeophtheirus salmonis, Caligus clemensi) infection on out-migrating chum (Oncorhynchus keta) and pink (O. gorbuscha) salmon in an area with Atlantic salmon (Salmo salar) farming.
A multivariable statistical model for sea louse parasitism of out-migrating chum and pink salmon was developed from 166,316 wild salmon sampled in the Broughton Archipelago, British Columbia, Canada from 2003 to 2012. We assessed for factors hypothesized to influence sea lice infection levels, at the non-motile life stage, including spatial scales of infection sources.
Fish length, sampling year and method were strong explanatory factors. Infection was greatest in higher salinity water. Farmed and wild juvenile salmon infection levels were correlated, on average, within 30 km. Except for 2004, sea lice infection on farms were typically well below the regulatory level (3 motiles per fish). Average intensity of non-motile infections observed on the wild fish were 6.36 (SD = 9.98) in 2004 compared to 1.66 (SD = 1.25) for the other years.
Accuracy of future model estimates will benefit by including hydrodynamic data accounting for anisotropic spread of sea lice from sources. Multivariable statistical modelling over long time series data strengthens understanding of factors impacting wild juvenile salmon infection levels and informs spatial patterns of aquatic epidemiology.
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Anderson RM, May RM (1991) Infectious disease of humans: dynamics and control, 1st edn. Oxford University Press, New York, p 757
Beamish R, Wade J, Pennell W, Gordon E, Jones S, Neville C, Lange K, Sweeting R (2009) A large, natural infection of sea lice on juvenile Pacific salmon in the Gulf Islands area of British Columbia, Canada. Aquaculture 297:31–37
Beamish RJ, Jones S, Neville C-E, Sweeting R, Karreman G, Saksida S, Gordon E (2006) Exceptional marine survival of pink salmon that entered the marine environment in 2003 suggests that farmed Atlantic salmon and Pacific salmon can coexist successfully in a marine ecosystem on the Pacific coast of Canada. ICES J Mar Sci 63:1326–1337
Brauner CJ, Sackville M, Gallagher Z, Tang S, Nendick L, Farrell AP (2012) Physiological consequences of the salmon louse (Lepeophtheirus salmonis) on juvenile pink salmon (Oncorhynchus gorbuscha): implications for wild salmon ecology and management, and for salmon aquaculture. Phil Trans R Soc B 367:1770–1779
Bravo S, Erranz F, Lagos C (2009) A comparison of sea lice, Caligus rogercresseyi, fecundity in four areas in southern Chile. J Fish Dis 32:107–113
Bricknell IR, Dalesman SJ, Shea BO, Pert CC, Luntz AJM (2006) Effect of environmental salinity on sea lice Lepeophtheirus salmonis settlement success. Dis Aquat Organ 71:201–212
Brooks KM (2005) The effects of water temperature, salinity, and currents on the survival and distribution of the infective copepodid stage of sea lice (Lepeophtheirus Salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada. Rev Fish Sci 13:177–204
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York, p 488
Butterworth KG, Cubitt KF, McKinley RS (2008) The prevalence, density and impact of Lepeophtheirus salmonis (Krøyer) infestation on juvenile pink salmon (Oncorhynchus gorbuscha) from the central coast of British Columbia, Canada. Fish Res 91:35–41
Connors BM, Juarez-Colunga E, Dill LM (2008) Effects of varying salinities on Lepeophtheirus salmonis survival on juvenile pink and chum salmon. J Fish Biol 72:1825–1830
Costello MJ (2006) Ecology of sea lice parasitic on farmed and wild fish. Trends Parasitol 22:475–483
Costello MJ (2009) How sea lice from salmon farms may cause wild salmonid declines in Europe and North America and be a threat to fishes elsewhere. Proc R Soc B Biol Sci 276:3385–3394
Cullingham CI, Nakada SM, Merrill EH, Bollinger TK, Pybus MJ, Coltman DW (2011) Multiscale population genetic analysis of mule deer (Odocoileus hemionus hemionus) in western Canada sheds new light on the spread of chronic wasting disease. Can J Zool 89:134–147
Fast MD, Ross NW, Mustafa A, Sims DE, Johnson SC, Conboy GA, Speare DJ, Johnson G, Burka JF (2002) Susceptibility of rainbow trout Oncorhynchus mykiss, Atlantic salmon Salmo salar and coho salmon Oncorhynchus kisutch to experimental infection with sea lice Lepeophtheirus salmonis. Dis Aquat Organ 52:57–68
Foreman MGG, Czajko P, Stucchi DJ, Guo M (2009) A finite volume model simulation for the Broughton Archipelago, Canada. Ocean Model 30:29–47
Freeland HJ, Farmer D (1980) Circulation and energetics of a deep, strongly stratified inlet. Can J Fish Aquat Sci 37:1398–1410
Gilligan CA, van den Bosch F (2008) Epidemiological models for invasion and persistence of pathogens. Annu Rev Phytopathol 46:385–418
Gottesfeld AS, Proctor B, Rolston LD, Carr-Harris C (2009) Sea lice, Lepeophtheirus salmonis, transfer between wild sympatric adult and juvenile salmon on the north coast of British Columbia, Canada. J Fish Dis 32:45–57
Gustafson LL, Ellis SK, Beattie MJ, Chang BD, Dickey DA, Robinson TL, Marenghi FP, Moffett PJ, Page FH (2007) Hydrographics and the timing of infectious salmon anemia outbreaks among Atlantic salmon (Salmo salar L.) farms in the Quoddy region of Maine, USA and New Brunswick, Canada. Prev Vet Med 78:35–56
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162
Heard WR (1991) Life history of pink salmon (Oncorhynchus gorbuscha). In: Groot C, Margolis L (eds) Pacific Salmon Life Histories, 1st edn. University of British Columbia Press, Vancouver, pp 119–230
Heuch PA (1995) Experimental evidence for aggregation of salmon louse copepodids (Lepeophtheirus salmonis) in step salinity gradients. J Mar Biol Assoc UK 75:927–939
Hosmer DW, Lemeshow S (2004) Applied logistic regression, 2nd edn. Wiley, New York, p 392
Jansen PA, Kristoffersen AB, Viljugrein H, Jimenez D, Aldrin M, Stien A (2012) Sea lice as a density-dependent constraint to salmonid farming. Proc R Soc B Biol Sci 279:2330–2338. doi:10.1098/rspb.2012.0084
Johansen L-H, Jensen I, Mikkelsen H, Bjørn PA, Jansen PA, Bergh O (2011) Disease interaction and pathogens exchange between wild and farmed fish populations with special reference to Norway. Aquaculture 315:167–186
Jones S, Kim E, Bennett W (2008) Early development of resistance to the salmon louse, Lepeophtheirus salmonis (Krøyer), in juvenile pink salmon, Oncorhynchus gorbuscha (Walbaum). J Fish Dis 31:591–600
Jones SRM, Fast MD, Johnson SC, Groman DB (2007) Differential rejection of salmon lice by pink and chum salmon: disease consequences and expression of proinflammatory genes. Dis Aquat Organ 75:229–238
Jones SRM, Hargreaves NB (2009) Infection threshold to estimate Lepeophtheirus salmonis-associated mortality among juvenile pink salmon. Dis Aquat Organ 84:131–137
Jones SRM, Hargreaves NB (2007) The abundance and distribution of Lepeophtheirus salmonis (Copepoda: Caligidae) on pink (Oncorhynchus gorbuscha) and chum (O. Keta) salmon in coastal British Columbia. J Parasitol 93:1324–1331
Jones SRM, Prosperi-Porta G, Kim E, Callow P, Hargreaves NB (2006a) The occurrence of Lepeophtheirus salmonis and Caligus clemensi (Copepoda: Caligidae) on three-spine stickleback Gasterosteus aculeatus in coastal British Columbia. J Parasitol 92:473–480
Jones SRM, Wosniok W, Hargreaves NB (2006b) The salmon louse Lepeophtheirus salmonis on salmonid and non-salmonid fishes in British Columbia. In: Proceedings of the 11th international symposium on veterinary epidemiology and economics.
Kristoffersen AB, Rees EE, Stryhn H, Ibarra R, Campisto JL, Revie C, St-Hilaire S (2012) Understanding sources of sea lice for salmon farms in Chile. Prev Vet Med 111:165–175
Krkosek M, Ford JS, Morton A, Lele S, Myers RA, Lewis MA (2007) Declining wild salmon populations in relation to parasites from farm salmon. Science 318:1772–1775
Krkosek M, Lewis MA, Volpe JP (2005a) Transmission dynamics of parasitic sea lice from farm to wild salmon. Proc R Soc B Biol Sci 272:689–696
Krkosek M, Morton A, Volpe JP (2005b) Nonlethal assessment of juvenile pink and chum salmon for parasitic sea lice infections and fish health. Trans Am Fish Soc 134:711–716
Krkosek M, Morton A, Volpe JP, Lewis MA (2009) Sea lice and salmon population dynamics: effects of exposure time for migratory fish. Proc R Soc B Biol Sci 276:2819–2828
Krkosek M, Revie CW, Gargan PG, Skilbrei OT, Finstad B, Todd CD (2013) Impact of parasites on salmon recruitment in the Northeast Atlantic Ocean. Proc R Soc B Biol Sci 280:2012–2359
Liu L, Ma JZ, Johnson BA (2008) A multi-level two-part random effects model, with application to an alcohol-dependence study. Stat Med 27:3528–3539
Marty GD, Saksida SM, Quinn TJ (2010) Relationship of farm salmon, sea lice, and wild salmon populations. Proc Natl Acad Sci USA 107:22599–22604
McCullagh P, Nelder J (1989) Generalized linear models, 2nd edn. Chapman & Hall Inc., London
Middlemas SJ, Fryer RJ, Tulett D, Armstrong JD (2012) Relationship between sea lice levels on sea trout and fish farm activity in western Scotland. Fish Manag Ecol 20:68–74
Morton AB, Williams R (2003) First report of a sea louse, Lepeophtheirus salmonis, infestation on juvenile pink salmon, Oncorhynchus gorbuscha, in nearshore habitat. Can Field Nat 117:634–641
Moss JH, Murphy JM, Farley EV, Eisner LB, Andrews AG (2009) Juvenile pink and chum salmon distribution, diet, and growth in the northern Bering and Chukchi Seas. North Pac Anadromous Fish Comm 5:191–196
Okabe A, Boots B, Sugihara K, Chiu SN (2000) Spatial tessellations––concepts and applications of Voronoi diagrams, 2nd edn. Wiley, Chichester, p 696
Patanasatienkul T, Sanchez J, Rees EE, Krkosek M, Jones SRM, Revie CW (2013) Sea lice infestations on juvenile chum and pink salmon in the Broughton Archipelago, Canada from 2003 to 2012. Dis Aquat Organ 105:149–161
Peacock SM, Krkosek M, Proboscsz S, Orr C (2013) Cessation of a salmon decline with control of parasites. Ecol Appl 23:606–620
R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/
Real LA, Biek R (2007) Spatial dynamics and genetics of infectious diseases on heterogeneous landscapes. J R Soc Interface 4:935–948
Saksida SM, Greba L, Morrison D, Revie CW (2011) Sea lice on wild juvenile Pacific salmon and farmed Atlantic salmon in the northernmost salmon farming region of British Columbia. Aquaculture 320:193–198
Salo EO (1991) Life history of chum salmon (Oncorhynchus keta). In: Groot C, Margolis L (eds) Pacific salmon life histories, 1st edn. University of British Columbia Press, Vancouver, pp 231–309
Stucchi DJ, Guo M, Foreman MGG, Czajko P, Galbraith M, Mackas DL, Gillibrand PA (2011) Modeling sea lice production and concentrations in the Broughton Archipelago, British Columbia. In: Jones S, Beamish R (eds) Salmon lice: an integrated approach to understanding parasite abundance and distribution, 1st edn. Wiley, Chichester, pp 117–150
Sutherland BJG, Jantzen SG, Sanderson DS, Koop BF, Jones SRM (2011) Differentiating size-dependent responses of juvenile pink salmon (Oncorhynchus gorbuscha) to sea lice (Lepeophtheirus salmonis) infections. Comp Biochem Physiol 6:213–223
Tooze JA, Grunwald GK, Jones RH (2002) Analysis of repeated measures data with clumping at zero. Stat Methods Med Res 11:341–355
Tucker CS, Sommerville C, Wootten R (2002) Does size really matter? Effects of fish surface area on the settlement and initial survival of Lepeophtheirus salmonis, an ectoparasite of Atlantic salmon Salmo salar. Dis Aquat Organ 49:145–152
Tully O, Gargan P, Poole WR, Whelan KF (1999) Spatial and temporal variation in the infestation of sea trout (Salmo trutta L.) by the caligid copepod Lepeophtheirus salmonis (Krøyer) in relation to sources of infection in Ireland. Parasitology 119:41–51
van Etten J (2012) gdistance: distances and routes on geographical grids. R package version 1.1–4. http://CRAN.Rproject.org/package=gdistance
Viljugrein H, Staalstrøm A, Molvaelr J, Urke HA, Jansen PA (2009) Integration of hydrodynamics into a statistical model on the spread of pancreas disease (PD) in salmon farming. Dis Aquat Organ 88:35–44
Wagner GN, Fast MD, Johnson SC (2008) Physiology and immunology of Lepeophtheirus salmonis infections of salmonids. Trends Parasitol 24:176–183
Werkman M, Green DM, Murray AG, Turnbull JF (2011) The effectiveness of fallowing strategies in disease control in salmon aquaculture assessed with an SIS model. Prev Vet Med 98:64–73
The authors would like to thank Broughton Archipelago Monitoring Plan (BAMP) Science Team members and sponsors who provided data sets, funding and valuable review and comment to support the undertaking and writing of the research summarized in this publication. BAMP (www.bamp.ca) began in 2010 as a multi-year sea lice monitoring and research program involving federal government, salmon farm producers, conservationists and academic researchers. We are grateful to Henrik Stryhn, University of Prince Edward Island, for statistical advice and coding of the two-part model. This research was undertaken, in part, thanks to funding from the Canada Excellence Research Chairs Program.
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Rees, E.E., St-Hilaire, S., Jones, S.R.M. et al. Spatial patterns of sea lice infection among wild and captive salmon in western Canada. Landscape Ecol 30, 989–1004 (2015). https://doi.org/10.1007/s10980-015-0188-2
- Atlantic salmon aquaculture
- British Columbia
- Caligus clemensi
- Lepeophtheirus salmonis
- Pacific salmon
- Sea lice
- Spatial–temporal modeling