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Chapter Nineteen - Ecology of a marine ectoparasite in farmed and wild salmon

from Part III - Understanding wildlife disease ecology at the community and landscape level

Published online by Cambridge University Press:  28 October 2019

Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
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Summary

Parasitism can affect every aspect of wildlife ecology, from predator avoidance and competition for food to migrations and reproduction. In the wild, these ecological effects can have implications for host fitness and parasite dynamics. In contrast, domestic environments are typically characterised by high host densities, low host diversity, and veterinary interventions, and are not subject to processes like predation, competition, and migration. When wild and domesticated hosts interact via shared parasite populations, understanding and predicting the outcomes of parasite ecology and evolution for wildlife conservation and sustainable farming can be a challenge. We describe the ecology and evolution of ectoparasitic sea lice that are shared by farmed and wild salmon and the insights that experiments, fieldwork, and mathematical modelling have generated for theory and applied problems of host–parasite interactions over the course of a long-term study in Pacific Canada. The salmon–sea lice host–parasite system provides a rich case study to examine the ecological context of host–parasite interactions and to shed light on the principal challenges of parasite management for wildlife health and conservation.

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Chapter
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Wildlife Disease Ecology
Linking Theory to Data and Application
, pp. 544 - 573
Publisher: Cambridge University Press
Print publication year: 2019

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References

Aaen, S.M., Helgesen, K.O., Bakke, M.J., Kaur, K. & Horsberg, T.E. (2015) Drug resistance in sea lice: a threat to salmonid aquaculture. Trends in Parasitology, 31, 7281.Google Scholar
Altizer, S., Harvell, D. & Friedle, E. (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology and Evolution, 18, 589596.Google Scholar
Anderson, R. M. & May, R. M. (1978) Regulation and stability of host–parasite population interactions: I. Regulatory processes. Journal of Animal Ecology, 47, 219247.CrossRefGoogle Scholar
Anderson, R. M. & May, R. M. (1979) Population biology of infectious diseases: Part I. Nature, 280, 361367.Google Scholar
Ashander, J. (2010) Effects of parasite exchange between wild and farmed salmon. MSc thesis, University of Alberta. DOI:10.6084/M9.FIGSHARE.1584651Google Scholar
Bateman, A.W., Peacock, S.J., Connors, B.M., et al. (2016) Recent failure in control of sea louse outbreaks on salmon in the Broughton Archipelago, British Columbia. Canadian Journal of Fisheries & Aquatic Sciences, 73, 11641172.CrossRefGoogle Scholar
Beamish, R.J., Mahnken, C. & Neville, C.M. (2004) Evidence that reduced early marine growth is associated with lower marine survival of coho salmon. Transactions of the American Fisheries Society, 133, 2633.Google Scholar
Bjørn, P.A., Finstad, B. & Kristoffersen, R. (2001) Salmon lice infection of wild sea trout and Arctic char in marine and freshwaters: the effects of salmon farms. Aquaculture Research, 32, 947962.Google Scholar
Brauner, C.J., Sackville, M., Gallagher, Z., et al. (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. Philosophical Transactions of the Royal Society of London: Series B, Biological Sciences, 367, 17701779.CrossRefGoogle ScholarPubMed
Burridge, L., Weis, J.S., Cabello, F., Pizarro, J. & Bostick, K. (2010) Chemical use in salmon aquaculture: a review of current practices and possible environmental effects. Aquaculture, 306, 723.Google Scholar
Chittenden, C.M., Jensen, J.L.A., Ewart, D., et al. (2010) Recent salmon declines: a result of lost feeding opportunities due to bad timing? PLoS ONE, 5, e12423.CrossRefGoogle ScholarPubMed
Comins, H.N. (1977) The development of insecticide resistance in the presence of migration. Journal of Theoretical Biology, 64, 177197.CrossRefGoogle ScholarPubMed
Connors, B.M., Braun, D.C., Peterman, R.M.M., et al. (2012) Migration links ocean-scale competition and local ocean conditions with exposure to farmed salmon to shape wild salmon dynamics. Conservation Letters, 5, 304312.Google Scholar
Connors, B.M., Hargreaves, N.B., Jones, S.R.M. & Dill, L.M. (2010a) Predation intensifies parasite exposure in a salmonid food chain. Journal of Applied Ecology, 47, 13651371.Google Scholar
Connors, B.M., Krkošek, M. & Dill, L.M. (2008) Sea lice escape predation on their host. Biology Letters, 4, 455457.Google Scholar
Connors, B.M., Krkošek, M., Ford, J. & Dill, L.M. (2010b) Coho salmon productivity in relation to salmon lice from infected prey and salmon farms. Journal of Applied Ecology, 47, 13721377.Google Scholar
Connors, B.M., Lagasse, C. & Dill, L.M. (2011) What’s love got to do with it? Ontogenetic changes in drivers of dispersal in a marine ectoparasite. Behavioral Ecology, 22, 588593.Google Scholar
Costello, M.J. (2004) A checklist of best practice for sea lice control on salmon farms. Caligus, 8, 18.Google Scholar
Costello, M.J. (2006) Ecology of sea lice parasitic on farmed and wild fish. Trends in Parasitology, 22, 475483.CrossRefGoogle ScholarPubMed
Costello, M.J. (2009) The global economic cost of sea lice to the salmonid farming industry. Journal of Fish Diseases, 32, 115.Google Scholar
Daszak, P., Cunningham, A. & Hyatt, A. (2000) Emerging infectious diseases of wildlife– threats to biodiversity and human health. Science, 287, 443.Google Scholar
De Castro, F. & Bolker, B. (2005) Mechanisms of disease-induced extinction. Ecology Letters, 8, 117126.Google Scholar
Dhondt, A., Dobson, A., Hochachka, W.M., et al. (2013) Multiple host transfers, but only one successful lineage in a continent-spanning emergent pathogen. Proceedings of the Royal Society of London B, 280, 20131068.Google Scholar
Eggers, D.M. (1978) Limnetic feeding behavior of juvenile sockeye salmon in Lake Washington and predator avoidance. Limnology and Oceanography, 23, 11141125.CrossRefGoogle Scholar
FAO (2016) The State of the World Fisheries and Aquaculture (SOFIA) 2016. Rome: FAO.Google Scholar
Frazer, L.N., Morton, A. & Krkošek, M. (2012) Critical thresholds in sea lice epidemics: evidence, sensitivity and subcritical estimation. Proceedings of the Royal Society of London B, 279, 19501958.Google Scholar
Furey, N.B., Hinch, S.G., Bass, A.L., et al. (2016) Predator swamping reduces predation risk during nocturnal migration of juvenile salmon in a high-mortality landscape. Journal of Animal Ecology, 85, 948959.Google Scholar
Godwin, S.C., Dill, L.M., Krkošek, M. & Price, M.H.H. (2017) Reduced growth in wild juvenile sockeye salmon Oncorhynchus nerka infected with sea lice. Journal of Fish Biology, 91, 4157.Google Scholar
Godwin, S.C., Dill, L.M., Reynolds, J.D. & Krkošek, M. (2015) Sea lice, sockeye salmon, and foraging competition: lousy fish are lousy competitors. Canadian Journal of Fisheries & Aquatic Sciences, 72, 11131120.Google Scholar
Godwin, S.C., Krkošek, M., Reynolds, J.D., Rogers, L.A. & Dill, L.M. (2017) Heavy sea louse infection is associated with decreased stomach fullness in wild juvenile sockeye salmon. Canadian Journal of Fisheries and Aquatic Sciences, 75, 15871595.Google Scholar
Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology, 43, 701726.Google Scholar
Groner, M.L., Gettinby, G., Stormoen, M., Revie, C.W. & Cox, R. (2014) Modelling the impact of temperature-induced life history plasticity and mate limitation on the epidemic potential of a marine ectoparasite. PLoS ONE, 9, e88465.Google Scholar
Groot, C. & Margolis, L. (1991) Pacific Salmon Life Histories. Vancouver, B.C.: UBC Press.Google Scholar
Hamre, L.A., Eichner, C., Caipang, C.M.A., et al. (2013) The salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae) life cycle has only two chalimus stages. PLoS ONE, 8, e73539.Google Scholar
Hargreaves, N. B. & LeBrasseur, R. J. (1985) Species selective predation on juvenile pink (Oncorhynchus gorbuscha) and chum salmon (O. keta) by coho salmon (O. kisutch). Canadian Journal of Fisheries and Aquatic Sciences, 42, 659668.Google Scholar
Hargreaves, N.B. & LeBrasseur, R.J. (1986) Size selectivity of coho (Oncorhynchus kisutch) preying on juvenile chum salmon (O. keta). Canadian Journal of Fisheries and Aquatic Sciences, 43, 581586.Google Scholar
Hatcher, M.J., Dick, J.T.A. & Dunn, A.M. (2006) How parasites affect interactions between competitors and predators. Ecology Letters, 9, 12531271.Google Scholar
Hatcher, M.J., Dick, J.T.A. & Dunn, A.M. (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment, 10, 186194.Google Scholar
Heuch, P.A., Nordhagen, J.R. & Schram, T.A. (2000) Egg production in the salmon louse [Lepeophtheirus salmonis (Krøyer)] in relation to origin and water temperature. Aquaculture Research, 31, 805814.Google Scholar
Holling, C.S. (1959) Some characteristics of simple types of predation and parasitism. The Canadian Entomologist, 91, 385398.Google Scholar
Hudson, P.J., Dobson, A.P. & Newborn, D. (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. Journal of Animal Ecology, 61, 681692.Google Scholar
Hudson, P. & Greenman, J. (1998) Competition mediated by parasites: biological and theoretical progress. Trends in Ecology and Evolution, 13, 387390.Google Scholar
Hudson, P.J., Rizzoli, A.P., Grenfell, B.T., Heesterbeek, J.A.P. & Dobson, A.P. (2002) Ecology of Wildlife Diseases. Oxford: Oxford University Press.Google Scholar
Ives, A.R. & Murray, D.L. (1997) Can sublethal parasitism destabilize predator–prey population dynamics? A model of snowshoe hares, predators and parasites. Journal of Animal Ecology, 66, 265278.Google Scholar
Jansen, P.A., Kristoffersen, A.B., Viljugrein, H., et al. (2012) Sea lice as a density-dependent constraint to salmonid farming. Proceedings of the Royal Society of London B, 279, 23302338.Google Scholar
Johnson, P.T.J., Stanton, D.E., Preu, E.R., Forshay, K.J. & Carpenter, S.R. (2006) Dining on disease: how interactions between infection and environment affect predation risk. Ecology, 87, 19731980.Google Scholar
Johnson, S.C. & Albright, L.J. (1991a) The developmental stages of Lepeophtheirus salmonis (Krøyer, 1837) (Copepoda: Caligidae). Canadian Journal of Zoology, 69, 929950.Google Scholar
Johnson, S.C. & Albright, L. J. (1991b) Development, growth, and survival of Lepeophtheirus salmonis (Copepoda: Caligidae) under laboratory conditions. Journal of the Marine Biological Association of the United Kingdom, 71, 425436.Google Scholar
Jones, K.E., Patel, N.G., Levy, M.A., et al. (2008) Global trends in emerging infectious diseases. Nature, 451, 990993.Google Scholar
Jones, S.R.M., Prosperi-Porta, G., Kim, E., Callow, P. & Hargreaves, N.B. (2006) The occurrence of Lepeophtheirus salmonis and Caligus clemensi (Copepoda: Caligidae) on three-spine stickleback Gasterosteus aculeatus in coastal British Columbia. The Journal of Parasitology, 92, 473480.CrossRefGoogle ScholarPubMed
Kennedy, D.A., Kurath, G., Brito, I.L., et al. (2016) Potential drivers of virulence evolution in aquaculture. Evolutionary Applications, 9, 344354.Google Scholar
Kreitzman, M., Ashander, J., Driscoll, J., et al. (2018) An evolutionary ecosystem service: wild salmon sustain the effectiveness of parasite control on salmon farms. Conservation Letters, 11, e12395.Google Scholar
Krkošek, M. (2016) Population biology of infectious diseases shared by wild and farmed fish. Canadian Journal of Fisheries & Aquatic Sciences, 74, 620628.Google Scholar
Krkošek, M., Ashander, J., Frazer, L.N., & Lewis, M.A. (2013a) Allee effect from parasite spill-back. American Naturalist, 182, 640652.CrossRefGoogle ScholarPubMed
Krkošek, M., Connors, B.M., Ford, H., et al. (2011a) Fish farms, parasites, and predators: implications for salmon population dynamics. Ecological Applications, 21, 897914.CrossRefGoogle ScholarPubMed
Krkošek, M., Connors, B.M., Lewis, M.A. & Poulin, R. (2012) Allee effects may slow the spread of parasites in a coastal marine ecosystem. The American Naturalist, 179, 401412.Google Scholar
Krkošek, M., Connors, B.M., Morton, A., et al. (2011b) Effects of parasites from salmon farms on productivity of wild salmon. Proceedings of the National Academy of Sciences of the United States of America, 108, 14,70014,704.Google Scholar
Krkošek, M., Ford, J.S., Morton, A., et al. (2007a) Declining wild salmon populations in relation to parasites from farm salmon. Science, 318, 1772.Google Scholar
Krkošek, M., Gottesfeld, A., Proctor, B., et al. (2007b) Effects of host migration, diversity and aquaculture on sea lice threats to Pacific salmon populations. Proceedings of the Royal Society of London B, 274, 31413149.Google Scholar
Krkošek, M., Lewis, M.A., Morton, A., Frazer, L.N. & Volpe, J.P. (2006) Epizootics of wild fish induced by farm fish. Proceedings of the National Academy of Sciences of the United States of America, 103, 15,50615,510.Google Scholar
Krkošek, M., Lewis, M.A., Volpe, J.P. & Krkošek, M. (2005) Transmission dynamics of parasitic sea lice from farm to wild salmon. Proceedings of the Royal Society of London B, 272, 689696.Google Scholar
Krkošek, M., Morton, A., Volpe, J.P. & Lewis, M.A. (2009) Sea lice and salmon population dynamics: effects of exposure time for migratory fish. Proceedings of the Royal Society of London B, 276, 28192828.Google Scholar
Krkošek, M., Revie, C.W., Gargan, P.G., et al. (2013b) Impact of parasites on salmon recruitment in the Northeast Atlantic Ocean. Proceedings of the Royal Society of London B, 280, 20122359.Google Scholar
Kutz, S.J., Hoberg, E.P., Molnár, P.K., Dobson, A. & Verocai, G.G. (2014) A walk on the tundra: host–parasite interactions in an extreme environment. International Journal for Parasitology: Parasites and Wildlife, 3, 198208.Google Scholar
Lafferty, K.D. (1992) Foraging on prey that are modified by parasites. The American Naturalist, 140, 854867.Google Scholar
Lafferty, K.D. (1999) The evolution of trophic transmission. Parasitology Today, 15, 111115.Google Scholar
Lafferty, K.D. & Ben-Horin, T. (2013) Abalone farm discharges the withering syndrome pathogen into the wild. Frontiers in Microbiology, 4, 15.Google Scholar
Lenski, R. & May, R. (1994) The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. Journal of Theoretical Biology, 169, 253265.Google Scholar
Liu, Y., Rosten, T.W., Henriksen, K., et al. (2016) Comparative economic performance and carbon footprint of two farming models for producing Atlantic salmon (Salmo salar): land-based closed containment system in freshwater and open net pen in seawater. Aquacultural Engineering, 71, 112.Google Scholar
Losos, C.J.C., Reynolds, J.D. & Dill, L.M. (2010) Sex-selective predation by three spine sticklebacks on sea lice: a novel cleaning behaviour. Ethology, 116, 981989.CrossRefGoogle Scholar
Marty, G.D., Saksida, S.M. & Quinn, T.J. (2010) Relationship of farm salmon, sea lice, and wild salmon populations. Proceedings of the National Academy of Sciences of the United States of America, 107, 22,59922,604.Google Scholar
May, R.M. & Anderson, R.M. (1991) Infectious Diseases of Humans. Oxford: Oxford University Press.Google Scholar
May, R.M. & Nowak, M.A. (1995) Coinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London B, 261, 209215.Google Scholar
McEwan, G.F., Groner, M.L., Fast, M.D., Gettinby, G. & Revie, C.W. (2015) Using agent-based modelling to predict the role of wild refugia in the evolution of resistance of sea lice to chemotherapeutants. PLoS ONE, 10, 123.Google Scholar
McKinnell, S., Curchitser, E., Groot, K., Kaeriyama, M. & Trudel, M. (2014) Oceanic and atmospheric extremes motivate a new hypothesis for variable marine survival of Fraser River sockeye salmon. Fisheries Oceanography, 23, 322341.Google Scholar
Mennerat, A., Nilsen, F., Ebert, D., & Skorping, A. (2010) Intensive farming: evolutionary implications for parasites and pathogens. Evolutionary Biology, 37, 5967.Google Scholar
Messmer, A.M., Rondeau, E.B., Jantzen, S.G., et al. (2011) Assessment of population structure in Pacific Lepeophtheirus salmonis (Krøyer) using single nucleotide polymorphism and microsatellite genetic markers. Aquaculture, 320, 183192.Google Scholar
Morton, A. & Routledge, R. (2005) Mortality rates for juvenile pink (Oncorhynchus gorbuscha) and chum (O. keta) salmon infested with sea lice (Lepeophtheirus salmonis) in the Broughton Archipelago. Alaska Fishery Research Bulletin, 11, 146152.Google Scholar
Morton, A., Routledge, R.D. & Williams, R. (2005) Temporal patterns of sea louse infestation on wild Pacific salmon in relation to the fallowing of Atlantic salmon farms. North American Journal of Fisheries Management, 25, 811821.Google Scholar
Moss, J.H., Beauchamp, D.A., Cross, A.D., et al. (2005) Evidence for size-selective mortality after the first summer of ocean growth by pink salmon. Transactions of the American Fisheries Society, 134, 13131322.Google Scholar
Murray, A. (2011) A simple model to assess selection for treatment-resistant sea lice. Ecological Modelling, 222, 18541862.Google Scholar
Murray, A.G. & Salama, N.K.G. (2016) A simple model of the role of area management in the control of sea lice. Ecological Modelling, 337, 3947.Google Scholar
Nilsen, A., Nielsen, K.V., Biering, E. & Bergheim, A. (2017) Effective protection against sea lice during the production of Atlantic salmon in floating enclosures. Aquaculture, 466, 4150.Google Scholar
Orobko, M. (2016) Alternate stable states in coupled fishery–aquaculture systems. MSc thesis, University of Toronto. ProQuest Number: 10130697.Google Scholar
Packer, C., Holt, R.D., Hudson, P.J., Lafferty, K.D. & Dobson, A.P. (2003) Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecology Letters, 6, 797802.Google Scholar
Parker, R.R. (1968) Marine mortality schedules of pink salmon of the Bella Coola River, central British Columbia. Journal of the Fisheries Research Board of Canada, 25, 757794.Google Scholar
Parker, R.R. (1969) Predator–prey relationship among pink and chum salmon fry and coho smolts in a central British Columbia inlet. Fisheries Research Board of Canada Manuscript Report Series, 1019.Google Scholar
Peacock, S.J., Bateman, A.W., Krkošek, M. & Lewis, M.A. (2016) The dynamics of coupled populations subject to control. Theoretical Ecology, 9, 365380.Google Scholar
Peacock, S.J., Connors, B.M., Krkošek, M., Irvine, J.R. & Lewis, M.A. (2014) Can reduced predation offset negative effects of sea louse parasites on chum salmon? Proceedings of the Royal Society of London B, 281, 20132913.Google Scholar
Peacock, S.J., Krkošek, M., Bateman, A. W. &. Lewis, M.A. (2015) Parasitism and food web dynamics of juvenile Pacific salmon. Ecosphere, 6, 116.Google Scholar
Peacock, S.J., Krkošek, M., Proboszcz, S., Orr, C. & Lewis, M.A. (2013) Cessation of a salmon decline with control of parasites. Ecological Applications, 23, 606620.Google Scholar
Pedersen, A.B., Jones, K.E., Nunn, C.L. & Altizer, S. (2007) Infectious diseases and extinction risk in wild mammals. Conservation Biology, 21, 12691279.CrossRefGoogle ScholarPubMed
Pike, A.W. & Wadsworth, S.L. (2000), Sealice on salmonids: their biology and control. Advances in Parasitology, 44, 233337.Google Scholar
Price, M.H.H., Morton, A. & Reynolds, J. D. (2010) Evidence of farm-induced parasite infestations on wild juvenile salmon in multiple regions of coastal British Columbia, Canada. Canadian Journal of Fisheries and Aquatic Sciences, 67, 19251932.Google Scholar
Price, M.H.H., Proboszcz, S.L., Routledge, R.D., et al. (2011) Sea louse infection of juvenile sockeye salmon in relation to marine salmon farms on Canada’s west coast. PLoS ONE, 6, e16851.Google Scholar
Pruvot, M., Lejeune, M., Kutz, S., et al. (2016) Better alone or in ill company? the effect of migration and inter-species comingling on Fascioloides magna infection in elk. PLoS ONE, 11, e0159319.Google Scholar
Pruvot, M., Seidel, D., Boyce, M.S., et al. (2014) What attracts elk onto cattle pasture? Implications for inter-species disease transmission. Preventive Veterinary Medicine, 117, 326339.Google Scholar
Pulkkinen, K., Suomalainen, L.-R., Read, A.F., et al. (2010) Intensive fish farming and the evolution of pathogen virulence: the case of columnaris disease in Finland. Proceedings of the Royal Society of London B, 277, 593600.Google ScholarPubMed
Revie, C.W., Gettinby, G., Treasurer, J.W. & Wallace, C. (2003) Identifying epidemiological factors affecting sea lice Lepeophtheirus salmonis abundance on Scottish salmon farms using general linear models. Diseases of Aquatic Organisms, 57, 8595.Google Scholar
Ritchie, G., Mordue (Luntz), A.J., Pike, A.W. & Rae, G.H. (1996) Observations on mating and reproductive behaviour of Lepeophtheirus salmonis, Krøyer (Copepoda: Caligidae). Journal of Experimental Marine Biology and Ecology, 201, 285298.Google Scholar
Ruggerone, G.T. & Connors, B.M. (2015) Productivity and life history of sockeye salmon in relation to competition with pink and sockeye salmon in the North Pacific Ocean. Canadian Journal of Fisheries & Aquatic Sciences, 72, 818833.CrossRefGoogle Scholar
Saksida, S. M., Morrison, D. & Revie, C.W. (2010) The efficacy of emamectin benzoate against infestations of sea lice, Lepeophtheirus salmonis, on farmed Atlantic salmon, Salmo salar L., in British Columbia. Journal of Fish Diseases, 33, 913917.CrossRefGoogle Scholar
Schumaker, B. (2013) Risks of Brucella abortus spillover in the Greater Yellowstone Area. Revue scientifique et technique (International Office of Epizootics), 32, 7177.Google Scholar
Shaw, D.J., Grenfell, B.T. & Dobson, A.P. (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology, 117, 597610.Google Scholar
Sundberg, L.-R., Ketola, T., Laanto, E., et al. (2016) Intensive aquaculture selects for increased virulence and interference competition in bacteria. Proceedings of the Royal Society of London B, 283, 20153069.Google Scholar
Tabashnik, B., Brévault, T. & Carrière, Y. (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nature Biotechnology, 31, 510521.Google Scholar
Thorstad, E.B., Todd, C.D., Uglem, I., et al. (2015) Effects of salmon lice Lepeophtheirus salmonis on wild sea trout Salmo trutta – a literature review. Aquaculture Environment Interactions, 7, 91113.Google Scholar
Tian, H., Zhou, S., Dong, L., et al. (2015) Avian influenza H5N1 viral and bird migration networks in Asia. Proceedings of the National Academy of Sciences of the United States of America, 112, 172177.Google Scholar
Tompkins, D.M., Carver, S., Jones, M.E., Krkošek, M. & Skerratt, L.F. (2015) Emerging infectious diseases of wildlife: a critical perspective. Trends in Parasitology, 31, 149159.Google Scholar
van Baalen, M. & Sabelis, M. (1995) The dynamics of multiple infection and the evolution of virulence. The American Naturalist, 146, 881.Google Scholar
Van Boeckel, T.P., Brower, C., Gilbert, M., et al. (2015) Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences of the United States of America, 112, 56495654.Google Scholar
Viana, M., Cleaveland, S., Matthiopoulos, J., et al. (2015) Dynamics of a morbillivirus at the domestic–wildlife interface: canine distemper virus in domestic dogs and lions. Proceedings of the National Academy of Sciences of the United States of America, 112, 14641469.Google Scholar
Vollset, K.W., Dohoo, I., Karlsen, Ø., et al. (2018) Disentangling the role of sea lice on the marine survival of Atlantic salmon. ICES Journal of Marine Science, 75, 5060.Google Scholar
Vollset, K.W., Krontveit, R.I., Jansen, P.A., et al. (2015) Impacts of parasites on marine survival of Atlantic salmon: a meta-analysis. Fish and Fisheries, 17, 714730.Google Scholar
Watson, M.J. (2013) What drives population-level effects of parasites? Meta-analysis meets life-history. International Journal for Parasitology: Parasites and Wildlife, 2, 190196.Google Scholar

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