Genetic and ecological effects of salmon farming on wild salmon: modelling from experimental results

Hindar, K., Fleming, I. A., McGinnity, P., and Diserud, O. 2006. Genetic and ecological effects of salmon farming on wild salmon: modelling from experimental results. � ICES Journal of Marine Science, 63: 1234e1247. Cultured salmonids are released or escape into the wild in large numbers and may make up significant proportions of wild salmonid populations in fresh- and saltwater, causing considerable concern for the fitness and productivity of these populations. This paper focuses on the effects of escaped farmed Atlantic salmon (Salmo salar) on wild salmon. Farmed salmon have been under artificial selection for growth and other economically important traits for 30 years and are genetically different in their origin at the molecular and quantitative genetic levels. Escaped farmed salmon spawn in the wild with limited success. Their offspring outgrow those of wild origin but suffer higher mortality. Whole-river experiments in Ireland and Norway have shown that the lifetime success of farmed salmon is reduced relative to wild salmon. Based on data from these experiments, we model the future of wild salmon populations experiencing invasions of escaped farmed salmon. Simulations with a fixed intrusion rate of 20% escaped farmed salmon at spawning suggest that substantial changes take place in wild salmon populations within ten salmon generations (w40 years). Low-invasion scenarios suggest that farmed offspring are unlikely to become established in the population, whereas high-invasion scenarios suggest that populations are eventually mixtures of hybrid and farmed descendants. Recovery of the wild population is not likely under all circumstances, even after many decades without further intrusion. Managers of wild salmon will have difficulty in obtaining broodstock of the original wild population after a few generations of high intrusion. We conclude that further measures to reduce escapes of farmed salmon and their spawning in wild populations are urgently needed.

[1]  S. Einum,et al.  Spawning behaviour and success of mature male Atlantic salmon (Salmo salar) parr of farmed and wild origin , 2005 .

[2]  Crozier.  Incidence of escaped farmed salmon, Salmo salar L., in commercial salmon catches and fresh water in Northern Ireland , 1998 .

[3]  D. Bradley,et al.  Microsatellite genetic variation between and within farmed and wild Atlantic salmon (Salmo salar) populations , 1999 .

[4]  I. Fleming,et al.  Lifetime success and interactions of farm salmon invading a native population , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  K. Jakobsen,et al.  Genetic differences between two wild and one farmed population of Atlantic salmon (Salmo salar) revealed by three classes of genetic markers , 2004 .

[6]  S. Gudjonsson.  Occurrence of reared salmon in natural salmon rivers in Iceland , 1991 .

[7]  Shizhen S. Wang,et al.  Genetic variation and fitness in salmonids , 2002, Conservation Genetics.

[8]  J. Tufto.  Effects of Releasing Maladapted Individuals: A Demographic‐Evolutionary Model , 2001, The American Naturalist.

[9]  N. Ryman,et al.  Population Genetics and Fishery Management , 1987 .

[10]  P. D. Harris,et al.  Diseases and parasites in wild Atlantic salmon (Salmo salar) populations , 1998 .

[11]  P. McGinnity,et al.  Differential lifetime success and performance of native and non-native Atlantic salmon examined under communal natural conditions , 2004 .

[12]  K. Hindar,et al.  Genetic Effects of Cultured Fish on Natural Fish Populations , 1991 .

[13]  L. Bernatchez,et al.  Alternative male life‐history tactics as potential vehicles for speeding introgression of farm salmon traits into wild populations , 2003 .

[14]  E. Verspoor,et al.  The Atlantic salmon : genetics, conservation and management , 2007 .

[15]  R. Lande,et al.  Hatcheries and Endangered Salmon , 2004, Science.

[16]  B. Gjerde,et al.  Genetic origin of Norwegian farmed Atlantic salmon , 1991 .

[17]  Neil B. Metcalfe,et al.  Determinants of geographical variation in the age of seaward-migrating salmon, Salmo salar , 1990 .

[18]  F. Økland,et al.  Content of synthetic astaxanthin in escaped farmed Atlantic salmon, Salmo salar L., ascending Norwegian rivers , 1994 .

[19]  L. Bernatchez,et al.  Rapid parallel evolutionary changes of gene transcription profiles in farmed Atlantic salmon , 2005, Molecular ecology.

[20]  McGinnity Pg.  The biological significance of genetic variation in Atlantic salmon. , 1997 .

[21]  A. Youngson,et al.  Spawning of Escaped Farmed Atlantic Salmon (Salmo salar): Hybridization of Females with Brown Trout (Salmo trutta) , 1993 .

[22]  N. Ryman,et al.  Fish Gene Pools. , 1983 .

[23]  M. Gross,et al.  An experimental study of the reproductive behaviour and success of farmed and wild Atlantic salmon (Salmo salar) , 1996 .

[24]  P. McGinnity,et al.  Genetic changes in Atlantic salmon (Salmo salar) populations of Northwest Irish rivers resulting from escapes of adult farm salmon , 1998 .

[25]  S. Kalinowski,et al.  Population structure of Atlantic salmon (Salmo salar L.): a range‐wide perspective from microsatellite DNA variation , 2001, Molecular ecology.

[26]  D. Gausen,et al.  Large-Scale Escapes of Farmed Atlantic Salmon (Salmo salar) into Norwegian Rivers Threaten Natural Populations , 1991 .

[27]  H. M. Gjøen,et al.  Past, present, and future of genetic improvement in salmon aquaculture , 1997 .

[28]  J. Butler,et al.  The prevalence of escaped farmed salmon, Salmo salar L., in the River Ewe, western Scotland, with notes on their ages, weights and spawning distribution , 2005 .

[29]  R. C. Simon,et al.  Introduction to the Proceedings of the 1980 Stock Concept International Symposium (STOCS) , 1981 .

[30]  M. Mangel,et al.  Fugitive Salmon: Assessing the Risks of Escaped Fish from Net-Pen Aquaculture , 2005 .

[31]  R. Lande,et al.  THE ROLE OF GENETIC VARIATION IN ADAPTATION AND POPULATION PERSISTENCE IN A CHANGING ENVIRONMENT , 1996, Evolution; international journal of organic evolution.

[32]  Jeffrey A. Hutchings,et al.  Life history variation and growth rate thresholds for maturity in Atlantic salmon, Salmo salar , 1998 .

[33]  A. Youngson,et al.  The spawning behaviour of escaped farmed and wild adult Atlantic salmon (Salmo salar L.) in a northern Scottish river , 1991 .

[34]  W. Jordan,et al.  Population structure in the Atlantic salmon: insights from 40 years of research into genetic protein variation , 2005 .

[35]  P. McGinnity,et al.  Genetic changes in an Atlantic salmon population resulting from escaped juvenile farm salmon , 1998 .

[36]  Matthew W. Jones,et al.  INDIVIDUAL VARIATION IN ATLANTIC SALMON FERTILIZATION SUCCESS: IMPLICATIONS FOR EFFECTIVE POPULATION SIZE , 2002 .

[37]  H. Sægrov,et al.  Documentation of successful spawning of escaped farmed female Atlantic salmon, Salmo salar, in Norwegian rivers , 1991 .

[38]  P. A. Heuch,et al.  A review of the Norwegian ‘National Action Plan Against Salmon Lice on Salmonids’: The effect on wild salmonids , 2005 .

[39]  W. Schaffer,et al.  The Adaptive Significance of Variations in Life History among Local Populations of Atlantic Salmon in North America , 1975 .

[40]  N. Ryman.  Minimizing adverse effects of fish culture: understanding the genetics of populations with overlapping generations , 1997 .

[41]  J. Anderson,et al.  The occurrence and spawning of cultured Atlantic salmon (Salmo salar) in a Canadian river , 1997 .

[42]  I. Fleming,et al.  Effects of early experience on the reproductive performance of Atlantic salmon , 1997 .

[43]  J. Taggart,et al.  Genetic impact of escaped farmed Atlantic salmon (Salmo salar L.) on native populations: use of DNA profiling to assess freshwater performance of wild, farmed, and hybrid progeny in a natural river environment , 1997 .

[44]  L. Hansen,et al.  The incidence of escaped farmed Atlantic salmon, Salmo salar L., in the Faroese fishery and estimates of catches of wild salmon , 1999 .

[45]  K. Hindar,et al.  Effective size in management and conservation of subdivided populations. , 2003, Journal of theoretical biology.

[46]  J. Taggart,et al.  Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[47]  R. Waples.  Genetic interactions Between Hatchery and Wild Salmonids: Lessons from the Pacific Northwest , 1991 .

[48]  S. Einum,et al.  Local-scale density-dependent survival of mobile organisms in continuous habitats: an experimental test using Atlantic salmon , 2005, Oecologia.

[49]  K. Hindar,et al.  Salmonid culture and interspecific hybridization , 1994 .

[50]  J. Hutchings.  The threat of extinction to native populations experiencing spawning intrusions by cultured Atlantic salmon , 1991 .

[51]  P. Fiske,et al.  Relationships between the frequency of farmed Atlantic salmon, Salmo salar L., in wild salmon populations and fish farming activity in Norway, 1989–2004 , 2006 .

[52]  I. Fleming,et al.  Chapter 12. Farm Escapes , 2007 .

[53]  M. Chilcote.  Relationship between natural productivity and the frequency of wild fish in mixed spawning populations of wild and hatchery steelhead (Oncorhynchus mykiss) , 2003 .

[54]  G Luikart,et al.  New methods employing multilocus genotypes to select or exclude populations as origins of individuals. , 1999, Genetics.

[55]  I. Fleming.  Pattern and variability in the breeding system of Atlantic salmon (Salmo salar), with comparisons to other salmonids , 1998 .

[56]  S. Einum,et al.  Dominance relationships and behavioural correlates of individual spawning success in farmed and wild male Atlantic salmon, Salmo salar , 2004 .

[57]  A. Jensen,et al.  The spread of furunculosis in salmonids in Norwegian rivers , 1994 .

[58]  K. Glover,et al.  Microsatellite analysis in domesticated and wild Atlantic salmon (Salmo salar L.): allelic diversity and identification of individuals , 2004 .

[59]  S. Einum,et al.  Experimental tests of genetic divergence of farmed from wild Atlantic salmon due to domestication , 1997 .

[60]  A. Youngson,et al.  Reared Atlantic salmon, Salmo salar L., in the catches of a salmon fishery on the western coast of Scotland , 1992 .

[61]  Nina Jonsson,et al.  The relative role of density‐dependent and density‐independent survival in the life cycle of Atlantic salmon Salmo salar , 1998 .

[62]  K. Hindar,et al.  Escaped farmed Atlantic salmon replace the original salmon stock in the River Vosso, western Norway , 1997 .