Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-23T20:36:38.069Z Has data issue: false hasContentIssue false
  • English
  • Français

Potential risks of trophic impacts by escaped transgenic salmon in marine environments

Published online by Cambridge University Press:  15 September 2014

LINGBO LI ,
TONY J. PITCHER  and
ROBERT H. DEVLIN
LINGBO LI
Affiliation:
Fisheries and Oceans Canada, 4160 Marine Drive, West Vancouver, BC, CanadaV7V 1N6 Fisheries Centre, the University of British Columbia, 2202 Main Mall, Vancouver, BC, V6T 1Z4, Canada
TONY J. PITCHER
Affiliation:
Fisheries Centre, the University of British Columbia, 2202 Main Mall, Vancouver, BC, V6T 1Z4, Canada
ROBERT H. DEVLIN*
Affiliation:
Fisheries and Oceans Canada, 4160 Marine Drive, West Vancouver, BC, CanadaV7V 1N6
*
*Correspondence: Dr Robert H. Devlin Tel: +1 604 666 7926 Fax: +1 604 666 3497 e-mail: robert.devlin@dfo-mpo.gc.ca
Get access Rights & Permissions [Opens in a new window]

Summary

There is significant concern about potential ecological effects of introduced organisms, including non-indigenous species and those created by genetic modification. This paper presents an Ecopath with Ecosim modelling approach, designed to examine long-term trophic effects of growth hormone (GH) transgenic coho salmon should they ever escape to a coastal salmonid ecosystem, namely the Strait of Georgia in British Columbia (Canada). The model showed that the effects of introduced GH transgenic coho salmon varied with their biomass, diet, structure of the invaded ecosystem, and environmental conditions. Occasional escapes of non-reproductive salmon did not have a significant impact on the example ecosystem. However, effects of GH coho salmon varied with their diet when large numbers of these fish were present in the simulated ecosystem (for example, when they constituted 20% of total current aquaculture production in the area). Further, climate-driven changes in the biomass of low trophic levels (bottom-up effects) could have a greater impact on the ecosystem than the introduction of large numbers of GH coho salmon. A new version of Ecopath with Ecosim's Monte Carlo approach showed that the model predictions were robust to GH coho salmon's Ecopath parameters, but more sensitive to vulnerabilities of prey to GH coho salmon. Modelling ecosystem effects of genetically modified organisms provides a complementary approach for risk assessments when data from nature are not readily obtainable.

Keywords

bottom-up effectsEcopath with Ecosimecosystemgrowth hormoneMonte Carlo simulationsalmontransgenictrophic interactionsvulnerabilities
Type
Papers
Information
Environmental Conservation , Volume 42 , Issue 2 , June 2015 , pp. 152 - 161
Copyright
Copyright © Foundation for Environmental Conservation 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahrens, R. N. M. & Devlin, R. H. (2011) Standing genetic variation and compensatory evolution in transgenic organisms: a growth-enhanced salmon simulation. Transgenic Research 20: 583–597.Google Scholar
Ahrens, R. N. M., Walters, C. J. & Christensen, V. (2012) Foraging arena theory. Fish and Fisheries 13: 41–59.Google Scholar
Ainsworth, C. H., Kaplan, I. C., Levin, P. S. & Mangel, M. (2010) A statistical approach for estimating fish diet compositions from multiple data sources: Gulf of California case study. Ecological Applications 20: 2188–2202.Google Scholar
Bax, N., Williamson, A., Aguero, M., Gonzalez, E. & Geeves, W. (2003) Marine invasive alien species: a threat to global biodiversity. Marine Policy 27: 313–323.CrossRefGoogle Scholar
Bessey, C., Devlin, R. H., Liley, N. R. & Biagi, C. A. (2004) Reproductive performance of growth-enhanced transgenic coho salmon. Transactions of the American Fisheries Society 133: 1205–1220.Google Scholar
Cheung, W. W. L., Lam, V. W. Y., Sarmiento, J. L., Kearney, K., Watson, R. & Pauly, D. (2009) Projecting global marine biodiversity impacts under climate change scenarios. Fish and Fisheries 10: 235–251.Google Scholar
Christensen, V. & Walters, C. J. (2004) Ecopath with Ecosim: methods, capabilities and limitations. Ecological Modelling 172: 109–139.Google Scholar
Christensen, V., Walters, C. J., Pauly, D. & Forrest, R. (2008) Ecopath with Ecosim version 6 user guide [www document]. URL http://www.ecopath.org Google Scholar
Coumou, D. & Rahmstorf, S. (2012) A decade of weather extremes. Nature Climate Change 2: 491–496.Google Scholar
Davis, S. A., Catchpole, E. A. & Pech, R. P. (1999) Models for the introgression of a transgene into a wild population within a stochastic environment, with applications to pest control. Ecological Modelling 119: 267–275.Google Scholar
Devlin, R. H. & Donaldson, E. M. (1992) Containment of genetically altered fish with emphasis on salmonids. In: Transgenic Fish, ed. Hew, C. L. & Fletcher, G. L., pp. 229–66. Singapore: World Scientific.Google Scholar
Devlin, R. H., Biagi, C. A. & Yesaki, T. Y. (2004a) Growth, viability and genetic characteristics of GH transgenic coho salmon strains. Aquaculture 236: 607–632.CrossRefGoogle Scholar
Devlin, R. H., D’Andrade, M., Uh, M. & Biagi, C. A. (2004 b) Population effects of growth hormone transgenic coho salmon depend on food availability and genotype by environment interactions. Proceedings of the National Academy of Sciences USA 101: 9303–9308.Google Scholar
Devlin, R. H., Johnsson, J. I., Smailus, D. E., Biagi, C. A., Joensson, E. & Bjoernsson, B. T. (1999) Increased ability to compete for food by growth hormone-transgenic coho salmon Oncorhynchus kisutch (Walbaum). Aquaculture Research 30: 479–482.CrossRefGoogle Scholar
Devlin, R. H., Sundström, L. F. & Muir, W. M. (2006) Interface of biotechnology and ecology for environmental risk assessments of transgenic fish. Trends in Biotechnology 24: 89–97.Google Scholar
Devlin, R. H., Yesaki, T. Y., Biagl, C. A., Donaldson, E. M., Swanson, P. & Chan, W. (1994) Extraordinary salmon growth. Nature 371: 209–210.Google Scholar
Espinosa-Romero, M. J., Gregr, E. J., Walters, C., Christensen, V. & Chan, K. (2011) Representing mediating effects and species reintroductions in Ecopath with Ecosim. Ecological Modelling 222: 1569–1579.Google Scholar
Falk-Petersen, J., Renaud, P. & Anisimova, N. (2011) Establishment and ecosystem effects of the alien invasive red king crab (Paralithodes camtschaticus) in the Barents Sea: a review. ICES Journal of Marine Science: Journal du Conseil 68: 479–488.Google Scholar
Farrell, A. P., Bennett, W. & Devlin, R. H. (1997) Growth-enhanced transgenic salmon can be inferior swimmers. Canadian Journal of Zoology 75: 335–337.Google Scholar
Grosholz, E. D., Ruiz, G. M., Dean, C. A., Shirley, K. A., Maron, J. L. & Connors, P. G. (2000) The impacts of a nonindigenous marine predator in a California Bay. Ecology 81: 1206–1224.Google Scholar
Harvey, C. J. & Kareiva, P. M. (2005) Community context and the influence of non-indigenous species on juvenile salmon survival in a Columbia River reservoir. Biological Invasions 7: 651–663.Google Scholar
Hoover, C., Pitcher, T. & Christensen, V. (2013) Effects of hunting, fishing and climate change on the Hudson Bay marine ecosystem: I. Re-creating past changes 1970–2009. Ecological Modelling 264: 130–142.Google Scholar
Hutchings, J. A. & Fraser, D. J. (2008) The nature of fisheries- and farming-induced evolution. Molecular Ecology 17: 294–313.Google Scholar
Jensen, Ø., Dempster, T., Thorstad, E. B., Uglem, I. & Fredheim, A. (2010) Escapes of fishes from Norwegian sea-cage aquaculture: causes, consequences and prevention. Aquatic Environmental Interactions 1: 71–83.Google Scholar
Kaplan, I. C., Brown, C. J., Fulton, E. A., Gray, I. A., Field, J. C. & and Smith, A. D. M. (2013) Impacts of depleting forage species in the California Current. Environmental Conservation 40: 380–393.Google Scholar
Kolar, C. S. & Lodge, D. M. (2002) Ecological predictions and risk assessment for alien fishes in North America. Science 298: 1233–1236.Google Scholar
Langseth, B. J., Rogers, M. & Zhang, H. (2012) Modeling species invasions in Ecopath with Ecosim: An evaluation using Laurentian Great Lakes models. Ecological Modelling 247: 251–261.Google Scholar
Lee, C. G., Devlin, R. H. & Farrell, A. P. (2003) Swimming performance, oxygen consumption and excess post-exercise oxygen consumption in adult transgenic and ocean-ranched coho salmon. Journal of Fish Biology 62: 753–766.Google Scholar
Li, L., Ainsworth, C. & Pitcher, T. (2010) Presence of harbour seals (Phoca vitulina) may increase exploitable fish biomass in the Strait of Georgia. Progress in Oceanography 87: 235–241.Google Scholar
Liu, Y., Diserud, O. H., Hindar, K. & Skonhoft, A. (2013) An ecological–economic model on the effects of interactions between escaped farmed and wild salmon (Salmo salar). Fish and Fisheries 14: 148–173.Google Scholar
Li, L., Mackas, D., Hunt, B., Schweigert, J., Pakhomov, E., Ian Perry, R., Galbraith, M. & Pitcher, T. J. (2013) Zooplankton communities in the Strait of Georgia, British Columbia, track large-scale climate forcing over the Pacific Ocean. Progress in Oceanography 115: 90–102.Google Scholar
Lõhmus, M., Björklund, M., Sundström, L. F. & Devlin, R. H. (2010) Effects of temperature and growth hormone on individual growth trajectories of wild-type and transgenic coho salmon Oncorhynchus kisutch . Journal of Fish Biology 76: 641–654.Google Scholar
Mackas, D., Galbraith, M., Faust, D., Masson, D., Young, K., Shaw, W., Romaine, S., Trudel, M., Dower, J. & Campbell, R. (2013) Zooplankton time series from the Strait of Georgia: Results from year-round sampling at deep water locations, 1990–2010. Progress in Oceanography 115: 129–159.Google Scholar
Muir, W. M. & Howard, R. D. (1999) Possible ecological risks of transgenic organism release when transgenes affect mating success: Sexual selection and the Trojan gene hypothesis. Proceedings of the National Academy of Sciences USA 96: 13853–13856.Google Scholar
Muir, W. M. & Howard, R. D. (2002) Assessment of possible ecological risks and hazards of transgenic fish with implications for other sexually reproducing organisms. Transgenic Research 11: 101–114.Google Scholar
Parker, I. M., Simberloff, D., Lonsdale, W. M., Goodell, K., Wonham, M., Kareiva, P. M., Williamson, M. H., Von Holle, B. M. P. B., Moyle, P. B. & Byers, J. E. (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biological Invasions 1: 3–19.Google Scholar
Perry, R. I., Barange, M., Hofmann, E., Moloney, C., Ottersen, G. & Sakurai, Y. (2010) Introduction to the GLOBEC 3rd Open Science Meeting: From ecosystem function to ecosystem prediction. Progress in Oceanography 87: 1–5.Google Scholar
Pitcher, T. J. & Hart, P. J. B. (1995) The Impact of Species Changes in African Lakes. London, UK: Chapman & Hall.Google Scholar
Rahmstorf, S. & Coumou, D. (2011) Increase of extreme events in a warming world. Proceedings of the National Academy of Sciences USA 108: 17905–17909.Google Scholar
Ricciardi, A. (2003) Predicting the impacts of an introduced species from its invasion history: an empirical approach applied to zebra mussel invasions. Freshwater Biology 48: 972–981.Google Scholar
Ruesink, J. L. (2005) Global analysis of factors affecting the outcome of freshwater fish introductions. Conservation Biology 19: 1883–1893.Google Scholar
Smith, A. D. M., Brown, C. J., Bulman, C. M., Fulton, E. A., Johnson, P., Kaplan, I. C., Lozano-Montes, H., Mackinson, S., Marzloff, M., Shannon, L. J., Shin, Y. & Jorge Tam, J. (2011) Impacts of fishing low–trophic level species on marine ecosystems. Science 333: 1147–1150.Google Scholar
Sundström, L. F., Lohmus, M., Devlin, R. H., Johnsson, J. I., Biagi, C. A. & Bohlin, T. (2004) Feeding on profitable and unprofitable prey: comparing behaviour of growth-enhanced transgenic and normal coho Salmon (Oncorhynchus kisutch). Ethology 110: 381–396.Google Scholar
Sundström, L. F., Lohmus, M. & Devlin, R. H. (2005) Selection on increased intrinsic growth rates in coho salmon, Oncorhynchus kisutch . Evolution 59: 1560–1569.Google Scholar
Sundström, L. F., Lohmus, M., Tymchuk, W. E. & Devlin, R. H. (2007) Gene-environment interactions influence ecological consequences of transgenic animals. Proceedings of the National Academy of Sciences USA 104: 3889–3894.Google Scholar
Thomsen, M. S., Olden, J. D., Wernberg, T., Griffin, J. N. & Silliman, B. R. (2011) A broad framework to organize and compare ecological invasion impacts. Environmental Research 111: 899–908.Google Scholar
Valosaari, K. R., Aikio, S. & Kaitala, V. (2008) Male mating strategy and the introgression of a growth hormone transgene. Evolutionary Applications 1: 608–619.Google Scholar
Walters, C. & Kitchell, J. F. (2001) Cultivation/depensation effects on juvenile survival and recruitment: implications for the theory of fishing. Canadian Journal of Fisheries and.Aquatic.Science 58: 39–50.Google Scholar
Walther, G. R., Roques, A., Hulme, P. E., Sykes, M. T., Pyšek, P., Kühn, I., Zobel, M., Bacher, S., Botta-Dukát, Z. & Bugmann, H. (2009) Alien species in a warmer world: risks and opportunities. Trends in Ecology and Evolution 24: 686–693.Google Scholar
Zhu, Z., He, L. & Chen, S. (1985) Novel gene transfer into the fertilized eggs of gold fish (Carassius auratus L. 1758). Journal of Applied Ichthyology 1: 31–34.Google Scholar
Supplementary material: File

Li Supplementary Material

Supplementary Material

Download Li Supplementary Material(File)
File 30.9 KB