Estuaries and Coasts

, Volume 40, Issue 1, pp 187–199 | Cite as

Nonnative Species in British Columbia Eelgrass Beds Spread via Shellfish Aquaculture and Stay for the Mild Climate

  • Megan E. MachEmail author
  • Colin D. Levings
  • Kai M. A. Chan


Nonnative species cause economic and ecological impacts in habitats they invade, but there is little information on how they spread and become abundant. This is especially true for nonnative species in native Zostera marina eelgrass beds in coastal British Columbia, Canada, which play a vital role in estuarine ecosystems. We tested how nonnative species richness and abundance were related to both arrival vectors and environmental factors in northeast Pacific eelgrass. Using correlation tests and generalized linear models, we examined how nonnative macroinvertebrates (benthic, epifaunal, and large mobile) and some algae species were related to arrival vectors (shipping and aquaculture) and environmental factors (climate variables, human population density, and native richness and abundance). We found 12 nonnative species, 50 % with known negative impacts within eelgrass habitats. For benthic organisms, both nonnative richness and abundance were strongly correlated with shellfish aquaculture activities, and not with shipping activity. For epifaunal nonnative richness and abundance, neither vector was significantly correlated. Climate (temperature and salinity) helped explain nonnative richness but not abundance; there was no relationship of nonnative richness or abundance to native species richness and abundance or population density. Results suggest that aquaculture activities are responsible for many primary introductions of benthic nonnative species, and that temperature and salinity tolerances are responsible for post-introduction invasion success. While aquaculture and shipping vectors are becoming increasingly regulated to prevent further international spread of nonnative species, it will be important when managing nonnatives to consider secondary spread from intraregional transport through local shellfish aquaculture and shipping.


British Columbia Seagrass Nonnative Invasive Exotic Aquaculture Zostera marina 



The authors would like to thank T. Goodman for help with collection and identification of species, taxonomists R.E. Ruff and J.R. Cordell for identification support, and C.C. Murray and R. Naidoo for constructive comments on writing and analysis. Funding for this research came from the Canadian Aquatic Invasive Species Network. Sampling equipment was provided by the Department of Fisheries and Oceans, Canada.

Supplementary material

12237_2016_124_MOESM1_ESM.docx (401 kb)
ESM 1 (DOCX 400 kb)
12237_2016_124_MOESM2_ESM.docx (158 kb)
ESM 2 (DOCX 158 kb)
12237_2016_124_MOESM3_ESM.docx (172 kb)
ESM 3 (DOCX 171 kb)


  1. Altman, S., and R.B. Whitlatch. 2007. Effects of small-scale disturbance on invasion success in marine communities. Journal of Experimental Marine Biology and Ecology 342: 15–29.CrossRefGoogle Scholar
  2. Anderson, D.R. 2008. Model based inference in the life sciences: primer on evidence. New York: Springer.CrossRefGoogle Scholar
  3. Ban, N., and J. Alder. 2008. How wild is the ocean? Assessing the intensity of anthropogenic marine activities in British Columbia, Canada. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 55–85.CrossRefGoogle Scholar
  4. BCStats. 2006. 2006 Census, Statistics Canada. In. Accessed Jan 2010.
  5. Berry, H.D., A.T. Sewell, S. Wyllie-Echeverria, et al. 2003. Puget sound submerged vegetation monitoring project: 2000–2002 monitoring report, 60. Olympia: Nearshore Habitat Program, Washington State Department of Natural Resources.Google Scholar
  6. Burnham, K.P., and D.R. Anderson. 2002. Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. New York: Springer.Google Scholar
  7. Canadian Food Inspection Agency. 2011. Aquatic animal imports. In. Accessed May 2012.
  8. Carlton, J.T. 1987. Patterns of transoceanic marine biological invasions in the Pacific Ocean. Bulletin of Marine Science 41: 452–465.Google Scholar
  9. Carlton, J.T. 2009. Chapter 2. Deep invasion ecology and the assembly of communities in historical time. In Biological invasions in marine ecosystems, eds. G. Rilov, and J.A. Crooks, 13–56. Berlin: Springer-Verlag.CrossRefGoogle Scholar
  10. Carlton, J.T., and G.M. Ruiz. 2005. Vector science and integrated vector management in bioinvasion ecology: conceptual frameworks. In Invasive alien speices: a new synthesis, eds. H.A. Mooney, R.N. Mack, J.A. Mc Neely, L.E. Neville, P.J. Schei, and J.K. Waage, 36–58. Covelo: Island Press.Google Scholar
  11. Carman, M.R., K.E. Hoagland, E. Green-Beach, et al. 2009. Tunicate faunas of two North Atlantic-New England islands: Martha’s vineyard, Massachusetts and Block Island, Rhode Island. Aquatic Invasions 4: 65–70.CrossRefGoogle Scholar
  12. Choi, F.M. 2011. Assessing intertidal marine non-indigenous species in Canadian ports. Earth and Ocean Sciences. University of British Columbia, Vancouver, Masters Thesis, pp. 118.Google Scholar
  13. Clark, G.F., and E.L. Johnston. 2005. Manipulating larval supply in the field: a controlled study of marine invasibility. Marine Ecology-Progress Series 298: 9–19.CrossRefGoogle Scholar
  14. Clarke Murray, C. 2012. The role of recreatinal boating in the introduction and spread of marine invasive species. Earth and Ocean Sciences. University of British Columbia, Vancouver, Ph.D. Thesis, pp. 191.Google Scholar
  15. Clarke Murray, C., E.A. Pakhomov, and T.W. Therriault. 2011. Recreational boating: a large unregulated vector transporting marine invasive species. Diversity and Distributions 17: 1161–1172.CrossRefGoogle Scholar
  16. Cohen, A.N., and J.T. Carlton. 1998. Accelerating invasion rate in a highly invaded estuary. Science 279: 555–558.CrossRefGoogle Scholar
  17. Cohen, A.N., and C.J. Zabin. 2009. Oyster shells as vectors for exotic organisms. Journal of Shellfish Research 28: 163–167.CrossRefGoogle Scholar
  18. Colautti, R.I., S.A. Bailey, C.D.A. van Overdijk, et al. 2006. Characterised and projected costs of nonindigenous species in Canada. Biological Invasions 8: 45–59.CrossRefGoogle Scholar
  19. Cordell, J.R., R. Draheim, and M. Sytsma. 2007. First record of the harpacticoid genus Harpacticella in the Pacific northwest, USA: another probable introduction. Aquatic Biology 1: 17–20.CrossRefGoogle Scholar
  20. Dafforn, K.A., T.M. Glasby, and E.L. Johnston. 2009. Links between estuarine condition and spatial distributions of marine invaders. Diversity and Distributions 15: 807–821.CrossRefGoogle Scholar
  21. Davidson, I.C., L.D. McCann, P.W. Fofonoff, et al. 2008. The potential for hull-mediated species transfers by obsolete ships on their final voyages. Diversity and Distributions 14: 518–529.CrossRefGoogle Scholar
  22. Davis, R.C., F.T. Short, and D.M. Burdick. 1998. Quantifying the effects of green crab damage to eelgrass transplants. Restoration Ecology 6: 297–302.CrossRefGoogle Scholar
  23. denHartog, C. 1997. Is Sargassum muticum a threat to eelgrass beds? Aquatic Botany 58: 37–41.CrossRefGoogle Scholar
  24. deRivera, C., Ruiz, G., Crooks, J., et al. 2005. Broad-scale nonindigenous species monitoring along the west coast in National Marine Sanctuaries and National Estuarine Research Reserves. Report to the National Fish and Wildlife Foundation, pp. 126.Google Scholar
  25. deRivera, C.E., B.P. Steves, P.W. Fofonoff, et al. 2011. Potential for high-latitude marine invasions along western North America. Diversity and Distributions 17: 1198–1209.CrossRefGoogle Scholar
  26. Dethier, M.N., and S.D. Hacker. 2005. Physical factors vs. biotic resistance in controlling the invasion of an estuarine marsh grass. Ecological Applications 15: 1273–1283.CrossRefGoogle Scholar
  27. DiBacco, C., D.B. Humphrey, L.E. Nasmith, et al. 2011. Ballast water transport of non-indigenous zooplankton to Canadian ports. ICES Journal of Marine Science. doi: 10.1093/icesjms/fsr133.Google Scholar
  28. Didham, R.K., J.M. Tylianakis, M.A. Hutchison, et al. 2005. Are invasive species the drivers of ecological change? Trends in Ecology & Evolution 20: 470–474.CrossRefGoogle Scholar
  29. Dudas, S.E., and J.F. Dower. 2006. Reproductive ecology and dispersal potential of the varnish clam Nuttallia obscurata, a recent invader in the Northeast Pacific. Marine Ecology-Progress Series 320: 195–205.CrossRefGoogle Scholar
  30. Elahi, R., and K. Sebens. 2012. Consumers mediate natural variation between prey richness and resource use in a benthic marine community. Marine Ecology-Progress Series 452: 131–143.CrossRefGoogle Scholar
  31. Environment Canada. 2011. Shellfish aquaculture statistics for British Columbia. In: Oceans and Marine Fisheries Branch, Ministry of the Environment Accessed March 2012.
  32. Foreman, M.G.G., W.R. Crawford, J.Y. Cherniawsky, et al. 2008. Dynamic Ocean topography for the Northeast Pacific and its continental margins. Geophysical Research Letters 35: 1–5.CrossRefGoogle Scholar
  33. Gillespie, G., Phillips, A., Paltzat, D., et al. 2007. Status of the European green crab, Carcinus maenas, in British Columbia - 2006. Department of Fisheries and Oceans, Canadian Technical Report of Fisheries and Aquatic Sciences, 2700, pp. 49.Google Scholar
  34. Gillespie, G.E. 2007. Distribution of non-indigenous intertidal species on the Pacific coast of Canada. Bulletin of the Japanese Society of Scientific Fisheries (Nippon Suisan Gakkaishi) 73: 1133–1137.CrossRefGoogle Scholar
  35. Glasby, T.M., S.D. Connell, M.G. Holloway, et al. 2007. Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions? Marine Biology 151: 887–895.CrossRefGoogle Scholar
  36. Gotelli, N.J., and R.K. Colwell. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4: 379–391.CrossRefGoogle Scholar
  37. Haupt, T.M., C.L. Griffiths, T.B. Robinson, et al. 2010. Oysters as vectors of marine aliens, with notes on four introduced species associated with oyster farming in South Africa. African Zoology 45: 52–62.CrossRefGoogle Scholar
  38. Hemminga, M.A., and C.M. Duarte. 2000. Seagrass ecology. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  39. Hewitt, C.L., and M.L. Campbell. 2010. Relative contribution of vectors to the introduction and translocation of marine invasive species. Canberra City: Australian Government Department of Agriculture, Fisheries and Forestry.Google Scholar
  40. Incera, M., C. Olbarria, J.S. Troncoso, et al. 2009. Response of the invader Sargassum muticum to variability in nutrients supply. Marine Ecology-Progress Series 377: 91–101.CrossRefGoogle Scholar
  41. International Council for the Exploration of the Sea (ICES). 2005. ICES code of practice on the introductions and transfers of marine organisms. Copenhagen: ICES.Google Scholar
  42. Kask, B.A., J.R. Sibert, and B. Windecker. 1982. A check list of marine and brackish water harpacticoid copepods from the Nanaimo estuary, southwestern British Columbia. Syesis 15: 25–38.Google Scholar
  43. Kruskal, J.B., and M. Wish. 1978. Multidimensional scaling. Beverly Hills: Sage Publications, Inc..CrossRefGoogle Scholar
  44. Legendre, P., and L. Legendre. 1998. Numerical ecology, 2nd edn. Amsterdam: Elsevier Science B.V.Google Scholar
  45. Levings, C.D., R.E. Foreman, and V.J. Tunnicliffe. 1983. A review of the benthos of the strait of Georgia and contiguous fjords. Canadian Journal of Fisheries and Aquatic Sciences 40: 1120–1141.CrossRefGoogle Scholar
  46. Levings, C.D., D. Kieser, G.S. Jamieson, et al. 2002. Marine and estuarine alien species in the strait of Georgia, British Columbia. In Alien invaders in Canada’s waters, wetlands, and forests, eds. R. Claudi, P. Nantel, and E. Muckle-Jeffs, 113–131. Canada: Canadian Forest Service, Natural Resoures.Google Scholar
  47. Lo, V.B., C.D. Levings, and K.M.A. Chan. 2012. Quantifying potential propagule pressure of aquatic invasive species from the commercial shipping industry in Canada. Marine Pollution Bulletin 64: 295–302.CrossRefGoogle Scholar
  48. Lockwood, J.L., P. Cassey, and T. Blackburn. 2005. The role of propagule pressure in explaining species invasions. Trends in Ecology & Evolution 20: 223–228.CrossRefGoogle Scholar
  49. Mach, M.E. 2012. Research on marine coastal impacts to promote ecosystem-based management: Nonnative species in northeast Pacific estuaries. Resource Management and Environmental Studies. University of British Columbia, Vancouver, Ph.D. Thesis, pp. 189.Google Scholar
  50. MacLeod, C.J., S.E. Newson, G. Blackwell, et al. 2009. Enhanced niche opportunities: can they explain the success of New Zealand’s introduced bird species? Diversity and Distributions 15: 41–49.CrossRefGoogle Scholar
  51. Mann, R., and J.M. Harding. 2003. Salinity tolerance of larval Rapana venosa: implications for dispersal and establishment of an invading predatory gastropod on the north American Atlantic coast. Biological Bulletin 204: 96–103.CrossRefGoogle Scholar
  52. Maron, J.L., and M. Marler. 2007. Native plant diversity resists invasion at both low and high resource levels. Ecology 88: 2651–2661.CrossRefGoogle Scholar
  53. Martone, R.G., and K. Wasson. 2008. Impacts and interactions of multiple human perturbations in a California salt marsh. Oecologia 158: 151–163.CrossRefGoogle Scholar
  54. Mazerolle, M.J. 2012. AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 1.24 Available at: Accessed Feb 2012.
  55. Miller, A.W., G.M. Ruiz, M.S. Minton, et al. 2007. Differentiating successful and failed mollusan invaders in estuarine ecosystems. Marine Ecology-Progress Series 332: 41–51.CrossRefGoogle Scholar
  56. Mineur, F., T. Belsher, M.P. Johnson, et al. 2007. Experimental assessment of oyster transfers as a vector for macroalgal introductions. Biological Conservation 137: 237–247.CrossRefGoogle Scholar
  57. Mineur, F., A.J. Davies, C.A. Maggs, et al. 2010. Fronts, jumps and secondary introducitons suggested as different invasion patterns in marine species, with an increase in spread rates over time. Proceedings of the Royal Society B 277: 2693–2701.CrossRefGoogle Scholar
  58. Morales, M. 2011. Sciplot: scientific graphing functions for factorial designs. R package version 1.0–9, Available at: Accessed Apr 2012.
  59. Moyle, P.B., and T. Light. 1996. Fish invasions in California: do abiotic factors determine success? Ecology 77: 1666–1670.CrossRefGoogle Scholar
  60. Oksanen, J., Blanchet, F.G., Kindt, R., et al. 2012. Vegan: community ecology package. R package version 2.0–3. Available at: Accessed Feb 2012.
  61. Orth, R.J., T.J.B. Carruthers, W.C. Dennison, et al. 2006. A global crisis for seagrass ecosystems. Bioscience 56: 987–996.CrossRefGoogle Scholar
  62. Piercey, G.E., C.D. Levings, M. Elfert, et al. 2000. Invertebrate fauna in ballast water collected in vessels arriving in British Columbia ports, especially those from the western North Pacific. Canadian Data Report of Fisheries and Aquatic Sciences 1060: 50.Google Scholar
  63. Piola, R.F., and E.L. Johnston. 2007. Pollution reduces native diversity and increases invader dominance in marine hard-substrate communities. Diversity and Distributions 14: 329–342.CrossRefGoogle Scholar
  64. Powers, S.P., M.A. Bishop, J.H. Grabowski, et al. 2006. Distribution of the invasive bivalve Mya arenaria L. On intertidal flats of southcentral Alaska. Journal of Sea Research 55: 207–216.CrossRefGoogle Scholar
  65. Quayle, D. 1964. Distribution of introduced marine mollusca in British Columbia waters. Journal of the Fisheries Research Board of Canada 21: 1155–1181.CrossRefGoogle Scholar
  66. R Development Core Team. 2012. A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing ISBN 3-900051-07-0, Scholar
  67. Ruiz, G.M., P.W. Fofonoff, J.T. Carlton, et al. 2000. Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annual Review of Ecology and Systematics 31: 481–531.CrossRefGoogle Scholar
  68. Ruiz, G.M., P.W. Fofonoff, B. Steves, et al. 2011. Marine invasion history and vector analysis of California: a hotspot for western North America. Diversity and Distributions 17: 362–373.CrossRefGoogle Scholar
  69. Shea, K., and P. Chesson. 2002. Community ecology theory as a framework for biological invasions. Trends in Ecology & Evolution 17: 170–176.CrossRefGoogle Scholar
  70. Short, F.T., and R.G. Coles. 2001. Global seagrass research methods. Amsterdam: Elsevier Science.Google Scholar
  71. Short, F.T., and S. Wyllie-Echeverria. 1996. Natural and human-induced disturbance of seagrasses. Environmental Conservation 23: 17–27.CrossRefGoogle Scholar
  72. Sloan, N.A., and P.M. Bartier. 2004. Introduced marine species in the Haida Gwaii (queen Charlotte Islands) region, British Columbia. Canadian Field-Naturalist 118: 77–84.Google Scholar
  73. Sokal, R.R., and F.J. Rohlf. 1995. Biometry: the principals and practice of statistics in biological research, 3rd edn. New York: W.H. Freeman and Company.Google Scholar
  74. Sortie, C.J.B., I. Ibanez, D.M. Blumenthal, et al. 2013. Poised to prosper? A cross-system pomparison of climate change effects on native and non-native species performance. Ecology Letters 16: 261–270.CrossRefGoogle Scholar
  75. Stachowicz, J., R. Whitlatch, and R. Osman. 1999. Species diversity and invasion resistance in a marine ecosystem. Science 286: 1577.CrossRefGoogle Scholar
  76. Stachowicz, J.J., J.R. Terwin, R.B. Whitlatch, et al. 2002. Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proceedings of the National Academy of Sciences of the United States of America 99: 15497–15500.CrossRefGoogle Scholar
  77. Sylvester, F., O. Kalaci, B. Leung, et al. 2011. Hull fouling as an invasion vector: can simple models explain a complex problem? Journal of Applied Ecology 48: 415–423.CrossRefGoogle Scholar
  78. Thompson, R.E. 1981. Oceanography of the British Columbia coast. Canadian Special Publication of Fisheries and Aquatic Sciences 56: 291.Google Scholar
  79. Tilman, D. 1997. Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78: 81–92.CrossRefGoogle Scholar
  80. Transport Canada. 2006. Ballast water control and management regulations. In. Accessed May 2012.
  81. Vermonden, K., R.S.E.W. Leuven, and G. van der Velde. 2010. Environmental factors determining invasibility of urban waters for exotic macroinvertebrates. Diversity and Distributions 16: 1009–1021.CrossRefGoogle Scholar
  82. Waycott, M., C.M. Duarte, T.J.B. Carruthers, et al. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences 106: 12377–12381.CrossRefGoogle Scholar
  83. Wilcove, D.S., D. Rothstein, J. Dubow, et al. 1998. Quantifying threats to imperiled species in the United States. Bioscience 48: 607–615.CrossRefGoogle Scholar
  84. Williams, S.L. 2007. Introduced species in seagrass ecosystems: status and concerns. Journal of Experimental Marine Biology and Ecology 350: 89–110.CrossRefGoogle Scholar
  85. Wonham, M.J., and E. Pachepsky. 2006. A null model of temporal trends in biological invasion records. Ecology Letters 9: 663–672.CrossRefGoogle Scholar
  86. Wyatt, A.S.J., C.L. Hewitt, D.I. Walker, et al. 2005. Marine introductions in the Shark Bay world heritage property, Western Australia: a preliminary assessment. Diversity and Distributions 11: 33–44.CrossRefGoogle Scholar
  87. Yamada, S.B., and G.E. Gillespie. 2008. Will the European green crab (Carcinus maenas) persist in the Pacific northwest? ICES Journal of Marine Science 65: 725–729.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2016

Authors and Affiliations

  • Megan E. Mach
    • 1
    • 2
    Email author
  • Colin D. Levings
    • 3
  • Kai M. A. Chan
    • 1
  1. 1.Institute for Resources, Environment and Sustainability, Resource Management and Environmental SustainabilityUniversity of British ColumbiaVancouverCanada
  2. 2.Center for Ocean SolutionsMontereyUSA
  3. 3.Department of Fisheries and Oceans CanadaCentre for Aquaculture and Environment ResearchWest VancouverCanada

Personalised recommendations