Skip to main content

Advertisement

SpringerLink
Log in

Testing the generality of the trophic cascade paradigm for sea otters: a case study with kelp forests in northern Washington, USA

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Trophic cascade hypotheses for biological communities, linking predation by upper trophic levels to major features of ecological structure and dynamics at lower trophic levels, are widely subscribed and may influence conservation policy. Few such hypotheses have been evaluated for temporal or spatial generality. Previous studies of sea otter (Enhydra lutris) predation along the outer coast of North America suggest a pattern, often elevated to the status of paradigm, in which sea otter presence leads to reduced sea urchin (Strongylocentrotus spp.) biomass and rapid increases in abundance and diversity of annual algal species, followed by a decline in diversity as one or a few perennial algal species become dominant. Both sea otter predation and commercial sea urchin harvest are ecologically and economically important sources of urchin mortality in nearshore benthic systems in northern Washington marine waters. We recorded changes in density of macroalgae in San Juan Channel, a marine reserve in the physically protected inland waters of northern Washington, resulting from three levels of experimental urchin harvest: (1) simulated sea otter predation (monthly complete harvest of sea urchins), (2) simulated commercial urchin harvest (annual size-selective harvest of sea urchins), and (3) no harvest (control). The two experimental urchin removal treatments did not significantly increase the density of perennial (Agarum and Laminaria) or annual (Desmarestia, Costaria, Alaria and Nereocystis) species of macroalgae after 2 years, despite significant and persistent decreases in urchin densities. Our results suggest that other factors such as grazing by other invertebrates, the presence of dense Agarum stands, and recruitment frequency of macroalgae and macroinvertebrates may play a large role in influencing community structure in San Juan Channel and other physically protected marine waters within the range of sea otters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Breen, P. A. & K. H. Mann, 1976. Destructive grazing of kelp by sea urchins in eastern Canada. Journal of the Fisheries Research Board of Canada 33: 1278–1283.

    Google Scholar 

  • Breen, P. A., B. E. Adkins & D. C. Miller, 1978. Recovery rate in three exploited sea urchin populations from 1972 to 1977. Fisheries and Marine Services Manuscript Report 1446: 1–27.

    Google Scholar 

  • Breen, P. A., D. C. Miller & B. E. Adkins, 1976. An examination of harvested sea urchin populations in the Tofino area. Fisheries Research Board of Canada Manuscript Report Series 1401: 1–23.

    Google Scholar 

  • Carter, S. K., 1999. Ecosystem effects of simulated sea otter predation and commercial sea urchin harvest on nearshore benthic communities in northern Washington. M. S. Thesis. University of Washington, Seattle.

  • Carter, S. K. & G. R. VanBlaricom, 2002. Effects of experimental harvest on red sea urchins, Strongylocentrotus franciscanus, in northern Washington. Fisheries Bulletin 100: 662–673.

    Google Scholar 

  • Chapman, A. R. O., 1981. Stability of sea urchin dominated barren grounds following destructive grazing of kelp in St Margaret’s Bay, eastern Canada. Marine Biology 62: 307–311.

    Article  Google Scholar 

  • Cowen, R. K., C. R. Agegian & M. S. Foster, 1982. The maintenance of community structure in a central California giant kelp forest. Journal of Experimental Marine Biology and Ecology 64: 189–201.

    Article  Google Scholar 

  • Dayton, P. K., 1975. Experimental studies of algal canopy interactions in a sea otter-dominated kelp community at Amchitka Island, Alaska. Fishery Bulletin 73: 230–238.

    Google Scholar 

  • Dayton, P. K., 1985a. Ecology of kelp communities. Annual Review of Ecology and Systematics 16: 215–245.

    Article  Google Scholar 

  • Dayton, P. K., 1985b. The structure and regulation of some South American kelp communities. Ecological Monographs 55: 447–468.

    Article  Google Scholar 

  • Dayton, P. K., V. Currie, T. Gerrodette, B. D. Keller, R. Rosenthal & D. Ven Tresca, 1984. Patch dynamics and stability of some California kelp communities. Ecological Monographs 54: 253–289.

    Article  Google Scholar 

  • Dean, T. A., S. C. Schroeter & J. D. Dixon, 1984. Effects of grazing by two species of sea urchins (Strongylocentrotus franciscanus and Lytechinus anamesus) on recruitment and survival of two species of kelp (Macrocystis pyrifera and Pterygophora californica). Marine Biology 78: 301–313.

    Article  Google Scholar 

  • Dean, T. A., J. L. Bodkin, S. C. Jewett, D. H. Monson & D. Jung, 2000. Changes in sea urchins and kelp following a reduction in sea otter density as a result of the Exxon Valdez oil spill. Marine Ecology Progress Series 199: 281–291.

    Google Scholar 

  • Duggins, D. O., 1980. Kelp beds and sea otters: an experimental approach. Ecology 61: 447–453.

    Article  Google Scholar 

  • Estes, J. A. & D. O. Duggins, 1995. Sea otters and kelp forests in Alaska: generality and variation in a community ecological paradigm. Ecological Monographs 65: 75–100.

    Article  Google Scholar 

  • Estes, J. A. & C. Harrold, 1988. Sea otters, sea urchins, and kelp beds: some questions of scale. In VanBlaricom, G. R. & J. A. Estes (eds), The Community Ecology of Sea Otters. Springer-Verlag, Berlin, 116–150.

    Google Scholar 

  • Estes, J. A. & J. F. Palmisano, 1974. Sea otters: their role in structuring nearshore communities. Science 185: 1058–1060.

    Article  PubMed  Google Scholar 

  • Estes, J. A. & G. R. VanBlaricom, 1985. Sea-otters and shellfisheries. In Beddington, J. R., R. J. H. Beverton & D. M. Lavigne (eds), Marine Mammals and Fisheries. George Allen and Unwin, London, UK, 187–235.

    Google Scholar 

  • Estes, J. A., R. J. Jameson & E. B. Rhode, 1982. Activity and prey election in the sea otter: influence of population status on community structure. American Naturalist 120: 242–258.

    Article  Google Scholar 

  • Estes, J. A., N. S. Smith & J. F. Palmisano, 1978. Sea otter predation and community organization in the western Aleutian Islands, Alaska. Ecology 59: 822–833.

    Article  Google Scholar 

  • Estes, J. A., M. T. Tinker, T. M. Williams & D. F. Doak, 1998. Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282: 473–476.

    Article  PubMed  CAS  Google Scholar 

  • Fanshawe, S., G. R. VanBlaricom & A. A. Shelly, 2003. Restored top carnivores as detriments to the performance of marine protected areas intended for fishery sustainability: a case study with red abalones and sea otters. Conservation Biology 17: 273–283.

    Article  Google Scholar 

  • Foster, M. S., 1990. Organization of macroalgal assemblages in the Northeast Pacific: the assumption of homogeneity and the illusion of generality. Hydrobiologia 192: 21–33.

    Article  Google Scholar 

  • Foster, M. S. & D. R. Schiel, 1988. Kelp communities and sea otters: keystone species or just another brick in the wall? In VanBlaricom, G. R. & J. A. Estes (eds), The Community Ecology of Sea Otters. Springer-Verlag, Berlin, 92–115.

    Google Scholar 

  • Foster, M. S. & G. R. VanBlaricom, 2001. Spatial variation in kelp forest communities along the Big Sur coast of central California, USA. Cryptogamie et Algologie 22: 173–186.

    Article  Google Scholar 

  • Gerber, L. R. & G. R. VanBlaricom, 1999. Potential fishery conflicts involving sea otters (Enhydra lutris [L]) in Washington state waters. Final report, contract T30917202. Marine Mammal Commission, Washington, DC.

  • Gerber, L. R., K. E. Buenau & G. R. VanBlaricom, 2004. Density dependence and risk of extinction in a small population of sea otters. Biodiversity and Conservation 13: 2741–2757.

    Article  Google Scholar 

  • Harrold, C. & D. C. Reed, 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66: 1160–1169.

    Article  Google Scholar 

  • Himmelman, J. H., A. Cardinal & E. Bourget, 1983. Community development following removal of urchins, Strongylocentrotus droebachiensis, from the rocky subtidal zone of the St Lawrence Estuary, eastern Canada. Oecologia 59: 27–39.

    Article  Google Scholar 

  • Himmelman, J. H. & H. Nédélec, 1990. Urchin foraging and algal survival strategies in intensely grazed communities in eastern Canada. Canadian Journal of Fisheries and Aquatic Sciences 47: 1011–1026.

    Article  Google Scholar 

  • Hoines, L., 1998. 1995 Fisheries statistical report. Washington State Department of Fish and Wildlife, Olympia.

  • Jameson, R. J., 1998. Translocated sea otter populations off the Oregon and Washington coasts. In Mac, M. J., P. A. Opler, C. E. Puckett-Haecker & P. D. Doran (eds), Status and Trends of the Nation’s Biological Resources, Vol. 2. U.S. Geological Survey, Washington, DC, 684–686.

    Google Scholar 

  • Jameson, R. J., S. Jeffries & K. W. Kenyon, 1997. Status and trends of the Washington translocated sea otter population. Presentation at the Sixth Joint US-Russia Sea Otter Workshop, November 9–15, 1997, Forks, Washington.

  • Jameson, R. J., K. W. Kenyon, A. M. Johnson & H. N. Wight, 1982. History and status of translocated sea otter populations in North America. Wildlife Society Bulletin 10: 100–107.

    Google Scholar 

  • Johnson, C. R. & K. H. Mann, 1988. Diversity, patterns of adaptation, and stability of Nova Scotian kelp beds. Ecological Monographs 58: 129–154.

    Article  Google Scholar 

  • Kalvass, P. E. & J. M. Hendrix, 1997. The California red sea urchin, Strongylocentrotus franciscanus, fishery: catch, effort, and management trends. Marine Fisheries Review 59(2): 1–17.

    Google Scholar 

  • Keats, D. W., G. R. South & D. H. Steele, 1990. Effects of an experimental reduction in grazing by green sea urchins on a benthic macroalgal community in eastern Newfoundland. Marine Ecology Progress Series 68: 181–193.

    Google Scholar 

  • Kvitek, R. G., P. J. Iampietro & C. E. Bowlby, 1998. Sea otters and benthic prey communities: a direct test of the sea otter as keystone predator in Washington state. Marine Mammal Science 14: 895–902.

    Article  Google Scholar 

  • Lai, H. L. & A. Bradbury, 1998. A modified catch-at-size analysis model for a red sea urchin (Strongylocentrotus franciscanus) population. In Jamieson, G. S. & A. Campbell (eds), Proceedings of the North Pacific Symposium on Invertebrate Stock Assessment and Management. Canadian Special Publications in Fisheries and Aquatic Sciences 125: 85–96.

  • Laidre, K. L., R. J. Jameson, S. J. Jeffries, R. C. Hobbs, C. E. Bowlby & G. R. VanBlaricom, 2002. Estimates of carrying capacity for sea otters in Washington State. Wildlife Society Bulletin 30: 1172–1181.

    Google Scholar 

  • Laur, D. R., A. W. Ebeling & D. A. Coon, 1988. Effects of sea otter foraging on subtidal reef communities off central California. In VanBlaricom, G. R. & J. A. Estes (eds), The Community Ecology of Sea Otters. Springer-Verlag, Berlin, 151–168.

    Google Scholar 

  • Lawrence, J. M., 1975. On the relationships between marine plants and sea urchins. Oceanogr Marine Biology Annual Review 13: 213–286.

    Google Scholar 

  • Lebednik, P. A., F. C. Weinmann & R. E. Norris, 1971. Spatial and seasonal distributions of marine algal communities at Amchitka Island, Alaska. Bioscience 21: 656–660.

    Article  Google Scholar 

  • Mattison, J. E., J. D. Trent, A. L. Shanks, T. B. Akin & J. S. Pearse, 1977. Movement and feeding activity of red sea urchins (Strongylocentrotus franciscanus) adjacent to a kelp forest. Marine Biology 39: 25–30.

    Article  Google Scholar 

  • Neushul, M., 1967. Studies of subtidal marine vegetation in western Washington. Ecology 48: 83–94.

    Article  Google Scholar 

  • Ostfeld, R. S., 1982. Foraging strategies and prey switching in the California sea otter. Oecologia 53: 170–178.

    Article  Google Scholar 

  • Pace, D., 1981. Kelp community development in Barkley Sound, British Columbia following sea urchin removal. In Fogg, G. E. & W. E. Jones (eds), Proceedings of the Eighth International Seaweed Symposium, 18–23 August, 1974. Bangor, North Wales, The Marine Science Laboratories, Menai Bridge, United Kingdom, 457–463.

  • Paine, R. T., 1966. Food web complexity and species diversity. American Naturalist 100: 65–75.

    Article  Google Scholar 

  • Paine, R. T., 1974. Intertidal community structure: experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia 15: 93–120.

    Article  Google Scholar 

  • Paine, R. T., 1969. A note on trophic complexity and community stability. American Naturalist 103: 91–93.

    Article  Google Scholar 

  • Paine, R. T. & R. L. Vadas, 1969. The effects of grazing by sea urchins, Strongylocentrotus spp., on benthic algal populations. Limnology and Oceanography 14: 710–719.

    Article  Google Scholar 

  • Pearse, J. S. & A. H. Hines, 1979. Expansion of a central California kelp forest following the mass mortality of sea urchins. Marine Biology 51: 83–91.

    Article  Google Scholar 

  • Pearse, J. S. & A. H. Hines, 1987. Long-term population dynamics of sea urchins in a central California kelp forest: rare recruitment and rapid decline. Marine Ecology Progress Series 39: 275–283.

    Google Scholar 

  • Pfister, C. A. & A. Bradbury, 1996. Harvesting red sea urchins: recent effects and future predictions. Ecological Applications 6: 298–310.

    Article  Google Scholar 

  • Quinn, G. P. & M. J. Keough, 2002. Experimental Design and Data Analysis for Biologists. University Press Cambridge, United Kingdom.

    Google Scholar 

  • Reed, D. C., 1990. The effects of variable settlement and early competition on patterns of kelp recruitment. Ecology 71: 776–787.

    Article  Google Scholar 

  • Reed, D. C., D. R. Laur & A. W. Ebeling, 1988. Variation in algal dispersal and recruitment: the importance of episodic events. Ecological Monographs 58: 321–335.

    Article  Google Scholar 

  • Riedman, M. L. & J. A. Estes, 1988. A review of the history, distribution and foraging ecology of sea otters. In VanBlaricom, G. R. & J. A. Estes (eds), The Community Ecology of Sea Otters. Springer-Verlag, Berlin, 4–21.

    Google Scholar 

  • Riedman, M. L. & J. A. Estes, 1990. The sea otter (Enhydra lutris): behavior, ecology, and natural history US Fish and Wildlife Service. Biological Report 90(14): 1–126.

    Google Scholar 

  • Rogers-Bennett, L., H. C. Fastenau & C. M. Dewees, 1998. Recovery of red sea urchin beds following experimental harvest. In Mooi, R. & M. Telford (eds), Echinoderms: San Francisco, Proceedings of the Ninth International Echinoderm Conference, August 5–9, 1996. San Francisco, California, 805–809.

  • Schroeter, S. C., J. D. Dixon, J. Kastendiek, R. O. Smith & J. R. Bence, 1993. Detecting the ecological effects of environmental impacts: a case study of kelp forest invertebrates. Ecological Applications 3: 331–350.

    Article  Google Scholar 

  • Schiel, D. R. & M. S. Foster, 1986. The structure of subtidal algal stands in temperate waters. Oceanography and Marine Biology Annual Reviews 24: 265–307.

    Google Scholar 

  • SPSS, 1996. SPSS® Base 7.5 for Windows™. User’s guide. Prentice-Hall, Paramus.

  • Tegner, M. J., 1980. Multispecies consideration of resource management in southern California kelp beds. In Pringle, J. D., G. J. Sharp & J. F. Caddy (eds), Proceedings of the Workshop on the Relationship between Sea Urchin Grazing and Commercial Plant/animal Harvesting. Canadian Technical Reports of Fisheries and Aquatic Sciences 954: 125–143.

  • Vadas, R. L., 1968. The Ecology of Agarum and the Kelp Bed Community. PhD dissertation, University of Washington, Seattle.

  • Vadas R. L., 1972. Ecological implications of culture studies on Nereocystis luetkeana. Journal of Phycology 8: 196–203.

    Google Scholar 

  • Vadas, R. L., 1977. Preferential feeding: an optimization strategy in sea urchins Ecological Monographs 47: 337–371.

    Article  Google Scholar 

  • Van Alstyne, K. L., J. J. McCarthy, C. L. Hustead & D. O. Duggins, 1999. Geographic variation in polyphenolic levels of Northeastern Pacific kelps and rockweeds. Marine Biology 133: 371–379.

    Article  Google Scholar 

  • VanBlaricom, G. R., 1996. Saving the sea otter population in California: contemporary problems and future pitfalls. Endangered Species UPDATE 13(12): 85–91.

    Google Scholar 

  • VanBlaricom, G. R. & J. A. Estes (eds), 1988. The Community Ecology of Sea Otters. Ecological Studies. Springer-Verlag, Heidelberg, Germany.

    Google Scholar 

  • Watanabe, J. M. & C. Harrold, 1991. Destructive grazing by sea urchins Strongylocentrotis spp in a central California kelp forest: potential roles of depth, recruitment, and predation. Marine Ecology Progress Series 71: 125–141.

    Google Scholar 

  • Watson, J. C., 1993. The effects of sea otter (Enhydra lutris) foraging on shallow rocky communities off northwestern Vancouver Island, British Columbia. PhD Dissertation, University of California, Santa Cruz.

  • Wendell, F. E., 1994. Relationship between sea otter range expansion and red abalone abundance and size distribution in central California. California Fish and Game 80: 45–56.

    Google Scholar 

  • Wendell, F. E., 1996. The State of California’s role in the conservation of sea otters and other aquatic resources. Endangered Species UPDATE 13(12): 82–84.

    Google Scholar 

  • Wendell, F. E., R. Hardy, J. Ames & R. Burge, 1986. Temporal and spatial patterns in sea otter, Enhydra lutris, range expansion and in the loss of Pismo clam fisheries. California Fish and Game 72: 197–212.

    Google Scholar 

  • Witman, J. D., 1987. Subtidal coexistence: storms, grazing, mutualism, and the zonation of kelps and mussels. Ecological Monographs 57: 167–187.

    Article  Google Scholar 

  • Zar, J. H., 1984. Biostatistical Analysis, 2nd edn. Prentice Hall, Englewood Cliffs, New Jersey.

    Google Scholar 

Download references

Acknowledgements

This work was conducted as part of the requirements for a Master of Science degree for S.K. Carter in the School of Aquatic and Fishery Sciences at the University of Washington. Drs. D.O. Duggins, T. Klinger, C.J. Foote, and K.K. Chew provided helpful suggestions and guidance on many aspects of the project. S. Sublett, J.M. Grassley, and many others assisted with data collection. Dr. A.O.D. Willows and the staff and faculty at Friday Harbor Laboratories provided logistical support and use of the facilities and equipment. A.H. Fayram facilitated completion of the project and final manuscript, and P. Rasmussen assisted with statistical analysis and interpretation. Funding for the project was provided by the U.S. Geological Survey-Biological Resources Division, the Washington Department of Fish and Wildlife, the North Pacific Universities Marine Mammal Research Consortium, the Washington Cooperative Fish and Wildlife Research Unit, the H. Mason Keeler Endowment for Excellence, the Egtvedt Endowment Scholarship, the John N. Cobb Scholarship and the School of Aquatic and Fishery Sciences, University of Washington. We offer sincere thanks to all.

Author information

Author notes

  1. Sarah K. Carter

    Present address: Wisconsin Department of Natural Resources, Bureau of Endangered Resources, 3911 Fish Hatchery Road, Fitchburg, WI, 53711, USA

  2. Brian L. Allen

    Present address: Puget Sound Restoration Fund, 590 Madison Avenue South, Bainbridge Island, WA, 98110, USA

Authors and Affiliations

  1. Washington Cooperative Fish and Wildlife Research Unit, School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, WA, 98195-5020, USA

    Sarah K. Carter, Glenn R. VanBlaricom & Brian L. Allen

Authors
  1. Sarah K. Carter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Glenn R. VanBlaricom
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brian L. Allen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Glenn R. VanBlaricom.

Additional information

Handling editor: J. Trexler

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carter, S.K., VanBlaricom, G.R. & Allen, B.L. Testing the generality of the trophic cascade paradigm for sea otters: a case study with kelp forests in northern Washington, USA. Hydrobiologia 579, 233–249 (2007). https://doi.org/10.1007/s10750-006-0403-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-006-0403-x

Keywords

Search

Navigation