Hydrobiologia

, Volume 579, Issue 1, pp 233–249 | Cite as

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

  • Sarah K. Carter
  • Glenn R. VanBlaricom
  • Brian L. Allen
Primary Research Paper

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.

Keywords

Apex predator Sea otter Sea urchin fishery Community structure Benthic ecosystem Herbivory 

References

  1. 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
  2. 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
  3. 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
  4. 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.Google Scholar
  5. 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
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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
  9. Dayton, P. K., 1985a. Ecology of kelp communities. Annual Review of Ecology and Systematics 16: 215–245.CrossRefGoogle Scholar
  10. Dayton, P. K., 1985b. The structure and regulation of some South American kelp communities. Ecological Monographs 55: 447–468.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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
  14. Duggins, D. O., 1980. Kelp beds and sea otters: an experimental approach. Ecology 61: 447–453.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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
  17. Estes, J. A. & J. F. Palmisano, 1974. Sea otters: their role in structuring nearshore communities. Science 185: 1058–1060.CrossRefPubMedGoogle Scholar
  18. 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
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.PubMedCrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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
  25. 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.CrossRefGoogle Scholar
  26. 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.Google Scholar
  27. 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.CrossRefGoogle Scholar
  28. Harrold, C. & D. C. Reed, 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66: 1160–1169.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. Hoines, L., 1998. 1995 Fisheries statistical report. Washington State Department of Fish and Wildlife, Olympia.Google Scholar
  32. 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
  33. 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.Google Scholar
  34. 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
  35. Johnson, C. R. & K. H. Mann, 1988. Diversity, patterns of adaptation, and stability of Nova Scotian kelp beds. Ecological Monographs 58: 129–154.CrossRefGoogle Scholar
  36. 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
  37. 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
  38. 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.CrossRefGoogle Scholar
  39. 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.Google Scholar
  40. 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
  41. 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
  42. Lawrence, J. M., 1975. On the relationships between marine plants and sea urchins. Oceanogr Marine Biology Annual Review 13: 213–286.Google Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. Neushul, M., 1967. Studies of subtidal marine vegetation in western Washington. Ecology 48: 83–94.CrossRefGoogle Scholar
  46. Ostfeld, R. S., 1982. Foraging strategies and prey switching in the California sea otter. Oecologia 53: 170–178.CrossRefGoogle Scholar
  47. 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.Google Scholar
  48. Paine, R. T., 1966. Food web complexity and species diversity. American Naturalist 100: 65–75.CrossRefGoogle Scholar
  49. Paine, R. T., 1974. Intertidal community structure: experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia 15: 93–120.CrossRefGoogle Scholar
  50. Paine, R. T., 1969. A note on trophic complexity and community stability. American Naturalist 103: 91–93.CrossRefGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. 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
  54. Pfister, C. A. & A. Bradbury, 1996. Harvesting red sea urchins: recent effects and future predictions. Ecological Applications 6: 298–310.CrossRefGoogle Scholar
  55. Quinn, G. P. & M. J. Keough, 2002. Experimental Design and Data Analysis for Biologists. University Press Cambridge, United Kingdom.Google Scholar
  56. Reed, D. C., 1990. The effects of variable settlement and early competition on patterns of kelp recruitment. Ecology 71: 776–787.CrossRefGoogle Scholar
  57. 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.CrossRefGoogle Scholar
  58. 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
  59. 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
  60. 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.Google Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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
  63. SPSS, 1996. SPSS® Base 7.5 for Windows™. User’s guide. Prentice-Hall, Paramus.Google Scholar
  64. 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.Google Scholar
  65. Vadas, R. L., 1968. The Ecology of Agarum and the Kelp Bed Community. PhD dissertation, University of Washington, Seattle.Google Scholar
  66. Vadas R. L., 1972. Ecological implications of culture studies on Nereocystis luetkeana. Journal of Phycology 8: 196–203.Google Scholar
  67. Vadas, R. L., 1977. Preferential feeding: an optimization strategy in sea urchins Ecological Monographs 47: 337–371.CrossRefGoogle Scholar
  68. 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.CrossRefGoogle Scholar
  69. 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
  70. VanBlaricom, G. R. & J. A. Estes (eds), 1988. The Community Ecology of Sea Otters. Ecological Studies. Springer-Verlag, Heidelberg, Germany.Google Scholar
  71. 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
  72. 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.Google Scholar
  73. 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
  74. 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
  75. 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
  76. Witman, J. D., 1987. Subtidal coexistence: storms, grazing, mutualism, and the zonation of kelps and mussels. Ecological Monographs 57: 167–187.CrossRefGoogle Scholar
  77. Zar, J. H., 1984. Biostatistical Analysis, 2nd edn. Prentice Hall, Englewood Cliffs, New Jersey.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Sarah K. Carter
    • 1
    • 2
  • Glenn R. VanBlaricom
    • 1
  • Brian L. Allen
    • 1
    • 3
  1. 1.Washington Cooperative Fish and Wildlife Research Unit, School of Aquatic and Fishery SciencesUniversity of WashingtonSeattleUSA
  2. 2.Wisconsin Department of Natural ResourcesBureau of Endangered ResourcesFitchburgUSA
  3. 3.Puget Sound Restoration FundBainbridge IslandUSA

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