Abstract
The structuring and organizing effects of apex predators on ecosystems are becoming increasingly well documented. The enhancement of kelp forests via sea otter predation on herbivorous sea urchins is among the earliest and best known examples. This study provides evidence for direct and indirect trophic interactions among sea otters, predatory sea stars, and filter-feeding mussels (Mytilus trossulus) and barnacles (Semibalanus cariosis). In western Massacre Bay at Attu Island (173°E, 53°N), subtidal transects showed sea star body size and biomass density declined markedly between 1983 and 1994 as sea otters reinhabited this area. Mussels and barnacles translocated from the rocky intertidal zone to shallow subtidal habitats to assess loss rates from sea star predation showed lower mortality rates after the arrival of sea otters. Prey mortality rates in subtidal caged controls were consistently low and similar to those of intertidal controls in both years. These findings elucidate a trophic pathway by which sea otters can influence ecosystems separate from the well-known sea otter/sea urchin/macroalgae cascade.
Similar content being viewed by others
References
Anthony RG, Estes JA, Ricca MA, Miles AK, Forsman ED (2008) Bald eagles and sea otters in the Aleutian archipelago: indirect effects of trophic cascades. Ecology 89:2725–2735
Birkeland C, Lucas JS (1990) Acanthaster planci: major management problem of coral reefs. CRC Press, Boca Raton
Breen PA, Carson TA, Foster JB, Stewart EA (1982) Changes in subtidal community structure associated with British Columbia sea otter transplants. Mar Eco Prog Ser 7:13–20
Calkins DG (1978) Feeding behavior and major prey species of the sea otter, Enhydra lutris, in Montague Strait, Prince William Sound, Alaska. Fish Bull 76:125–131
Carlson HR, Pfister CA (1999) A seventeen-year study of the rose star Crossaster papposus in a coastal bay in southeast Alaska. Mar Biol 133:223–230
Clark RN, Jewett SC (2010) A new genus and 13 new species of sea stars (Asteroidea:Echinasteridae) from the Aleutian Archipelago. Zootaxa 2571:1–36
Doroff AM, Estes JA, Tinker MT, Burn DM, Evans TJ (2003) Sea otter population declines in the Aleutian archipelago. J Mammal 84:55–64
Duggins DO (1983) Starfish predation and the creation of mosaic patterns in a kelp-dominated community. Ecology 64:1610–1619
Duggins DO, Simenstad CA, Estes JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245:170–173
Estes JA (1990) Growth and equilibrium in sea otter populations. J Anim Ecol 59:385–400
Estes JA, Duggins DO (1995) Sea otters and kelp forests in Alaska: generality and variation in a community ecological paradigm. Ecol Monogr 65:75–100
Estes JA, Palmisano JF (1974) Sea otters: their role in structuring nearshore communities. Science 185:1058–1060
Estes JA, Steinberg PD (1988) Predation, herbivory and kelp evolution. Paleobiology 14:19–36
Estes JA, VanBlaricom GR (1985) Sea otters and shellfisheries. In: Beverton RH, Lavigne D, Beddington J (eds) Conflicts between marine mammals and fisheries. Allen and Unwin, London, pp 187–235
Estes JA, Jameson RJ, Johnson AM (1981) Food selection and some foraging tactics of sea otters. In: Chapman JA, Pursley D (eds) Worldwide furbearer conference proceedings. Worldwide Furbearer Conference, Inc. Frostburg, pp 606–642
Estes JA, Jameson RJ, Rhode EB (1982) Activity and prey selection in the sea otter: influence of population status on community structure. Am Nat 120:242–258
Estes JA, Tinker MT, Williams TM, Doak DF (1998) Killer whale predation on sea otters linking coastal with oceanic ecosystems. Science 282:473–476
Estes JA, Lindberg DR, Wray C (2005) Evolution of large body size in abalones (Haliotis): patterns and implications. Paleobiology 31:591–606
Estes JA, Peterson CH, Steneck R (2010a) Some effects of apex predators in higher-latitude coastal oceans. In: Terborgh J, Estes JA (eds) Trophic cascades: predators, prey, and the changing dynamics of nature. Island Press, Washington, DC, pp 37–53
Estes JA, Tinker MT, Bodkin JL (2010b) Using ecological function to develop recovery criteria for depleted species: sea otters and kelp forests in the Aleutian archipelago. Conserv Biol 24:852–860
Feder H, Christensen AM (1966) Aspects of Asteroid Biology. In: Boolotian RA (ed) Physiology of echinodermata. Interscience Publishers (division of Wiley), New York, pp 87–127
Garshelis DL, Garshelis JA, Kimker AT (1986) Sea otter time budgets and prey relationships. J Wild Man 50:637–647
Gaymer CF, Himmelman JH (2002) Mussel beds in deeper water provide and unusual situation for competitive interactions between the sea stars Leptasterias polaris and Asterias vulgaris. J Exp Mar Biol Ecol 277:13–24
Gaymer CF, Himmelman JH, Johnson LE (2001) Distribution and feeding ecology of the seastars Leptasterias polaris and Asterias vulgaris in the Northern Gulf of St. Lawrence, Canada. J Mar Biol Assoc UK 81:827–843
Himmelman JH, Dutil C (1991) Distribution, population structure and feeding of subtidal seastars in the northern Gulf of St. Lawrence. Mar Ecol Prog Ser 76:61–72
Irons DB, Anthony RG, Estes JA (1986) Foraging strategies of Glaucous-winged Gulls in rocky intertidal communities. Ecology 67:1460–1474
Jones RD (1965) Sea otters in the Near Islands, Alaska. J Mammal 46:702
Kenyon KW (1969) The sea otter in the eastern Pacific Ocean. North Am Fauna 68:1–352
Kvitek RG, Oliver JS (1992) Influence of sea otters on soft-bottom prey communities in southeast Alaska. Mar Ecol Prog Ser 82:103–113
Kvitek RG, Oliver JS, DeGange AR, Anderson BS (1992) Changes in Alaskan soft-bottom prey communities along a gradient in sea otter predation. Ecology 73:413–428
Lensink CJ (1962) The history and status of sea otters in Alaska. Dissertation, Purdue University
MacGinitie GE, MacGinitie N (1949) Natural history of marine animals. McGraw Hill, New York
Mauzey KP, Birkeland C, Dayton PK (1968) Feeding behavior of asteroids and escape responses of their prey in the Puget Sound region. Ecology 49:603–619
Oftedal OT, Ralls K, Tinker MT, Green A (2007) Nutritional constraints on the southern sea otter. Fin Rep Mont Bay Mar Sanc & Mar Mam Com. ftp://brd1.ucsc.edu/Otter/Nutrition/Otter%20Nutrition%20Final%20Report.pdf
Ostfeld RS (1982) Foraging strategies and prey switching in the California sea otter. Oecologia 53:170–178
Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75
Paine RT (1974) Intertidal community structure. Oecologia 15:93–120
Paine RT (1980) Food webs: linkage, interaction strength, and community infrastructure. J Anim Ecol 49:667–685
Paine RT (2010) Food chain dynamics and trophic cascades in intertidal habitats. In: Terborgh T, Estes JA (eds) Trophic cascades: predators, prey, and the changing dynamics of nature. Island Press, Washington, DC, pp 21–35
Reidman ML, Estes JA (1990) The sea otter (Enhydra lutris): behavior, ecology, and natural history. Biol Rep 90(14):1–126 (US Fish and Wildlife Service)
Reisewitz SE, Estes JA, Simenstad SA (2006) Indirect food web interactions: sea otters and kelp forest fishes in the Aleutian archipelago. Oecologia 146:623–631
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Steinberg PD, Estes JA, Winter FC (1995) Evolutionary consequences of food chain length in kelp forest communities. Proc Natl Acad Sci 92:8145–8148
Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2003) Kelp forest ecosystem: biodiversity, stability, resilience and future. Environ Conserv 29:436–459
Terborgh J, Estes JA (eds) (2010) Trophic cascades: predators, prey, and the changing dynamics of nature. Island Press, Washington, DC
VanBlaricom GR (1988) Effects of foraging sea otters on mussel-dominated intertidal communities. In: VanBlaricom GR, Estes JA (eds) The community ecology of sea otters. Springer, Berlin, pp 44–88
Watson J, Estes JA (2011) Stability, resilience, and phase shifts in kelp forest communities along the west coast of Vancouver Island, Canada. Ecol Monogr 81:215–239
Williams TM, Estes JA, Doak DF, Springer AM (2004) Killer appetites: assessing the role of predators in ecological communities. Ecology 85:3373–3384
Acknowledgments
Funding for this project was provided by the US Geological Survey and grant NSF/DPP-9101134-02 from the United States National Science Foundation. We thank Lynda Browne, David Irons, C. Melissa Minor, Dan Reed, and Glenn VanBlaricom for field assistance and Christopher Harley, John Pearse, Gerald Singh, and three anonymous referees for comments on earlier drafts of the manuscript. The Alaska Maritime National Wildlife Refuge provided field logistical support and the US Coast Guard transported personnel and equipment to and from Attu Island.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Connell.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Vicknair, K., Estes, J.A. Interactions among sea otters, sea stars, and suspension-feeding invertebrates in the western Aleutian archipelago. Mar Biol 159, 2641–2649 (2012). https://doi.org/10.1007/s00227-012-2021-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-012-2021-7