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Testing the Generality of the Trophic Cascade Paradigm for Sea Otters: a Case Study with Kelp Forests in Northern Washington, USA

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Testing the Generality of the Trophic Cascade Paradigm for Sea Otters: a Case Study with Kelp Forests in Northern Washington, USA Hydrobiologia (2007) 579:233–249 DOI 10.1007/s10750-006-0403-x PRIMARY RESEARCH PAPER Testing the generality of the trophic cascade paradigm for sea otters: a case study with kelp forests in northern Washington, USA Sarah K. Carter Æ Glenn R. VanBlaricom Æ Brian L. Allen Received: 6 April 2006 / Revised: 24 August 2006 / Accepted: 15 September 2006 / Published online: 31 January 2007 Ó Springer Science+Business Media B.V. 2007 Abstract Trophic cascade hypotheses for biolog- followed by a decline in diversity as one or a few ical communities, linking predation by upper tro- perennial algal species become dominant. Both sea phic levels to major features of ecological structure otter predation and commercial sea urchin harvest and dynamics at lower trophic levels, are widely are ecologically and economically important subscribed and may influence conservation policy. sources of urchin mortality in nearshore benthic Few such hypotheses have been evaluated for systems in northern Washington marine waters. We temporal or spatial generality. Previous studies of recorded changes in density of macroalgae in San sea otter (Enhydra lutris) predation along the outer Juan Channel, a marine reserve in the physically coast of North America suggest a pattern, often protected inland waters of northern Washington, elevated to the status of paradigm, in which sea otter resulting from three levels of experimental urchin presence leads to reduced sea urchin (Strongylo- harvest: (1) simulated sea otter predation (monthly centrotus spp.) biomass and rapid increases in complete harvest of sea urchins), (2) simulated abundance and diversity of annual algal species, commercial urchin harvest (annual size-selective harvest of sea urchins), and (3) no harvest (control). The two experimental urchin removal treatments Handling editor: J. Trexler did not significantly increase the density of perennial (Agarum and Laminaria) or annual S. K. Carter Á G. R. VanBlaricom (&) Á B. L. Allen (Desmarestia, Costaria, Alaria and Nereocystis) Washington Cooperative Fish and Wildlife Research species of macroalgae after 2 years, despite Unit, School of Aquatic and Fishery Sciences, significant and persistent decreases in urchin den- University of Washington, Box 355020, Seattle, WA sities. Our results suggest that other factors such as 98195-5020, USA e-mail: [email protected] grazing by other invertebrates, the presence of dense Agarum stands, and recruitment frequency Present Address: of macroalgae and macroinvertebrates may play a S. K. Carter large role in influencing community structure in Wisconsin Department of Natural Resources, Bureau of Endangered Resources, 3911 Fish Hatchery Road, San Juan Channel and other physically protected Fitchburg, WI 53711, USA marine waters within the range of sea otters. Present Address: Keywords Apex predator Á Sea otter Á Sea B. L. Allen Puget Sound Restoration Fund, 590 Madison Avenue urchin fishery Á Community structure Á Benthic South, Bainbridge Island, WA 98110, USA ecosystem Á Herbivory 123 234 Hydrobiologia (2007) 579:233–249 Introduction (e.g., VanBlaricom, 1996; Wendell, 1996). If trophic cascades involving sea otters are afforded Predation by top trophic level consumers, or credibility without rigorous scrutiny, there is a ‘apex predators’ may influence local community risk that reasonable shellfish management activ- structure and dynamics through mechanisms such ities could be inappropriately discarded in favor as trophic cascades (e.g., Paine, 1966; Estes & of unjustified ecological benefits associated with Palmisano, 1974; Estes & Duggins, 1995; Estes sea otters. et al., 1998). In the marine ecological literature, We suggest that there is an inadequate record two of the most compelling and celebrated cases in the technical literature establishing the gener- linking apex predation with community structure ality of trophic cascades driven by sea otter and function are studies of sea star predation on predation across the geographic range of sea rocky intertidal benthic invertebrates for which otters and productive coastal kelp forest habitats space is a limiting resource (Paine, 1966, 1974, on rocky substrata along the North Pacific Rim and related subsequent studies), and studies of (i.e., from northern Japan to the outer coast of sea otter (Enhydra lutris [L.]) predation on her- Baja California Sur, Mexico). In our view, the bivorous benthic invertebrates that otherwise applicability of trophic cascade hypotheses driven limit nearshore macrophyte abundance and pro- by sea otter predation has not been established ductivity (Estes & Palmisano, 1974; Estes et al., among geographic locations with similar physical 1978; Duggins, 1980; Estes & Duggins, 1995 and settings or among geographically proximate hab- related studies). Our study focuses on the latter. itats with different physical settings. The most Application of trophic cascade models involv- widely cited study of the geographic generality of ing sea otters to conservation policy has long been trophic cascades driven by sea otters (Estes & controversial (e.g., Estes & VanBlaricom, 1985; Duggins, 1995) involves a longitudinally broad VanBlaricom & Estes, 1988). Controversy results region that arguably lacks profound variation in from two categories of problems. First, there is oceanographic or geologic attributes and occurs concern that portrayals of trophic cascades across a relatively limited latitudinal range com- involving sea otters and kelp forests oversimplify pared to the range of sea otters and many types of the realities of kelp forest ecology, inappropri- kelp forest communities in the North Pacific. ately minimizing consideration of effects of other Thus, we believe there is a need for additional factors, such as physical disturbance and substra- evaluation of the generality of trophic effects of tum type, on kelp forest structure and dynamics sea otters on kelp forests in the coastal North (e.g., Cowen et al., 1982; Schiel & Foster, 1986; Pacific. Foster & Schiel, 1988; Foster, 1990). Second, Here we offer an experimental evaluation of there is concern that uncritical application of some aspects of kelp forest community structure trophic cascade hypotheses may facilitate inap- and dynamics often said to be a general result of propriate conservation and management deci- sea otter predation in the North Pacific. We also sions involving sea otters. For example, sea evaluate potential effects of a fishery for sea otters are known to preempt the long-term urchins on nearshore North Pacific coastal eco- sustainability of certain shellfish fisheries by systems, recognizing that commercial urchin har- virtue of foraging activities, a matter of significant vests often mimic effects of sea otters by causing concern to some resource management agencies significant reduction in urchin densities. (e.g., Estes & VanBlaricom, 1985; Wendell et al., Sea otter predation and commercial sea urchin 1986; Wendell, 1994, 1996; Fanshawe et al., 2003). (Strongylocentrotus spp.) harvest are ecologically However, conservation-oriented initiatives to and economically important sources of urchin protect and expand sea otter numbers and distri- mortality in nearshore benthic systems in north- bution are often supported by arguments for the ern Washington marine waters. Commercial har- importance of predation by sea otters in restoring vest of sea urchins has occurred in the Strait of trophic cascades said to be natural in the absence Juan de Fuca and the San Juan Islands for nearly of anthropogenic intrusions to marine ecosystems four decades and supports several hundred 123 Hydrobiologia (2007) 579:233–249 235 harvesters and processors statewide (Pfister & Hines, 1987; Reed, 1990), may also be important Bradbury, 1996; Lai & Bradbury, 1998). During in structuring nearshore communities in the the 1980s and 1990s, the Washington sea otter absence of otter predation. population grew rapidly and expanded its range Sea otters were exterminated from Washington into the western Strait of Juan de Fuca, with the in the early 1900s due to the largely unmanaged rate of numerical and geographic growth slowing commercial fur trade (Riedman & Estes, 1988). somewhat after 2000 (Laidre et al., 2002; Gerber Sea otters were reestablished in the state in 1969 et al., 2004). Both otters and harvesters may (Jameson et al., 1982), but the population has not substantially reduce urchin biomass (e.g., Estes yet expanded its range to include the San Juan et al., 1978; Kalvass & Hendrix, 1997), and Islands, the apparent eastern limit of the pre- reduction in urchin densities is known to have exploitation sea otter range in Washington (Ger- important consequences for benthic plant com- ber & VanBlaricom, 1999). Application of the munities in many locations (Lawrence, 1975). As sea-otter paradigm to the San Juan Islands would a result, both sea otters and commercial urchin suggest the presence of high urchin densities and harvesters may significantly impact the structure low macroalgal densities. Instead moderate urch- and composition of nearshore benthic ecosystems. in densities coexist with abundant macroalgae, a Observations of the dramatically different situation that has apparently persisted across communities associated with sea otter presence recent decades (e.g., Neushul, 1967; Vadas, have prompted various authors to suggest that sea 1968, this study). This brings into question the otters are a keystone species (e.g., Estes & generality of the sea otter paradigm, and suggests Palmisano, 1974; Estes & Duggins,
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