‘The Keystone Species Concept: Variation in Interaction Strength in a Rocky Intertidal Habitat Bruce A. Menge, Bric L, Berlow, Carol A. Blanchette, Sergio A. Navarrete, Sylvia B. Yamada Ecological Monographs, Volume 64, Issue 3 (Aug., 1994), 249-286. Stable URL: fyp:flinks jstor-org/sic sici=0012-9615%28199408%2964%3 A3%3C249%3 ATKSCVIF3E20.CO%SB2-T ‘Your use of the ISTOR archive indicates your acceptance of ISTOR’s Terms and Conditions of Use, available at fp (fw. stor orglaboutitermshrnl. ISTOR's Terms and Conditions of Use provides, in part, that unless You. have obtained prior permission, you ray not download an entire issue of &joumal or multiple copies of aricies, and You may use content in the ISTOR archive only for your personal, non-commercial use Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the sereen or printed page of such transmission, Ecological Monographs is published by The Ecological Society of America. Please contact the publisher for further permissions regaiding the use of this work. Publisher contact information may be obtained at bupsferw.jstoc.org/joumals/esahtanl. Ecological Monographs ©1994 The Ecological Society of America ISTOR and the ISTOR logo are trademarks of ISTOR, and are Registered in the U.S. Patent and Trademark Office. For mote information on ISTOR contact jstor-inio@umich edu, ©2002 STOR, hup:shrwwjstor.orgy Tue Nov 26 16:42:19 2002Esa Monapap 64), 1084, 9 M-206 Saye Rael Se a Rec THE KEYSTONE SPECIES CONCEPT: VARIATION IN INTERACTION STRENGTH IN A ROCKY INTERTIDAL HABITAT! Bauce A. MeNGe, Eric L. BeRLow, Canot A. BLANCHETTE, SERGIO A. NAVARRETE, AND SVLVIA B. YAMADA Department of Zeology, Oregon State University, Corvallis, regan 97341-2914 USA ‘We dedicate this paner tothe merry of John P. Subecland, a gret siemtis, 2 great human being Abstract. The usefulness and generality of the keystone species concept has recently been questioned. We investigated variation in interaction strength between the original keystone predator, the seastar Pisaster achra- ceus, and its primary prey, mussels (Afyitlus califarnianus and M. tressulus). The study was prompted by differences in community stcuctuce at two law zane sites along the central Oregon, coast, Boller Bay (BB) and Strawberry Hill (SH). Predators, especially seastars, were larger and more abundant at SH than at BB. Further, sessile animals were more abundant and macrophytes were less abundant at SH. Predators were more abundant ‘at wave-exposed sites at both sites, and at SH, sessile invertebrates were tore abundant at the wave-exposed location and sand cover was high at the wave-protected location. To test the bypothesis that vania predation strength explained some of these differences, we examined the seastar-mussel interaction at locations ‘with high aad low wave exposure at hoth sites. Predation intensity was quantified by determining the survival of mussels in clumps (50 mussels per clump, shell length 4-7 em) transplanted to large plots (18-163 m*) with ‘or without seastars in the low intertidal zone. Predation effects were quantified by determining prey recolonization rates in marked quadrats in the same large plots. Spatial variation in interaction strength was quantified by examining predation at scales of metces (among transplants within plots), 10°s af metres (between replicate plots Within each exposure ar each size), 100's of metres (between wave exposures widhia locations), and 10 000"s of metres (between sites), Temporal variation was evaluated by performing the experiments in 1990 and 1991 ‘The relation berween prey (russel) recruitment and growth to differences in community structure was evaluated by quantifying recruitment density in plastic mesh balls (collectars) and growth of individually marked trans- planted mussels, respectively, at each site x exposure » tide level combination each month for 4 yr Predation intensity varied greatly at all spatial scales, At the two largest spatial scales (10's of kilometres, 100°s of metces), differences in both survival of transplanted mussels and prey recolonization depended on variation in seastar abundarice with site, wave expasure, prey recruitment and grawth, and at SH protected, the extent of sand burial. Variation at the two smallest scales (metres, 10's of metres) was high when seastars, were scarce and low when seastars were abundant, Transplanted mussels suffered 100% mortality in 2 wl at wave-exposed SH, but took > 52 wk at wave-protected BB. Seastar effects on prey tecolonization were detected only at the SH wave-exposed site. Here, where prey recruitment and growth were unusually high, the mussel AZ. troseulus invaded and dominated space within 9 mo. After 14 mo, whelks, which increased in hoth size and ‘abundance in the absence of Pisaster, arrested this increase in mussel abundance. Similar changes did not occur at other site * exposure combinations, evidently because prey recruitment was low and possibly also due to ‘whelk predation on juveniles. Longer term results indicate that, as in Washington state, seastars prevent large adult Af ealfornianus from invading lower intertidal regions, but only at wave-exposed, not wave-protected sices. Thus, theee distinct predation regimes were observed: (1) sirang keystone predation by seastars at wave ‘exposed headlands; (2) less-strong diffise predation by seastars, whelks, aad possibly other predators at a wave- protected cove, and (3) weak predation at a wave-protected site buried regularly by sand. Comparable experimental results at four wave-exposed headlands (our two in Oregon and two others in Washington), and similarities between these and communities on other West Caast headlands suggest keystone predation occurs broadly in this system. Results in wave-protected habitats, however, suggest itis aot universal In Oregon, keystone predation was evidently contingent on conditions of high prey production (Lc. recruitment and growth), while diffuse predation occurred when prey production was low, and weak predation accurred ‘when environmental steess was high. Combining our results with examples from other marine and non-matine habitats suggests a need to consider a broader range of models than just keystone predation. The predictive and explanatory value of an expanded set of models depends on identifying factors distinguishing them. Although. evidence is linited, a survey of 17 examples sugzests (1) keystone predation is evidently not distinguished from diffuse predation by any of 11 previously proposed differences, but CO) may be distinguished by rates of prey production. Further, (3) differential predation on competitively dominant prey does not distinguish keystone from nonkeystone systems, since this interaction occurs in both types of community, Instead, differential predation on dominant prey evidently distinguishes strong-from weak-predation communities. While the key- stone predation concept has been and will continue to be useful, a broadened focus on testing and developing, ‘more general models of community regulation is needed, \ Manuscript received 3 October 1952; revied 30 October 199%; accepted 2 November 1993,230 key words BRUCE A. MENGE ET AL, Ecologia! Manogranhs Volssethe 3 commit regulation: diffe predation: distribution; ecological eneratisanon: experiment, iteration sirength Aeystone predation: Mytlus spp. Oregon coast Psaster acareceus, predation intensity, rocky tkertida; spatial seale- nave expanure gradient Isteapuction Since it vas first introduced by Paine (1969), che keystone species concept has been a centeal organizing principle in community ecology (Mills et al. 1993). Recently, however, both the usefulness and generality of this concept have been questioned (Strong 1992, Mills et al. 1993). Some criticism derives from am- ‘Diguities in definition, leading to cither very broad or very narrow usage. For instance, the term" although originally applied 10 atop carnivore, has been used broadly to refer ca important but noncacnivorous species (e.g, herbivores, prey, mutualists, hosts, Orspe~ cies modifying habitats through nontrophie mterac~ tions; National Research Council 1986, Bond 1993, Mills etal, 1993). In contrast, Strong (1992:747), im his stimulating critique of the traphic cascade concept, states “inte trophic cascades ienply Keystone species axa with such top-down dominance that their removal causes precipitous change in the system.” He later constrains “precipitous change” to mean either near-elimination of aurotrophs (theee-level systems) or rapid increase to high abundance of autotrophs (four evel systems) This usage seems unnecessarily restrict- ed, however, as it implicitly excludes other changes resulting fram the activities of keystone species, such as those in species composition or size (eg, Paine 1966, 1974, Carpenter et al. 1987). Definttions Here we consider just one type of keystone species, keystone predators. To avoid ambiguity, a “keystone predator” is defined as only one of several predators in a community that alone determines most patterns of rey community structure, including distribution, abundance, composition, size, and diversity. Thus, a predator is not a keystone if; (1) total predation is ‘uaderate to strong but each of the predators alone has little measurable effect (here termed “diffuse” preda- ‘dan, see Menge aad Lubhenco 1981, Rables and Robb 1993), or (2) total predation is slight (here termed, weak’ predation). Ultimately, the keystone predator concept will be most useful if many communities ate characterstically controlled by such a species, particulacly if keystone ‘and nonkeystone predators (or their communities) have specific distinguishing characteristics. If such distinct and predictable properties were identified, the concept ‘Would have important theoretical implications and could be an invaluable tool in management and con- servation of ecosystems (e.g, Bond 1993, Lawton and. Brown 1993, Mills et al, 1993). For example, Paine 1969) suggested two important properties were (1) the predator preferentially consumed and controlled the abundance of a prey species, and (2) this prey species could competitively exclude other species from the ‘community, In the absence af such general, identifiable properties the concept would be less useful, Variation in interaction serength Mills etal. (1993) and Strong (1992) also consider a second issue: the variability of keystone predator ef- feces, both within and berween broad habitat types (.e., marine, freshwater, terrestrial), For somewhat diferent reasons, both conclude a primary focus should be more fon factors underlying variation in predation effects, or the strength of the interaction hetween predators and. prey, than on 2 “keystone/non-keystone dualism’ (Mills ‘etal, 1993) or “true trophic cascades” (Strong 1992). Mills et al. (1993:223) explicitly advocate abandon- ‘ment of the keystone species concept, We believe this concept remains useful but agree that clarification is needed. Moreover, a focus on variation, in imteraction strength, here defined as the impact of fone population on the distribution, abundance, and/ ‘er body size of another population of major importance in the community, scems important to further progress in ecology (e-,, see Menge and Sutherland 1987, Menge and Olsen 1990). Evaluation of the issues of variation in interaction strength and the generality and impor= tance of the keystone species concept will depend at least parly on developing a set of detailed multifac- torial studies in a variety of communities and habitats. This assumes that, by studying how and why interac tions vary in relation to factors such as enviconmental stress, reeuitment, habitat complexity, or produetiv- ity, insight can. be gained imo both, the importance of different types of interactions and the forces underlying their variability. Determination of interaction strength depends on field experimentation (¢¢,, Paine (980, 1992, Menge and Sutherland 1987, Mills ecal, 1993). However, field ‘manipulation of factors such as wave forces or temn= perature is usually unfeasible, and the spatial seale of experimentation may be limited (Diamond 1986). 4 useful technique in such cases is the “comparative ex- perimental” approach (Menge and Sutherland 1987, Lubchenco and Real 1991, Menige 19910), in. which replicated, identically designed, controlled field exper- iments are done at different sites along environmental sradients. Nesting such experiments at diferent spatial seales, and repeating them through time, can indicate the importance and generality of the phenomena, Oh- servations and measurements of relevant environmen- ‘al conditions and comparisons among sites can pro Vide insight into the importance of different factors ‘varying along environmental gradients (for examples, of this approach, see Dayton 1971, 1975, Menge 1976,