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For Keystones Identifying Keystone Species Is Difficukt--But Essential to Understanding Bow Loss of Species Will Affect Ecosystems Mary E

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For Keystones Identifying Keystone Species Is Difficukt--But Essential to Understanding Bow Loss of Species Will Affect Ecosystems Mary E Challenges in the Quest for Keystones Identifying keystone species is difficukt--but essential to understanding bow loss of species will affect ecosystems Mary E. Power, David Tilman, James A. Estes, Bruce A. Menge, William J. Bond, L. Scott Mills, Gretchen Daily, Juan Carlos Castilla, Jane Lubchenco, and Robert T. Paine any ecologists believe that Defining keystones all species were not cre- A keystone species is M ated equal. For example, We offer a definition of keystone it is well known that the most abun- one whose effect is that has been expanded from the dant species play a major role in original usage of Paine (1969), in controlling the rates and directions large, and which keystone referred to a species of many community and ecosystem that preferentially consumed and held processes. These dominant species disproportionately in check another species that would are often crucial for the mainte- otherwise dominate the system. To large relative to better reflect its current use, we de- Mary E. Power is a professor in the fine a keystone species as one whose Department of Integrative Biology, Uni- its abundance impact on its community or ecosys- versity of California, Berkeley, CA tem is large, and disproportionately 94720. David Tilman is a professor in large relative to its abundance. the Department of Ecology, Evolution, nance of thejr communities, be- To develop a more operational and Behavior, University of Minnesota, cause they typically provide the definition for keystone species, one St. Paul, MN 55108. James A. Estes is a major energy flow and the three- must define the strength of the effect wildlife biologist in the National Bio- dimensional structure that supports of a species on a community or eco- logical Service, Institute of Marine Sci- system trait. This measure, which we ence, University of California, Santa and shelters other organisms call community importance (CI), is Cruz, CA 95064. Bruce A. Menge is a (Ashton 1992, Dayton 1985, Duran professor in the Department of Zool- and Castilla 1989, Gentry and the change in a community or eco- ogy, Oregon State University, Corvallis, Dodson 1987, Paine and Suchanek system trait per unit change in the OR 97331. William J. Bond is a profes- 1983, Strong 1977). abundance of the species. (Our ap- sor doctor in the Department of Botany, Many experiments, however, have proach is a generalization of the con- University of Cape Town, Rondebosch demonstrated that some less abun- cept of community importance in 7700 South Africa. L. Scott Mills is an dant species, often called keystone Mills et al. [1993].) In mathematical assistant professor in the Wildlife Biol- species, also have strong effects on terms, ogy Program, School of Forestry, Uni- versity of Montana, Missoula, MT 59812. communities and ecosystems (e.g., Gretchen Daily is Bing Interdisciplinary Paine 1969). Keystone species differ CI = [d(trait)/dp][l/(trait)] Research Scientist, Department of Bio- from dominant species in that their logical Science, Stanford University, effects are much larger than would where p is the proportional abun- Stanford, CA 94305. Juan Carlos Castilla be predicted from their abundance. dance (in most cases, proportional is a full professor and marine biology Ambiguity in the use of the term biomass relative to the total biomass head in Facultad de Ciencias Biologicas, keystone and the lack of an opera- of all other species in the commu- Pontificia Universidad Catolica de Chile, tional definition have led to criticism nity) of the species whose abundance Casilla 114-D, Santiago, Chile. Jane of its continued application in re- is modified. Trait refers to a quanti- Lubchenco is a distinguished professor search and policy contexts (Mills et tative trait of a community or eco- in the Department of Zoology, Oregon State University, Corvallis, OR 97331. al. 1993, Simberloff 1991). In this system. Potential community or eco- Robert T. Paine is a professor in the article we clarify the keystone con- system traits include productivity, Department of Zoology, NJ-15, Univer- cept, discuss its relevance to man- nutrient cycling, species richness, or sity of Washington, Seattle, WA 98195. agement processes, and suggest ad- the abundance of one or more func- 0 1996 American Institute of Biological ditional research that needs to be tional groups of species or of domi- Sciences. performed. nant species. Experiments that evalu- September 1996 609 a proportional abundance of species i a 15: before it was deleted. If a species has an effect in direct proportion to its 10- abundance, CI, would be 1 (if, after the species deletion, the community 5- or ecosystem characteristic de- creased) or -1 (if the characteristic increased). If species i is a keystone, the absolute value of CI, is much cr 15- greater than 1. $b Although the frequency distribu- tions of community importance val- 10- ues for species in natural communi- ties are unknown, several shapes seem 5- plausible (Figure 1). In some com- munities, the distribution may be 0, II - 0 + close to normal, with its mean near Community importance zero (Figure la).Three experimental studies of interaction strength have Figure 1. Possible frequency distribu- found, however, that although the tions of community importance values majority of species in the guilds or for all species in a given community. assemblages studied had impacts Positive values occur when a community close to zero, a few species exerted characteristic decreases after a species is strong effects (Figure 2).Paine (1992) deleted; in the absence of a mutualist, for instance, the target dominant species measured the impacts of seven inver- would also decrease. Negative values tebrate grazers on a rocky intertidal occur when a community characteristic kelp sporeling assemblage; Fagan and increases after removal of a species, as Hurd (1994) studied impacts of a would be the case if the characteristic preying mantid on more than 12 were the abundance of another species orders or families of arthropod prey and the first species were a consumer of in an old field; and Rafaelli and Hall that species. Community importance (CI) (1992) studied impacts of predatory values may be normally distributed birds, fish, and invertebrates on ma- around zero (a), in which case most species would have immeasurably small rine invertebrates in mudflats and effects, and keystones would be rare. (b) mussel beds. Fagan and Hurd (1994) In some communities, the CI distribu- did not resolve prey to species, and tion may have several modes, with key- Rafaelli and Hall (1992) could ma- stone species falling into modes that are nipulate predators such as shorebirds sufficiently far from zero. only as groups of species. By con- trast, Paine’s (1992) was a pairwise study, but only because he measured ate the community importance of a the impacts of each consumer on a species by changing its abundance simplified reference state composed should proceed long enough for in- almost entirely of a single, competi- direct effects to become evident. The tively superior prey species. Never- full derivative is used here, rather theless, these studies show the feasi- than a partial derivative, because it bility of using experimental field includes all the direct and indirect approaches to estimate interaction effects of the species. strength. In practice, it is difficult to mea- How are interaction strengths and sure the effects of small changes in community importance values of species abundance. More commonly, species related? Paine’s interaction an attempt is made to study a spe- strength (Paine 1992)was computed cies’ impacts by removing it entirely. as [(t - t,) /to] (l/n),where t, is the If it can be removed, then abungance of the prey in the pres- ence of the consumer, t, is prey abun- dance in the absence of the con- sumer, and n is the number of where tN is a quantitative measure of consumer individuals stocked in ex- the trait in the intact community or perimental arenas. This measure dif- ecosystem, t, is the trait when spe- fers from our index of community cies i has been deleted, and p, is the importance, [(t, - to) / tN] (l/pl),in 610 BioScience Vol. 46 No. 8 correlated, and if the distributions of cies are not always of high trophic interaction strengths documented in status. Third, keystone species can these studies prove widespread, com- exert effects, not only through the munity importance should also com- commonly known mechanism of con- monly be distributed as in Figure 1 b. sumption, but also through such Clearly, the variance, skew, and num- interactions and processes as compe- ber of modes of any such distribu- tition, mutualism, dispersal, polli- tions are of great ecological impor- nation, disease, and by modifying tance. The greater the variance and habitats and abiotic factors (as “key- skew, the more species have CI val- stone modifiers”; Bond 1993, Mills RoDortlonai biomass of species ues with unusually high absolute et al. 1993). values. Such species would be key- Both diversity and trophic-level Figure 3. Total (collective) impact of a stones, with a disproportionate considerations suggest that keystone species (absolute value of community effect on the composition and/or species are most likely to occur near impact x proportional abundance of a functioning of communities and eco- the top of the food chain. Top preda- species: lCI,l x p,) versus its proportional systems. Our intuition and limited tors typically have high per capita abundance, p,. Points representing a spe- experience suggest that only a small effects and low collective biomass, cies whose total impact is proportional proportion of the species in most relative to lower trophic levels. Nev- to its abundance would fall along the communities are likely to be key- ertheless, keystones may occur at diagonal line X = Y.
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