Ecology, 89(9), 2008, pp. 2426–2435 Ó 2008 by the Ecological Society of America CONSUMPTIVE AND NONCONSUMPTIVE EFFECTS OF PREDATORS ON METACOMMUNITIES OF COMPETING PREY 1,2,9 3 4 5 6 JOHN L. ORROCK, JONATHAN H. GRABOWSKI, JELENA H. PANTEL, SCOTT D. PEACOR, BARBARA L. PECKARSKY, 7 8 ANDREW SIH, AND EARL E. WERNER 1National Center for Ecological Analysis and Synthesis, 735 State Street, Suite 300, Santa Barbara, California 93101 USA 2Department of Biology, Washington University, Saint Louis, Missouri 63130 USA 3Gulf of Maine Research Institute, 350 Commercial Street, Portland, Maine 04101 USA 4Section of Integrative Biology, University of Texas, Austin, Texas 78712 USA 5Department of Fisheries and Wildlife, Michigan State University, Ann Arbor, Michigan 48105 USA 6Department of Zoology, University of Wisconsin, Madison, Wisconsin 53706 USA 7Department of Environmental Science and Policy, University of California, Davis, California 95616 USA 8Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109 USA Abstract. Although predators affect prey both via consumption and by changing prey migration behavior, the interplay between these two effects is rarely incorporated into spatial models of predator–prey dynamics and competition among prey. We develop a model where generalist predators have consumptive effects (i.e., altering the likelihood of local prey extinction) as well as nonconsumptive effects (altering the likelihood of colonization) on spatially separated prey populations (metapopulations). We then extend this model to explore the effects of predators on competition among prey. We find that generalist predators can promote persistence of prey metapopulations by promoting prey colonization, but predators can also hasten system-wide extinction by either increasing local extinction or reducing prey migration. By altering rates of prey migration, predators in one location can exert remote control over prey dynamics in another location via predator-mediated changes in prey flux. Thus, the effect of predators may extend well beyond the proportion of patches they visit. In the context of prey metacommunities, predator-mediated shifts in prey migration and mortality can EATURE F shift the competition–colonization trade-off among competing prey, leading to changes in the prey community as well as changes in the susceptibility of prey species to habitat loss. Consequently, native prey communities may be susceptible to invasion not only by exotic prey species that experience reduced amounts of mortality from resident predators, but also by exotic PECIAL prey species that exhibit strong dispersal in response to generalist native predators. Ultimately, S our work suggests that the consumptive and nonconsumptive effects of generalist predators may have strong, yet potentially cryptic, effects on competing prey capable of mediating coexistence, fostering invasion, and interacting with anthropogenic habitat alteration. Key words: behavior; competition; consumptive effects; habitat loss; invasion; metacommunity; metapopulation; migration; nonconsumptive effects; predator–prey interactions. INTRODUCTION among species (Holyoak et al. 2005). Colonization and Spatial dynamics affect the persistence of populations extinction are key parameters of both metapopulation (Levins 1969, Hanski and Gilpin 1997), alters the and metacommunity dynamics (Hanski and Gilpin 1997, outcome of competition (e.g., the competition–coloni- Holyoak et al. 2005). Although often treated as fixed zation trade-off [Nee and May 1992, Tilman 1994, and intrinsic in metacommunity models (Mouquet et al. Amarasekare 2003]), mediates the stability of predator– 2005), substantial evidence suggests that colonization prey interactions (Holt 1997, Melian and Bascompte and extinction are subject to alteration by biotic 2002, Mouquet et al. 2005), and thus has important interactions (Wooster and Sih 1995, Reed and Levine implications for ecological invasions (Fagan et al. 2002) 2005, Resetarits et al. 2005). Such interaction-mediated and conservation, e.g., minimum viable metapopula- changes in extinction and colonization are likely to be tions (Hanski et al. 1996). Recently, the emerging especially relevant in the context of metacommunities, paradigm of metacommunity dynamics has stressed the because metacommunities explicitly contain multiple interplay between spatial dynamics and interactions species (Holyoak et al. 2005). Predators are likely to affect prey colonization and extinction by consuming prey (‘‘consumptive effects’’) as Manuscript received 26 June 2007; revised 27 September well as by causing changes in prey activity, behavior, 2007; accepted 7 November 2007. Corresponding Editor: S. and development (‘‘nonconsumptive effects’’; see Plate Naeem. For reprints of this Special Feature, see footnote 1, p. 2414. 1); empirical data suggest that both effects are important 9 E-mail: [email protected] components of predator–prey interactions (Werner and 2426 September 2008 NONCONSUMPTIVE PREDATOR EFFECTS 2427 PLATE 1. Drunella doddsi (Ephemeroptera: Ephemerellidae) is one of several invertebrate predators on Baetis bicaudatus (Ephemeroptera: Baetidae) in Rocky Mountain streams of western Colorado, USA. Other invertebrate predators include stoneflies (Plecoptera) and caddisflies (Trichoptera). Baetis has evolved numerous behaviors and life-history strategies to reduce consumption by both invertebrate and vertebrate (Salmonidae) predators, resulting in non-consumptive effects on prey fitness that often exceed those of consumption (Peckarsky and McIntosh 1998). Photo credit: A. McIntosh. S Hall 1988, Lima and Dill 1990, Brown et al. 1999, dynamics are driven by specialist predators explicitly PECIAL Werner and Peacor 2003, Preisser et al. 2005, Stanko- linked to prey populations. Taken together, these wich and Blumstein 2005). Metacommunity models of models suggest that predator-mediated changes in prey consumptive effects (Holt 1997, Nee et al. 1997, migration can alter prey dynamics, and predators can F Bascompte and Sole 1998, Diehl et al. 2000, Swihart et alter the outcome of interactions among indirectly EATURE al. 2001, Melian and Bascompte 2002) have shown that competing prey. Given the theoretical importance of predator-mediated changes in prey extinction can have predator-mediated shifts in colonization for single prey important consequences for the dynamics of specialist species dynamics, and the prevalence of empirical predators and their prey. In the metacommunity evidence for nonconsumptive alteration of prey migra- context, a key nonconsumptive effect involves the tion, a framework is clearly needed to unify spatial influence of predators on prey movement and migration. dynamics and the consumptive and nonconsumptive For example, predators may alter prey colonization via components of predator-mediated shifts in competitive habitat selection (Krivan and Sirot 2002, Resetarits et al. dynamics. 2005, Abrams et al. 2007) or by dispersal behavior (Sih We extend previous metacommunity models of and Wooster 1994, Wooster and Sih 1995, Reed and predator–prey dynamics by incorporating both con- Levine 2005). To this end, a handful of metacommunity sumptive and nonconsumptive effects of predators. Our models have examined how predator-mediated changes work is a departure from previous models in that it in prey behavior affect the dynamics between specialist incorporates both consumptive and nonconsumptive predators and a single prey species (Holt 1997, Diehl et effects among prey as well as direct competition among al. 2000, Prakash and de Roos 2002). These studies have prey for patches of habitat. We model generalist shown that the nonconsumptive effects of specialist predators whose dynamics are not dependent upon the predators on single prey species can be counterintuitive, prey they consume. We use this approach because such such as potentially promoting prey abundance and generalist predators may constitute the bulk of predator persistence (e.g., Prakash and de Roos 2002, Reed and biomass in many systems (Sih et al. 1985, Holt and Levine 2005). Lawton 1994, Swihart et al. 2001), suggesting that their When extended to include predators and competing consumptive and nonconsumptive effects may be prey (Holt 1997, Melian and Bascompte 2002), meta- important for affecting the dynamics of competing prey. community models clearly demonstrate that the spatial First, we develop a model of spatial interactions dynamics of predator and prey can alter the nature of among generalist predators and a single prey species. metacommunity dynamics. In these models, prey com- Upon this foundation, we add competitive interactions pete indirectly via apparent competition (Holt 1997, among prey to examine how predator-mediated changes Melian and Bascompte 2002) and asymmetrical intra- in prey colonization and extinction affect the dynamics guild predation (Melian and Bascompte 2002), and their of prey metacommunities. Finally, we extend our model 2428 JOHN L. ORROCK ET AL. Ecology, Vol. 89, No. 9 to examine how habitat destruction affects prey prey (Stephens and Krebs 1986, Swihart et al. 2001) and communities subjected to generalist predators. We show may not be spatially aggregated near prey (Walde and that generalist predators can alter the dynamics of prey Murdoch 1988). Moreover, a review of empirical studies extinction and persistence, change the outcome of suggests that foragers often encounter their prey at competition among prey, and interact with