Cascading Effects of Predator Diversity and Omnivory in a Marine Food Web
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Ecology Letters, (2005) 8: 1048–1056 doi: 10.1111/j.1461-0248.2005.00808.x LETTER Cascading effects of predator diversity and omnivory in a marine food web Abstract John F. Bruno1* and Mary Over-harvesting, habitat loss and exotic invasions have altered predator diversity and I. O’Connor2 composition in a variety of communities which is predicted to affect other trophic levels 1Department of Marine and ecosystem functioning. We tested this hypothesis by manipulating predator identity Sciences, CB 3300, The University and diversity in outdoor mesocosms that contained five species of macroalgae and a of North Carolina at Chapel Hill, macroinvertebrate herbivore assemblage dominated by amphipods and isopods. We used Chapel Hill, NC 27599, USA five common predators including four carnivores (crabs, shrimp, blennies and killifish) 2Curriculum in Ecology, CB 3275, and one omnivore (pinfish). Three carnivorous predators each induced a strong trophic The University of North Carolina cascade by reducing herbivore abundance and increasing algal biomass and diversity. at Chapel Hill, Chapel Hill, NC 27599, USA Surprisingly, increasing predator diversity reversed these effects on macroalgae and *Correspondence: E-mail: altered algal composition, largely due to the inclusion and performance of omnivorous [email protected] fish in diverse predator assemblages. Changes in predator diversity can cascade to lower trophic levels; the exact effects, however, will be difficult to predict due to the many complex interactions that occur in diverse food webs. Keywords Biodiversity, ecosystem functioning, food web, macroalgae, omnivory, predator, primary production, trophic cascade. Ecology Letters (2005) 8: 1048–1056 considered plant or animal biodiversity in a food web INTRODUCTION context (Ives et al. 2005) (but see Wardle et al. 2003; Despite decades of research on the importance of predation, Aquilino et al. 2005; Duffy et al. 2005). Thus, little is known the role of predator diversity in regulating food web about the community-wide effects of diversity at any single dynamics, community structure, and ecosystem functioning trophic level (Paine 2002; Schmitz 2003; Worm & Duffy is largely unknown. Speculation about the role of predator 2003; Petchey et al. 2004). diversity and its potential importance in ecosystem man- Predators can indirectly increase plant biomass by agement and restoration is common (e.g. Jackson et al. 2001; suppressing herbivore populations (Silliman & Bertness Duffy 2003) and descriptive data has frequently been used 2002). Such trophic cascades are common (Schmitz et al. to estimate predator diversity effects (Sinclair et al. 2003). 2000; Shurin et al. 2002) and could become stronger if But because there have been few experimental investigations increasing predator diversity further reduces the intensity of the effects of predator diversity (Cardinale et al. 2003; of herbivory (Sih et al. 1998; Ives et al. 2005). Food web Worm & Duffy 2003; Finke & Denno 2004; Ives et al. ecology and biodiversity–ecosystem functioning research 2005), and none on the importance of vertebrate predator support multiple predictions about the strength and diversity or in the ocean, we cannot predict and may not direction of predator diversity effects on other trophic even recognize the cascading effects of predator extinctions. levels. For example, dietary complementarity or inter- Recent research indicates that in many ecosystems, plant specific facilitation among predators could increase diversity can substantially increase primary production and herbivore suppression (Sih et al. 1998; Duffy 2002). can influence several other ecosystem properties (Hooper Diverse predator assemblages are more likely to include et al. 2005). However, work on the effects of consumer predators with traits that enhance prey consumption such diversity is rare (Duffy 2002; Petchey et al. 2004) (but see as a keystone predator or facilitator (Ives et al. 2005). Naeem & Li 1998; Duffy et al. 2003) and few studies have The probability of selecting such species in either natural Ó2005 Blackwell Publishing Ltd/CNRS Cascading effects of predator diversity 1049 or experimental communities increases with species acting effects, the magnitude and direction of the influence diversity. on community and ecosystem properties is difficult to The net effects of multispecies predator assemblages are predict. sometimes referred to as the nonlinear or ‘emergent’ effects Here we report an experimental test of the importance of of multiple predators (Sih et al. 1998; Schmitz & Sokol- predator identity and diversity in controlling the structure Hessner 2002). For instance, high levels of predator of lower trophic levels using coastal marine food webs of diversity could induce indirect interactions that modify 18–23 species (Fig. 1). We reconstructed a well-studied predator behaviour and decrease herbivore consumption estuarine food web in outdoor mesocosms that mimicked (Cardinale et al. 2003; Finke & Denno 2004; Siddon & natural field conditions and included most common species Witman 2004). Predators can indirectly affect plants by of macroalgae, macroinvertebrate herbivores, and vertebrate altering herbivore density, a density-mediated indirect and invertebrate predators. We measured the effects of interaction (DMII), and by altering herbivore foraging predator monocultures and polycultures of three and five behaviour, a trait-mediated indirect interaction (TMII) species on herbivore populations and macroalgal biomass, (Trussell et al. 2002). Both trait-mediated and density- composition and diversity. mediated interactions are important determinants of the strength and direction of cascading predator effects (Trussell et al. 2002, 2003; Schmitz et al. 2004) and changes METHODS in predator diversity could influence the nature of DMIIs Experimental design and TMIIs. Intraguild predation and cannibalism could increase with predator diversity, also reducing the suppres- The experiment was performed at The University of North sion of herbivore populations (Sih et al. 1998; Finke & Carolina at Chapel Hill’s Institute of Marine Science (IMS) Denno 2004). Additionally, by consuming plants, omnivor- in Morehead City, NC. The experiment began on 25 ous predators could weaken or reverse the generally September 2004, ran for 22 days, and included eight predicted positive relationship between predator diversity treatments (n ¼ 11): no predators, monocultures of each and plant biomass (Petchey et al. 2004) (Fig. 1). Because of the five predators, a mixture of three predators (the predator diversity could potentially have multiple counter- composition of each replicate was chosen randomly from the five-species pool) and five predator polycultures (i.e. the high diversity treatment). The initial richness, composition Predators and biomass of herbivores and algae were the same in all 88 mesocosms. We used a replacement design, manipulating Shrimp predator identity and richness while holding predator Blennies density constant at five individuals per mesocosm (c. 16 g _ Killifish predator wet biomass/mesocosm), which is comparable Crabs with natural predator densities in North Carolina subtidal Pinfish communities (Nelson 1979a; Powers 2005). One limitation of a replacement design is that species-specific densities are + lower in mixture than in monoculture treatments, potentially Herbivores dampening important intraspecific interactions. However, Isopods this likely reflects natural conditions in the field, where _ Amphipods negative interspecific interactions (including intraguild pre- dation, competition and antagonistic behaviour) likely _ reduce population densities when predator diversity is high. Plants Additionally, the replacement design provides the clearest test of predator diversity effects, unlike the additive design Green algae in which predator diversity and density are confounded as in Red algae most multiple predator effect experiments (Sih et al. 1998) Brown algae and most recent attempts to test the predator diversity hypothesis (e.g. Finke & Denno 2004). Figure 1 Interaction web of the experimental ecosystem illustra- ting the positive and negative effects of direct (solid lines) and indirect (dashed lines) species interactions on the production, Study system and experimental organisms biomass and diversity of lower trophic levels. Interactions among species within a given trophic level are not included. Pinfish are Hard-substratum communities in the South Atlantic Bight omnivorous predators. are composed of a diverse assemblage of macroalgae, Ó2005 Blackwell Publishing Ltd/CNRS 1050 J. F. Bruno and M. I. O’Connor invertebrates and fishes, including both temperate and three types of predators but possibly more than three species tropical species (Hay & Sutherland 1988). Macroalgae are (i.e. some of those that included two shrimp or blennies). The the main primary producers in these ecosystems and are five predators are similar in size, ranging in wet mass from an grazed intensely by macroinvertebrate herbivores (e.g. average of 1.8 to 6.1 g and from 3.4 to 7.2 cm in length (or amphipods and isopods), urchins and some fishes, although maximum width for crabs) (Table S1). The mean mass of the palatability is highly alga- and herbivore-specific (Miller & three fish predators only varied slightly (1.8–3.6 g) and the wet Hay 1996; Duffy & Hay 2000). The macroinvertebrate mass of the heaviest predators, swimming crabs, was likely herbivore assemblage is diverse (Nelson 1979a) and is exaggerated by water retention