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Interactions Among Predators and the Cascading Effects of Vertebrate Insectivores on Arthropod Communities and Plants Kailen A

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Interactions Among Predators and the Cascading Effects of Vertebrate Insectivores on Arthropod Communities and Plants Kailen A Interactions among predators and the cascading effects of vertebrate insectivores on arthropod communities and plants Kailen A. Mooneya,1, Daniel S. Grunerb, Nicholas A. Barberc, Sunshine A. Van Baeld, Stacy M. Philpotte, and Russell Greenbergf aDepartment of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697-2525; bDepartment of Entomology, University of Maryland, College Park, MD 20742-4454; cDepartment of Biology, University of Missouri, St. Louis, MO 63121; dSmithsonian Tropical Research Institute, Apartado 0843- 03092, Balboa, Ancon, Panama; eDepartment of Environmental Sciences, University of Toledo, Toledo, OH 43606; and fSmithsonian Migratory Bird Center, National Zoological Park, Washington, DC 20008 Communicated by Thomas W. Schoener, University of California, Davis, CA, March 4, 2010 (received for review August 5, 2009) Theory on trophic interactions predicts that predators increase plant arthropod predators and herbivores. Theory predicts that any di- biomass by feeding on herbivores, an indirect interaction called a rect negative effect of vertebrate insectivores on herbivores would trophic cascade. Theory also predicts that predators feeding on be counterbalanced, in part or in whole, by the simultaneous sup- predators, or intraguild predation, will weaken trophic cascades. Al- pression of the arthropod predators of those herbivores (12, 13). though past syntheses have confirmed cascading effects of terrestrial Consequently, predicting the net effects of vertebrate insectivores arthropod predators, we lack a comprehensive analysis for verte- on plants requires knowledge of their relative effects on both brate insectivores—which by virtue of their body size and feeding predatory and herbivorous arthropods (11). Resolving the func- habits are often top predators in these systems—and of how intra- tional role of vertebrate insectivores is increasingly important in guild predation mediates trophic cascade strength. We report here on light of their vulnerability to global change (14). a meta-analysis of 113 experiments documenting the effects of insec- Despite the expectation that intraguild predation dampens the tivorous birds, bats, or lizards on predaceous arthropods, herbivorous strength of trophic cascades, past meta-analyses have not tested this ECOLOGY arthropods, and plants. Although vertebrate insectivores fed as intra- prediction. Meta-analyses of experiments from terrestrial systems guild predators, strongly reducing predaceous arthropods (38%), have focused primarily on the top-down effects of predaceous they nevertheless suppressed herbivores (39%), indirectly reduced arthropods (Table 1) (2, 3). To the extent that these meta-analyses plant damage (40%), and increased plant biomass (14%). Further- included vertebrate insectivores, they emphasized effects on her- more, effects of vertebrate insectivores on predatory and herbivo- bivores, and the role of predatory arthropods as mediators of tro- rous arthropods were positively correlated. Effects were strongest on phic cascade strength has not been studied. Vance-Chalcraft et al. arthropods and plants in communities with abundant predaceous (15) investigated the consequences of intraguild predation for arthropods and strong intraguild predation, but weakincommunities herbivore suppression, but their review included few studies on depauperate in arthropod predators and intraguild predation. The vertebrate insectivores and did not address the indirect effects of naturally occurring ratio of arthropod predators relative to herbi- such dynamics for plants. Consequently, fundamental aspects of vores varied tremendously among the studied communities, and how vertebrate insectivores affect arthropods and plants remain the skew to predators increased with site primary productivity and unclear, despite extensive evidence for the importance of vertebrate in trees relative to shrubs. Although intraguild predation among arthropod predators has been shown to weaken herbivore suppres- insectivores (10, 16, 17). sion, we find this paradigm does not extend to vertebrate insecti- To redress these gaps, we conducted a meta-analysis of 113 vores in these communities. Instead, vertebrate intraguild preda- published studies from 63 publications in which vertebrate insec- tivores (birds, bats, or lizards) were removed, and their effects tion is associated with strengthened trophic cascades, and insecti- fi vores function as dominant predators in terrestrial plant-arthropod quanti ed not only for herbivores and plants but also for preda- communities. ceous arthropods (for a summary table and list of source pub- lications, see Table S1). With these data, we tested a set of predic- bottom-up and top-down control | intraguild predation | meta-analysis | tions arising from theory on trophic interactions (12, 18) for the trophic cascade | vertebrate predator exclusion effects of vertebrate insectivores on arthropod predators (also referred to as intermediate predators), herbivores, and plants: (P1) generalist predators such as vertebrate insectivores should suppress esearch demonstrates that predators, by feeding on herbi- both predatory and herbivorous arthropods, supporting our asser- vores, can increase plant biomass via the indirect interaction R tion that they feed as intraguild predators; (P2) because of the commonly labeled a trophic cascade (1). In recent years, meta- buffering influence of intermediate predators, the effect strengths analyses have quantified trophic cascades separately in terrestrial of vertebrate insectivores on herbivores and plants should attenu- (2, 3) and aquatic systems (4, 5) and in multiple habitats together ate in communities where intermediate predators are more abun- to compare the strength of trophic cascades among ecosystem dant relative to herbivores; (P3) Because intermediate predators types (6). Although the strengths of trophic cascades vary across should diminish the indirect effects of vertebrate insectivores, the ecosystem types, explanations for the significant residual varia- tion within ecosystems remain enigmatic (6–8). Vertebrate insectivores such as birds, bats, and lizards often Author contributions: K.A.M., D.S.G., N.A.B., S.A.V.B., and S.M.P. designed research; K.A.M., feed as top predators on terrestrial arthropod communities, but D.S.G., N.A.B., S.A.V.B., S.M.P., and R.G. performed research; K.A.M., D.S.G., and N.A.B. based upon current theory it is unclear whether their effects should analyzed data; and K.A.M., D.S.G., N.A.B., S.A.V.B., and S.M.P. wrote the paper. cascade down to affect plant biomass. Because of their large body The authors declare no conflict of interest. size relative to arthropod prey, vertebrate insectivores can con- Freely available online through the PNAS open access option. sume both predatory and herbivorous arthropods (9, 10). As a 1To whom correspondence should be addressed. E-mail: [email protected]. consequence, vertebrate insectivores may feed as so-called intra- This article contains supporting information online at www.pnas.org/cgi/content/full/ guild predators (11), simultaneously consuming intermediate 1001934107/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1001934107 PNAS Early Edition | 1 of 6 Table 1. Summary of results from published trophic cascade meta-analyses involving terrestrial communities Arthropods Plants Source Predators* Herbivores* Damage* Biomass* (3) — −0.49 −0.95 +0.22 (−0.63 –0.35) (−1.18 –0.72) (+0.11 +0.33) 22% 32% 0% (2) — −0.41 −0.53 +0.12 (−0.49 –0.33) (−0.64 –0.42) (+0.03 +0.20) 37% 48% 10% † (6) — −0.44 — +0.11 (−0.72 –0.16) (−0.06 +0.27) 17% 17% (9) −0.71 −0.60 −0.32 — (−0.95 –0.49) (−0.90 –0.30) (−0.45 –0.20) 100% 100% 100% This study −0.49 −0.47 −0.34 +0.13 (−0.69 –0.29) (−0.66 –0.28) (−0.46 –0.22) (−0.02 +0.28) 100% 100% 100% 100% *Values reported in each cell: log response ratios, 95% confidence intervals, and % of studies with vertebrate predators. †Based on studies measuring plant biomass of whole communities, limited to grassland and agricultural fields, found stronger effects of vertebrate predators (across terrestrial and aquatic communities). Other meta-analyses use responses of individual plant species and show no effect of predator type. net effects of vertebrate insectivores should be more strongly metric of arthropod community trophic composition under natural negative upon intermediate predators than herbivores, and these conditions. In communities deficient in intermediate predators (low effects should tradeoff such that strong effects on intermediate values of ln[IP:H+]), vertebrate insectivores had relatively weak predators are associated with weak effects on herbivores; (P4) as a effects on intermediate predators, herbivores and plants (Fig. 2 and result of this asymmetry in their net effects on intermediate pred- Table S4). In contrast, in communities with a high relative abun- ators and herbivores, vertebrate insectivores should alter the tro- dance of intermediate predators (high values of ln[IP:H+]) trophic phic composition of the communities on which they prey; and (P5) cascades were strong, with strong negative effects of vertebrate the results of our analysis should show relatively weak indirect effects on plant biomass as compared to past meta-analyses focused on experimental exclusions of arthropod predators that may more often feed directly upon herbivores without intraguild predation. Results and Discussion Tests of Predictions. Consistent with P1, vertebrate insectivores suppressed the abundance of both predaceous
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