Effects of multiple enemies on pests
An extensive literature has established that combinations of multiple predator species can have any of three outcomes on prey suppression: (i) additive, independent effects; (ii) greater than additive, or synergistic effects; or (iii) less than additive, or disruptive effects (Jonsson et al. 2017). Much of this literature has emphasized consumptive effects as the drivers of these outcomes; thus, synergistic effects may be generated by various forms of complementarity, including complementary use of space (e.g., consuming prey in different microhabitats) or time (e.g., consuming prey during different times of day, or seasons), or differences in the host/prey stages or species attacked (Finke & Snyder 2008; Straub & Snyder 2008; Northfield et al. 2010), whereas disruptive effects may be generated by intraguild predation or various forms of competitive interference (Vance-Chalcraft et al. 2007).
Enemy-risk effects may, however, also play important roles in shaping non-additive effects of multiple predators (Sih et al. 1998). In particular, when prey defensive responses to one predator increase vulnerability to a second predator (“risk enhancement”), the outcome is often predator facilitation and synergistic impacts on prey mortality. This is the case when pea aphids are attacked by combinations of the ladybird beetle Coccinella septempunctata and the carabid beetle Harpalus pennsylvanicus. Pea aphids drop off plants when threatened by the foliage-foraging C. septempunctata, and despite adaptations for re-grasping the plant as they fall (Meresman et al. 2017), some still reach the ground, where they are attacked by the strictly ground-foraging H. pennsylvanicus (Losey & Denno 1998). Similarly, strong risk enhancement is seen when Tetranychus kanzawai spider mites are driven out of their web refuges by specialized predatory mites Neoseiulus womersleyi, only to fall prey to ants that forage only outside of their webbing (Otsuki & Yano 2014a).
Enemy-risk effects can also contribute to predator interference. If defensive responses to one predator also confer protection against a second predator (“risk reduction”), then total predation may be less than expected when both predators are present (Vance-Chalcraft & Soluk 2005). Alternatively, even when defensive responses appear to conflict, the presence of multiple predators may sometimes improve prey survival. For example, Meadows et al. (2017) showed that Culex mosquito larvae respond to a complex of mesopredators by diving towards the bottom of water bodies; however, in the presence of top predators, dragonfly larvae, which forage lower in the water column, diving responses by Culex are suppressed. Because the diving behavior is costly, suppression of this response doubled the survival of larval mosquitoes to pupation. Thus, enemy-risk effects often play key roles in shaping the emergent non-additive impacts of multiple predators.