A central pursuit in the study of tri-trophic interactions is understanding how plant traits affect the interplay between predators and herbivores. Prior studies, however, only quantify the impact of plant heterogeneity on consumption and ignore the potentially overriding influence of non-consumptive predator effects. We studied a diverse assemblage of phytophagous and predaceous insects to test the strength of consumptive and non-consumptive effects along a gradient of plant resistance. We used a combination of genetically modified tomato plants and foliar application of defense elicitors to enhance or diminish the magnitude of jasmonate- and salicylate-mediated resistance. On each plant-type we exposed a series of herbivores to their respective enemies, including either ‘lethal’ predators or ‘risk’ predators with their mouthparts surgically altered to prevent killing. More specifically, we assessed the interaction between plant resistance and predation risk in field cage experiments using: (a) leaf-chewing insects (tobacco hornworm, Manduca sexta; Colorado potato beetle, Leptinotarsa decemlineata; cabbage looper, Trichoplusia ni) and predaceous stinkbugs (Podisus maculiventris); and (b) sap-feeding insects (potato aphid, Macrosiphum euphorbiae) and ladybugs (convergent lady beetle, Hippodamia convergens).

Results/Conclusions

For leaf-chewing insects, elevated jasmonate expression reduced herbivore performance and weakened the magnitude of predator effects, including both consumptive and non-consumptive pathways. For example, the total cascading effect of predators on M. sexta leaf damage was 80.4% lower on jasmonate-overexpressing (highly resistant) plants compared to that on wild-type or jasmonate-insensitive (low resistance) plants. This dramatic attenuation of predator effects was due in part to a 66% reduction in consumption on high resistance plants, and also because of a 65% decline in non-consumptive effects. Aphids, however, responded very differently to predator and plant manipulations. Unlike chewing herbivores that responded to poor quality host-plants and predation risk by reducing their feeding rate (i.e., a behavior-mediated response), aphids increased production of winged morphs (alates) when exposed to predation risk and plants with either their jasmonate or salicylate pathways induced. Notably, risk predators elicited a far stronger wing response in prey feeding on highly resistant plants. Thus, unlike the chewer guild where non-consumptive effects attenuate with elevated plant resistance, sap-feeder responses amplify.