Plant resistance attenuates the consumptive and non-consumptive impacts of predators on prey

Plant resistance and predation have strong independent and interacting effects on herbivore survival, behavior, and patterns of herbivory. Historically, research has emphasized variation in the consumption of herbivores by enemies. Recent work, however, demonstrates that predators also elicit important changes in the traits of their prey, but we do not know how this is influenced by plant quality. In this study, we quantify how the consumptive and non-consumptive effects of predators vary along a gradient of plant resistance using tomato plants (Solanum lycopersicum), tobacco hornworms (Manduca sexta), and predaceous stinkbugs (Podisus maculiventris). We manipulated resource quality using three tomato lines that vary in the expression of the jasmonate pathway, a phytohormonal pathway that is central in mediating resistance to insects. Resistant plants had higher levels of defensive proteins and glandular trichomes than low resistance plants. The consumptive and non-consumptive effects of predators were quantified on the three tomato lines by comparing the impact of 'lethal' predators that both kill and scare prey with 'risk' predators whose mouthparts were surgically impaired to prevent killing. Across several field experiments, the total cascading effect of predators on plant damage was 80.4% lower on jasmonate-overex-pressing (highly resistant) plants compared to that on wild-type or jasmonate-insensitive (low resistance) plants. This dramatic attenuation of predator effects was due to a 66% reduction in consumption on high resistance plants, and also because of a 65% decline in non-consumptive effects. Numerous studies in natural and agricultural habitats have documented that predator effects tend to be weaker on well-defended plants; our results provide novel mechanistic insight into this pattern by demonstrating that plant resistance substantially weakens both the consumptive and non-consumptive impacts of predators.