Co‐evolution of foraging behaviour in herbivores and their natural enemies predicts multifunctionality of herbivore‐induced plant volatiles

Abstract

Summary Herbivorous arthropods often induce phenotypic changes in plants of terrestrial systems, which include increased direct resistance to herbivores. In addition, infested plants release quantitatively and qualitatively different volatiles from those of uninfested plants, which are so‐called herbivore‐induced plant volatiles (HIPVs). Due to HIPVs, plants are more conspicuous to herbivorous arthropods and their natural enemies (carnivorous arthropods) than uninfested plants, thus acting as foraging cues in tri‐trophic systems. Intriguingly, herbivore and natural enemy responses to HIPVs are highly diverse. Whether they are attracted or repelled by HIPVs depend on the plant–herbivore–natural enemy species combination, suggesting a HIPV multifunctionality. We hypothesized that co‐evolutionary diversification of foraging strategies in herbivores and natural enemies, where arthropods adapted to diverse plant ecological traits, served to explain HIPV multifunctionality. We developed a food chain model of plant–herbivore–natural enemy to test our hypothesis, where plants exhibited three different states and different apparency (uninfested < lightly infested < highly infested) and quality (lightly infested > highly infested). The shifts between plant states were mediated by herbivore life cycle, interactions among herbivores, natural enemies and plant reproduction. The natural enemy evolutionary stable strategy (ESS) was predicted to choose the lightly and heavily infested plants in broad ranges of induced direct resistance and plant apparency (HIPV levels), implying that HIPVs acted as the induced indirect resistance. The corresponding herbivore ESS was to choose (or avoid) HIPVs when HIPV levels were low (or high). When the induced direct resistance was very high and thus herbivore quality was low, natural enemies tended to avoid increased HIPVs with increasing herbivory levels. This was associated with herbivore ESS choice for HIPVs, leading to intraspecific enemy‐free space. These predicted ESS diversities explained observed herbivore and natural enemy responses to HIPVs in several contrasting plant systems, including willow trees, lima bean and wild tobacco. Our findings suggest that non‐lethal herbivory and variations in induced plant responses are key mechanisms for evolutionary diversification of animal foraging behaviour and thus structure of ecological networks.