Flipping indirect defense: chemical cues from natural enemies mediate multitrophic interactions.

Plants and invertebrates use chemical signals and cues to construct information about their environment. It is well reviewed that chemical signals play key roles in interactions between conspecific insects, such as sex pheromones for finding mates, and that plants transmit chemical signals to recruit natural enemies that kill herbivores. However, it is also known that chemicals emitted by natural enemies can influence insect herbivore physiology and behavior. The detection of chemical cues associated with the presence of natural enemies can influence herbivore movement, feeding, and reproduction, which may limit the damage herbivores inflict on their host plants. Plants detect chemical cues associated with herbivores, but less is known about whether plants also detect chemical cues of natural enemies or how this detection affects plant defense responses. In this review, we highlight what is known about how natural enemy chemical cues directly affect herbivores, how natural enemy cues indirectly affect herbivores through changes in host plant defenses, and we discuss the evolutionary ecology of plant and herbivore responses to natural enemy cues. Finally, we consider application of these concepts for insect pest management. Improving our understanding of how natural enemy chemical cues mediate multitrophic interactions provides a great opportunity for future exploration. CONDENSED ABSTRACT: Plants and invertebrates use chemical signals and cues to construct information about their environment. Detection of chemical cues from natural enemies can influence herbivore behavior and reduce herbivory. Plants detect chemical cues associated with herbivores, but less is known about whether plants detect cues of natural enemies or how detection affects plant defense responses. Here, we highlight what is known about how natural enemy chemical cues directly affect herbivores and how natural enemy cues indirectly affect herbivores through changes in plant defenses. We discuss the evolutionary ecology of plant and herbivore responses to natural enemy cues and consider applications for pest management.