Protection via parasitism: Datura odors attract parasitoid flies, which inhibit Manduca larvae from feeding and growing but may not help plants

Insect carnivores frequently use olfactory cues from plants to find prey or hosts. For plants, the benefits of attracting parasitoids have been controversial, partly because parasitoids often do not kill their host insect immediately. Furthermore, most research has focused on the effects of solitary parasitoids on growth and feeding of hosts, even though many parasitoids are gregarious (multiple siblings inhabit the same host). Here, we examine how a gregarious parasitoid, the tachinid fly Drino rhoeo, uses olfactory cues from the host plant Datura wrightii to find the sphingid herbivore Manduca sexta, and how parasitism affects growth and feeding of host larvae. In behavioral trials using a Y-olfactometer, female flies were attracted to olfactory cues emitted by attacked plants and by cues emitted from the frass produced by larval Manduca sexta. M. sexta caterpillars that were parasitized by D. rhoeo grew to lower maximum weights, grew more slowly, and ate less of their host plant. We also present an analytical model to predict how tri-trophic interactions change with varying herbivory levels, parasitization rates and plant sizes. This model predicted that smaller plants gain a relatively greater benefit compared to large plants in attracting D. rhoeo. By assessing the behavior, the effects of host performance, and the variation in ecological parameters of the system, we can better understand the complex interactions between herbivorous insects, the plants they live on and the third trophic level members that attack them.