The Roles of Semiochemical Perception and Surface Compounds in a Pharmacophagous Sawfly

Pharmacophagy is a fascinating phenomenon, where animals take up specialized plant metabolites unrelated to nutrition, but with benefits for, for example, defense and mating. Adults of the turnip sawfly Athalia rosae engage in pharmacophagy of neo-clerodane diterpenoids (clerodanoids) from the bugleweed Ajuga reptans, but can also take up metabolites sequestered from the plant and modified from conspecifics. Here, we investigated the perception of odors associated with pharmacophagy from long and close distances in bioassays, using leaves and washes of surface compounds, mainly cuticular hydrocarbons, from female and male adults of different pharmacophagy treatments. Extracts were analyzed by GC-MS to test whether the treatment affected the cuticular surface composition. We hypothesized that sawflies perceive compounds related to pharmacophagy at close distances, that sexes differ in surface compound profiles, and that contact with A. reptans leaves or previously A. reptans-exposed conspecifics alters the cuticular hydrocarbon composition. Our results demonstrate that sawflies indeed perceive both plant leaves and surface washes from previously A. reptans-exposed conspecifics at close distance. We characterized the major cuticular hydrocarbons of A. rosae and uncovered sexual dimorphism in surface compound abundance, but found no pharmacophagy-induced changes in the surface compound composition. We discuss that other compounds than cuticular hydrocarbons are likely involved in the observed effects. Our research provides insights into how specialized plant metabolites may drive the evolution of the insect sensory behavior and into the complexity of insect chemical communication.