Root herbivory affects oviposition and feeding behavior of a foliar herbivore

Performance and distribution of phytophagous insects are driven by direct and indirect competitive interactions. Plant-feeding arthropods have been shown to interact indirectly through the plants' response to herbivory. In the case of systemically induced plant responses, this interaction extends to herbivores inhabiting different parts of a plant, for example, above- and belowground herbivores. Plant-induced responses elicited by root herbivores have been shown to affect feeding and development of aboveground herbivores. However, little is known about how root feeding affects host choice behavior of aboveground herbivores, including both adult oviposition behavior and larval host acceptance. Here, we report that root feeding by the wireworm, Agriotes lineatus, influences oviposition decisions and larval leaving rate of an aboveground herbivore, Spodoptera littoralis. In choice experiments, female S. littoralis deposited more and larger egg batches on undamaged plants when compared with wireworm-infested plants. In a larval feeding experiment, a higher percentage S. littoralis larvae moved away from the wireworm-infested plant onto a neighboring undamaged plant as compared with larvae feeding on previously undamaged plants. Larvae did not show an increased tendency to leave when feeding on plants previously exposed to conspecific larvae. Our results show that indirect interactions between belowground and aboveground herbivores extend to behavioral avoidance, both in terms of oviposition and larval feeding decisions. This allows the foliar herbivore to avoid systemic plant responses elicited by root herbivory, which likely represent reduced food quality and increased apparency toward natural enemies.