Plants typically release large quantities of volatiles in response to herbivory by insects. This benefits the plants by, for instance, attracting the natural enemies of the herbivores. We show that the brown planthopper (BPH) has cleverly turned this around by exploiting herbivore-induced plant volatiles (HIPVs) that provide safe havens for its offspring. BPH females preferentially oviposit on rice plants already infested by the rice striped stem borer (SSB), which are avoided by the egg parasitoid Anagrus nilaparvatae, the most important natural enemy of BPH. Using synthetic versions of volatiles identified from plants infested by BPH and/or SSB, we demonstrate the role of HIPVs in these interactions. Moreover, greenhouse and field cage experiments confirm the adaptiveness of the BPH oviposition strategy, resulting in 80% lower parasitism rates of its eggs. Besides revealing a novel exploitation of HIPVs, these findings may lead to novel control strategies against an exceedingly important rice pest.

Normally, when different species of herbivorous arthropods feed on the same plant this leads to fitness-reducing competition. We found this to be different for two of Asia’s most destructive rice pests, the brown planthopper and the rice striped stem borer. Both insects directly and indirectly benefit from jointly attacking the same host plant. Double infestation improved host plant quality, particularly for the stemborer because the planthopper fully suppresses caterpillar-induced production of proteinase inhibitors. It also reduced the risk of egg parasitism, due to diminished parasitoid attraction. Females of both pests have adapted their oviposition behaviour accordingly. Their strong preference for plants infested by the other species even overrides their avoidance of plants already attacked by conspecifics. This cooperation between herbivores is telling of adaptations resulting from the evolution of plant-insect interactions, and points out mechanistic vulnerabilities that can be targeted to control these major pests.

The area planted with insect-resistant genetically engineered crops expressing Bacillus thuringiensis (Bt) genes has greatly increased in many areas of the world. Given the nearby presence of non-Bt crops (including those planted as refuges) and non-crop habitats, pests targeted by the Bt trait have a choice between Bt and non-Bt crops or weeds, and their host preference may greatly affect insect management and management of pest resistance to Bt proteins. In this study, we examined the oviposition preference of the target pest of Bt rice, Chilo suppressalis, for Bt versus non-Bt rice plants as influenced by previous damage caused by C. suppressalis larvae. The results showed that C. suppressalis females had no oviposition preference for undamaged Bt or non-Bt plants but were repelled by conspecific-damaged plants whether Bt or non-Bt. Consequently, C. suppressalis egg masses were more numerous on Bt plants than on neighbouring non-Bt plants both in greenhouse and in field experiments due to the significantly greater caterpillar damage on non-Bt plants. We also found evidence of poorer performance of C. suppressalis larvae on conspecific-damaged rice plants when compared with undamaged plants. GC-MS analyses showed that larval damage induced the release of volatiles that repelled mated C. suppressalis females in wind tunnel experiments. These findings suggest that Bt rice could act as a dead-end trap crop for C. suppressalis and thereby protect adjacent non-Bt rice plants. The results also indicate that the oviposition behaviour of target pest females should be considered in the development of Bt resistance management strategies.