Herbivory of a biocontrol agent on a native plant causes an indirect trait-mediated non-target effect on a native insect

Identifying food web linkages between biocontrol agents of invasive plants and native species is crucial for predicting indirect non-target effects. Biocontrol insects can integrate into food webs within recipient habitats and influence native insects through apparent competition (altering shared natural enemies) or density-mediated exploitation competition (changing density of native plants). However, whether and how trait-mediated exploitation competition (modifying native plant chemicals and volatiles profiles) can produce indirect non-target effects remains largely overlooked, despite plant phenotypic responses to insect herbivory being common and widely documented. The flea beetle Agasicles hygrophila was introduced into China for management of alligator weed Alternanthera philoxeroides, but it also attacks the native congener sessile joyweed Alternanthera sessilis, which may cause indirect non-target effects on the native tortoise beetle Cassida piperata that also feeds on sessile joyweed. Here, we examined the relationships among abundances of the flea beetle and tortoise beetle, and coverage of sessile joyweed in the field. Then, we investigated the impact of flea beetle herbivory on tortoise beetle development and oviposition, as well as on sessile joyweed primary metabolites and leaf volatiles. Tortoise beetle abundance was not related to sessile joyweed coverage, but they were less abundant on plants with more flea beetles in the field survey, and produced fewer offspring on plants with more prior flea beetle damage in the field cage experiment. Tortoise beetle development was inhibited by prior flea beetle herbivory in bioassays in enemy-free conditions and they preferred to oviposit on sessile joyweed that had experienced little or no flea beetle damage. Flea beetle herbivory decreased sessile joyweed foliar glucose and protein, and substantially changed its leaf volatile blend. Synthesis. Our results show that the flea beetle has major indirect non-target effects on the tortoise beetle through trait-mediated exploitation competition, rather than apparent competition or density-mediated exploitation competition. Our results demonstrate a new example for indirect non-target effects of biocontrol agents. Furthermore, our results indicate that minor brief negative impacts of biocontrol agents on non-target plants might propagate to higher trophic levels and such negative impacts can strengthen with increasing intensity of the direct non-target effect.