Whitefly aggregation on tomato is mediated by feeding-induced changes in plant metabolites that influence the behaviour and performance of conspecifics

1. Leaf damage caused by herbivore feeding often triggers induced resistance in plants. However, some herbivores can take advantage of the resulting metabolic changes in host plants and may even manipulate plant resistance, leading to a phenomenon known as induced susceptibility. 2. Previous work has shown that feeding by the whitefly Bemisia tabaci can reduce tomato Solanum lycopersicum resistance and that whiteflies tended to aggregate on infested plants. However, metabolomic changes in the plant and associated whitefly behavioural responses underlying this phenomenon remain poorly understood. We, therefore, investigated how B. tabaci infestation affects host physiology and the preference and performance of conspecific feeders. 3. Bemisia tabaci adults exhibited consistent behavioural preferences for plants that experienced actual and simulated herbivory by conspecifics (consistent with observed effects on whitefly performance), but not for plants that were only mechanically wounded. Leaf volatiles and extracts of B. tabaci-infested plants showed altered terpenoid and flavonoid profiles. Manipulative behavioural experiments indicated that suppression of the monoterpenes alpha-phellandrene and alpha-terpinene and of flavonoids by B. tabaci infestation influenced the foraging and oviposition preferences of conspecifics. 4. These findings document key metabolic changes in plants exhibiting induced susceptibility and demonstrate their role in mediating herbivore foraging behaviour and aggregation on susceptible plants, thereby providing new insight into a relatively unexplored aspect of plant-herbivore interactions.