Herbivore-induced plant volatiles, not natural enemies, mediate a positive indirect interaction between insect herbivores

Many insect herbivores engage in apparent competition whereby two species interact through shared natural enemies. Upon insect attack, plants release volatile blends that attract natural enemies, but whether these volatiles mediate apparent competition between herbivores is not yet known. We investigate the role of volatiles that are emitted by bean plants upon infestation by Acyrthosiphon pisum aphids on the population dynamics and fitness of Sitobion avenae aphids, and on wheat phloem sap metabolites. In a field experiment, the dynamics of S. avenae aphids on wheat were studied by crossing two treatments: exposure of aphid colonies to A. pisum-induced bean volatiles and exclusion of natural enemies. Glasshouse experiments and analyses of primary metabolites in wheat phloem exudates were performed to better understand the results from the field experiment. In the field, bean volatiles did not affect S. avenae dynamics or survival when aphids were exposed to natural enemies. When protected from them, however, volatiles led to larger aphid colonies. In agreement with this observation, in glasshouse experiments, aphid-induced bean volatiles increased the survival of S. avenae aphids on wheat plants, but not on an artificial diet. This suggests that volatiles may benefit S. avenae colonies via metabolic changes in wheat plants, although we did not find any effect on wheat phloem exudate composition. We report a potential case of associational susceptibility whereby plant volatiles weaken the defences of receiving plants, thus leading to increased herbivore performance.