Ant-mealybug mutualism modulates the performance of co-occurring herbivores

Mutualism between ants and honeydew producing hemipterans has been extensively studied. However, little is known on how ant-hemipteran mutualism impacts the co-occurring herbivores, which in turn affect the mutual relationship in ecosystems. Herein, we investigated the effect of ant-mealybug mutualism on the oviposition preference and spatial distribution of cotton leaf roller Sylepta derogata, a polyphagous herbivore, and in Apantetes derogatae performance, a larvae parasitoid of S. derogata. Leaf rollers constructed shelters for mealybugs to prevent them from enemy attack and preferred to lay eggs on plants with ant-mealybug mutualism. Egg abundance on mutualism-present plants was higher than on mutualism-absent plants. Leaf roller parasitoid A. derogatae showed higher parasitism on mutualism-absent plants. No obvious change in leaf roller egg abundance was observed when A. derogatae was excluded, suggesting that the parasitic pressure can also regulate the oviposition behavior of S. derogate. Apantetes derogatae showed higher aggressiveness in parasitizing leaf roller larvae at the absence of the mutualism. There was a definite correlation between leaf roller egg abundance and the number of patrolling ants on plants. Without ant-mealybug mutualism, S. derogata eggs showed a significantly aggregated distribution pattern, but a uniform distribution pattern was observed when the mutualism was present. Ant workers showed a consistently uniform distribution on plants. The results reveal a novel mediation effect of ant-mealybug association on the composition and structure of food webs in cotton field, which may contribute to a better understanding of the cascading effects of ant-hemipteran mutualism on other niche-related species in ecosystem.