Herbivore Identity and Species Richness Shape Fruit Chemical and Quality Responses to Foliar Herbivory

The cascading consequences of foliar herbivory on fruit chemistry and quality remain relatively underexplored, with most existing studies focusing on the effects of only one or two attackers. In this study, we examine how increasing herbivore species richness during foliar herbivory alters strawberry (Fragaria × ananassa Duch) fruit quality and phenolic chemistry. We conducted a greenhouse experiment with single species feeding and different combinations of feeding by three generalist lepidopteran species: Spodoptera frugiperda, Heliothis virescens, Helicoverpa zea. Species fed on leaves for 72 h as fruits ripened, and fully ripe fruits were harvested 72 h after feeding for quality and phenolic analysis. We tested three hypotheses: (1) foliar herbivory induces complex changes in fruit traits, including specialized chemistry (phenolic content, richness, and composition) and quality (fruit weight, sugar content, and pH); (2) these changes may vary depending on the species of foliar herbivore; and (3) attack from multiple herbivores leads to more intense and complex changes, including higher diversity of specialized metabolites. We found that foliar herbivory, regardless of herbivore identity, decreased fruit pH and increased phenolic richness. Other effects of herbivory varied depending on the identity of the herbivore. Notably, Spodoptera frugiperda induced greater changes in soluble sugar content and flavanol, flavan-3-ols, and benzoic acid content and richness. We observed a directional decrease in average fruit weight in response to increased species richness during foliar herbivory. Synthesis: Plant responses to foliar herbivory are highly variable and context dependent. We found that foliar herbivory by combinations of three generalist species induced distinct changes in fruit chemistry and quality. This study provides a key insight into the complexity of plant-herbivore interactions, with implications for broader ecosystem function.