Leaf-chewing but not sap-feeding herbivores create soil legacies that shape plant resistance through trait-mediated, guild-specific effects in Baccharis salicifolia

Abstract

Herbivory can affect the soil microbiome, creating legacies that affect plant resistance, but how these effects vary by feeding guild and the plant traits involved remain underexplored. We tested how soil legacies created by a leaf-chewing caterpillar (Spodoptera exigua) and a sap-feeding aphid (Aphis gossypii) influence resistance in Baccharis salicifolia by evaluating changes in plant traits and soil microbial diversity. We conditioned soil with three herbivory treatments on B. salicifolia: caterpillar herbivory, aphid herbivory or control (no herbivory). Then, we grew new plants in sterile soil inoculated with 10% conditioned soil from each treatment and conducted resistance bioassays, measured plant nutritional and defence traits and analysed microbial diversity. Caterpillar, but not aphid herbivory, created legacies that affected resistance to both herbivores in opposite directions: plants in caterpillar-conditioned soil had 16% smaller aphid colonies than plants in control soil, and a 76% increase in caterpillar performance relative to aphid-conditioned soil, suggesting guild-specific trade-offs in resistance. These plants also showed a 12% higher carbon-to-nitrogen ratio than plants in control soil, mediating resistance to the aphid but not to the caterpillar. Herbivory did not affect microbial taxonomic diversity, suggesting shifts in microbiome biomass or function underlie the observed effects. Our findings highlight that herbivory-induced soil legacies are guild-specific and can alter plant resistance via trait-mediated pathways, underscoring the importance of considering herbivore identity when evaluating above–below-ground feedbacks. Read the free Plain Language Summary for this article on the Journal blog.