Soil lead pollution alters plant chemical profiles and herbivore responses across feeding guilds

Soil pollution by metal contaminants threatens ecosystems through accumulation in plants and disruption of trophic interactions. However, how metal contaminants alter plant chemistry, including volatile and non-volatile metabolites, and whether these changes affect herbivores from distinct feeding guilds, have received little attention. We investigated how soil contamination with lead (Pb; 180 mg kg -1 , the agricultural investigation value under Brazilian regulation), a relevant contaminant in agroecosystems, influences the chemical defenses of kale plants ( Brassica oleracea L. var. acephala ) and their interactions with the leaf-chewing Ascia monuste orseis (Godart) (Lepidoptera: Pieridae) and the phloem-feeding aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae). Herbivore survival, performance, and host selection were assessed on Pb-contaminated and control plants, together with targeted and untargeted metabolic responses and volatile organic compound (VOC) emissions. Pb contamination reduced aphid survival and fecundity in the first generation, while lepidopteran performance remained unaffected despite Pb accumulation in adults. Both herbivore species showed reduced preference for Pb-contaminated plants, indicating that Pb-induced changes in plant traits influence host selection. Consistently, Pb contamination altered the VOC blend emitted by kale, decreasing β-myrcene levels and increasing limonene emissions. Metabolic responses were guild-dependent: Pb combined with aphid feeding significantly increased local amino acid accumulation while attenuating the aphid-induced accumulation of JA, JA-Ile, and SA, whereas caterpillar feeding on contaminated plants tended to amplify jasmonate induction, although this effect was not statistically significant. Untargeted metabolite profiling confirmed that herbivory type was the primary driver of metabolic variation, whereas Pb effects were restricted to specific hormonal and amino acid responses to herbivory. Together, these findings show that Pb contamination modulates plant responses to herbivory in a guild-dependent manner, highlighting the ecological significance of pollutant-driven changes in soil-plant-insect systems.