Heavy metal pollution enhances herbivore resistance of male poplars over females through modifying volatile-mediated tritrophic interactions.

Environmental stress can disrupt multi-trophic interactions between plants and associated insects through modifying plant volatile organic compound (VOC) emissions. Dioecious plant species exhibit sexual dimorphism in metal accumulation and tolerance between males and females under heavy metal stress. However, whether these differences lead to sex-specific variations in VOC emissions and herbivore resistance across multi-trophic levels remains unclear. In this study, we used full-sibs of female and male poplars to investigate how soil cadmium (Cd) stress and plant sex influence emissions of constitutive plant volatiles (CPVs) and herbivore-induced plant volatiles (HIPVs) as well as associated multi-trophic interactions. We showed that Cd exposure qualitatively and quatitatively affected CPV and HIPV emissions in both sexes, particularly in males, which emitted less CPVs but more HIPVs than females under Cd stress. Insect bioassays demonstrated that Cd-exposed males were more effective at deterring generalist and specialist herbivores, while becoming more attractive to parasitic wasps than Cd-exposed females. We identified 3-methylbutyronitrile as the key compound driving enhanced repellency against herbivorous insects, while methyl salicylate was primarily responsible for increased attractiveness to parasitic wasps. These results suggest that male plants may be better suited for phytoremediation in metal-contaminated areas amid escalating global pollution and herbivory pressure.