Soil cadmium pollution elicits sex-specific plant volatile emissions in response to insect herbivory in eastern cottonwood Populus deltoides.

Abstract

Soil heavy metal pollution is a major abiotic stressor frequently encountered by plants in conjunction with other biotic stresses like insect herbivory. Yet, it remains largely unexplored how soil metal pollution and insect herbivory act together to influence emissions of plant volatile organic compounds (VOCs), which mediate multiple ecological functions and play crucial roles in atmospheric processes. Here, we assessed the individual and combined effects of soil cadium (Cd) pollution and insect herbivory by Clostera anachoreta on VOC emissions from the seedlings of eastern cottonwood Populus deltoides, and whether these effects depend on plant sex. We found that plant sex notably influenced VOC emission and altered blend compositions, with male seedlings emitting higher amounts of monoterpenes, sesquiterpenes, homoterpenes and green leaf volatiles (GLVs) than females. Soil Cd exposure significantly increased emissions of monoterpenes, GLVs, and nitrogenous VOCs in males but not in females. Comparatively, larval feeding exerted the strongest effects on VOC emissions and their composition, albeit to varying extent between males and females, and among different VOC classes. Importantly, Cd exposure amplified herbivore-induced VOC emissions in males. For instance, under both Cd and herbivory conditions, male seedlings showed a 68.1-fold increase in nitrogenous VOC emissions, almost twice the combined effects of Cd (8.7-fold) and herbivory (26.3-fold). Taken together, these results suggest that soil metal pollution can boost herbivore-induced VOC emissions in a sex-specific manner, with potential implications for ecological interactions and atmospheric processes.