Elevated atmospheric carbon dioxide impairs the performance of root-feeding vine weevils by modifying root growth and secondary metabolites

Predicting how insect crop pests will respond to global climate change is an important part of increasing crop production for future food security, and will increasingly rely on empirically based evidence. The effects of atmospheric composition, especially elevated carbon dioxide (eCO2), on insect herbivores have been well studied, but this research has focussed almost exclusively on aboveground insects. However, responses of root-feeding insects to eCO2 are unlikely to mirror these trends because of fundamental differences between aboveground and belowground habitats. Moreover, changes in secondary metabolites and defensive responses to insect attack under eCO2 conditions are largely unexplored for root herbivore interactions. This study investigated how eCO2 (700 μmol mol−1) affected a root-feeding herbivore via changes to plant growth and concentrations of carbon (C), nitrogen (N) and phenolics. This study used the root-feeding vine weevil, Otiorhynchus sulcatus and the perennial crop, Ribes nigrum. Weevil populations decreased by 33% and body mass decreased by 23% (from 7.2 to 5.4 mg) in eCO2. Root biomass decreased by 16% in eCO2, which was strongly correlated with weevil performance. While root N concentrations fell by 8%, there were no significant effects of eCO2 on root C and N concentrations. Weevils caused a sink in plants, resulting in 8-12% decreases in leaf C concentration following herbivory. There was an interactive effect of CO2 and root herbivory on root phenolic concentrations, whereby weevils induced an increase at ambient CO2, suggestive of defensive response, but caused a decrease under eCO2. Contrary to predictions, there was a positive relationship between root phenolics and weevil performance. We conclude that impaired root-growth underpinned the negative effects of eCO2 on vine weevils and speculate that the plant's failure to mount a defensive response at eCO2 may have intensified these negative effects.