Climate and atmospheric change impacts on sap‐feeding herbivores: a mechanistic explanation based on functional groups of primary metabolites

Abstract

Summary Global climate and atmospheric change are widely predicted to affect many ecosystems. Herbivorous insects account for 25% of the planet's species so their responses to environmental change are pivotal to how future ecosystems will function. Atmospheric change affects feeding guilds differently, however, with sap‐feeding herbivores consistently identified as net beneficiaries of predicted increases in atmospheric carbon dioxide concentrations (eCO2). The mechanistic basis for these effects remains largely unknown, and our understanding about how multiple environmental changes, acting in tandem, shape plant–insect interactions is incomplete. This study investigated how increases in temperature (eT) and eCO2 affected the performance of the pea aphid (Acyrthosiphon pisum) via changes in amino acid concentrations in the model legume, lucerne (Medicago sativa). Aphid performance increased under eCO2 at ambient temperatures, whereby aphid fecundity, longevity, colonization success and rm increased by 42%, 30%, 25% and 21%, respectively. eT negated the positive effects of eCO2 on both fecundity and rm, however, and performance was similar to when aphids were reared at ambient CO2. We identified discrete functional groups of amino acids that underpinned the effects of climate and atmospheric change, in addition to plant genotype, on aphid performance. Effects of eT and eCO2 held true across five M. sativa genotypes, demonstrating the generality of their effects. Combining this knowledge with amino acid profiles of existing cultivars raises the possibility of predicting future susceptibility to aphids and preventing outbreaks of a global pest. Moreover, environmentally induced changes in the nutritional ecology of aphids have the capacity to change life‐history strategies of aphids and their direct and indirect interactions with many other organisms, including mutualists and antagonists. A Lay Summary is available for this article.