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 http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12715/suppinfo is available for this article.

Elevated atmospheric carbon dioxide concentrations promote ant tending of aphids

“…As anticipated, eCO 2 had a strong positive effect on plant growth; similar increases in biomass have been found in lucerne under eCO 2 (Johnson et al., ; Ryalls et al., , ). Nodulation was unaffected by eCO 2 , which was also the case for this cultivar (Hunter River) when investigated by Johnson et al.…”

“…Amino acid concentrations in the foliage were analysed as these have been shown to be equivalent to the amino acid concentration of phloem sap in lucerne (Ryalls et al., ). Amino acids were analysed by reverse‐phase high‐performance liquid chromatography (HPLC) in an Agilent 1260 Infinity HPLC system after precolumn derivatisation using phenyl isothiocyanate (PITC) as described by Ryalls et al.…”

Silicon‐induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance

“…Acyrthosiphon pisum used in the experiment were taken from an established culture originating from an individual parthenogenetic adult female collected from a lucerne field on campus (Ryalls et al . ). Cultures were maintained on spare lucerne plants (cv.…”

“…Foliar amino acid composition is tightly correlated with phloem amino acids in M. sativa , so analysing foliar material is a reliable proxy for phloem quality (Ryalls et al . ). Amino acid standards within the AAS‐18 (Fluka, Sigma‐Aldrich) reference amino acid mixture were supplemented with asparagine and glutamine (A0884 and G3126, respectively, from Sigma‐Aldrich).…”

Mycorrhizal‐mediated plant–herbivore interactions in a high CO2 world

“…This general increase in the C:N ratio, which implies a reduction in protein, can have significant negative consequences for insects as they are typically limited by protein in their diet (Robinson et al, ; Zvereva & Kozlov, ). However, sucking insects which feed on phloem are sometimes able to compensate for this reduction in sap quality, or even benefit from changes in the phloem amino acid profile (Ryalls et al, ; Sun, Jing, & Ge, ). Still, an increase in the C:N ratio typically translates to a reduction in the nutritional quality of the host plant.…”