The impacts of climate change and belowground herbivory on aphids via primary metabolites

Global climate and atmospheric change (summarised as climate change for brevity) may alter patterns of crop damage by insect herbivores, but little is known about how multiple climate change factors, acting in tandem, shape such interactions. Crucially, the specific plant-mediated mechanisms underpinning these effects remain largely unknown. Moreover, research into the effects of climate change on leguminous plant species, which have the ability to fix atmospheric nitrogen (N2) via their association with root nodule-dwelling rhizobial bacteria, and their associated insect herbivores, is surprisingly scarce considering their increasing importance in terrestrial ecosystems worldwide. Using a model legume, lucerne, otherwise known as alfalfa, Medicago sativa (Fabaceae), and a model pest species, the pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae), this work addresses how predicted changes in carbon dioxide (CO2) concentrations, temperature and rainfall patterns as well as interactions with other organisms, including the root-feeding weevil Sitona discoideus (Coleoptera: Curculionidae), might shape legume-feeding aphid populations in the future. Recent literature on the impacts of climate change on aphids and the biology and trophic interactions of lucerne aphids specifically were synthesised in chapters one and two, respectively. These chapters highlighted the importance of the interactions between multiple abiotic and biotic variables in shaping aphid population dynamics. Empirical research chapters three to six, using up to five lucerne genotypes (i.e. cultivars) in glasshouse and field experiments, addressed how A. pisum responded to the isolated and combined effects of climate change and root herbivory. In particular, chapter three determined the effects of elevated temperatures (eT) and elevated atmospheric CO2 concentrations (eCO2) on root-feeding S. discoideus larvae and their interaction with A. pisum. Chapter four addressed whether the effects of eT, eCO2 and simulated root damage on aphids could be explained by changes in plant amino acid concentrations. Chapter five built on the mechanistic findings from chapter four to determine whether specific groups of amino acids were responsible for driving the effects of eT and eCO2 on aphid fecundity, longevity and intrinsic rate of increase (rm). Chapter six extended this research to the field to determine the plant-mediated effects of water stress and root herbivory on aphids in a mixed grass–legume system. Lucerne demonstrated an over compensatory growth response to root herbivory by S. discoideus larvae by increasing net root biomass and nodulation by 31% and 45%, respectively. eT negated the positive effects of eCO2 on weevil larval development, as well as on a number of lucerne characteristics (e.g. nodulation and amino acid concentrations) and aphid performance parameters (e.g. population growth, fecundity and rm). Root herbivory by S. discoideus negatively impacted aphids in general, although effects were dependent on feeding duration and herbivore arrival sequence (i.e. whether aphids fed on the plant before or after root herbivory). While drought negatively impacted aphid abundance, potentially via reduced phloem turgor and sap viscosity, the effects of eT, eCO2 and root herbivory on aphids were often driven by concentrations of specific amino acid groups. Nitrogen (N) leached from lacerated lucerne root nodules by S. discoideus led to increased concentrations of N in a neighbouring grass, Phalaris aquatica (Poaceae), with knock-on effects on plant competition and community dynamics. The opposing effects of eT and eCO2 on plant characteristics and both aboveground and belowground herbivores demonstrates the importance of combining trophic complexity with multiple climatic factors as a means of gaining realistic insights into how insect and plant communities will respond under future conditions. Identifying the specific amino acid changes underpinning aphid responses to climate change and root herbivory offers the potential for breeding aphid resistance traits into lucerne cultivars and informing adaptation strategies against future threats. Changes in precipitation patterns and plant-mediated indirect aboveground–belowground herbivore interactions can alter the outcome of competition between N-fixing legumes and non-N-fixing grasses, with important implications for plant community structure and productivity. Avenues for future research are explored and other causal agents of changes in aphid performance are discussed, which may further elucidate the mechanisms underpinning climate change and belowground herbivory impacts on aphid pests