Prolonged drought legacies influence the performance of foliar herbivores on legumes through shifts in plant–soil biotic interactions

Drought may impact plant–soil biotic interactions in ways that modify aboveground herbivore performance, but the outcomes of such biotic interactions under future climate are not yet clear. We performed a growth chamber experiment to assess how long-term, drought-driven changes in belowground communities influence plant growth and herbivore performance using a plant–soil feedback experimental framework. We focussed on two common pasture legumes—lucerne, Medicago sativa L., and white clover, Trifolium repens L. (both Fabaceae)—and foliar herbivores—cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), and two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae). Soil was collected from a field facility where rainfall had been manipulated for 6 years, focussing on treatments representing ambient rainfall and prolonged drought (50% reduction relative to ambient), to consider the effects of biological legacies mediated by the prolonged drought. All soils were sterilized and re-inoculated to establish the respective home (i.e. where a given plant is cultivated in its own soil) and away (i.e. where a given plant is cultivated in another species' soil) treatments in addition to a sterile control. We found that the relative growth rate (RGR) and relative consumption of larvae were significantly lower on lucerne grown in soil with ambient rainfall legacies conditioned by white clover. Conversely, the RGR of insect larvae was lower on white clover grown in soil with prolonged drought legacies conditioned by lucerne. Two-spotted spider mite populations and area damage (mm²) were significantly reduced on white clover grown in lucerne-conditioned soil in drought legacies. The higher number of nodules found on white clover in lucerne-conditioned soil suggests that root–rhizobia associations may have reduced foliar herbivore performance. Our study provides evidence that foliar herbivores are affected by plant–soil biotic interactions and that prolonged drought may influence aboveground–belowground linkages with potential broader ecosystem impacts.