A polyphagous chewing herbivore induces positive plant-soil feedback of two legumes in soil with prolonged drought legacies

Plant-soil feedbacks (PSFs) occur when a plant species modifies soil physicochemical and biological properties in ways that affect growth of a plant subsequently grown in the same soil. PSFs are influenced by both herbivory, and climatic conditions, but it is unclear how foliar herbivory and climate change interact to modify PSFs. A PSF experiment was conducted to assess the effect of foliar herbivory on Medicago sativa and Trifolium repens, when grown in monoculture and mixture. PSFs were assessed in soils from a field experiment simulating ambient rainfall and prolonged drought (50% reduction) for six years. All soils were sterilized and then re-inoculated to create the respective biological rainfall legacy treatments including a sterile control. The cotton bollworm, Helicoverpa armigera, was used to induce herbivore treatments. Neither legume showed significant PSFs in the absence of herbivory. However, foliar herbivory induced positive PSFs for legumes in soil with drought legacies, and negative to neutral PSFs in soil with ambient rainfall legacies, when grown in monocultures. By contrast, herbivory induced strong positive PSFs in soils with ambient rainfall legacies, and negative PSFs in soils with drought legacies, in mixtures, possibly due to competition for space and resources. Herbivory-induced PSFs in soils with prolonged drought legacies appeared to be related to differences in leaf N concentration and rhizobia colonization likely due to effects on herbivore-induced systemic resistance. Our results indicate that foliar herbivores alter plant species co-existence and community dynamics under future climate change scenarios through changes in PSFs.