Earthworms suppress thrips attack on tomato plants by concomitantly modulating soil properties and plant chemistry

Abstract

How plants cope with herbivore attack is partially modulated by the biotic and abiotic environment where the plant lives. For instance, theory predicts that soil fertility should drive patterns of plant resource allocation and defensive strategies. Earthworms, by their burrowing and casting activities, modify soil physicochemical properties and soil fertility. Therefore, earthworm-mediated changes in soil properties could alter plant physiology, plant nutritional quality, and ultimately, plant resistance against insect herbivores. We tested this hypothesis by measuring the combinatorial effects of two earthworm species, an epi-endogeic earthworm (Amynthas corticis) and an endo-anecic earthworm (Metaphire guillelmi), on soil properties, tomato plants’ physiological traits and plant resistance against the western flower thrips (Frankliniella occidentalis). We found that A. corticis alone increased plant resistance more than M. guillelmi alone or the combination of two species. The increased plant resistance was associated with a significant increase in the defence-related phytohormone jasmonic acid and the production of phenolic compounds. Furthermore, we observed a strong link between earthworm-mediated changes in soil properties and plant eco-physiological traits. Our results thus build toward a better predictive model of how earthworms can simultaneously influence soil parameters, plant productivity and resistance against herbivore pests.