Non-host plant odors influence the tritrophic interaction between tomato, its foliar herbivore Tuta absoluta and mirid predator Nesidiocoris tenuis

Abstract

The tomato leafminer, Tuta absoluta is a destructive invasive pest of cultivated tomato and other Solanaceae plants, with yield losses of 80-100%. Mirid predators are key natural enemies of T. absoluta, but they also feed on host plants in the absence of their prey. Management of T. absoluta is a challenge due to its high biotic potential, resistance to many insecticides and the absence of sufficiently adapted auxiliary fauna in its new dispersion zones. Olfaction plays an important role in the tritrophic interaction between tomato, its herbivore pest T. absoluta and its mirid predators, which can be influenced by non-host plant odors. However, how non-host odours shape this interaction is poorly understood. Previously, we had demonstrated belowground crop protection properties of certain Asteraceae plants against the root-knot nematode Meloidogyne incognita, pest of tomato and other Solanaceae plants. Additionally, Asteraceae plants impact negatively on feeding behavior of above-ground pests of Solanaceae plants, including the greenhouse whitefly (Trialeurodes vaporariorum) and green peach aphid (Myzus persicae). Here, we tested the hypothesis that foliar volatiles from some of these non-host Asteraceae plants can influence the tomato-T. absoluta-mirid predator tritrophic interaction. In olfactometer assays, T. absoluta females were attracted to volatiles of the Solanaceae host plants tomato and giant nightshade but avoided volatiles of the Asteraceae plants, blackjack and marigold, and the positive control, wild tomato, when tested alone or in combination with the host plants. Coupled gas chromatography-mass spectrometry analysis showed that host and non-host plants varied in their emission of volatiles, mainly monoterpenes and sesquiterpenes. Random forest analysis combined with behavioral assays identified monoterpenes as the host plant attractive blend to T. absoluta and its mirid predator, with sesquiterpenes identified as the non-host plant repellent blend against T. absoluta. Contrastingly, the mirid predator was indifferent to the non-host plant repellent sesquiterpenes. Our findings indicate that terpenes influence the tomato-T. absoluta-mirid predator tritrophic interaction. Further, our results emphasize the importance of studying crop protection from a holistic approach to identify companion crops that serve multi-functional roles.