Beyond Predation: The Zoophytophagous Predator Macrolophus pygmaeus Induces Tomato Resistance against Spider Mites

Abstract

Many predatory insects that prey on herbivores also feed on the plant, but it is unknown whether plants affect the performance of herbivores by responding to this phytophagy with defence induction. We investigate whether the prior presence of the omnivorous predator Macrolophus pygmaeus (Rambur) on tomato plants affects plant resistance against two different herbivore species. Besides plant-mediated effects of M. pygmaeus on herbivore performance, we examined whether a plant defence trait that is known to be inducible by herbivory, proteinase inhibitors (PI), may also be activated in response to the interactions of this predator with the tomato plant. We show that exposing tomato plants to the omnivorous predator M. pygmaeus reduced performance of a subsequently infesting herbivore, the two-spotted spider mite Tetranychus urticae Koch, but not of the greenhouse whitefly Trialeurodes vaporariorum (Westwood). The spider-mite infested tomato plants experience a lower herbivore load, i.e., number of eggs deposited and individuals present, when previously exposed to the zoophytophagous predator. This effect is not restricted to the exposed leaf and persists on exposed plants for at least two weeks after the removal of the predators. The decreased performance of spider mites as a result of prior exposure of the plant to M. pygmaeus is accompanied by a locally and systemically increased accumulation of transcripts and activity of proteinase inhibitors that are known to be involved in plant defence. Our results demonstrate that zoophytophagous predators can induce plant defence responses and reduce herbivore performance. Hence, the suppression of populations of certain herbivores via consumption may be strengthened by the induction of plant defences by zoophytophagous predators.