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.

Zoophytophagous mirids provide pest control by inducing direct defences, antixenosis and attraction to parasitoids in sweet pepper plants

“…VOCs inside the box might be mixed up, and hence differences in preference may be attributed to the contact and feeding upon the plants with high content on JA, which can be a feeding deterrent for arthropod pests . Macrolophus pygmaeus‐ punctured tomato plants were observed to increase locally and systematically the accumulation of transcripts and the activity of protease inhibitors that are known to be involved in plant responses, resulting in detrimental effects on the life history traits of of the two‐spotted spider mite Tetranychus urticae (Koch) (Acari: Tetranychidae) . In the case of sweet pepper , further research should be carried out to elucidate these direct defence effects on subsequent herbivore development and reproduction.…”

“…Tomato plants exposed to M. pygmaeus with all individuals subsequently removed, as in this study, were previously described to remain vaccinated for up to 2 weeks . The defence response induced by N. tenius in sweet pepper was demonstrated to remain active for 7 to 14 days.…”

“…This flexibility in their behaviour increases survival rates by taking advantage of plant resources when prey is either less abundant or completely absent . As in herbivores, the phytophagous behaviour of mirid predators may also induce indirect plant defences . It is well known that plants can respond to the damage induced by phytophagous insects, with this response involving several signal transduction pathways that are mediated by phytohormones.…”

Induced plant defences in biological control of arthropod pests: a double‐edged sword

“…Plant responses induced by herbivores, omnivores, pathogens or endophytes can affect food web interactions in various ways. For example, a pre‐infestation by whiteflies reduced the response of specialist predatory mites to spider mites, which can disrupt biological control (A), whereas pre‐infestation by omnivorous predatory bugs decreased oviposition rates of spider mites, which may enhance biological control (B). Induced plant responses may also alter the feeding behaviour of omnivorous predators.…”

“…zoophytophagous predators, beneficial microbes) may be mediated by interacting plant signalling pathways. For example, plant susceptibility to a pathogen may increase in the presence of a zoophytophagous predator as a result of antagonism between salicylic acid and jasmonic acid mediated plant responses to the pathogen and the predator, respectively . To enhance biological control, it is therefore important to identify and apply biological control agents that not only can cope with the induction of defences by pests but also can manipulate these in favour of plant productivity.…”