Plants possess various inducible defences that result in synthesis of specialized metabolites in response to herbivory, which can interfere with the performance of herbivores of the same and other species. Much less is known of the effects of plant feeding by omnivores. We found that previous feeding of the omnivorous predator Macrolophus pygmaeus on sweet pepper plants significantly reduced reproduction of the two-spotted spider mite Tetranychus urticae and western flower thrips Frankliniella occidentalis on the same plants, also on leaves that had not been exposed to the omnivore. In contrast, no effect was found on the reproduction of the green peach aphid Myzus persicae. Juvenile survival and developmental time of T. urticae and M. persicae, and larval survival of F. occidentalis were not affected by plant feeding by M. pygmaeus. Larvae of F. occidentalis feeding on leaves previously exposed to M. pygmaeus required longer to develop into adults. Defence-related plant hormones were produced locally and systemically after exposure to M. pygmaeus. The concentrations of 12-oxo-phytodienoic acid and jasmonic acid–isoleucine in the attacked leaves were significantly higher than in the corresponding leaves on the uninfested plants, and jasmonic acid concentrations showed the same trend, suggesting that jasmonic-acid-related defence pathways were activated. In contrast, similar concentrations of salicylic acid were found in the attacked leaves of M. pygmaeus-infested plants and uninfested plants. Our results show that plant feeding by omnivorous predators decreases the performance of herbivores, suggesting that it induces plant defences.Electronic supplementary materialThe online version of this article (10.1007/s00442-017-4000-7) contains supplementary material, which is available to authorized users.
Herbivorous arthropods use various cues to choose suitable host plants. We investigated whether three species of herbivores use cues associated with their omnivorous predator Macrolophus pygmaeus to select host plants. Earlier, we found that this omnivore induces plant defences which decreased the performance of two of the herbivores, i.e. the spider mite Tetranychus urticae and the western flower thrips Frankliniella occidentalis, whereas the green peach aphid Myzus persicae was not affected. Hence, the spider mite and thrips were expected to avoid plants that were previously exposed to M. pygmaeus because of their lower quality, and the aphid was not expected to avoid exposed plants because they were of equal quality as unexposed plants. However, the cues left behind by M. pygmaeus may also be indicative of predation risk, in which case all three herbivores were expected to avoid exposed plants. Spider mites and western flower thrips preferred clean plants over plants that had previously been exposed to M. pygmaeus, but no longer harboured this omnivore. Aphids showed no preference, in agreement with their performance, but not in agreement with reducing predation risk. We furthermore showed that the preference of spider mites and thrips for clean plants increased through time. Higher proportions of aphids left plants previously exposed to M. pygmaeus than clean plants through time. Hence, omnivorous predators can decrease herbivore densities on plants not only by killing them but also by indirectly affecting herbivore host plant selection.
Several biological control agents of the hemipteran insect families Miridae, Anthocoridae and Pentatomidae, as well as mites of the family Phytoseiidae are known as zoophytophagous predators, a subset of omnivores, which are primarily predaceous but also feed on plants. It has been recently demonstrated that zoophytophagous predators are capable of inducing defenses in plants through their phytophagy. Despite the vast fundamental knowledge on plant defense mechanisms in response to herbivores, our understanding of defense induction by zoophytophagous predators and applied implications is relatively poor. In this review, we present the physiological basis of the defense mechanisms that these predators activate in plants. Current knowledge on zoophytophagous predator-induced plant defenses is summarized by groups and species for the predators of economic importance. Within each group, feeding habits and the effects of their induced-plant defenses on pests and natural enemies are detailed. Also, the ecological implications of how the induction of defenses mediated by zoophytophagous predators can interact with other plant interactors such as beneficial soil microorganisms and plant viruses are addressed. Based on the above, we propose three approaches to exploit zoophytophagous predator-induced defenses in crop protection and to guide future research. These include using predators as vaccination agents, employing biotechnological approaches, as well as applying elicitors to elicit/mimic predator-induced defenses.
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