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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., This work was partly supported by the Spanish Ministry of Science and Innovation through the projects RTA2017-00073-00-00 and PID2020-113234RR-I00. MLP was supported by the Onassis Foundation under the Special Grant and Support Program for Scholars’ Association Members (Grant No. R ZJ 003-2/2019–2020). GM was supported by the Dutch topsector project KV 1509-020. SB is an employee of Koppert Spain, a private company that markets benefcial arthropods. RM works for Biobest Group NV, a private company that markets benefcial arthropods.

Background The use of zoophytophagous predators in protected crops has been widely adopted to manage pests in southern Europe. We hypothesized that plant defence responses would be induced by zoophytophagous predators and this induction could affect plant virus occurrence; the phytophagy of these predators induces plant defences similarly to that of viral infection. Therefore, we evaluated whether or not mirid predator-activated plant defences limited the accumulation of Tomato Spotted Wilt Virus (TSWV) in mechanically infected sweet pepper. Results Our results revealed TSWV accumulation in mirid-punctured plants to be significantly lower than in intact plants. This is most likely associated with the upregulation of the jasmonate acid pathway triggered by mirid phytophagy. Conclusion Activation of induced defences by mirid predators has been demonstrated for the first time to limit the accumulation of TSWV in sweet pepper. This novel approach can offer new control strategies for the management of plant diseases. © 2019 Society of Chemical Industry.

Pest management in protected sweet pepper crops mainly rely on biological control (BC) strategies. Recently, the zoophytophagous predatory mirids, Nesidiocoris tenuis, Macrolophus pygmaeus, and Dicyphus maroccanus, proved to be effective in the control of aphids on sweet pepper, for which the current biological control strategies have been meagre. The next step to integrate the possible use of these mirids in sweet pepper BC practices would be to ascertain their potential control on other sweet pepper pests. In this research, a comparative study to assess the establishment and the efficacy of N. tenuis, M. pygmaeus, and D. maroccanus on the two sweet pepper key pests; the thrips, Frankliniella occidentalis, and the whitefly, Bemisia tabaci was conducted. This study was carried out with two different temperature regimes, 20 °C and 27 °C, which simulated the mean temperatures registered in the two main crop cycles in Spain (the winter and summer planting period). Both, N. tenuis and M. pygmaeus were able to establish on sweet pepper and significantly reduced the number of F. occidentalis and B. tabaci adults, larvae and nymphs. Macrolophus pygmaeus had the highest density at 20 °C, whereas N. tenuis was more abundant at 27 °C. In contrast, D. maroccanus was less abundant under both temperatures studied; and did not reduce neither F. occidentalis nor B. tabaci infestations in this crop. None of the three mirids were observed to cause any damage to the pepper plant. The implications of these results applied to the use of mirids in sweet pepper crops are discussed.

The combined release of Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) with Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae) provides effective control of sweet pepper key pests, such as thrips and whiteflies. However, the management of the aphids can still be improved. Recently, the predatory mirids Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) and Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae) have been found to be effective in the control of aphids, thrips and whiteflies when tested alone. Hence, integrating one of these two mirids with A. swirskii might enhance sweet pepper pest management. In this work, we began by investigating the co-occurrence of both mirid species when released together with A. swirskii. This was compared to the standard release of O. laevigatus with A. swirskii. N. tenuis and A. swirskii were involved in a bidirectional intraguild predation (IGP). On the contrary, this interaction (IGP) was apparently unidirectional in the case of M. pygmaeus with A. swirskii and O. laevigatus with A. swirskii. Both, M. pygmaeus and O. laevigatus significantly reduced the abundance of A. swirskii. Secondly, in a greenhouse experiment, where the same release combinations were tested (either N. tenuis, M. pygmaeus or O. laevigatus combined with A. swirskii), IGP seemed to be neutralized. Mirids with A. swirskii significantly suppressed thrips, whitefly, and aphid infestations. Contrarily, the combined use of O. laevigatus with A. swirskii did not reached a satisfactory control for aphids, despite the reduction in thrips and whitefly densities. Therefore, our results suggest that the use of mirids combined with A. swirskii could result in more efficient and robust biological control programs in sweet pepper crops.

Plant responses induced by zoophytophagous plant bugs (Miridae) have not been thoroughly studied. Here, we show that three different zoophytophagous predators (Nesidiocoris tenuis, Macrolophus pygmaeus and Dicyphus maroccanus) have different capacities for the induction of responses in tomato plants, resulting in varying degrees of attractiveness of the plants to pests and natural enemies. Tomato plants punctured by N. tenuis were less attractive to the whitefly Bemisia tabaci and to the lepidopteran Tuta absoluta. In contrast, tomato plants punctured by M. pygmaeus and D. maroccanus were not able to repel B. tabaci and, more interestingly, became more attractive to T. absoluta. The ability of N. tenuis to make tomato plants less attractive to B. tabaci was attributed to the activation of the abscisic acid (ABA) signaling pathway, which was only up-regulated in plants punctured by N. tenuis. However, the phytohormones involved in the behavioral responses of T. absoluta could not be identified; therefore, further studies are required. Additionally, all three zoophytophagous mirid predators activated jasmonic acid (JA) signaling pathways, which resulted in the parasitoid Encarsia formosa being attracted to tomato plants. Here, the implications of these results on the efficacy of these three predators as biocontrol agents are discussed. The research leading to these results has received funding from the European Union Seventh Framework Programme (FP7/2007-2013) under the Grant agreement n°265865 and by the Spanish Ministry of Science and Innovation (AGL2011-30538-C03) and the Conselleria d’Agricultura, Pesca i Alimentació de la Generalitat Valenciana. The authors thank Javier Calvo (KOPPERT BS) for supplying the insects and Universitat Jaume I-SCIC for providing technical support.