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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.

The authors regret that values of χ2 and P were published incorrectly. Therefore, the authors would like to include the following changes in the published article.

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.

[EN] Orius laevigatus is a generalist predator that is widely used in augmentative strategies against the key pest of sweet pepper, Frankliniella occidentalis. Despite being a zoophytophagous predator, the phytophagous behavior of O. laevigatus has not been previously explored in depth nor has the impact of phytophagy on plant physiology. Here, the hierarchical significance of O. laevigatus feeding on sweet pepper is compared with other behaviors. O. laevigatus spends the majority of its time (38%) feeding on apical meristems and apical fresh leaves, which were also preferred residence locations. Here, the phytophagous feeding behavior of O. laevigatus on sweet pepper is shown to trigger defensive responses in the plant. These O. laevigatus plant-induced defenses are then shown to contribute to the repellence or attraction of pests or natural enemies, respectively. Specifically, O. laevigatus-punctured sweet pepper plants induce repellency for the whitefly Bemisia tabaci and the thrips species F. occidentalis. In contrast, the whitefly parasitoid Encarsia formosa was significantly attracted to O. laevigatus-punctured plants. The plant responses to O. laevigatus punctures include the release of an altered blend of volatiles and activation of the jasmonic acid and salicylic acid signalling pathways. These results highlight an interesting facet to the biology of O. laevigatus, in which the ability of the predator to induce defensive responses in sweet pepper plants may serve to improve the biological control of both thrips and whiteflies., The research leading to these results was partially funded by the Spanish Ministry of Economy and Competitiveness (AGL2014-55616-C3) and the Conselleria d'Agricultura, Pesca i Alimentacio de la Generalitat Valenciana. The authors thank Dr. Javier Calvo (KOPPERT BS, Spain) for supplying the insects, Dr. Pablo Bielza (Universidad Politecnica de Cartagena, Spain) for thrips colonies, Dimitrios Afentoulis, Zoi Thanou and Konstantinos Birmpilis (Erasmus + from Agricultural University of Athens) for providing support in the behavior experiments and Alice Mockford (University of Worcester) and two anonymous reviewers for their constructive review of this manuscript. MP-H was the recipient of a postdoctoral fellowship from the MEC (Juan de la Cierva program-FPDI-2013-17968) and SB was the recipient of a grant from Russell IPM Ltd.

During the last decades pest management in sweet pepper has shown noticeable development through the replacement of chemical control by biological control. The augmentative release of the predatory bug Orius laevigatus and the phytoseiid predatory mite Amblyseius swirskii satisfactory manage major pests invading sweet pepper, thrips and whiteflies. In order to enhance even more this biological control program and surmounted aphids problem, recent success was attributed to zoophytophagous mirid predators. The use of mirid predators is rare in sweet pepper greenhouses, however thesis results showed that mirid can enhance pest management in sweet pepper by the exploitation of zoophytophagy. The ability of mirids and O. laevigatus to predate open sweet pepper key pest and to induce plant defence was the most important found result in this thesis. A possible augmentative release of predatory mirids with A. swirskii is the new strategy that we propose to sustain sweet pepper pest management., Durante las últimas décadas, el control de plagas en el pimiento ha mostrado un desarrollo notable a través el reemplazo del control químico por control biológico. La liberación aumentativa del chinche depredadora Orius laevigatus y el ácaro depredador Amblyseius swirskii manejan satisfactoriamente las principales plagas, trips y mosca blanca. Con el fin de mejorar aún más este programa y superar el problema de los áfidos, se atribuyó el éxito reciente a los depredadores miridos zoofitofagos. El uso de miridos es raro en los invernaderos de pimiento, sin embargo, los resultados de la tesis mostraron que mediante la explotación de la zoofitáfia se puede mejorar el manejo de trips, mosca blanca y áfidos. La capacidad de los miridos y de O. laevigatus de preceder a la plaga clave del pimiento e inducir la defensa de la planta fue el resultado más importante encontrado en esta tesis. Una posible liberación aumentativa de los mirídos con A. swirskii es la nueva estrategia que proponemos para mantener el control de plagas del pimiento.

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.

Pest management in protected sweet pepper crops primarily relies on biological control strategies. The release of the phytoseiid Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) and the anthocorid Orius laevigatus Fieber (Hemiptera: Anthocoridae) provides effective control of the two key pests of this crop, the thrips Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) and the whitefly Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) (Sanchez et al., 2000; Calvo et al., 2009; van der Blom et al., 2009). A part of their direct effect on pest predation, zoophytophagous predators may induce defensive plant responses due to their plant feeding behaviour which involves the release of diverse volatiles through different pathways that are triggered by phytohormones (De Puysseleyr et al., 2011; Naselli et al., 2016; Pappas et al., 2015, 2016; Pérez-Hedo et al., 2015a,b). These responses may result in the repellence or attraction of pests and natural enemies. It is hence hypothesized that O. laevigatus would be able to induce plant responses in sweet pepper as has been demonstrated in other plantzoophytophage systems. As a first step to better understand the interaction between O. laevigatus and sweet pepper, the behavior of O. laevigatus on the plants was studied and plant feeding behaviour quantified to compare general behaviors. Orius laevigatus spends the majority of its time (38%) feeding on apical meristems and apical fresh leaves, which were also preferred residence locations (Bouagga et al., 2017).

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.