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Parasitoids need to find their plant-feeding hosts in complex environments that contain multiple other plant and insect species. They usually rely on herbivore-induced plant volatiles to locate herbivore-infested plants from a distance and their foraging efficiency may be reduced when volatile information is not available. Downwind foraging during times when high wind speeds prevent odour-guided upwind flights may create foraging situations with limited accessibiliy to volatile information. We hypothesized that parasitoids forage less efficiently by landing on nonhost-damaged or undamaged plants when they are forced to fly downwind and tested this in a wind tunnel experiment. We released the parasitoid Cotesia glomerata (Hymenoptera, Braconidae) either upwind or downwind of a plant stand and observed their foraging behaviour. During downwind foraging, parasitoids were less successful in host finding and needed more time until they managed to oviposit in a host caterpillar compared to the upwind foraging situation. The observed increase in foraging time was caused by prolonged foraging on nonhost-infested and undamaged plants in the downwind situation, indicating that parasitoids leave an unprofitable patch that does not contain host caterpillars earlier, when they perceive volatiles from other herbivore-infested plants located upwind. Volatile information on the availability of herbivore-infested plants within a plant stand seems to be crucial for efficient foraging in plant stands that contain a mixture of host-infested, nonhost-infested and undamaged plants. Parasitoid foraging efficiency may thus be strongly reduced when high wind speed prevents odour-guided upwind flight.

Context Tritrophic interactions may be affected by local factors and the broader landscape context. At small spatial scales, carnivorous enemies of herbivorous insects use herbivore-induced plant volatiles (HIPVs) to find herbivores, but it is unknown whether variation in plant attractiveness due to differential HIPV emission can enhance recruitment of carnivores from the wider landscape. Objectives We studied whether parasitism of caterpillars of the butterfly Pieris brassicae on white cabbage was influenced by landscape composition and cover with brassicaceous species that provide hosts for parasitoids of P. brassicae in 19 landscapes in the Netherlands. We also investigated whether differential attraction of parasitoids to herbivore-infested plants affected parasitism of P. brassicae caterpillars by using different accessions as proxies for HIPV emission. Results The cabbage accession that is highly attractive to parasitic wasps recruited more wasps than a less attractive accession, but only when parasitism rates were high. Parasitism rate as proxy of wasp recruitment correlated positively with the cover of brassicaceous plants and area of arable land, suggesting that these habitats support hosts for the wasps and their population growth. In contrast, forest area was negatively associated with parasitism rates. Conclusions Our study shows that the degree of attractiveness of plants to parasitoids, which is probably mediated by HIPVs, can be a useful predictor of parasitism, but needs to be considered within the landscape context. To understand the strength of tritrophic interactions it is crucial to consider local-scale processes driven by plant-trait variation in combination with landscape-scale processes that determine carnivore abundance.

The fall armyworm (FAW), Spodoptera frugiperda (Smith), is a polyphagous pest whose larval feeding threatens several economically important crops worldwide with especially severe damage to corn (Zea mays L.). Field-derived resistance to several conventional pesticides and Bt toxins have threatened the efficacy of current management strategies, necessitating the development of alternative pest management methods and technologies. One possible avenue is the use of volatile organic compounds (VOCs) and other secondary metabolites that are produced and sequestered by plants as a response to larval feeding. The effects of conspecific larval feeding on fall armyworm oviposition preferences and larval fitness were examined using two-choice oviposition experiments, larval feeding trials, targeted metabolomics, and VOC analyses. There was a significant preference for oviposition on corn plants that lacked larval feeding damage, and larvae fed tissue from damaged plants exhibited reduced weights and head capsule widths. All larval feeding promoted significantly increased metabolite and VOC concentrations compared to corn plants without any feeding. Metabolite differences were driven primarily by linoleic acid (which is directly toxic to fall armyworm) and tricarboxylic acids. Several VOCs with significantly increased concentrations in damaged corn plants were known oviposition deterrents that warrant further investigation in an integrated pest management context.

Zoophytophagous arthropods can elicit plant defense responses affecting potential prey beyond predation. Phytophagy prevails as the main trigger for these responses, as in the case of Euseius stipulatus (Athias-Henriot) (Mesostigmata: Phytoseiidae), a predator occurring in citrus. Because other triggers cannot be excluded, our aim was to examine whether other phytoseiids co-occurring with E. stipulatus but not engaged in plant feeding [Neoseiulus californicus (McGregor) and Phytoseiulus persimilis Athias-Henriot] could induce similar responses (in terms of herbivore induced plant volatiles, HIPVs, and main defensive pathways), and how these affected the behavior of conspecifics and the shared prey, Tetranychus urticae Koch (Prostigmata: Tetranychidae). N. californicus triggered plant genotype-specific defense responses, including the production of different HIPVs compared to clean plants. However, we could not observe these effects for P. persimilis. T. urticae avoided better protected plants, because of stronger direct or indirect defense. As plants with weaker direct defense levels should offer higher prey densities, and those harboring conspecific predators represent higher risk of cannibalism, predators were expected to behave similarly. However, they did not. Our results demonstrate that plant defense triggered by phytoseiids is species-specific, depend on plant genotype and can be triggered by non-feeding activities. As N. californicus is a highly efficient predator used worldwide, further studies with this species are needed. Likewise, cineol, one of the volatiles identified in the blends triggered by this phytoseiid, could be used to manipulate the prey. These studies could pave the way for a more efficient use of phytoseiids in agroecosystems.

Summary Herbivore‐induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this ‘cry for help’ has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs.To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR‐Cas9) and chemical (GC‐MS analysis) approaches.We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)‐3‐hexenol, (Z)‐jasmone and (Z)‐3‐hexenyl acetate, which are important airborne signals in plant defenses.Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.

[EN] Sour orange, Citrus aurantium, displays higher constitutive and earlier inducible direct defenses against the two-spotted spider mite, Tetranychus urticae, than Cleopatra mandarin, Citrus reshni. Moreover, herbivore-induced plant volatiles (HIPVs) produced by sour orange upon infestation can induce resistance in Cleopatra mandarin but not vice versa. Because the role of these HIPVs in indirect resistance remains ignored, we have carried out a series of behavioral assays with three predatory mites with different levels of specialization on this herbivore, from strict entomophagy to omnivory. We have further characterized the volatile blend associated with T. urticae, which interestingly includes the HIPV methyl salicylate, as well as that produced by induced Cleopatra mandarin plants. Although a preference for less defended plants with presumably higher prey densities (i.e., C. reshni) was expected, this was not always the case. Because predators' responses changed with diet width, with omnivore predators responding to both HIPVs and prey-related odors and specialized ones mostly to prey, our results reveal that these responses depend on plant genotype, prey presence and predator diet specialization. As the different volatile blends produced by infested sour orange, induced Cleopatra mandarin and T. urticae itself are attractive to T. urticae natural enemies but not to the herbivore, they may provide clues to develop new more sustainable tools to manipulate these agriculturally relevant species., The research leading to these results was partially funded by the Spanish Ministry of Economy and Competitiveness (AGL2014-55616-C3; AGL2015-64990-2R). The authors thank M. Piquer (UJI) for technical assistance. MC received a pre-doctoral fellowship from the Spanish Ministry of Economy and Competitiveness (BES-2015-074570), and MP was the recipient of a research fellowship from INIA, Spain (subprogram DOC INIA-CCAA).

BACKGROUND Zoophytophagous predators can trigger plant defenses affecting prey populations beyond predation. Euseius stipulatus is a presumed zoophytophagous phytoseiid common in citrus. The response of citrus to one of its potential prey, Tetranychus urticae, is genotype dependent, with Citrus reshni and C. aurantium exhibiting extreme susceptibility and resistance, respectively. Volatile blends produced upon infestation affected the behavior of these two mites. We wondered whether E. stipulatus could trigger similar responses. RESULTS Euseius stipulatus triggered genotype-dependent defense responses in citrus. Whereas C. aurantium upregulated the Jasmonic Acid, Salicylic Acid and flavonoids defensive pathways, C. reshni upregulated JA only. Likewise, different volatile blends were induced. These blends were exploited by E. stipulatus to select less-defended plants (i.e., those in which higher pest densities are expected) and, interestingly, did not prevent T. urticae from choosing E. stipulatus-infested plants. To the best of our knowledge, this is the first time that this type of response has been described for a zoophytophagous phytoseiid. CONCLUSION The observed responses could affect herbivore populations through plant-mediated effects. Although further research is needed to fully characterize them and include other arthropods in the system, these results open opportunities for more sustainable and effective pest control methods (i.e., combining semiochemicals and biological control). © 2018 Society of Chemical Industry.

Silicon (Si) is important in plant defenses that operate in a direct manner against herbivores, and work in rice (Oryza sativa) has established that this is mediated by the jasmonate signaling pathway. Plant defenses also operate indirectly, by the production of herbivore induced plant volatiles (HIPVs) that attract predators and parasitoids of herbivores. These indirect defenses too are mediated by the jasmonate pathway but no earlier work has demonstrated an effect of Si on HIPVs. In this study, we tested the effect of Si supplementation versus Si deprivation to rice plants on subsequent HIPV production following feeding by the important pest, rice leaffolder (Cnaphalocrocis medinalis). Gas chromatography-mass spectrometry analyses showed lower production of α-bergamotene, β-sesquiohellandrene, hexanal 2-ethyl, and cedrol from +Si herbivore-infested plants compared with -Si infested plants. These changes in plant chemistry were ecologically significant in altering the extent to which parasitoids were attracted to infested plants. Adult females of Trathala flavo-orbitalis and Microplitis mediator both exhibited greater attraction to the HIPV blend of +Si plants infested with their respective insect hosts compared to -Si infested plants. In equivalent studies using RNAi rice plants in which jasmonate perception was silenced there was no equivalent change to the HIPV blend associated with Si treatment; indicating that the effects of Si on HIPVs are modulated by the jasmonate pathway. Further, this work demonstrates that silicon alters the HIPV blend of herbivore-infested rice plants. The significance of this finding is that there are no earlier-published studies of this phenomenon in rice or any other plant species. Si treatment to crops offers scope for enhancing induced, indirect defenses and associated biological control of pests because parasitoids are more strongly attracted by the HIPVs produced by +Si plants.

© 2016 Reynolds, Padula, Zeng and Gurr. Silicon has generally not been considered essential for plant growth, although it is well recognized that many plants, particularly Poaceae, have substantial plant tissue concentrations of this element. Recently, however, the International Plant Nutrition Institute [IPNI] (2015), Georgia, USA has listed it as a “beneficial substance”. This reflects that numerous studies have now established that silicon may alleviate both biotic and abiotic stress. This paper explores the existing knowledge and recent advances in elucidating the role of silicon in plant defense against biotic stress, particularly against arthropod pests in agriculture and attraction of beneficial insects. Silicon confers resistance to herbivores via two described mechanisms: physical and biochemical/molecular. Until recently, studies have mainly centered on two trophic levels; the herbivore and plant. However, several studies now describe tri-trophic effects involving silicon that operate by attracting predators or parasitoids to plants under herbivore attack. Indeed, it has been demonstrated that silicon-treated, arthropod- attacked plants display increased attractiveness to natural enemies, an effect that was reflected in elevated biological control in the field. The reported relationships between soluble silicon and the jasmonic acid (JA) defense pathway, and JA and herbivore- induced plant volatiles (HIPVs) suggest that soluble silicon may enhance the production of HIPVs. Further, it is feasible that silicon uptake may affect protein expression (or modify proteins structurally) so that they can produce additional, or modify, the HIPV profile of plants. Ultimately, understanding silicon under plant ecological, physiological, biochemical, and molecular contexts will assist in fully elucidating the mechanisms behind silicon and plant response to biotic stress at both the bi- and tri-trophic levels.

Many parasitoids use volatiles produced by plants as important cues during their food and host search process. We investigated the attraction of the parasitic wasp Trybliographa rapae Westwood (Hymenoptera: Figitidae) to volatiles emitted from plants infested by the cabbage root fly Delia radicum L. (Diptera: Anthomyiidae), as well as to volatiles from a nectar food plant. Behavioural choice tests showed that male parasitoids were not attracted to any volatiles from plants infested by D. radicum or from nectar plants, while females showed clear attraction to both volatile sources. Young females were more attracted to combined volatiles of host and food plants over those from only the host plant, whereas older females showed no differences in attraction to the two odour sources. This suggests that intercropping attractive flowers with host plants could potentially be used to recruit newly emerged parasitoids from surrounding fields while older parasitoids invest more energy in host location than in additional food search. Volatiles from a whole infested plant were chosen over those emitted from separated above- and below-ground parts from infested plants. It is important to consider the availability of both energy and host resources for parasitoids when designing an eco-compatible management of a vegetable crop system.

In response to insect herbivory, plants emit volatile organic compounds which may act as indirect plant defenses by attracting natural enemies of the attacking herbivore. In nature, plants are often attacked by multiple herbivores, but the majority of studies which have investigated indirect plant defenses to date have focused on the recruitment of different parasitoid species in a single-herbivore context. Here, we report our investigation on the attraction of egg parasitoids of lepidopteran hosts (Trichogramma brassicae and T. evanescens) toward plant volatiles induced by different insect herbivores in olfactometer bioassays. We used a system consisting of a native crucifer, Brassica nigra, two naturally associated herbivores [the butterfly Pieris brassicae (eggs and caterpillars) and the aphid Brevicoryne brassicae] and an alien invasive herbivore (eggs and caterpillars of the moth Spodoptera exigua). We found that Trichogramma wasps were attracted by volatiles induced in the plants by P. brassicae eggs, but not by those induced in the plants by S. exigua eggs, indicating the specificity of the plant responses toward lepidopteran herbivores. The results of the chemical analysis revealed significant differences between the volatile blends emitted by plants in response to attack by P. brassicae and S. exigua eggs which were in agreement with the behavioural observations. We investigated the attraction of Trichogramma wasps toward P. brassicae egg-induced volatiles in plants simultaneously attacked by larvae and nymphs of different non-hosts. The two chewing caterpillars P. brassicae and S. exigua, but not the phloem-feeding aphid B. brassicae, can disrupt the attraction of Trichogramma species toward P. brassicae egg-induced volatiles. Indirect plant defenses are discussed in the context of multiple herbivory by evaluating the importance of origin, dietary specialization and feeding guild of different attackers on the recruitment of egg-killing parasitoids.

Despite a large number of studies on herbivore-induced plant volatiles (HIPVs), little is known about which specific compounds are used by natural enemies to locate prey- or host- infested plants. In addition, the role of HIPVs in attracting natural enemies has been restricted largely to agricultural systems. Differences in volatile blends emitted by cultivars and plants that originate from wild populations may be attributed to potentially contrasting selection regimes: natural selection among the wild types and artificial selection among cultivars. A more realistic understanding of these interactions in a broader ecological and evolutionary framework should include studies that involve insect herbivores, parasitoids, and wild plants on which they naturally interact in the field. We compared the attractiveness of HIPVs emitted by wild and cultivated cabbage to the parasitoid Cotesia rubecula, and determined the chemical composition of the HIPV blends to elucidate which compounds are involved in parasitoid attraction. Wild and cultivated cabbage differed significantly in their volatile emissions. Cotesia rubecula was differentially attracted to the wild cabbage populations and preferred wild over cultivated cabbage. Isothiocyanates, which were only emitted by the wild cabbages, may be the key components that explain the preference for wild over cultivated cabbage, whereas terpenes may be important for the differential attraction among the wild populations. Volatile analysis revealed that parasitoid attraction cannot be explained by simple linear relationships. Our results suggest that unraveling which compound(s) are innately attractive to parasitoids of cabbage pests should include wild Brassicaceae.