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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.

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.