Plants release volatiles induced by herbivore feeding that may affect the diversity and composition of plant-associated arthropod communities. However, the specificity and role of plant volatiles induced during the early phase of attack, i.e. egg deposition by herbivorous insects, and their consequences on insects of different trophic levels remain poorly explored. In olfactometer and wind tunnel set-ups, we investigated behavioural responses of a specialist cabbage butterfly (Pieris brassicae) and two of its parasitic wasps (Trichogramma brassicae and Cotesia glomerata) to volatiles of a wild crucifer (Brassica nigra) induced by oviposition of the specialist butterfly and an additional generalist moth (Mamestra brassicae). Gravid butterflies were repelled by volatiles from plants induced by cabbage white butterfly eggs, probably as a means of avoiding competition, whereas both parasitic wasp species were attracted. In contrast, volatiles from plants induced by eggs of the generalist moth did neither repel nor attract any of the tested community members. Analysis of the plant’s volatile metabolomic profile by gas chromatography-mass spectrometry and the structure of the plant-egg interface by scanning electron microscopy confirmed that the plant responds differently to egg deposition by the two lepidopteran species. Our findings imply that prior to actual feeding damage, egg deposition can induce specific plant responses that significantly influence various members of higher trophic levels.

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Summary1. Plants respond to insect herbivores with changes in physical and chemical traits, both locally and systemically, in leaves and flowers. Such phenotypic changes may influence the behaviour of every community member that interacts with the plant. Here, we address effects of plant responses to eggs and subsequent herbivory by caterpillars on plant-mediated interactions with pollinators and consequences for plant fitness. 2. Using a common garden set-up, we have investigated responses of Brassica nigra plants to herbivore exposure from egg deposition onwards throughout larval development. We quantified effects of infestation by the specialist Pieris brassicae on: 1. behaviour of pollinators; 2. volatile emission and 3. timing and number of seeds produced. 3. Egg deposition and folivory did not influence visitation by pollinators to plots of infested or control plants. Effects of herbivore infestation on both pollinator visitation and volatile emission were observed only at a later stage, when caterpillars were feeding on the flowers. 4. Remarkably, before eggs had hatched, infested plants accelerated seed production. The caterpillars that developed from the eggs fed on flowers but not on seeds and thus seed production prior to herbivory on flowers safeguarded reproductive output. 5. The results of this study show that early plant investments in reproduction can successfully prevent consumption of expensive reproductive tissues. By accelerating seed production, plants prevented consumption of flowers and effectively defended themselves against the herbivores.

2. In this study, we investigated whether a broad range of herbivores feeding on the annual plant Brassica nigra affect interactions with flower visitors, whether the direction of interactions is predicted by the feeding modes (chewing and sap-feeding) and sites (above-and belowground) of the herbivores, and whether it results in fitness consequences for the plant. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.