BackgroundPlants under herbivore attack release volatiles that attract natural enemies, and herbivores in turn avoid such plants. Whilst herbivore-induced plant volatile blends appeared to reduce the attractiveness of host plants to herbivores, the volatiles that are key in this process and particularly the way in which deterrence is coded in the olfactory system are largely unknown. Here we demonstrate that herbivore-induced cotton volatiles suppress orientation of the moth Spodoptera littoralis to host plants and mates.ResultsWe found that (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), an induced volatile, is key in herbivore deterrence: DMNT suppressed plant odour- and pheromone-induced behaviours. We then dissected the neurophysiological basis of this interaction. DMNT-responding glomeruli were also activated by other plant compounds, suggesting that S. littoralis possesses no segregated olfactory circuit dedicated exclusively to DMNT. Instead, DMNT suppressed responses to the main pheromone component, (Z)-9-(E)-11-tetradecenyl acetate, and primarily to (Z)-3-hexenyl acetate, a host plant attractant.ConclusionOur study shows that olfactory sensory inhibition, which has previously been reported without reference to an animal’s ecology, can be at the core of coding of ecologically relevant odours. As DMNT attracts natural enemies and deters herbivores, it may be useful in the development or enhancement of push-pull strategies for sustainable agriculture.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0188-3) contains supplementary material, which is available to authorized users.

Summary1. Plants produce herbivore-induced plant volatiles (HIPVs) in response to damage by herbivores. Although HIPVs are known to enhance plant resistance by affecting herbivore host plant preferences and by attracting natural enemies, little is known about the role of HIPVs on the resistance of neighbouring plants and the mechanism behind this associational resistance. 2. This study examined the effect of HIPVs from herbivore-damaged host plants (alfalfa (Medicago sativa), clover (Trifolium alexandrinum) and cotton (Gossypium hirsutum)) on oviposition by Egyptian cotton leafworm (Spodoptera littoralis) (Lepidoptera: Noctuidae) on neighbouring, undamaged host plants.3. There was a significant reduction in oviposition by S. littoralis on undamaged plants adjacent to herbivore-damaged cotton plants under both field and laboratory conditions. The results showed that the associational resistance by HIPVs depends on direct effects on oviposition behaviour in S. littoralis. There were also indications that other mechanisms may be involved. 4. Associational resistance via HIPVs was not observed for all plant species tested. Emission of HIPVs from damaged cotton increased the resistance of undamaged cotton and alfalfa plants to oviposition by S. littoralis, but HIPVs from damaged alfalfa and clover neighbours did not provide resistance to undamaged cotton plants. 5. Synthesis. Our results suggest that the presence of HIPV-emitting plant neighbours can reduce herbivory on undamaged plants and enhance plant resistance by affecting oviposition behaviour in insect herbivores.

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SUMMARYAnimals depend on reliable sensory information for accurate behavioural decisions. For herbivorous insects it is crucial to find host plants for feeding and reproduction, and these insects must be able to differentiate suitable from unsuitable plants. Volatiles are important cues for insect herbivores to assess host plant quality. It has previously been shown that female moths of the Egyptian cotton leafworm, Spodoptera littoralis (Lepidoptera: Noctuidae), avoid oviposition on damaged cotton Gossypium hirsutum, which may mediated by herbivore-induced plant volatiles (HIPVs). Among the HIPVs, some volatiles are released following any type of damage while others are synthesized de novo and released by the plants only in response to herbivore damage. In behavioural experiments we here show that oviposition by S. littoralis on undamaged cotton plants was reduced by adding volatiles collected from plants with ongoing herbivory. Gas chromatography-electroantennographic detection (GC-EAD) recordings revealed that antennae of mated S. littoralis females responded to 18 compounds from a collection of headspace volatiles of damaged cotton plants. Among these compounds, a blend of the seven de novo synthesized volatile compounds was found to reduce oviposition in S. littoralis on undamaged plants under both laboratory and ambient (field) conditions in Egypt. Volatile compounds that are not produced de novo by the plants did not affect oviposition. Our results show that ovipositing females respond specifically to the de novo synthesized volatiles released from plants under herbivore attack. We suggest that these volatiles provide reliable cues for ovipositing females to detect plants that could provide reduced quality food for their offspring and an increased risk of competition and predation.