Volatile organic compounds released by maize following herbivory or insect extract application and communication between plants

To protect themselves from herbivory, plants have evolved an arsenal of physical and chemical defences and release a variety of volatile organic compounds (VOCs). By releasing these VOCs, a signalling plant can both reduce herbivory, sometimes by more than 90%, and also warn neighbouring plants about an attack. The aim of this study was to assess the influence of herbivory and insect extract application on VOC release by damaged/treated and nearby undamaged/untreated maize plants. We confirmed that European corn borer (Ostrinia nubilalis) larvae attack or larvae extract application induced maize VOC release. Greater amounts of (Z)‐3‐hexenal, (E)‐2‐hexenal, (Z)‐3‐hexen‐1‐ol, (E)‐2‐hexen‐1‐ol, β‐myrcene, (Z)‐3‐hexen‐1‐yl acetate, 1‐hexyl acetate, (Z)‐ocimene, linalool, benzyl acetate, methyl salicylate, indole, methyl anthranilate, geranyl acetate, β‐caryophyllene, (E)‐β‐farnesene and (Z)‐3‐hexenal, (Z)‐3‐hexen‐1‐ol, (Z)‐3‐hexen‐1‐yl acetate, (Z)‐ocimene, linalool, indole, methyl anthranilate, geranyl acetate, β‐caryophyllene and (E)‐β‐farnesene were released as a result of biotic stress after insect attack or insect extract application. The amounts of each VOC released were qualitatively and quantitatively distinct and dependent on time after biotic stress exposure. However, for all biotic stresses, significantly lower VOC induction was measured when leaves were damaged/treated for three days, as compared to seven days. Our work also demonstrated that undamaged/untreated neighbouring plants also release significant amounts of VOCs. This suggests that VOC emission by a damaged/treated plant stimulates VOC induction in nearby undamaged/untreated plants. However, the concentrations of all VOCs released by neighbouring undamaged/untreated maize plants were lower than those from damaged/treated plants and were negatively correlated with distance from a damaged/treated plant. Still, significant VOC induction occurred in undamaged/untreated plants even at 3 m distance from a damaged/infected plant. Our work suggests that maize plant protective defence responses (VOC emission) can be induced via application of European corn borer extracts.     

Effects of water stress on plant volatile emission and insect oviposition preference in an agroecosystem

1. Drought has become more common and severe in many parts of the world due to climate change. The effect of water stress on insect oviposition preference that is key determinant for their fitness has received less attention.
2. Here, we examined how water stress may affect oviposition selection of Ostrinia furnacalis for maize plants in the greenhouse, and tested difference in volatile compounds emitted from treated maize, and electronantennogram and bioassay responses of O. furnacalis to the volatile profiles in maize plants.
3. Ostrinia furnacalis were more prone to lay eggs on the well-watered maize. Most plant volatile compounds differed significantly among the three water treatments, including increased emissions of β-caryophyllene, (E)-2-hexenal, and linalool, and decreased emission of (Z)-3-hexen-1-ol when subjected to increasing intensity of drought.
4. Varied volatile profiles of maize may drive oviposition decision of O. furnacalis, because O. furnacalis showed a clear oviposition preference for (Z)-3-hexen-1-ol, while not for β-caryophyllene, (E)-2-hexenal, and linalool, at the concentration of 1000 ppm.
5. This study advances understanding of drought effects on plant–insect interactions through volatile profiles. Our finding calls for attention to oviposition selection for insect pest management in agricultural settings, especially in regions under changing precipitation patterns.

     

Behavioural and electrophysiological responses of the European corn borer Ostrinia nubilalis to host‐plant volatiles and related chemicals

The European corn borer Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae) is a worldwide pest of maize (Zea mays L.) and other crops. The semiochemicals released by maize plants and structurally‐related compounds can be used by adult female O. nubilalis for host‐plant location and oviposition. Headspace volatile compounds emitted by watered and water‐deprived maize plants are collected and identified by their retention indices and mass spectra. The most abundant compounds from watered plants are limonene, linalool, benzoic acid, indole, β‐caryophyllene and acetophenone, whereas, in water‐deprived plants, limonene, acetophenone, hexanoic acid, benzoic acid and indole are dominant. In addition, (E)‐4,8‐dimethyl‐1,3,7‐nonatriene, 6‐methyl‐5‐hepten‐2‐one, anisole and 1‐carvone are undetected in the water‐deprived plants. Some of the identified compounds show electrophysiological activity (electroantennogram) in the antennae of both sexes, with the responses elicited by tridecane, tetradecane, dodecane, nonanal, decanal and 2‐ethylhexanol on males being particularly noteworthy. In a dual‐choice olfactometer, adult females show a preference for 2‐hexanol, heptanal, methyl salicylate, hexyl acetate, nonanal, methyl dodecanoate, β‐pinene and (E)‐2‐hexenyl acetate over hexane controls. Tetradecane, linalool, methyl hexanoate, methyl nonanoate, (Z)‐3‐hexenyl benzoate, tridecane, 2‐cyclopentylcyclopentanone, 3‐methylbutyl acetate, β‐myrcene and (Z)‐3‐hexenyl butanoate result in fewer females in the test arm compared with the control arm. No single compound displays an activity similar to watered maize plants, supporting the hypothesis that blends of volatiles in specific ratios are more effective than single volatile chemicals. The results of the present study suggest that methyl salicylate, which elicits also one of the highest electrophysiological responses in female antennae, plays a role in host preference by O. nubilalis females.     

Volatiles induced by the larvae of the Asian corn borer (Ostrinia furnacalis) in maize plants affect behavior of conspecific larvae and female adults

Abstract  Effects of maize ( Zea mays L.) volatiles induced by larvae of the Asian corn borer, Ostrinia furnacalis (Guenée), on the orientation behaviors of Asian corn borer larvae and oviposition of the females were investigated. Nineteen volatile chemicals, with terpenes being the major components, were identified from maize plants attacked by third instar Asian corn borer larvae. Coupled gas chromatographic-electroantennographic detection (GC-EAD) analyses revealed some electroantennographic differences between female and male Asian corn borer antennae in response to larvae-induced maize volatiles; female responded to ( E )-2-hexenal, nonanal, ( Z )-3-hexen-1-ol and three unknown compounds while the male only responded to ( E )-2-hexenal, nonanal and one unknown compound. In laboratory orientation bioassays, Asian corn borer neonate larvae were attracted to extracts collected from Asian corn borer-damaged plants as well as to synthetic farnesene, but were repelled by ( Z )-3-hexen-1-ol. In laboratory oviposition bioassays, gravid females laid fewer eggs on plants damaged by larvae than on mechanically damaged plants or undamaged plants. Adult Asian corn borer females deposited fewer eggs on wax paper treated with ( E )-2-hexenal or ( Z )-3-hexen-1-ol than on wax paper treated with hexane (control). The results suggest that Asian corn borer can affect the behaviors of conspecific larvae and adults by changing host plant volatiles.     

Distribution of second generation European corn borer,Ostrinia nubilalis, egg masses in field corn and relationship to subsequent tunneling damage

The relationship between second generation European corn borer (Ostrinia nubilalis Hübner) egg mass numbers and subsequent field corn damage, as measured by stalk cavity numbers, was studied in 79 fields in northeastern North Carolina over three years. A mean of 0.028 egg masses per plant (645 egg masses/23400 plants) was found over the course of the study. Significant differences in oviposition rate were detected between fields and years. Ca. 85% of egg masses were deposited in a five leaf zone surrounding the primary ear; of these, 89% were found on the lower four leaves in this zone. Egg masses appeared to be distributed randomly within fields but at low rates of incidence, and oviposition was relatively uniform between sampling areas within individual fields. Under moderate to high oviposition pressure (mean number of egg masses per plant over the duration of the oviposition period >ca. 0.02), eggs laid during the early phases of the oviposition period account for more subsequent stalk damage than eggs laid during the later phases of the oviposition period. Variations in second generation egg mass numbers accounted for ca. 70% of variation in stalk cavity numbers.     

Fitness costs associated with Cry1F resistance in the European corn borer

Crops producing insecticidal toxins derived from the bacterium Bacillus thuringiensis (Bt) are widely planted to manage insect pests. Bt crops can provide an effective tool for pest management; however, the evolution of Bt resistance can diminish this benefit. The European corn borer, Ostrinia nubilalis Hübner, is a significant pest of maize and is widely managed with Bt maize in the Midwest of the United States. When Bt crops are grown in conjunction with non‐Bt refuges, fitness costs of Bt resistance can delay the evolution of resistance. Importantly, fitness costs often vary with ecological factors, including host‐plant genotype and diapause. In this study, we examined fitness costs associated with Cry1F resistance in O. nubilalis when insects were reared on three maize lines. Fitness costs were tested in two experiments. One experiment assessed the fitness costs when Cry1F‐resistant and Cry1F‐susceptible insects were reared on plants as larvae and experienced diapause. The second experiment tested resistant, susceptible and F1 heterozygotes that were reared on plants but did not experience diapause. Despite some evidence of greater adult longevity for Cry1F‐resistant insects, these insects produced fewer fertile eggs than Cry1F‐susceptible insects, and this occurred independent of diapause. Reduced fecundity was not detected among heterozygous individuals, which indicated that this fitness cost was recessive. Additionally, maize lines did not affect the magnitude of this fitness cost. The lower fitness of Cry1F‐resistant O. nubilalis may contribute to the maintenance of Cry1F susceptibility in field populations more than a decade after Cry1F maize was commercialized.     

Experience-induced preference for oviposition repellents derived from a non-host plant by a specialist herbivore

Foraging adults of phytophagous insects are attracted by host‐plant volatiles and supposedly repelled by volatiles from non‐host plants. In behavioural control of pest insects, chemicals derived from non‐host plants applied to crops are expected to repel searching adults and thereby reduce egg laying. How experience by searching adults of non‐host volatiles affects their subsequent searching and oviposition behaviour has been rarely tested. In laboratory experiments, we examined the effect of experience of a non‐host‐plant extract on the oviposition behaviour of the diamondback moth (DBM), Plutella xylostella, a specialist herbivore of cruciferous plants. Naive ovipositing DBM females were repelled by an extract of dried leaves of Chrysanthemum morifolium, a non‐host plant of DBM, but experienced females were not repelled. Instead they were attracted by host plants treated with the non‐host‐plant extract and laid a higher proportion of eggs on treated than on untreated host plants. Such behavioural changes induced by experience could lead to host‐plant range expansion in phytophagous insects and play an important role in determining outcome for pest management of some behavioural manipulation methods.     

Diamondback moth egg susceptibility to rainfall: effects of host plant and oviposition behavior

Oviposition patterns of the diamondback moth (DBM), Plutella xylostella L. (Lepidoptera: Plutellidae), differ between common cabbage (Brassica oleracea L. var. capitata) and Chinese cabbage (Brassica rapa L. var. pekinensis) (Brassicaceae) host plants. This study shows that the moth prefers to oviposit on adaxial rather than abaxial leaf surfaces and petioles of both host plants. More eggs were laid in leaf veins than on leaf laminas of both host plants, especially in Chinese cabbage, where 94.6% of eggs were laid in veins. On Chinese cabbage, very few eggs were laid in clusters (≥2 eggs), whereas on common cabbage approximately 30% of eggs were laid in groups of 2 or more eggs. Removal of wax from common cabbage leaves dramatically increased the number of eggs laid singly on the leaf lamina of treated plants, suggesting that leaf waxes affect how eggs are distributed by ovipositing DBM. Eggs were most susceptible to removal by rainfall from the plant surface immediately (<1 h) after oviposition and when close to hatching (>72h old) whereas they were least susceptible 24 h after oviposition. Eggs laid on common cabbage plants were more susceptible to simulated rainfall than eggs laid on Chinese cabbage plants. On common cabbage plants, egg susceptibility to rainfall on different plant parts ranked adaxial leaf surfaces>petioles = abaxial leaf surfaces>stem, but there was no difference in egg susceptibility to rainfall on the various plant parts of Chinese cabbage. Furthermore, on common cabbage plants, eggs laid on both adaxial and abaxial leaf surfaces were afforded significant protection from the effects of rainfall by leaves higher in the plant canopy. On common cabbage plants, oviposition patterns reduce the potential impact of rainfall on eggs, possibly reducing the effect of this important abiotic mortality factor in the field.     

Olfactory responses ofTrichogramma maidis Pint,et Voeg.: Effects of chemical cues and behavioral plasticity

Oriented responses of Trichogramma maidisPint, et Voeg. to airborne odors were observed in a four-armed olfactometer. Experiments were carried out with odors of host eggs, the sex pheromone of Ostrinia nubilalisHbn, and maize extract, offered singly or in combination, both to naive wasps and to wasps previously exposed to the tested odor during an oviposition experience. The exploratory behavior in the olfactometer was quantified by means of a computer program which performed a space-time analysis of the insect 's movements. Whereas the naive wasps did not respond to the odor of the eggs, the synthetic sex pheromone of O. nubilalis,or the maize extract presented singly, they did react to a mixture of these three volatile cues. Prior oviposition in the odor of maize extract or in the combination of odors induced an increased preference toward the conditioning scent. This phenomenon did not occur when the wasps were conditioned to egg odor or sex pheromone alone. These results suggest that females can learn to associate some olfactory cues with the presence of the host. Immediately following the presentation of the combination of odors, a strong attraction of experienced wasps occurred; it decreased as the experiment progressed and finally reached the level presented by naive insects. Adult conditioning to the combination of odors also resulted in reduced variability in the behavioral responses.     

Genetic structure of European and Mediterranean maize borer populations on several wild and cultivated host plants

Target pests may become resistant to Bacillus thuringiensis (Bt) toxins produced by trangenic maize (Zea mays L.). Untreated refuge areas are set aside to conserve high frequencies of susceptibility alleles: a delay in resistance evolution is expected if susceptible individuals from refuges mate randomly with resistant individuals from Bt fields. In principle, refuges can be toxin‐free maize or any other plant, provided it hosts sufficiently large pest populations mating randomly with populations from Bt‐maize fields. Our aim was to examine the suitability of several cultivated or weedy plants [pepper (Capsicum frutescens L.), sorghum (Sorghum spec.), sunflower (Helianthus annuus L.), cocklebur (Xanthium spec.), cantaloupe (Cucumis melo L.), and hop (Humulus lupulus L.)] as refuges for Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae) and Sesamia nonagrioides Lefebvre (Lepidoptera: Noctuidae), two major maize pests in southern Europe. Larvae of both species were collected on these plants. Their genetic population structure was examined at several allozyme loci. We found little or no evidence for an influence of geographic distance, but detected a significant host‐plant effect on the genetic differentiation for both species. Ostrinia nubilalis populations from sunflower, pepper, cocklebur, and sorghum appear to belong to the same genetic entity as populations collected on maize, but to differ from populations on hop. Accordingly, females from pepper and cocklebur produced exclusively the ‘Z’ type sexual pheromone, which, in France, characterizes populations developing on maize. Qualitatively, these plants (except hop) could thus serve as refuges for O. nubilalis; however, they may be of little use quantitatively as they were found much less infested than maize. Sesamia nonagrioides populations on maize and sorghum reached comparable densities, but a slight genetic differentiation was detected between both. The degree of assortative mating between populations feeding on both hosts must therefore be assessed before sorghum can be considered as a suitable refuge for this species.     

Suitability of brachiaria grass as a trap crop for management of Chilo partellus

The cereal stemborer Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) is a major insect pest of sorghum (Sorghum bicolor L. Moench) and maize (Zea mays L.) in Africa. Trap cropping systems have been shown to be a valuable tool in management of this pest. To optimize trap cropping strategies, an understanding of host‐plant preference for moth oviposition and host suitability for larval survival on potential trap plants is a prerequisite. Therefore, we assessed seven brachiaria accessions (Poaceae) for preference by C. partellus moths and subsequent larval performance. In two‐choice tests with a local open‐pollinated maize variety (cv. Nyamula), significantly higher numbers of eggs were deposited on brachiaria accessions Marandu, Piata, and Xaraes than on maize, whereas fewer eggs were recorded on plants of Mulato II, Mulato I, and Cayman. There was a significant and negative correlation between the trichome density on plant leaves and C. partellus oviposition preference for brachiaria. In addition to poor larval performance on brachiaria, there was no clear ranking in the accessions regarding larval orientation, settling, arrest, and food ingestion and assimilation. First instars did not consume leaf tissues of brachiaria plants but consumed those of maize, which also suffered more stem damage than brachiaria plants. No larvae survived on brachiaria plant tissue for longer than 5 days, whereas 79.2% of the larvae survived on maize. This study highlights the preferential oviposition of C. partellus on brachiaria plants over maize and the negative effects that these accessions have on subsequent larval survival and development. Our findings support the use of brachiaria as a trap crop for management of C. partellus through a push‐pull technology.     

Pollen beetle (Meligethes aeneus) oviposition and feeding preference on different host plant species

The oviposition and feeding preferences of the pollen beetle, Meligethes aeneus, were determined in choice and no-choice tests in field, semi-field and greenhouse trials. Plant species used were Brassica napus, B. campestris, B. juncea, B. nigra, B. carinata, Sinapis alba and Crambe abyssinica. With respect to number of eggs laid, S. alba and C. abyssinica were inferior to the other species. Pollen beetles laid fewer eggs on B. nigra than on the other Brassica spp. in no-choice tests, however this difference was partly due to fewer eggs laid per bud rather than fewer buds used for oviposition. Most eggs, for all plant species, were deposited in buds sized 2–3 mm. Feeding damage on all plant species was relatively similar. Pollen beetles seem to have a wider host range for feeding than for oviposition. There was good agreement in plant species ranking as oviposition hosts between the field, semi-field and greenhouse trials.     

Volatiles from Botrytis cinerea‐infected and healthy berries of Vitis vinifera influence the oviposition behaviour of Epiphyas postvittana

Interactions among plants, plant‐feeding insects, and plant – pathogenic fungi are partially mediated by volatile compounds. Herbivorous insects use sensory cues to choose host plants for feeding and/or oviposition that are likely to support survival and development of progeny. It is known that some fungus‐induced alterations in plants can modify plant volatiles, which are recognized by the olfactory receptors of the insect, either as an attractant or as a deterrent. We tested for the presence of behaviour‐modifying volatiles emanating from the berries of Vitis vinifera L. (Vitaceae) infected with Botrytis cinerea Pers. (Helotiales). We tested the olfactory behaviour of adults of Epiphyas postvittana Walker (Lepidoptera: Tortricidae) to these volatiles using two‐choice and wind‐tunnel experiments. We hypothesized that olfactory cues influence E. postvittana's oviposition behaviour. We found that volatiles emanating from B. cinerea‐infected berries did not significantly attract the gravid females of E. postvittana; consequently, they laid significantly fewer eggs on infected berries. Furthermore, significantly fewer females of E. postvittana were found attracted to infected berries in the wind tunnel assay. Ethanol and 3‐methyl‐1‐butanol were abundant in B. cinerea‐infected berries. Oviposition assays made with laboratory standards of ethanol and 3‐methyl‐1‐butanol confirmed their role in regulating the olfactory behaviour of E. postvittana site selection.     

Influence of host plant,geography and pheromone strain on genomic differentiation in sympatric populations of Ostrinia nubilalis

Patterns of mating for the European corn borer (Ostrinia nubilalis) moth depend in part on variation in sex‐pheromone blend. The ratio of (E)‐11‐ and (Z)‐11‐tetradecenyl acetate (E11‐ and Z11‐14:OAc) in the pheromone blend that females produce and males respond to differs between strains of O. nubilalis. Populations also vary in female oviposition preference for and larval performance on maize (C4) and nonmaize (C3) host plants. The relative contributions of sexual and ecological trait variation to the genetic structure of O. nubilalis remains unknown. Host‐plant use (¹³C/¹⁴C ratios) and genetic differentiation were estimated among sympatric E and Z pheromone strain O. nubilalis males collected in sex‐pheromone baited traps at 12 locations in Pennsylvania and New York between 2007 and 2010. Among genotypes at 65 single nucleotide polymorphism marker loci, variance at a position in the pheromone gland fatty acyl‐reductase (pgfar) gene at the locus responsible for determining female pheromone ratio (Pher) explained 64% of the total genetic differentiation between males attracted to different pheromones (male response, Resp), providing evidence of sexual inter‐selection at these unlinked loci. Principal coordinate, Bayesian clustering, and distance‐based redundancy analysis (dbRDA) demonstrate that host plant history or geography does not significantly contribute to population variation or differentiation among males. In contrast, these analyses indicate that pheromone response and pgfar‐defined strain contribute significantly to population genetic differentiation. This study suggests that behavioural divergence probably plays a larger role in driving genetic variation compared to host plant‐defined ecological adaptation.     

The influence of planting date,transgenic Bt maize and hybrid relative maturity on European corn borer Ostrinia nubilalis (Lepidoptera: Crambidae) ovipositional patterns

A three year study was carried out at Hoytville and at Wooster, Ohio, USA from 2006 to 2008 to investigate the influence of planting date, transgenic maize and hybrid maturity on Ostrinia nubilalis (Hubner) population dynamics and oviposition patterns. Maize plants were planted in late April or early May, mid‐May and early June during each year. The moth flight pattern showed bivoltine generations during the three years. The first moth flight peaked in June, with the populations declining during July. The second moth flight peaked in August and declined towards the end of September or early October. Egg mass density did not differ significantly between transgenic and non‐transgenic maize of different maturities. Significant differences were observed, however, among planting dates, sampling dates, and sampling date × planting date interactions. Generally higher numbers of egg masses from second generation moths were deposited on late planted maize than middle and early plantings.     

Host plant constituents as oviposition stimulants for a generalist herbivore: European corn borer

Oviposition response of the polyphagous European corn borer,Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae), to chemical constituents in host plants was investigated in the laboratory using two-choice bioassays. Foliar extracts of corn (Zea mays L.), pepper (Capsicum annuum L.) and potato (Solanum tuberosum L.) were prepared using the solvents pentane, acetone and methanol. In all three host plants, chemicals soluble in pentane stimulated oviposition. In potato, chemicals extractable in acetone also elicited a positive oviposition response. When presented with a choice between pentane extracts of corn and pepper, females preferred corn. No preferences were exhibited between pentane extracts of corn and potato or pepper and potato. Pentane extracts of corn husks, tassels, silk, and corn leaves from plants at early whorl and tassel (pre-pollen shed) stages of development also stimulated oviposition. Similar extracts from plants at 2-leaf and blister (when kernels resemble blisters) stages were not stimulatory. This indicates that plant phenology affects chemically mediated oviposition response in European corn borer. The potential use of plant chemicals for management ofO. nubilalis in the field is suggested.     

Diamondback moth oviposition: effects of host plant and herbivory

The oviposition behaviour of Plutella xylostella L. (Lepidoptera: Plutellidae) on Chinese cabbage (Brassica rapa L. Pekinensis, cv. Wombok), canola (Brassica napus L. cv. Thunder TT), and cabbage (Brassica oleracea L. Capitata, cv. sugarloaf) (Brassicaceae) was studied in the laboratory. In no‐choice experiments moths laid most eggs on the stems and lower three leaves of cabbage plants, the lower three leaves of canola plants, but on the upper three leaves of Chinese cabbage plants. The effects of conspecific herbivore damage to foliage could be replicated by mechanical damage. When foliage was damaged, injured cabbage and canola plants were preferred for oviposition over intact conspecifics, whereas injured Chinese cabbage plants were less preferred than intact conspecifics. However, when root tissue was damaged, intact cabbage and canola plants were preferred over injured conspecifics, whereas moths did not discriminate between root‐damaged and intact Chinese cabbage plants. Injury to upper leaves significantly affected the intra‐plant distribution of eggs. In cabbage and canola plants, injury to leaf 6 significantly increased the number of eggs laid on this leaf, resulting in a significant decrease in the number of eggs laid on the lower foliage/stem of plants, whereas in Chinese cabbage plants it significantly decreased the number of eggs laid on leaf 6. Following oviposition on intact plants, neonate larvae established the vast majority of feeding sites on leaves 5–8 in all three host plants, indicating that larvae moved a considerable distance from preferred oviposition sites in cabbage and canola plants. The growth rate of neonates fed on leaf‐6 tissue was significantly greater than that of those fed on leaf‐1 tissue; >90% of larvae completed development when fed exclusively on leaf‐6 tissue but no larvae completed development when fed exclusively on leaf‐1 tissue. The study demonstrates the complex and unpredictable interactions between P. xylostella and its host plants and provides a basis from which we can begin to understand observed distributions of the pest in Brassica crops.     

Associational susceptibility in broccoli: mediated by plant volatiles,impeded by ozone

Plant‐emitted volatile organic compounds (VOCs) mediate interactions within a plant community. Typically, receiving a signal from a damaged neighbour enhances the defensive attributes of a receiver plant. The mechanisms underlying plant–plant interactions may be divided into active and passive processes, both of which involve transit of VOCs between plants and are vulnerable to environmental perturbation. Numerous studies have documented between‐plant interactions, but the specific effects on a receiver plant's interactions with herbivores have received little attention. Moreover, the relative contributions of active and passive processes to plant defence and the effects of environmental pollutants on the processes have been largely unexplored. We used a system comprising Brassica oleracea var. italica (broccoli) and the specialist herbivore Plutella xylostella to test whether plants previously exposed to herbivore‐damaged neighbours differed from nonexposed plants in their susceptibility to oviposition. We then investigated the roles of active and passive mechanisms in our observations and whether differences in susceptibility remained under elevated ozone concentrations. Plants exposed to herbivore‐damaged neighbours were more susceptible to oviposition than plants exposed to undamaged neighbours, which indicates associational susceptibility. Mechanistically, active and passive volatile‐mediated processes occurred in tandem with the passive process – involving adsorption of sesquiterpenes to receiver plants – appearing to structure the oviposition response. Exposure to ozone rapidly degraded the sesquiterpenes and eliminated the associational susceptibility. Plant volatiles have typically been thought to play roles in between‐plant interactions and to promote receiver plant defence. Here, we show that receiver plants may also become more susceptible to oviposition and thus more likely to be damaged. Extensive disruption of volatile‐mediated interactions by an atmospheric pollutant highlights the need to consider the pervading environment and changes therein when assessing their ecological significance.