Herbivore-induced Volatile Organic Compounds Research Articles

Effects of far-red light on tritrophic interactions between the two-spotted spider mite (Tetranychus urticae) and the predatory mite Phytoseiulus persimilis on tomato.

The use of light-emitting diode (LED) lights in horticulture allows growers to adjust the light spectrum to optimize crop production and quality. However, changes in light quality can also influence plant-arthropod interactions, with possible consequences for pest management. The addition of far-red light has been shown to interfere with plant immunity, thereby increasing plant susceptibility to biotic stress and increasing pest performance. Far-red light also influences plant emission of volatile organic compounds (VOCs) and might thus influence tritrophic interactions with biological control agents. We investigated how far-red light influences the VOC-mediated attraction of the predatory mite Phytoseiulus persimilis to tomato plants infested with Tetranychus urticae, and its ability to control T. urticae populations. Far-red light significantly influences herbivore-induced VOC emissions of tomato plants, characterized by a change in relative abundance of terpenoids, but this did not influence the attraction of P. persimilis to herbivore-induced plants. Supplemental far-red light led to an increased population growth of T. urticae and increased numbers of P. persimilis. This resulted in a stronger suppression of T. urticae populations under supplemental far-red light, to similar T. urticae numbers as in control conditions without supplemental far-red light. We conclude that supplemental far-red light can change herbivore-induced VOC emissions but does not interfere with the attraction of the predator P. persimilis. Moreover, far-red light stimulates biological control of spider mites in glasshouse tomatoes due to increased population build-up of the biocontrol agent. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Plant genetic relatedness and volatile-mediated signalling between Solanum tuberosum plants in response to herbivory by Spodoptera exigua

It has been proposed that plant-plant signalling via herbivore-induced volatile organic compounds (VOCs) should be stronger between closely related than unrelated plants. However, empirical tests remain limited and few studies have provided detailed assessments of induced changes in VOCs emissions across plant genotypes to explain genetic relatedness effects. In this study, we tested whether airborne signalling in response to herbivory between Solanum tuberosum (potato) plants was contingent on plant genetic relatedness, and further investigated genotypic variation in VOCs potentially underlying signalling and its contingency on relatedness. We carried out a greenhouse experiment using 15 S. tuberosum varieties placing pairs of plants in plastic cages, i.e. an emitter and a receiver, where both plants were of the same genotype or different genotype thereby testing for self-recognition, an elemental form genetic relatedness effects. Then, for half of the cages within each level of relatedness the emitter plant was damaged by Spodoptera exigua larvae whereas for the other half the emitter was not damaged. Three days later, we placed S. exigua larvae on receivers to test for emitter VOC effects on leaf consumption and larval weight gain (i.e. induced resistance). In addition, we used a second group of plants subjected to the same induction treatment with the same S. tuberosum varieties to test for herbivore-induced changes in VOC emissions and variation in VOC emissions among these plant genotypes. We found that herbivory drove changes in VOC composition but not total emissions, and also observed quantitative and qualitative variation in constitutive and induced VOC emissions among varieties. Results from the bioassay showed that the amount of leaf area consumed and larval weight gain on receiver plants exposed to damaged emitters were significantly lower compared to mean values on receivers exposed to control emitters. However, and despite genotypic variation in induced VOCs, this signalling effect was not contingent on plant genetic relatedness. These findings provide evidence of VOCs-mediated signalling between S. tuberosum plants in response to S. exigua damage, but no evidence of self-recognition effects in signalling contingent on variation in VOC emissions among S. tuberosum varieties.

Plant Responses to Herbivory, Wounding, and Infection.

Plants have various self-defense mechanisms against biotic attacks, involving both physical and chemical barriers. Physical barriers include spines, trichomes, and cuticle layers, whereas chemical barriers include secondary metabolites (SMs) and volatile organic compounds (VOCs). Complex interactions between plants and herbivores occur. Plant responses to insect herbivory begin with the perception of physical stimuli, chemical compounds (orally secreted by insects and herbivore-induced VOCs) during feeding. Plant cell membranes then generate ion fluxes that create differences in plasma membrane potential (Vm), which provokes the initiation of signal transduction, the activation of various hormones (e.g., jasmonic acid, salicylic acid, and ethylene), and the release of VOCs and SMs. This review of recent studies of plant–herbivore–infection interactions focuses on early and late plant responses, including physical barriers, signal transduction, SM production as well as epigenetic regulation, and phytohormone responses.

Belowground plant-plant signaling of root infection by nematodes

Communication between plants mediated by herbivore-induced volatile organic compounds has been extensively studied aboveground. However, the role of root herbivory in belowground plant-plant communication is much less understood. We here investigated whether root herbivores can trigger plant roots to emit warning signals to neighbouring plants that are not yet in direct contact with them.We used a split-root system and infected half of the roots of Agrostis stolonifera plants with root-knot nematodes (Meloidogyne minor) and left the other half uninfected. As a control, we grew plants without nematodes in separate pots. Leachates from each split-root soil compartment and from soils with control plants were applied to separate pots with A. stolonifera plants, of which biomass allocation and morphological traits were measured one month after leachate addition.Plants receiving leachates from the soil with the nematode-free roots of the nematode-infected plants showed a significantly larger total biomass, more root branches, and deeper rooting than plants receiving leachates from the soil with the nematode-infected roots or from soil with control plants. Plants were taller and the root/shoot ratio was higher in plants receiving leachates from soil with the nematode-free roots than in plants receiving leachates from soil with nematode-infected roots. Shoot tiller number was higher in plants receiving leachates from either root compartment of the nematode-infected plants than in plants receiving control leachates.Our results suggest that an overcompensation response was triggered by systemically induced root-derived compounds from nematode-free roots of a plant locally infected with root-feeding nematodes. Signals from directly attacked roots of the same nematode-infected plant only caused receiver plants to develop more shoot tillers, possibly for future stolon development to grow away from the infected area. This may indicate an anticipatory tolerance response to root feeders that are still distant and an additional generalized escape response to root feeding.

Herbivore-induced volatile emissions are altered by soil legacy effects in cereal cropping systems

Aims (main purpose and research question)Soil properties, including microbial composition and nutrient availability, can influence the emissions of plant volatile organic compounds (VOCs) that serve as host-location cues for insect pests and their natural enemies. Agricultural practices have profound effects on soil properties, but how these influence crop VOCs remains largely unknown. The aim of this study was to investigate the effect of agricultural practices on constitutive and herbivore-induced VOC emissions by a major staple crop through soil legacy effects.MethodsIn a full factorial experiment, we measured VOC emissions by wheat (Triticum aestivum) grown in soil inoculum from wheat-fallow or wheat-cover crop rotations that was subjected to feeding by larval Cephus cinctus.Results (main findings)Under herbivory, plants grown in cover crop inoculum emitted greater total VOCs, including higher concentrations of 2-pentadecanone, an insect repellent, and nonanal, a compound important in the recruitment of natural enemies. Plants grown in fallow inoculum showed no differences in emissions whether under herbivory or not. Soil inoculum did not influence VOC emissions of plants in the absence of larval feeding.ConclusionsThese results suggest that agricultural practices influence crop VOC emissions through soil legacy effects. Additionally, crops grown in wheat-fallow rotations may be less successful recruiting natural enemies of pests through herbivore-induced VOC signaling.AbbreviationsVolatile organic compounds (VOCs); herbivore-induced plant volatiles (HIPV); green leaf volatiles (GLVs); northern Great Plains (NGP); wheat stem sawfly (WSS); gas chromatography-mass spectrometry (GC-MS); non-metric multidimensional scaling (NMDS); generalized linear mixed-effects model (GLMM).

The phytotoxic air-pollutant O3 enhances the emission of herbivore-induced volatile organic compounds (VOCs) and affects the susceptibility of black mustard plants to pest attack

Stress-induced changes to plant biochemistry and physiology can influence plant nutritional quality and subsequent interactions with herbivorous pests. However, the effects of stress combinations are unpredictable and differ to the effects of individual stressors. Here we studied the effects of exposure to the phytotoxic air-pollutant ozone (O3), feeding by larvae of the large cabbage white butterfly (Pieris brassicae), and a combination of the two stresses, on the emission of volatile organic compounds (VOCs) by black mustard plants (Brassica nigra) under field and laboratory conditions. Field-grown B. nigra plants were also measured for carbon-nitrogen (C–N) content, net photosynthetic activity (Pn), stomatal conductance (gs) and biomass. The effects of O3 on interactions between plants and a herbivorous pest were addressed by monitoring the abundance of wild diamondback moth larvae (Plutella xylostella) and feeding-damage to B. nigra plants in an O3-free air concentration enrichment (O3-FACE) field site. Herbivore-feeding induced the emission of VOCs that were not emitted by undamaged plants, both under field and laboratory conditions. The combination of O3 and herbivore-feeding stresses resulted in enhanced emission rates of several VOCs from field-grown plants. Short-term O3 exposure (of 10 days) and P. brassicae-feeding did not affect C–N content, but chronic O3 exposure (of 34 and 47 days) and P. brassicae-feeding exacerbated suppression of Pn. Ozone exposure also caused visible injury and decreased the plant biomass. Field-grown B. nigra under elevated O3 were infested with fewer P. xylostella larvae and received significantly less feeding damage. Our results suggest that plants growing in a moderately polluted environment may be of reduced quality and less attractive to foraging herbivores.

Plant volatile emission depends on the species composition of the neighboring plant community

BackgroundPlants grow in multi-species communities rather than monocultures. Yet most studies on the emission of volatile organic compounds (VOCs) from plants in response to insect herbivore feeding focus on one plant species. Whether the presence and identity of neighboring plants or plant community attributes, such as plant species richness and plant species composition, affect the herbivore-induced VOC emission of a focal plant is poorly understood.MethodsWe established experimental plant communities in pots in the greenhouse where the focal plant species, red clover (Trifolium pratense), was grown in monoculture, in a two species mixture together with Geranium pratense or Dactylis glomerata, or in a mixture of all three species. We measured VOC emission of the focal plant and the entire plant community, with and without herbivory of Spodoptera littoralis caterpillars caged on one red clover individual within the communities.ResultsHerbivory increased VOC emission from red clover, and increasing plant species richness changed emissions of red clover and also from the entire plant community. Neighbor identity strongly affected red clover emission, with highest emission rates for plants growing together with D. glomerata.ConclusionThe results from this study indicate that the blend of VOCs perceived by host searching insects can be affected by plant-plant interactions.

Species- and density-dependent induction of volatile organic compounds by three mite species in cassava and their role in the attraction of a natural enemy.

Upon damage by herbivores, plants induce an array of volatile organic compounds (VOCs) that mediate ecological interactions involving communication with organisms of thesecond and third trophic levels. VOC-mediated tritrophic interactions have largely been studied in various systems, including cassava (Manihot esculenta), but little is known about the chemical nature of herbivore-induced VOCs in this crop and the response they evoke in natural enemies. Several tetranychid and predatory mites are associated with cassava. Here, VOC emissions from uninfested plants and plants infested with 200 or 400 Mononychellus tanajoa, a specialist herbivore on cassava, and the generalists Tetranychus urticae and T. gloveri were measured. Dual-choice experiments were also conducted to assess the preference of inexperienced (reared on prey-infested bean plants) and experienced (adapted on prey-infested cassava plants) predatory mites, Neoseiulus idaeus (Phytoseiidae), between odors of uninfested plants versus odors of plants infested with M. tanajoa, T. urticae or T. gloveri. Two hundred individuals significantly increased the emissions of (Z)-3-hexen-1-ol, (E)-β-ocimene, β-caryophyllene, alloaromadendrene and (E)-geranyl acetone in T. urticae-infested plants, and (E)-β-ocimene and methyl salicylate (MeSA) in T. gloveri-infested plants. Four hundred individuals significantly increased the emissions of (Z)-3-hexen-1-ol, MeSA, α-pinene and D-limonene in M. tanajoa-infested plants. In addition, T. urticae at this density induced (E)-β-ocimene, D-limonene, (E)-geranyl acetone and six compounds that were not detected in other treatments. Tetranychus gloveri-infested plants induced the emissions of (E)-2-hexenal and D-limonene. Regardless of the infesting species, inexperienced N. idaeus did not discriminate between uninfested or infested plants. Upon experience, they discriminated between the odors of uninfested and T. urticae-damaged plants. Our findings reveal that mite infestations in cassava result in density-dependent and species-specific emission of VOCs, and that N. idaeus relies on associative learning to forage for its prey.

Priming of cowpea volatile emissions with defense inducers enhances the plant's attractiveness to parasitoids when attacked by caterpillars.

The manipulation of herbivore-induced volatile organic compounds (HI-VOCs) via the application of the inducers benzo(1,2,3)thiadiazole-7-carbothioic acid S-methyl ester (BTH) and laminarin (β-1,3-glucan) is known to enhance the attractiveness of caterpillar-damaged cotton and maize plants to parasitoids. To test if this is also the case for legumes, we treated cowpea (Vigna unguiculata var. unguiculata) with these inducers and studied the effects on HI-VOC emissions and the attraction of three generalist endoparasitoids. After the inducers had been applied and the plants subjected to either real or mimicked herbivory by Spodoptera littoralis caterpillars, females of the parasitoids Campoletis sonorensis and Microplitis rufiventris showed a strong preference for BTH-treated plants, whereas Cotesia females were strongly attracted to both BTH- and laminarin-treated plants with real or mimicked herbivory. Treated plants emitted more of certain HI-VOCs, but considerably less indole and linalool and less of several sesquiterpenes. Multivariate data analysis revealed that enhanced wasp attraction after treatment was correlated with high relative concentrations of nonanal, α-pinene, (E)-β-ocimene and (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), and with low relative concentrations of indole, (S)-linalool and (E)-β-farnesene. Inducer treatments had no significant effect on leaf consumption by the caterpillars. Our findings confirm that treating cowpea plants with inducers can enhance their attractiveness to biological control agents. © 2017 Society of Chemical Industry.

Herbivory by an Outbreaking Moth Increases Emissions of Biogenic Volatiles and Leads to Enhanced Secondary Organic Aerosol Formation Capacity.

In addition to climate warming, greater herbivore pressure is anticipated to enhance the emissions of climate-relevant biogenic volatile organic compounds (VOCs) from boreal and subarctic forests and promote the formation of secondary aerosols (SOA) in the atmosphere. We evaluated the effects of Epirrita autumnata, an outbreaking geometrid moth, feeding and larval density on herbivore-induced VOC emissions from mountain birch in laboratory experiments and assessed the impact of these emissions on SOA formation via ozonolysis in chamber experiments. The results show that herbivore-induced VOC emissions were strongly dependent on larval density. Compared to controls without larval feeding, clear new particle formation by nucleation in the reaction chamber was observed, and the SOA mass loadings in the insect-infested samples were significantly higher (up to 150-fold). To our knowledge, this study provides the first controlled documentation of SOA formation from direct VOC emission of deciduous trees damaged by known defoliating herbivores and suggests that chewing damage on mountain birch foliage could significantly increase reactive VOC emissions that can importantly contribute to SOA formation in subarctic forests. Additional feeding experiments on related silver birch confirmed the SOA results. Thus, herbivory-driven volatiles are likely to play a major role in future biosphere-vegetation feedbacks such as sun-screening under daily 24 h sunshine in the subarctic.

Herbivore-induced volatile organic compounds emitted by maize: Electrophysiological responses in Spodoptera frugiperda females

Herbivory induces the emission of volatile organic compounds (VOCs) which are involved in the attraction of predators and parasitoids. In spite of the large number of studies that have addressed the electrophysiological and behavioral responses of natural enemies to herbivore-induced VOCs, whether herbivores perceive these compounds remains largely unknown. By coupling chemical and electrophysiological (Gas Chromatography–Mass Spectrometry GC–MS and Gas Chromatography–Electroantennography GC–EAG) techniques we identified individual compounds emitted by maize upon feeding by Spodoptera frugiperda Walker (Lepidoptera: Noctuidae) that elicit a response in conspecific females. Herbivory induced significantly the emission of β-myrcene, (Z)-3-hexenyl acetate, (E)-β-ocimene, β-linalool, (E)-4,8-dimethyl-1,3,7-nonatriene [DMNT], indole, geranyl acetate, α-zingiberene, β-caryophyllene, (E)-α-bergamotene, (E)-β-farnesene, β-sesquiphellandrene, (E)-nerolidol, and 4,8,12-trimethyl-1,3,7,11-tridecatetraene [TMTT]. From these, eleven compounds elicited a response in the antennae of S. frugiperda females (virgin and mated). The antennae of virgin and mated females responded consistently to (Z)-3-hexenyl acetate, β-linalool, indole, (E)-β-farnesene and TMTT. In addition the sesquiterpenes ylangene/(+)-cycloisosativene evoked a response in the antennae even though these compounds were not significantly increased upon herbivory. The numbers of antennae of virgin or mated females responding to individual compounds were similar even though a higher percentage of the antennae of gravid female tested responded to geranyl acetate. The results show that S. frugiperda detects several herbivore-induced VOCs emitted by maize plants. These compounds may be responsible for repellence previously observed in this species by volatiles induced by conspecifics.

Optimizing Crops for Biocontrol of Pests and Disease.

Volatile compounds and extrafloral nectar are common defenses of wild plants; however, in crops they bear an as-yet underused potential for biological control of pests and diseases. Odor emission and nectar secretion are multigene traits in wild plants, and thus form difficult targets for breeding. Furthermore, domestication has changed the capacity of crops to express these traits. We propose that breeding crops for an enhanced capacity for tritrophic interactions and volatile-mediated direct resistance to herbivores and pathogens can contribute to environmentally-friendly and sustainable agriculture. Natural plant volatiles with antifungal or repellent properties can serve as direct resistance agents. In addition, volatiles mediating tritrophic interactions can be combined with nectar-based food rewards for carnivores to boost indirect plant defense.

Salinity stress effects on direct and indirect defence metabolites in maize

In nature, plants are often exposed to multiple stress factors at the same time. The effects of single biotic or abiotic stresses on plant metabolism are well documented but how plants respond to a combination of these is little researched. Here we studied the effects of high salinity and herbivory on levels of secondary compounds and gene expression associated with defences against insects. Hydroponically grown maize plants were subjected to sodium chloride (1, 50, 100mM NaCl) and/or damage by caterpillars of Spodoptera exigua. Salt-stressed plants showed stunted growth, reduced chlorophyll fluorescence and enhanced levels of reactive oxygen species and 1,4-benzoxazin-3-one aglycones (aBX). Herbivory induced higher transcript levels of the Zm-Bx1 gene involved in aBX biosynthesis and of the Zm-SerPIN gene coding for a serine proteinase inhibitor which might affect plant feeding insects. Herbivory also triggered the emission of volatile organic compounds (VOCs) that are attractive signals for parasitoids and predators and thus regarded as an indirect defence. Herbivore-induced metabolites were differentially affected in salt-stressed plants. High salinity resulted in transient priming of jasmonic acid while aBX levels were reduced in double-stressed plants. Salt stress led to lower herbivore-induced VOC emission per plant but not per unit biomass. However, quantitative shifts in individual compounds were found in both cases. Our study confirms the notion that combined stresses produce a unique phenotype that cannot be derived from single-stress effects. The ecological implications of these changes for organisms from different trophic levels and for plant fitness remain to be tested.

Soybean (Glycine max) plants genetically modified to express resistance to glyphosate: can they modify airborne signals in tritrophic interactions?

Upon herbivory, plants activate complex biochemical pathways that result in an array of defense responses including the emission of a novel blend of volatile organic compounds (VOCs). These compounds mediate the recruitment of predators and parasitoids that exert biological control of the attacking herbivore. Genetic manipulation of a particular trait to improve agricultural plant varieties may affect other traits as a result of possible pleiotropy or insertional mutations, which in turn can affect the interaction of the plant with other organisms. Changes in herbivore-induced VOC emissions are known to occur in transgenic plants engineered to express resistance to insects (mainly Bt-plants), not only as a result of modified insect behavior but also as a result of altered resource allocation. Transgenic glyphosate-resistant plants express a variant of the enzyme EPSPS (5-enolpyruvylshikimate-3-phosphate synthase) that is insensitive to the herbicide glyphosate. This enzyme is essential in metabolic routes that result in the synthesis of amino acids and secondary metabolites. We addressed whether the constitutive and Anticarsia gemmatalis-induced emissions of VOCs from a transgenic soybean line differ from those of the isoline, and whether changes may interfere in the foraging behavior of the predatory bug Podisus nigrispinus. Analyses showed that both herbivory and genotype influenced VOC emissions. In addition, the genotype affected the herbivore-induced VOC emission. Larger emissions were measured in the transgenic line than the non-transgenic line upon herbivory. The bioassays showed that P. nigrispinus significantly discriminated only between the odors of undamaged and damaged plants of the non-transgenic line. No preference was observed for herbivore-damaged plants of any of the two lines over the other. The results from this study suggest that despite a greater emission of volatiles the predators are less able to discriminate between herbivore-damaged and undamaged transgenic plants. This condition does not necessarily increase the preference of the predator for damaged non-transgenic plants over transgenic plants. This study opens possibilities for new studies of chemical ecology in tritrophic systems to assess the effect of transgenic glyphosate-resistant plants.

Indole is an essential herbivore-induced volatile priming signal in maize.

Herbivore-induced volatile organic compounds prime non-attacked plant tissues to respond more strongly to subsequent attacks. However, the key volatiles that trigger this primed state remain largely unidentified. In maize, the release of the aromatic compound indole is herbivore-specific and occurs earlier than other induced responses. We therefore hypothesized that indole may be involved in airborne priming. Using indole-deficient mutants and synthetic indole dispensers, we show that herbivore-induced indole enhances the induction of defensive volatiles in neighbouring maize plants in a species-specific manner. Furthermore, the release of indole is essential for priming of mono- and homoterpenes in systemic leaves of attacked plants. Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming. These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks.

Climate Change and Tritrophic Interactions: Will Modifications to Greenhouse Gas Emissions Increase the Vulnerability of Herbivorous Insects to Natural Enemies?

Insects are highly dependent on odor cues released into the environment to locate conspecifics or food sources. This mechanism is particularly important for insect predators that rely on kairomones released by their prey to detect them. In the context of climate change and, more specifically, modifications in the gas composition of the atmosphere, chemical communication-mediating interactions between phytophagous insect pests, their host plants, and their natural enemies is likely to be impacted. Several reports have indicated that modifications to plants caused by elevated carbon dioxide and ozone concentrations might indirectly affect insect herbivores, with community-level modifications to this group potentially having an indirect influence on higher trophic levels. The vulnerability of agricultural insect pests toward their natural enemies under elevated greenhouse gases concentrations has been frequently reported, but conflicting results have been obtained. This literature review shows that the higher levels of carbon dioxide, as predicted for the coming century, do not enhance the abundance or efficiency of natural enemies to locate hosts or prey in most published studies. Increased ozone levels lead to modifications in herbivore-induced volatile organic compounds (VOCs) released by damaged plants, which may impact the attractiveness of these herbivores to the third trophic level. Furthermore, other oxidative gases (such as SO2 and NO2) tend to reduce the abundance of natural enemies. The impact of changes in atmospheric gas emissions on plant-insect and insect-insect chemical communication has been under-documented, despite the significance of these mechanisms in tritrophic interactions. We conclude by suggesting some further prospects on this topic of research yet to be investigated.

The scent of danger: Volatile-mediated information transfer and defence priming in plants

Volatile organic compounds (VOCs) are constantly emitted by plants, and play a major role in information transfer between plants and other organisms. One of the consequences of VOC-mediated information transfer is that plants ‘warn’ neighbouring plants when they are attacked, enabling these neighbours to prime defence responses in anticipation of future attack. Priming refers to a memory effect in which previous exposure to a stimulus (i.e. VOCs) enables plants to respond faster and more strongly when presented with a future stimulus (i.e. herbivory, pathogen infection). In recent years, our knowledge of how VOCs are perceived by plants, and the broad-scale phenotypic changes they induce, has grown dramatically. Multiple plant species seem to prime defence responses following exposure to herbivore-induced VOCs. However, the mechanisms underlying priming remain speculative. In the present article we highlight recent advancements in our understanding of stress perception by plants and discuss hypotheses of what might be happening on a molecular level in primed plants. Furthermore, we discuss ecological consequences of priming responses such as consequences for plant competitive interactions, and interactions with mutualistic and antagonistic animals.

Herbivore‐induced plant volatiles: targets, perception and unanswered questions

SummaryPlants respond to mechanical wounding, herbivore feeding or infection by pathogens with the release of volatiles. Small C6 molecules termed green‐leaf volatiles form a general element in most of these blends; however, the overall composition is usually sufficiently specific that other organisms are able to determine the nature of the attacker. Receivers of herbivore‐induced volatile organic compounds (HI‐VOCs) comprise distant parts of the same plant (‘within‐plant signalling’), neighbouring plants (‘plant–plant signalling’), herbivores, and multiple carnivores that respond to the ‘plant's cry for help’, such as parasitoids and hyperparasitoids, entomopathogenic nematodes, and predatory mites, beetles, bugs and birds. In spite of intensive research efforts, many central questions still remain. How do plants perceive volatiles? What is the relative impact of each of the interactions with different receivers of HI‐VOCs on the fitness of the emitting plant and that of the interacting organisms? How long can these compounds remain stable in the atmosphere? Why are VOC‐mediated effects on herbivores and beneficial organisms not used as a common tool in sustainable agriculture? Here, I briefly summarize the ecological effects of HI‐VOC perception and discuss the most pertinent questions raised by participants at the 32nd New Phytologist Symposium in Buenos Aires.

Foraging leaf-cutting ants learn to reject Vitis vinifera ssp. vinifera plants that emit herbivore-induced volatiles.

Leaf-cutting ants (LCAs) are dominant herbivores of the Neotropics, as well as economically important pests. Their foraging ecology and patterns/mechanisms of food selection have received considerable attention. Recently, it has been documented that LCAs exhibit a delayed rejection of previously accepted food plants following treatment with a fungicide that makes the plants unsuitable as substrate for their symbiotic fungus. Here, we investigated whether LCAs similarly reject plants with induced chemical defenses, by combining analysis of volatile emissions with dual-choice bioassays that used LCA subcolonies (Atta sexdens L.). On seven consecutive days, foraging ants were given the choice between leaf disks from untreated control plants and test plants of Vitis vinifera ssp. vinifera L. treated with the phytohormone jasmonic acid (JA) to mimic herbivore attack. Chemical analysis revealed the emission of a characteristic set of herbivore-induced volatile organic compounds (VOC) from JA-induced plants. Dual-choice experiments indicated that workers did not show any preference initially, but that they avoided JA-treated plants from day five onwards. Our finding that A. sexdens foragers learn to avoid VOC-emitting plants, which are likely detrimental to their symbiotic fungus, represents the first evidence for avoidance learning in attine ants toward plants with induced defenses.

Induced defenses of Veronica spicata: Variability in herbivore-induced volatile organic compounds

Plants release volatile organic compounds (VOCs) that have many eco-physiological functions. Induction of plant VOCs is known to occur upon herbivory. Herbivore-induced VOCs are involved in the attraction of predators and parasitoids, a phenomenon known as an indirect defense of plants. We measured the VOC profiles of the wild species Veronica spicata with and without larval feeding and oviposition by the specialist butterfly Melitaea cinxia. V. spicata showed great plasticity when deploying indirect defences. The induction of several ubiquitous terpenoids and green leaf volatiles (GLVs) was associated with larval feeding, whereas the increase of two ketones, 6-methyl-5-hepten-2-one and t-geranylacetone and the suppression of GLVs were associated with oviposition by the butterfly.