Response of natural populations of predators and parasitoids to artificially induced volatile emissions in maize plants (Zea mays L.)

1 In response to herbivore attack, maize plants (Zea mays L.) emit a specific blend of induced volatiles. Artificial damage and subsequent treatment of the damaged site with caterpillar regurgitant induces the same response. The induced volatile chemicals are known to be highly attractive to several parasitoids of herbivores in laboratory bioassays, but very limited information is available on how the plant odours affect entomophagous insects in the field. 2 Experiments were conducted to determine if induced maize volatiles attract parasitic and predatory insects under field conditions and whether they affect their spatial distribution. 3 In a preliminary field experiment with blue sticky traps near treated (damaged and treated with caterpillar regurgitant) and healthy plants, more entomophagous insects (total number of parasitic Hymenoptera, Anthocoridae and Syrphidae) were trapped near treated plants than near healthy plants. 4 In a second experiment, attraction to the induced volatiles was monitored with sticky traps placed next to treated and healthy maize plants in a regular maize field. No significant differences between the two treatments were found, but significantly more insects (parasitic wasps, thrips and anthocorid bugs) were trapped near to the top of plants than on traps placed near the mid‐stem. Displacement of these insect groups within the field seemed to occur principally over the canopy, but under severe weather conditions they travelled lower in the canopy. 5 In a third experiment, the effect of induced maize odours on the spatial distribution of predators and parasitoids was investigated by placing sticky traps at different distances from healthy and treated plants. The higher catches of parasitoids near treated plants and the increased presence of these insects on the downwind side of treated plants support the notion that herbivore‐induced maize odours attract natural enemies of maize pests in the field.     

Shared signals -'alarm calls' from plants increase apparency to herbivores and their enemies in nature

The attraction of natural enemies of herbivores by volatile organic compounds as an induced indirect defence has been studied in several plant systems. The evidence for their defensive function originates mainly from laboratory studies with trained parasitoids and predators; the defensive function of these emissions for plants in natural settings has been rarely demonstrated. In native populations and laboratory Y-tube choice experiments with transgenic Nicotiana attenuata plants unable to release particular volatiles, we demonstrate that predatory bugs use terpenoids and green leaf volatiles (GLVs) to locate their prey on herbivore-attacked plants. By attracting predators with volatile signals, this native plant reduces its herbivore load – demonstrating the defensive function of herbivore-induced volatile emissions. However, plants producing GLVs are also damaged more by flea beetles. The implications of these conflicting ecological effects for the evolution of induced volatile emissions and for the development of sustainable agricultural practices are discussed.     

Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, shape Rhopalosiphum maidis

When maize plants, Zea mays L., are mechanically damaged and the damaged sites are treated with caterpillar regurgitant, the plants will release a specific blend of volatiles. It is known that these volatiles can be attractive to natural enemies of herbivores. We hypothesise that the plant volatiles constitute part of the induced plant defence and that herbivores will be affected by the odours as well. In laboratory and semi-field studies this hypothesis was tested for the aphid Rhopalosiphum maidis (Fitch) (Rhynchota, Sternorrhyncha, Aphididae).In a Y-tube olfactometer significantly more aphids chose the odour of healthy, undamaged maize seedlings when tested against clean air or plants treated with regurgitant. Clean air was chosen more often when tested next to the odour of treated plants. This apparently repellent effect of the odour of treated plants was significant for winged aphids, but not for the wingless aphids.In field experiments aphids were released in the centre of circles of eight potted maize plants. Four plants in each circle were damaged and treated with caterpillar regurgitant while the other plants were left unharmed. At different intervals after aphid release, the number of aphids was counted on each plant. Significantly fewer winged and wingless aphids were found back on treated plants than on healthy plants.We suggest that herbivores may be repelled by the odours because they could indicate that: 1) the plant has initiated the production of toxic compounds; 2) potential competitors are present on the plant; 3) the plant is attractive to parasitoids and predators. Aphids may be particularly sensitive to induced maize volatiles because one of the major compounds emitted by the plant is (E)--farnesene, which is a common alarm pheromone for aphids. Collections and analyses of the odours emitted by crushed R. maidis confirmed that it too emits (E)--farnesene when stressed. The results are discussed in context of plant defence strategies and their possible exploitation for the control of pest insects.     

High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines

Maize plants (Zea mays) attacked by caterpillars release a mixture of odorous compounds that attract parasitic wasps, natural enemies of the herbivores. We assessed the genetic variability of these induced volatile emissions among 31 maize inbred lines representing a broad range of genetic diversity used by breeders in Europe and North America. Odors were collected from young plants that had been induced by injecting them with caterpillar regurgitant. Significant variation among lines was found for all 23 volatile compounds included in the analysis: the lines differed enormously in the total amount of volatiles emitted and showed highly variable odor profiles distinctive of each genotype. Principal component analysis performed on the relative quantities of particular compounds within the blend revealed clusters of highly correlated volatiles, which may share common metabolic pathways. European and American lines belonging to established heterotic groups were loosely separated from each other, with the most clear-cut difference in the typical release of (E)-beta-caryophyllene by European lines. There was no correlation between the distances among the lines based on their odor profiles and their respective genetic distances previously assessed by neutral RFLP markers. This most comprehensive study to date on intraspecific variation in induced odor emission by maize plants provides a further example of the remarkably high genetic diversity conserved within this important crop plant. A better understanding of the genetic control of induced odor emissions may help in the development of maize varieties particularly attractive to parasitoids and other biological control agents and perhaps more repellent for herbivores.     

Differential Performance and Parasitism of Caterpillars on Maize Inbred Lines with Distinctly Different Herbivore-Induced Volatile Emissions

Plant volatiles induced by insect feeding are known to attract natural enemies of the herbivores. Six maize inbred lines that showed distinctly different patterns of volatile emission in laboratory assays were planted in randomized plots in the Central Mexican Highlands to test their ability to recruit parasitic wasps under field conditions. The plants were artificially infested with neonate larvae of the fall armyworm Spodoptera frugiperda, and two of its main endoparasitoids, Campoletis sonorensis and Cotesia marginiventris, were released in the plots. Volatiles were collected from equally treated reference plants in the neighbourhood of the experimental field. The cumulative amount of 36 quantified volatile compounds determined for each line was in good accordance with findings from the laboratory; there was an almost 15-fold difference in total emission between the two extreme lines. We found significant differences among the lines with respect to the numbers of armyworms recovered from the plants, their average weight gain and parasitism rates. Average weight of the caterpillars was negatively correlated with the average total amount of volatiles released by the six inbred lines. However, neither total volatile emission nor any specific single compound within the blend could explain the differential parasitism rates among the lines, with the possible exception of (E)-2-hexenal for Campoletis sonorensis and methyl salicylate for Cotesia marginiventris. Herbivore-induced plant volatiles and/or correlates thereof contribute to reducing insect damage of maize plants through direct plant defence and enhanced attraction of parasitoids, alleged indirect defence. The potential to exploit these volatiles for pest control deserves to be further evaluated.     

Antagonism between herbivore‐induced plant volatiles and trichomes affects tritrophic interactions

We used tomato genotypes deficient in the jasmonic acid (JA) pathway to study the interaction between the production of herbivore‐induced plant volatiles (HIPVs) that serve as information cues for herbivores as well as natural enemies of herbivores, and the production of foliar trichomes as defence barriers. We found that jasmonic acid‐insensitive1 (jai1) mutant plants with both reduced HIPVs and trichome production received higher oviposition of adult leafminers, which were more likely to be parasitized by the leafminer parasitoids than JA biosynthesis spr2 mutant plants deficient in HIPVs but not trichomes. We also showed that the preference and acceptance of leafminers and parasitoids to trichome‐removed plants from either spr2 or wild‐type (WT) genotypes over trichome‐intact genotypes can be ascribed to the reduced trichomes on treated plants, but not to altered direct and indirect defence traits such as JA, proteinase inhibitor (PI)‐II and HIPVs levels. Although the HIPVs of WT plants were more attractive to adult insects, the insects preferred trichome‐free jai1 plants for oviposition and also had greater reproductive success on these plants. Our results provide strong evidence that antagonism between HIPV emission and trichome production affects tritrophic interactions. The interactions among defence traits are discussed.     

Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant

In their defence against pathogens, herbivorous insects, and mites, plants employ many induced responses. One of these responses is the induced emission of volatiles upon herbivory. These volatiles can guide predators or parasitoids to their herbivorous prey, and thus benefit both plant and carnivore. This use of carnivores by plants is termed indirect defence and has been reported for many plant species, including elm, pine, maize, Lima bean, cotton, cucumber, tobacco, tomato, cabbage, and Arabidopsis thaliana. Herbivory activates an intricate signalling web and finally results in defence responses such as increased production of volatiles. Although several components of this signalling web are known (for example the plant hormones jasmonic acid, salicylic acid, and ethylene), our understanding of how these components interact and how other components are involved is still limited. Here we review the knowledge on elicitation and signal transduction of herbivory-induced volatile production. Additionally, we discuss how use of the model plant Arabidopsis thaliana can enhance our understanding of signal transduction in indirect defence and how cross-talk and trade-offs with signal transduction in direct defence against herbivores and pathogens influences plant responses.     

Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids

Direct and indirect plant defences are well studied, particularly in the Brassicaceae. Glucosinolates (GS) are secondary plant compounds characteristic in this plant family. They play an important role in defence against herbivores and pathogens. Insect herbivores that are specialists on brassicaceous plant species have evolved adaptations to excrete or detoxify GS. Other insect herbivores may even sequester GS and employ them as defence against their own antagonists, such as predators. Moreover, high levels of GS in the food plants of non-sequestering herbivores can negatively affect the growth and survival of their parasitoids. In addition to allelochemicals, plants produce volatile chemicals when damaged by herbivores. These herbivore induced plant volatiles (HIPV) have been demonstrated to play an important role in foraging behaviour of insect parasitoids. In addition, biosynthetic pathways involved in the production of HIPV are being unraveled using the model plant Arabidopsis thialiana. However, the majority of studies investigating the attractiveness of HIPV to parasitoids are based on experiments mainly using crop plant species in which defence traits may have changed through artificial selection. Field studies with both cultivated and wild crucifers, the latter in which defence traits are intact, are necessary to reveal the relative importance of direct and indirect plant defence strategies on parasitoid and plant fitness. Future research should also consider the potential conflict between direct and indirect plant defences when studying the evolution of plant defences against insect herbivory.     

Integration of two herbivore‐induced plant volatiles results in synergistic effects on plant defence and resistance

Plants can use induced volatiles to detect herbivore‐ and pathogen‐attacked neighbors and prime their defenses. Several individual volatile priming cues have been identified, but whether plants are able to integrate multiple cues from stress‐related volatile blends remains poorly understood. Here, we investigated how maize plants respond to two herbivore‐induced volatile priming cues with complementary information content, the green leaf volatile (Z)‐3‐hexenyl acetate (HAC) and the aromatic volatile indole. In the absence of herbivory, HAC directly induced defence gene expression, whereas indole had no effect. Upon induction by simulated herbivory, both volatiles increased jasmonate signalling, defence gene expression, and defensive secondary metabolite production and increased plant resistance. Plant resistance to caterpillars was more strongly induced in dual volatile‐exposed plants than plants exposed to single volatiles.. Induced defence levels in dual volatile‐exposed plants were significantly higher than predicted from the added effects of the individual volatiles, with the exception of induced plant volatile production, which showed no increase upon dual‐exposure relative to single exposure. Thus, plants can integrate different volatile cues into strong and specific responses that promote herbivore defence induction and resistance. Integrating multiple volatiles may be beneficial, as volatile blends are more reliable indicators of future stress than single cues.     

The spitting image of plant defenses: Effects of plant secondary chemistry on the efficacy of caterpillar regurgitant as an anti‐predator defense

In the arms race between plants, herbivores, and their natural enemies, specialized herbivores may use plant defenses for their own benefit, and variation in plant traits may affect the benefits that herbivores derive from these defenses. Pieris brassicae is a specialist herbivore of plants containing glucosinolates, a specific class of defensive secondary metabolites. Caterpillars of P. brassicae are known to actively spit on attacking natural enemies, including their main parasitoid, the braconid wasp Cotesia glomerata. Here, we tested the hypothesis that variation in the secondary metabolites of host plants affects the efficacy of caterpillar regurgitant as an anti‐predator defense. Using a total of 10 host plants with different glucosinolate profiles, we first studied natural regurgitation events of caterpillars on parasitoids. We then studied manual applications of water or regurgitant on parasitoids during parasitization events. Results from natural regurgitation events revealed that parasitoids spent more time grooming after attack when foraging on radish and nasturtium than on Brassica spp., and when the regurgitant came in contact with the wings rather than any other body part. Results from manual applications of regurgitant showed that all parameters of parasitoid behavior (initial attack duration, attack interruption, grooming time, and likelihood of a second attack) were more affected when regurgitant was applied rather than water. The proportion of parasitoids re‐attacking a caterpillar within 15 min was the lowest when regurgitant originated from radish‐fed caterpillars. However, we found no correlation between glucosinolate content and regurgitant effects, and parasitoid behavior was equally affected when regurgitant originated from a glucosinolate‐deficient Arabidopsis thaliana mutant line. In conclusion, host plant affects to a certain extent the efficacy of spit from P. brassicae caterpillars as a defense against parasitoids, but this is not due to glucosinolate content. The nature of the defensive compounds present in the spit remains to be determined, and the ecological relevance of this anti‐predator defense needs to be further evaluated in the field.     

Signal transduction downstream of salicylic and jasmonic acid in herbivory-induced parasitoid attraction by Arabidopsis is independent of JAR1 and NPR1

Plants can defend themselves indirectly against herbivores by emitting a volatile blend upon herbivory that attracts the natural enemies of these herbivores, either predators or parasitoids. Although signal transduction in plants from herbivory to induced volatile production depends on jasmonic acid (JA) and salicylic acid (SA), the pathways downstream of JA and SA are unknown. Use of Arabidopsis provides a unique possibility to study signal transduction by use of signalling mutants, which so far has not been exploited in studies on indirect plant defence. In the present study it was demonstrated that jar1‐1 and npr1‐1 mutants are not affected in caterpillar (Pieris rapae)‐induced attraction of the parasitoid Cotesia rubecula. Both JAR1 and NPR1 (also known as NIM1) are involved in signalling downstream of JA in induced defence against pathogens such as induced systemic resistance (ISR). NPR1 is also involved in signalling downstream of SA in defence against pathogens such as systemic acquired resistance (SAR). These results demonstrate that signalling downstream of JA and SA differs between induced indirect defence against herbivores and defence against pathogens such as SAR and ISR. Furthermore, it was demonstrated that herbivore‐derived elicitors are involved in induced attraction of the parasitoid Cotesia rubecula     

Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize

Plant volatiles function as important signals for herbivores, parasitoids, predators, and neighboring plants. Herbivore attack can dramatically increase plant volatile emissions in many species. However, plants do not only react to herbivore-inflicted damage, but also already start adjusting their metabolism upon egg deposition by insects. Several studies have found evidence that egg deposition itself can induce the release of volatiles, but little is known about the effects of oviposition on the volatiles released in response to subsequent herbivory. To study this we measured the effect of oviposition by Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) moths on constitutive and herbivore-induced volatiles in maize (Zea mays L.). Results demonstrate that egg deposition reduces the constitutive emission of volatiles and suppresses the typical burst of inducible volatiles following mechanical damage and application of caterpillar regurgitant, a treatment that mimics herbivory. We discuss the possible mechanisms responsible for reducing the plant’s signaling capacity triggered by S. frugiperda oviposition and how suppression of volatile organic compounds can influence the interaction between the plant, the herbivore, and other organisms in its environment. Future studies should consider oviposition as a potential modulator of plant responses to insect herbivores.     

Similar attractiveness of maize volatiles induced by Helicoverpa armigera and Pseudaletia separata to the generalist parasitoid Campoletis chlorideae

Campoletis chlorideae Uchida (Hymenoptera: Ichneumonidae), a major larval endoparasitoid of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), also attacks many other noctuid caterpillars. We investigated the attractiveness of H. armigera‐ and Pseudaletia separata (Lepidoptera: Noctuidae)‐infested maize [Zea mays L. (Poaceae)] plants to C. chlorideae, and analyzed the volatiles emitted from infested plants and undamaged plants. Considering the reported specific induction of plant volatiles by elicitors in the caterpillar regurgitant, we also tested the response of the parasitoid to mechanically damaged plants treated with caterpillar regurgitant or water and measured the volatiles released by these plants. In wind‐tunnel bioassays, C. chlorideae was strongly attracted to herbivore‐induced maize volatiles. Mechanically damaged plants, whether they were treated with caterpillar regurgitant or water, were more attractive to the parasitoid than undamaged plants. The parasitoid did not distinguish between maize seedlings infested by the two noctuid insects, nor did they show a difference in attraction to mechanically damaged plants treated with caterpillar regurgitant or water. Coupled gas chromatography–mass spectrometer (GC‐MS) analysis revealed that 15 compounds were commonly emitted by herbivore‐infested and mechanically damaged maize plants, whereas only two compounds were released in minor amounts from undamaged plants. Infestation by H. armigera specifically induced four terpenoids, β‐pinene, β‐myrcene, D‐limonene, and (E)‐nerolidol, which were not induced by infestation of P. separata and mechanical damage, plus caterpillar regurgitant or water. Two compounds, geranyl acetate and β‐sesquiphellandrene, were also induced by the infestation of H. armigera, but not by the infestation of P. separata. All treated maize plants released volatiles in significantly larger total amounts than did undamaged plants. Maize plants infested by H. armigera emitted greater amounts of volatiles than plants infested by P. separata. The treatment with caterpillar regurgitant resulted in larger amounts of volatile emission than the treatment with water did in mechanically damaged plants. The amounts of emissions of individual compounds were also different between differently treated plants.     

Herbivore-induced, indirect plant defences

Indirect responses are defensive strategies by which plants attract natural enemies of their herbivores that act as plant defending agents. Such defences can be either constitutively expressed or induced by the combined action of mechanical damage and low- or high-molecular-weight elicitors from the attacking herbivore. Here, we focus on two induced indirect defences, namely the de novo production of volatiles and the secretion of extrafloral nectar, which both mediate interactions with organisms from higher trophic levels (i.e., parasitoids or carnivores). We give an overview on elicitors, early signals, and signal transduction resulting in a complex regulation of indirect defences and discuss effects of cross-talks between the signalling pathways (synergistic and antagonistic effects). In the light of recent findings, we review molecular and genetic aspects of the biosynthesis of herbivore-induced plant volatiles comprising terpenoids, aromatic compounds, and metabolites of fatty acids which act as infochemicals for animals and some of which even induce defence genes in neighbouring plants. Finally, ecological aspects of these two indirect defences such as their variability, specificity, evolution as well as their ecological relevance in nature are discussed.     

Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host

Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids.     

Larval parasitism rate increases in herbivore‐damaged trees: a field experiment with cyclic birch feeding moths

Indirect plant defence mechanisms enhance the effectiveness of natural enemies of herbivores. Herbivore‐induced plant volatiles (HIPVs) attract the parasitoids of insect herbivores as shown both in numerous choice tests conducted under laboratory conditions and in relatively few common‐garden setups in agro‐ecosystems. However, the importance of this indirect defence trait at higher levels of biological organization has yet to be investigated through natural field experiments. Here, we report a field experiment of larval parasitism of two cyclic geometrid defoliators in herbivore‐damaged and fairly intact mountain birch Betula pubescens ssp. czerepanovii under natural conditions. Parasitism rates in larvae of the autumnal (Epirrita autumnata) and winter moth (Operophtera brumata) exposed for 30 h on defoliated trees were more than twice as high as those on control trees. This finding indicates that hymenopteran parasitoids were attracted to previously defoliated trees by some cues from the host plants, HIPVs being the most likely candidates. The third trophic level should thus be considered in natural plant herbivore interactions. Furthermore, parasitoids and food resources are key factors in the population regulation of forest insect pests, and indirect plant defences could be important in their interactions. Our research also emphasizes the quality of control treatments in field experiments, since immediate plant responses easily obscure the results as soon as control trees become infested by herbivorous insects.     

Induced defence in detached uninfested plant leaves: effects on behaviour of herbivores and their predators

Summary Induction of plant defence against herbivores may include the attraction by volatile infochemicals of natural enemies of the herbivore. The emitted volatiles that mediate this attraction may also affect the behaviour of the herbivore itself. In this paper we investigate the response of the herbivorous spider miteTetranychus urticae and the predatory mitePhytoseiulus persimilis towards volatiles whose production is induced in detached Lima bean leaves. Detached uninfested Lima bean leaves were incubated on wet cotton wool on which bean leaves infested with spider mites (T. urticae) were present simultaneously or had been present previously. These treatments induce the production of volatile infochemicals in the uninfested bean leaf tissue: predatory mites are attracted and spider mites are deterred. These are the first data on the response of predators and herbivores to plant volatiles whose production was induced in detached uninfested leaves.     

The influence of intact-plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays

Induced plant responses to insect attack include the release of volatile chemicals. These volatiles are used as host-location signals by foraging parasitoids, which are natural enemies of insect herbivores. A plant's response to herbivory can be influenced by factors present in insect oral secretions. Volicitin (N-(17-hydroxylinolenoyl)-L-glutamine), identified in beet armyworm (Spodoptera exigua) oral secretions, stimulates volatile release in corn (Zea mays L.) seedlings in a manner similar to beet armyworm herbivory. Volicitin is hypothesized to trigger release of induced volatiles, at least in part, by modulating levels of the wound hormone, jasmonic acid (JA). We compare the sesquiterpene volatile release of damaged leaves treated with aqueous buffer only or with the same buffer containing volicitin or JA. Leaves were damaged by scratching with a razor and test solutions were applied to the scratched area. The leaves were either excised from the plant or left intact shortly after this treatment. Plants were treated at three different times (designated as Evening, Midnight, and Morning) and volatiles were collected in the subsequent photoperiod. JA and volicitin treatments stimulated the release of volatile sesquiterpenes, namely beta-caryophyllene, (E)-alpha-bergamotene, and (E)-beta-farnesene. In all cases, JA stimulated significant sesquiterpene release above mechanical damage alone. Volicitin induced an increase in sesquiterpene volatiles for all excised-leaf bioassays and the Midnight intact plants. Volicitin treatments in the Evening and Morning intact plants produced more sesquiterpenes than the untreated controls, while mechanical damage alone produced an intermediate response that did not differ from either treatment group. Excised leaves produced a 2.5- to 8.0-fold greater volatile response than similarly treated intact plants. Excision also altered the ratio of JA-and volicitin-induced sesquiterpene release by preferentially increasing (E)-beta-farnesene levels relative to beta-caryophyllene. The inducibility of volatile release varied with time of treatment. On average, sesquiterpene release was highest in the Midnight excised leaves and lowest in the Morning intact plants. The duration of induced volatile release also differed between treatments. On average, JA produced a sustained release of sesquiterpenes over time, with over 20% of the combined sesquiterpenes released in the third and final volatile collection period. In contrast, less than 8% of the combined sesquiterpenes induced by volicitin were emitted during this period. The large quantitative differences between intact plants and detached leaves suggest that the results of assays using excised tissues should be cautiously interpreted when considering intact-plant models.     

An ecological cost of plant defence: attractiveness of bitter cucumber plants to natural enemies of herbivores

Plants produce defences that act directly on herbivores and indirectly via the attraction of natural enemies of herbivores. We examined the pleiotropic effects of direct chemical defence production on indirect defence employing near‐isogenic varieties of cucumber plants (Cucumis sativus) that differ qualitatively in the production of terpenoid cucurbitacins, the most bitter compounds known. In release–recapture experiments conducted in greenhouse common gardens, blind predatory mites were attracted to plants infested by herbivorous mites. Infested sweet plants (lacking cucurbitacins), however, attracted 37% more predatory mites than infested bitter plants (that produce constitutive and inducible cucurbitacins). Analysis of the headspace of plants revealed that production of cucurbitacins was genetically correlated with large increases in the qualitative and quantitative spectrum of volatile compounds produced by plants, including induced production of (E )‐β‐ocimene (3E )‐4,8‐dimethyl‐1,3,7‐nonatriene, (E,E)‐α‐farnesene, and methyl salicylate, all known to be attractants of predators. Nevertheless, plants that produced cucurbitacins were less attractive to predatory mites than plants that lacked cucurbitacins and predators were also half as fecund on these bitter plants. Thus, we provide novel evidence for an ecological trade‐off between direct and indirect plant defence. This cost of defence is mediated by the effects of cucurbitacins on predator fecundity and potentially by the production of volatile compounds that may be repellent to predators.     

Jasmonate-deficient plants have reduced direct and indirect defences against herbivores

Plants employ a variety of defence mechanisms, some of which act directly by having a negative effect on herbivores and others that act indirectly by attracting natural enemies of herbivores. In this study we asked if a common jasmonate‐signalling pathway links the regulation of direct and indirect defences in plants. We examined the performance of herbivores (direct defence) and the attraction of natural enemies of herbivores (indirect defence) to wild‐type tomato plants and mutant plants that are deficient in the production of the signalling hormone jasmonic acid. Wild‐type plants supported lower survivorship of caterpillars compared with jasmonic acid‐deficient plants. Damaged wild‐type plants were more attractive to predaceous mites compared with undamaged wild‐type plants, whereas damaged jasmonate‐deficient plants were not more attractive to predators. Damaged wild‐type plants induced a greater production of volatile compounds (primarily the sesquiterpene β‐caryophyllene and the monoterpenes α‐pinene, β‐pinene, 2‐carene and β‐phellandrene) compared with damaged jasmonate‐deficient plants. Treating jasmonate‐deficient plants with exogenous jasmonic acid restored both the direct and indirect defence capabilities, demonstrating that jasmonic acid is an essential regulatory component for the expression of direct and indirect plant defence.