Do plants use airborne cues to recognize herbivores on their neighbours?

Plants show defensive responses after exposure to volatiles from neighbouring plants infested by herbivores. When a plant’s neighbours host only species of herbivores that do not feed on the plant itself, the plant can conserve energy by maintaining a low defence level. An intriguing question is whether plants respond differently to volatiles from plants infested by herbivores that pose greater or lesser degrees of danger. We examined the secretion of extrafloral nectar (EFN) in lima bean plants exposed to volatiles from cabbage plants infested by common cutworm, two-spotted spider mites, or diamondback moth larvae. Although the first two herbivore species feed on lima bean plants, diamondback moth larvae do not. As a control, lima bean plants were exposed to volatiles from uninfested cabbage plants. Only when exposed to volatiles from cabbage plants infested by spider mites did lima bean plants significantly increase their EFN secretion compared with the control. Increased EFN secretion can function as an indirect defence by supplying the natural enemies of herbivores with an alternative food source. Of the three herbivore species, spider mites were the most likely to move from cabbage plants to lima bean plants and presumably posed the greatest threat. Although chemical analyses showed differences among treatments in volatiles produced by herbivore-infested cabbage plants, which compounds or blends triggered the increased secretion of EFN by lima bean plants remains unclear. Thus, our results show that plants may tune their defence levels according to herbivore risk level.     

Host plants alter their volatiles to help a solitary egg parasitoid distinguish habitats with parasitized hosts from those without

When attacked by herbivores, plants emit volatiles to attract parasitoids and predators of herbivores. However, our understanding of the effect of plant volatiles on the subsequent behaviour of conspecific parasitoids when herbivores on plants are parasitized is limited. In this study, rice plants were infested with gravid females of the brown planthopper (BPH) Nilaparvata lugens for 24 hr followed by another 24 hr in which the BPH eggs on plants were permitted to be parasitized by their egg parasitoid, Anagrus nilaparvatae; volatiles from rice plants that underwent such treatment were less attractive to subsequent conspecific parasitoids compared to the volatiles from plants infested with gravid BPH females alone. Chemical analysis revealed that levels of JA and JA-Ile as well as of four volatile compounds—linalool, MeSA, α-zingiberene and an unknown compound—from plants infested with BPH and parasitized by wasps were significantly higher than levels of these compounds from BPH-infested plants. Laboratory and field bioassays revealed that one of the four increased chemicals—α-zingiberene—reduced the plant's attractiveness to the parasitoid. These results suggest that host plants can fine-tune their volatiles to help egg parasitoids distinguish host habitats with parasitized hosts from those without.     

Host plant scents attract rolled-leaf beetles to Neotropical gingers in a Central American tropical rain forest

Leaf volatile chemicals are known to reduce herbivory rates by repelling or intoxicating insect herbivores and by attracting the predators and parasitoids of herbivores. However, leaf volatiles may also be used by insect herbivores as cues to locate their host plants. Leaf volatiles are suggested to be important host search cues for herbivores in structurally complex and diverse habitats, such as tropical rain forests. A group of insect herbivores, the rolled-leaf beetles (Coleoptera: Chrysomelidae: Hispinae), have maintained a highly specialized interaction with Neotropical gingers (Zingiberales) for ca. 60 million years. In this study, we explored chemical attraction to host plants under controlled laboratory conditions, using four sympatric rolled-leaf beetle species, Cephaloleia dorsalis Baly, Cephaloleia erichsonii Baly, Cephaloleia fenestrata Weise, and Cephaloleia placida Baly. For each beetle species, we investigated (i) whether it was repelled or attracted by leaf scents produced by four host and four non-host plant species, including Neotropical gingers in the families Marantaceae, Costaceae, and Zingiberaceae; and (ii) its ability to use scents to detect its host plant. We found that rolled-leaf beetles can detect and are attracted by leaf volatiles from both host and non-host gingers. Additionally, when beetles were simultaneously exposed to leaf volatiles from host and non-host plants, three rolled-leaf beetle species were significantly more attracted by volatiles from their host plants than from non-hosts. Only one of the beetle species was not able to discriminate between host and non-host scents.     

外源茉莉酸和茉莉酸甲酯诱导植物抗虫作用及其机理

综述了茉莉酸(jasmonic acid, JA)和茉莉酸甲酯(methyl jasmo nate, MJA)的分子结构和应用其诱导的植物抗虫作用及其机制。植物受外源茉莉酸或茉莉酸甲酯刺激后,一条反应途径是由硬脂酸途径激活防御基因,另一条途径是直接激活防御基因。防御基因激活后导致代谢途径重新配置,并可能诱导植物产生下列4种效应：（1）直接防御,即植物产生对害虫有毒的物质、抗营养和抗消化的酶类,或具驱避性和妨碍行为作用的化合物;（2）间接防御,即产生吸引天敌的挥发物;（3）不防御,即无防御反应;（4）负防御,即产生吸引害虫的挥发物。     

Damage to sagebrush attracts predators but this does not reduce herbivory

Emissions of volatiles increase following herbivory from many plant species and volatiles may serve multiple functions. Herbivore‐induced volatiles attract predators and parasitoids of herbivores and are often assumed to benefit plants by facilitating top‐down control of herbivores; this benefit of induced emissions has been tested only a few times. Volatile compounds released by experimentally clipped sagebrush shoots have been shown to reduce levels of chewing damage experienced by other shoots on the same plant and on neighboring sagebrush plants. In this study, I asked whether experimental clipping attracted predators of herbivorous insects to sagebrush shoots. I also evaluated aphid populations and chewing damage on clipped and unclipped shoots and whether predators were likely to have caused differences in aphids and chewing damage. Shoots that had been clipped recruited more generalist predators, particularly coccinellids and Geocoris spp. in visual surveys conducted during two seasons. Clipping also caused increased numbers of parasitized aphids in one season. Ants were common tending aphids but were not significantly affected by clipping. Despite the increase in generalist predators, clipped plants were more likely to support populations of aphids that increased during both seasons compared to aphids on unclipped control plants. Clipped shoots suffered less damage by chewing herbivores in the 1‐year in which this was measured. Chewing damage was not correlated with numbers of predators. These results suggest that predators and parasitoids were attracted to experimentally clipped sagebrush plants but that these predators were not effective at reducing net damage to the plant. This conclusion is not surprising as much of the herbivory is inflicted by grasshoppers and deer, herbivores that are not vulnerable to the predators attracted to sagebrush volatiles. More generally, it should not be assumed that predators that are attracted by herbivore‐induced volatiles necessarily benefit the plant without testing this hypothesis under field conditions.     

Evolution of signal emission by uninfested plants to help nearby infested relatives

Herbivory by arthropods often induces the emission of plant volatiles, which attract natural enemies of the herbivores. This induced emission of volatiles is considered to be a strategy of plants to effectively defend against herbivores by employing bodyguards. Recent empirical research has revealed that these volatiles can also affect neighboring undamaged plants and cause them to emit volatiles secondarily. Provided that signal emission imposes some cost on plants, the evolutionary advantage to undamaged plants in the emission of such secondary signals is unclear. We hypothesized that plants have evolved to emit a secondary signal to help nearby relatives by promoting the recruitment of natural enemies, whereby they increase inclusive fitness. We constructed a simulation model to evaluate this hypothesis. Our simulations suggest that a secondary signal evolves if the following five conditions are met: the cost of the signal is low; the potential risk of infestation is high; the attractiveness of the signal to natural enemies is highly positively correlated with the local density of the signal chemical; dispersal of offspring is spatially restricted, causing population viscosity, and; sufficient vacant space is available, allowing the population to be elastic.     

Acquired immunity to herbivory and allelopathy caused by airborne plant emissions

Numerous plant species respond to volatile cues to adjust their defenses against herbivores. Some volatile chemicals, such as terpenoids and green leaf volatiles, that are responsible for communication between plants and arthropods are also required for intraspecific communication between plants and for coordination among branches within a single plant. We are now aware that some ‘receiver’ plants are able to eavesdrop on their neighbors and tailor their defenses to their current and expected risks caused by herbivores. By contrast, a suite of volatiles also serve as natural herbicides (allelochemicals) that are detrimental for receiver plants. Since various molecular and ecological mechanisms underlying these phenomena have been clarified, it is time to ask whether more plants eavesdrop on infochemical cues, and if these cues that allow them to adjust their defenses to suit their risk also increase their fitness as a result.     

Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles

Feeding damage to plants by insect herbivores induces the production of plant volatiles, which are attractive to the herbivores natural enemies. Little is understood about the plant biochemical pathways involved in aphid-induced plant volatile production. The aphid parasitoid Diaeretiella rapae can detect and respond to aphid-induced volatiles produced by Arabidopsis thaliana. When given experience of those volatiles, it can learn those cues and can therefore be used as a novel biosensor to detect them. The pathways involved in aphid-induced volatile production were investigated by comparing the responses of D. rapae to volatiles from a number of different transgenic mutants of A. thaliana, mutated in their octadecanoid, ethylene or salicylic acid wound-response pathways and also from wild-type plants. Plants were either undamaged or infested by the peach-potato aphid, Myzus persicae. It is demonstrated that the octadecanoid pathway and specifically the COI1 gene are required for aphid-induced volatile production. The presence of salicylic acid is also involved in volatile production. Using this model system, in combination with A. thaliana plants with single point gene mutations, has potential for the precise dissection of biochemical pathways involved in the production of aphid-induced volatiles.     

Plant volatiles as method of communication

Plants emit volatile compounds that can act as a communication method to insects, neighboring plants and pathogens. Plants respond to leaf and root damage by herbivores and pathogens by emitting these compounds. The volatile compounds can deter the herbivores or pathogens directly or indirectly by attracting their natural enemies to kill them. The simultaneous damage of plants by herbivores and pathogens can influence plant defense. The induced plant volatiles can also make neighboring plants ready for defense or induce defense in parts distant from the damaged area of the same plant. Belowground root herbivory can alter the defense response to aboveground leaf herbivory. In addition, most plants normally emit volatile compounds from their flowers that directly attract foraging mutualistic insects for nectar, which in turn perform the very important function of pollination for subsequent reproduction. The volatile compounds emitted from the floral and vegetative parts of plants belong to three main classes of compounds: terpenoids, phenylpropanoids/benzenoids, and C6-aldehydes (green-leaf volatiles). The volatile phytohormones methyl salicylate and methyl jasmonate serve as important signaling molecules for communication purposes, and interact with each other to optimize the plant defense response. Here we discuss and integrate the current knowledge on all types of communication between plants and insects, neighboring plants and pathogens that are mediated through plant volatiles.     

Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context

Herbivorous and carnivorous arthropods use plant volatiles when foraging for food. In response to herbivory, plants emit a blend that may be quantitatively and qualitatively different from the blend emitted when intact. This induced volatile blend alters the interactions of the plant with its environment. We review recent developments regarding the induction mechanism as well as the ecological consequences in a multitrophic and evolutionary context. It has been well established that carnivores (predators and parasitoids) are attracted by the volatiles induced by their herbivorous victims. This concerns an active plant response. In the case of attraction of predators, this is likely to result in a fitness benefit to the plant, because through consumption a predator removes the herbivores from the plant. However, the benefit to the plant is less clear when parasitoids are attracted, because parasitisation does usually not result in an instantaneous or in a complete termination of consumption by the herbivore. Recently, empirical evidence has been obtained that shows that the plant's response can increase plant fitness, in terms of seed production, due to a reduced consumption rate of parasitized herbivores. However, apart from a benefit from attracting carnivores, the induced volatiles can have a serious cost because there is an increasing number of studies that show that herbivores can be attracted. However, this does not necessarily result in settlement of the herbivores on the emitting plant. The presence of cues from herbivores and/or carnivores that indicate that the plant is a competitor- and/or enemy-dense space, may lead to an avoidance response. Thus, the benefit of emission of induced volatiles is likely to depend on the prevailing faunal composition. Whether plants can adjust their response and influence the emission of the induced volatiles, taking the prevalent environmental conditions into account, is an interesting question that needs to be addressed. The induced volatiles may also affect interactions of the emitting plant with its neighbours, e.g., through altered competitive ability or by the neighbour exploiting the emitted information.Major questions to be addressed in this research field comprise mechanistic aspects, such as the identification of the minimally effective blend of volatiles that explains the attraction of carnivores to herbivore-infested plants, and evolutionary aspects such as the fitness consequences of induced volatiles. The elucidation of mechanistic aspects is important for addressing ecological and evolutionary questions. For instance, an important tool to address ecological and evolutionary aspects would be to have plant pairs that differ in only a single trait. Such plants are likely to become available in the near future as a result of mechanistic studies on signal-transduction pathways and an increased interest in molecular genetics.     

虫害诱导的植物挥发物:基本特性、生态学功能及释放机制

植物在遭受植食性昆虫攻击时,能通过释放挥发物调节植物、植食性昆虫及其天敌三者间的相互关系,并由此而防御植食性昆虫。主要就虫害诱导的植物挥发物的基本特性、生态学功能及其释放机制进行了系统性综述,并提出了今后的研究方向。     

Inbreeding in horsenettle (Solanum carolinense) alters night-time volatile emissions that guide oviposition by Manduca sexta moths

Plant volatiles serve as key foraging and oviposition cues for insect herbivores as well as their natural enemies, but little is known about how genetic variation within plant populations influences volatile-mediated interactions among plants and insects. Here, we explore how inbred and outbred plants from three maternal families of the native weed horsenettle (Solanum carolinense) vary in the emission of volatile organic compounds during the dark phase of the photoperiod, and the effects of this variation on the oviposition preferences of Manduca sexta moths, whose larvae are specialist herbivores of Solanaceae. Compared with inbred plants, outbred plants consistently released more total volatiles at night and more individual compounds—including some previously reported to repel moths and attract predators. Female moths overwhelmingly chose to lay eggs on inbred (versus outbred) plants, and this preference persisted when olfactory cues were presented in the absence of visual and contact cues. These results are consistent with our previous findings that inbred plants recruit more herbivores and suffer greater herbivory under field conditions. Furthermore, they suggest that constitutive volatiles released during the dark portion of the photoperiod can convey accurate information about plant defence status (and/or other aspects of host plant quality) to foraging herbivores.     

二化螟绒茧蜂对二化螟及其寄主植物挥发物的趋性反应

利用Y-型嗅觉仪研究了二化螟绒茧蜂Cotesia chilonis对寄主植物（水稻或茭白）、二化螟Chilo suppressalis幼虫、虫粪及虫害苗挥发物的行为反应。健康植株、二化螟幼虫和虫粪的挥发物对二化螟绒茧蜂具有显著引诱作用。在虫害苗与健康苗挥发物之间,二化螟绒茧蜂显著地偏好虫害苗,但当去除虫害苗中的幼虫和虫粪后,寄生蜂对去虫苗与机械损伤苗的选择无显著差异;在虫害苗与有虫健康苗之间,寄生蜂显著趋向虫害苗,表明虫害苗本身释放的挥发物对二化螟绒茧蜂引诱作用与机械损伤苗无显著差异,但与二化螟幼虫或虫粪挥发物之间可能具有协同增效作用。水稻苗经机械损伤或损伤后以二化螟幼虫唾液处理,其挥发物对二化螟绒茧蜂的引诱作用无显著改变。二化螟绒茧蜂对不同为害程度水稻挥发物的选择无显著差异。二化螟绒茧蜂对两种寄主植物的健康苗、虫害苗、取食两种植物的幼虫及虫粪的挥发物的选择无显著差异。结果表明,二化螟绒茧蜂栖境定位和寄主选择过程中所利用的挥发物主要来自寄主植物、二化螟幼虫和虫粪以及虫害苗与幼虫和虫粪的协同作用。     

Induction of plant responses to oviposition and feeding by herbivorous arthropods: a comparison

Plants may respond both to feeding and oviposition by herbivorous insects. While responses of plants to feeding damage by herbivores have been studied intensively during the past decades, only a few, but growing number of studies consider the reactions of plants towards egg deposition by herbivorous insects. Plants showing defensive response to oviposition by herbivores do not `wait' until being damaged by feeding, but may instead react towards one of the initial steps of herbivore attack, the egg deposition. Direct plant defensive responses to feeding act directly against the feeding stages of the herbivores. However, a plant may also show direct defensive responses to egg deposition by (a) formation of neoplasms, (b) formation of necrotic tissue (= hypersensitive response), and (c) production of oviposition deterrents. All these plant reactions have directly negative effects on the eggs, hatching larvae, or on the ovipositing females. Indirect plant defensive responses to feeding result in the emission of volatiles (= synomones) that attract predators or parasitoids of the feeding stages. A few recent studies have shown that plants are able to emit volatiles also in response to egg deposition and that these volatiles attract egg parasitoids. Studies on the mechanisms of induction of synomones by egg deposition show several parallels to the mechanisms of induction of plant responses by feeding damage. When considering induced plant defence against herbivores from an evolutionary point of view, the question arises whether herbivores evolved the ability to circumvent or even to exploit the plant's defensive responses. The reactions of herbivores to oviposition induced plant responses are compared with their reactions to feeding induced plant responses.     

Functional evolution of biosynthetic enzymes that produce plant volatiles*

Plants synthesize volatile compounds to attract pollinators. The volatiles emitted by flowers are often complex mixtures of organic compounds; pollinators are capable of distinctly recognizing different volatile compounds. Plants also produce volatile compounds to protect themselves against herbivores and pathogens. Some of the volatile compounds produced in floral and vegetative tissues are toxic to insects and microbes. To adapt changes in the environment, plants have evolved the ability to synthesize a unique set of volatiles. Intensive studies have identified and characterized the enzymes responsible for the formation of plant volatiles. In particular, many biosynthetic genes have been isolated and their enzymatic functions have been proposed. This review describes how plants have evolved the biosynthetic pathways leading to the formation of green leaf volatiles and phenylpropene volatiles.     

Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests

In response to feeding by arthropods, plants actively and systemically emit various volatile substances. It has been proposed that these herbivore-induced volatiles (HIPVs) can be exploited in agricultural pest control because they might repel herbivores and because they serve as attractants for the enemies of the herbivores. Indeed, recent studies with transgenic plants confirm that odour emissions can be manipulated in order to enhance the plants' attractiveness to beneficial arthropods. An additional advantage of manipulating HIPV emissions could be their effects on neighbouring plants, as a rapidly increasing number of studies show that exposure to HIPVs primes plants for augmented defence expression. Targeting the right volatiles for enhanced emission should lead to ecologically and economically sound ways of combating important pests.     

Herbivore-induced Blueberry Volatiles and Intra-plant Signaling

Herbivore-induced plant volatiles (HIPVs) are commonly emitted from plants after herbivore attack^1,2. These HIPVs are mainly regulated by the defensive plant hormone jasmonic acid (JA) and its volatile derivative methyl jasmonate (MeJA)^3,4,5. Over the past 3 decades researchers have documented that HIPVs can repel or attract herbivores, attract the natural enemies of herbivores, and in some cases they can induce or prime plant defenses prior to herbivore attack. In a recent paper⁶, I reported that feeding by gypsy moth caterpillars, exogenous MeJA application, and mechanical damage induce the emissions of volatiles from blueberry plants, albeit differently. In addition, blueberry branches respond to HIPVs emitted from neighboring branches of the same plant by increasing the levels of JA and resistance to herbivores (i.e., direct plant defenses), and by priming volatile emissions (i.e., indirect plant defenses). Similar findings have been reported recently for sagebrush⁷, poplar⁸, and lima beans⁹..Here, I describe a push-pull method for collecting blueberry volatiles induced by herbivore (gypsy moth) feeding, exogenous MeJA application, and mechanical damage. The volatile collection unit consists of a 4 L volatile collection chamber, a 2-piece guillotine, an air delivery system that purifies incoming air, and a vacuum system connected to a trap filled with Super-Q adsorbent to collect volatiles^5,6,10. Volatiles collected in Super-Q traps are eluted with dichloromethane and then separated and quantified using Gas Chromatography (GC). This volatile collection method was used n my study⁶ to investigate the volatile response of undamaged branches to exposure to volatiles from herbivore-damaged branches within blueberry plants. These methods are described here. Briefly, undamaged blueberry branches are exposed to HIPVs from neighboring branches within the same plant. Using the same techniques described above, volatiles emitted from branches after exposure to HIPVs are collected and analyzed.     

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.     

Costs of induced volatile production in maize

Herbivore‐induced plant volatiles have been shown to serve as indirect defence signals that attract natural enemies of herbivores. Parasitoids and predators exploit these plant‐provided cues to locate their victims and several herbivores are repelled by the volatiles. Recently, benefits, in terms of plant fitness, from the action of the parasitoids were shown for a few systems. However, the cost of production of herbivore‐induced volatiles for the plant remains unknown. Here, we estimate the fitness cost of the production of induced volatiles in maize, Zea mays. Plants were treated with regurgitant of Spodoptera littoralis or with the elicitor volicitin and we measured dry weight of plant parts at specific times after treatments. After a two‐week treatment period, the dry‐weight of leaves of induced plants was lower than that of un‐induced plants, suggesting a metabolic cost for induced defence. However, maize plants seem to compensate for this loss during subsequent growth, since seed production at maturity was not different for unharmed plants and plants treated with caterpillar regurgitant. For volicitin treated plants a small but significant reduction in seed production was found. It is likely that the treatments also induced the production of other defence compounds, which will contribute to the cost. Yet, a comparison of six maize inbred lines with distinct differences in volatile emissions showed a strong correlation between the intensity of induced emissions and reduction in plant performance. An analysis of the terpenoids that accumulated in the leaves of the inbred lines revealed non‐volatilised compounds are constitutively present in maize and only the volatilised compounds are induced. Interestingly, the lines that released the largest amounts of induced volatiles also contained more of the non‐volatile terpenoids. Based on these results and results from a previous study on the benefits of attracting parasitoids, we conclude that costs of induced volatile production in plants are counterbalanced by the benefits as long as natural enemies of the herbivores are present in the environment.