虫害诱导挥发物的生态调控功能

虫害诱导挥发物（herbivore-induced plant volatiles, HIPVs）是植物受害虫胁迫后释放的挥发性物质,是植物与周围环境进行信息交流的媒介。环境中的天敌、害虫和植物通过感知HIPVs所携带的信息,对各自的行为或生理生化反应做出相应的调整。介绍了挥发物的种类及主要的生物合成途径,概括了影响天敌依据HIPVs搜寻寄主和猎物的主要因素。综述了这类挥发性物质对植食性昆虫寄主选择或产卵行为的影响,介绍了植物地上部分和地下部分受害后对彼此间接防御的影响,讨论了多种害虫加害同种植物后对天敌搜寻猎物或寄主行为的影响。另外,作为损伤信号,HIPVs还能诱导同株植物未受害部位和邻近植株的防御反应。最后,对HIPVs在害虫防治中的应用现状及前景作了介绍和讨论。     

虫害诱导的植物挥发物代谢调控机制研究进展

长期受自然界的非生物/生物侵害,植物逐步形成了复杂的防御机制,为防御植食性昆虫的为害,植物释放虫害诱导产生的挥发性化合物(herbivore-induced plant volatiles,HIPVs)。HIPVs是植物-植食性昆虫-天敌三级营养关系之间协同进化的结果。HIPVs的化学组分因植物、植食性昆虫种类的不同而有差异。生态系统中,HIPVs可在植物与节肢动物、植物与微生物、虫害植物与邻近的健康植物、或同一植株的受害和未受害部位间起作用,介导防御性反应。HIPVs作为寄主定位信号,在吸引捕食性、寄生性天敌过程中起着重要作用。HIPVs还可以作为植物间信息交流的工具,启动植株的防御反应而增强抗虫性。不论从生态学还是经济学角度来看,HIPVs对于农林生态系中害虫综合治理策略的完善具有重要意义。前期的研究在虫害诱导植物防御的化学生态学方面奠定了良好基础,目前更多的研究转向阐述虫害诱导植物抗性的分子机制。为了深入了解HIPVs的代谢调控机制,主要从以下几个方面进行了综述。因为植食性昆虫取食造成的植物损伤是与昆虫口腔分泌物共同作用的结果,所以首先阐述口腔分泌物在防御反应中的作用。挥发物诱导素volicitin和β-葡萄糖苷酶作为口腔分泌物的组分,是产生HIPVs的激发子,通过调节伤信号诱发HIPVs的释放。接着阐述了信号转导途径对HIPVs释放的调节作用,并讨论了不同信号途径之间的交互作用。就HIPVs的代谢过程而言,其过程受信号转导途径(包括茉莉酸、水杨酸、乙烯、过氧化氢信号途径)的调控,其中茉莉酸信号途径是诱发HIPVs释放的重要途径。基于前人的研究,综述了HIPVs的主要代谢过程及其过程中关键酶类的调控作用。文中的HIPVs主要包括萜烯类化合物、绿叶挥发物和莽草酸途径产生的芳香族化合物,如水杨酸甲酯和吲哚等。作为化学信号分子,这些化合物中的一部分还能激活邻近植物防御基因的表达。萜烯合酶是各种萜烯类化合物合成的关键酶类,脂氧合酶、过氧化氢裂解酶也是绿叶挥发物代谢途径中的研究热点,而苯丙氨酸裂解酶和水杨酸羧基甲基转移酶分别是合成水杨酸及其衍生物水杨酸甲酯的关键酶类。这些酶类的基因在转录水平上调控着HIPVs代谢途径。最后展望了HIPVs的研究前景。     

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.     

The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects

Plants are faced with a trade-off between on the one hand growth, development and reproduction and on the other hand defence against environmental stresses. Yet, research on insect-plant interactions has addressed plant-pollinator interactions and plant-attacker interactions separately. Plants have evolved a high diversity of constitutive and induced responses to attack, including the systemic emission of herbivore-induced plant volatiles (HIPVs). The effect of HIPVs on the behaviour of carnivorous insects has received ample attention for leaf-feeding (folivorous) species and their parasitoids and predators. Here, we review whether and to what extent HIPVs affect the interaction of plants in the flowering stage with mutualistic and antagonistic insects. Whereas the role of flower volatiles in the interactions between plants and insect pollinators has received increased attention over the last decade, studies addressing both HIPVs and pollinator behaviour are rare, despite the fact that in a number of plant species herbivory is known to affect flower traits, including size, nectar secretion and composition. In addition, folivory and florivory can also result in significant changes in flower volatile emission and in most systems investigated, pollinator visitation decreased, although exceptions have been found. Negative effects of HIPVs on pollinator visitation rates likely exert negative selection pressure on HIPV emission. The systemic nature of herbivore-induced plant responses and the behavioural responses of antagonistic and mutualistic insects, requires the study of volatile emission of entire plants in the flowering stage. We conclude that approaches to integrate the study of plant defences and pollination are essential to advance plant biology, in particular in the context of the trade-off between defence and growth/reproduction.     

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.     

Fig volatiles: Their role in attracting pollinators and maintaining pollinator specificity

Each fig tree species (Ficus) is totally dependent on a specific species of wasp for pollination and the larvae of these wasps only develop in the ovules of their specificFicus host. Because the fig crop on any particular tree is generally highly synchronized, the shortlived female wasps must leave their natal tree in order to find figs which are suitable for oviposition. Chemical volatiles produced by figs when they are ready for pollination are thought to be the means by which the wasps detect a suitable host. Gas chromatograms of the fig volatiles of 7 species ofFicus showed them to be species specific. Age related changes in the volatile profiles were noted as extra volatiles are produced when the figs were ready for pollination.     

Electrophysiological response to herbivore-induced host plant volatiles in the moth Spodoptera littoralis

In cotton, Gossypium hirsutum (Malvacae), the volatiles emitted from the plant change in response to herbivory. Ovipositing females of the Egyptian cotton leaf worm, Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) can discriminate between cotton plants subjected to larval feeding and undamaged plants during oviposition. In this study we investigate whether females of this moth can detect the herbivore-induced cotton volatiles. The response of female S. littoralis antennae to volatiles collected from cotton plants subjected to larval feeding was studied using GC-EAD (coupled gas chromatography electroantennographic-detection). By GC-EAD, responses to over 10 different cotton volatiles were observed. Using single sensillum technique the responses of short sensilla trichodea on the antennae of S. littoralis females to 19 cotton volatiles and 12 general plant volatiles were investigated. Responses to these volatiles were recorded from 108 receptor neurones. Several neurones activated by herbivore-induced cotton volatiles were recorded. For example, a neurone type responding to two homoterpenes [(E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene and (E)-4,8-dimethyl-1,3,7-nonatriene] and (E,E)-α-farnesene was frequently found. We also observed sensitive neurones responding specifically to the herbivore-induced volatiles (+/–)-linalool and indole. In general, a stimulus load of less than 1 ng was needed to activate these neurones. In addition, specific neurones were found for constitutive cotton volatiles released in connection with damage to the plant. An abundant neurone type responded to β-caryophyllene and α-humulene. Another neurone type responded specifically to the non-induced cotton volatile (Z)-jasmone. These results show that females of S. littoralis have receptor neurones that would make it possible to discriminate between damaged and undamaged plants using volatile signals.     

Mixed blends of herbivore-induced plant volatiles and foraging success of carnivorous arthropods

Food webs are overlaid with infochemical webs that mediate direct and indirect interactions. Behavioural ecologists have extensively documented that carnivorous arthropods exploit herbivore-induced plant volatiles during foraging for herbivorous arthropods. Most studies on the role of infochemicals in multitrophic interactions have been conducted against an odour-free background, although field studies show that carnivores also use herbivore-induced plant volatiles under more complex conditions. Here we investigated the effect of mixing the blends of volatiles emitted by two plant species on the foraging behaviour of the predatory mite Phytoseiulus persimilis . This was done in an olfactometer under laboratory conditions and in a semi-field setup under greenhouse conditions. The olfactometer setup ensured directed mixing of the two odour blends, while odour mixing in the greenhouse setup was much less controlled and resulted from diffusion. In 4 out of 5 olfactometer experiments the behaviour towards volatiles from spider-mite ( Tetranychus urticae ) infested Lima bean plants was not affected by mixing with volatiles from caterpillar ( Pieris brassicae ) infested Brussels sprouts plants. In the fifth olfactometer experiment the response shifted significantly towards the volatiles from infested Lima bean leaves without volatiles from infested cabbage leaves. In the greenhouse setup no effect of infested cabbage plants or their volatiles on the location of spider-mite infested bean plants was recorded. The two odour blends used in this study, i.e. those from spider-mite infested Lima bean leaves and from caterpillar-infested Brussels sprouts plants, are very different and there is no overlap in compounds that are known to attract the predators. The results are discussed in the context of other types of odour-blend mixing and the effects on food web interactions.     

Evaluation of herbivore-induced plant volatiles for monitoring green lacewings in Washington apple orchards

We evaluated five herbivore-induced plant volatiles plus a male-produced pheromone as attractants for adult green lacewings in Washington apple orchards in 2008. We found at least five attractants or combinations of attractants were attractive to the three most abundant green lacewing species in our trials. Chrysopa nigricornis and Chrysopa oculata were attracted to the combination of methyl salicylate and iridodial with iridodial alone being the second best attractant. Chrysoperla plorabunda was found in lower numbers than C. nigricornis and C. oculata, but did exhibit a significant attraction to benzaldehyde. In mid-summer, we added the herbivore-induced plant volatile squalene to the study and found it to be exceedingly attractive, but only to male C. nigricornis. Whether alone or in combination, squalene attracted 4–5-fold more C. nigricornis than any other compound tested. Our data have revealed C. nigricornis to be an abundant orchard predator that can be readily monitored with squalene-baited traps. Despite the obvious promise of HIPVs in biological control programs, we urge caution in their deployment as large-scale attractants, at least until further studies have investigated potential disruption of natural enemy population dynamics.     

Starvation and herbivore-induced plant volatiles affect the color preferences of parasitic wasps

Using light-emitting diode spotlights, we examined the responses of Cotesia vestalis, a parasitoid of diamondback moth (DBM), Plutella xylostella larvae, with different hunger level to different chromatic cues. Naïve satiated female wasps showed no significant preference for either green, yellow, orange, or red spotlighted areas over a control area with background fluorescent light. When starved for 2 h, female wasps preferred yellow and green light over the control area, but not orange or red light. We also tested the effects of DBM-larvae-induced cabbage-plant volatiles, which attract female wasps, on wasp responses to green versus yellow light. In control experiments with no plant volatiles, starved wasps showed no color preference. However, when synthetic volatiles were present, the wasps preferred green over yellow light. We concluded that both hunger level and herbivore-induced plant volatiles were important factors affecting the response of parasitic wasps to light of different color.     

Phytoseiulus persimilis response to herbivore-induced plant volatiles as a function of mite-days

The predatory mite, Phytoseiulus persimilis (Acari: Phytoseiidae), uses plant volatiles (i.e., airborne chemicals) triggered by feeding of their herbivorous prey, Tetranychus urticae (Acari: Tetranychidae), to help locate prey patches. The olfactory response of P. persimilis to prey-infested plants varies in direct relation to the population growth pattern of T. urticae on the plant; P. persimilis responds to plants until the spider mite population feeding on a plant collapses, after which infested plants do not attract predators. It has been suggested that this represents an early enemy-free period for T. urticae before the next generation of females is produced. We hypothesize that the mechanism behind the diminished response of predators is due to extensive leaf damage caused by T. urticae feeding, which reduces the production of volatiles irrespective of the collapse of T. urticae population on the plant. To test this hypothesis we investigated how the response of P. persimilis to prey-infested plants is affected by: 1) initial density of T. urticae, 2) duration of infestation, and 3) corresponding leaf damage due to T. urticae feeding. Specifically, we assessed the response of P. persimilis to plants infested with two T. urticae densities (20 or 40 per plant) after 2, 4, 6, 8, 10, 12 or 14 days. We also measured leaf damage on these plants. We found that predator response to T. urticae-infested plants can be quantified as a function of mite-days, which is a cumulative measure of the standing adult female mite population sampled and summed over time. That is, response to volatiles increased with increasing numbers of T. urticae per plant or with the length of time plant was infested by T. urticae, at least as long at the leaves were green. Predatory mites were significantly attracted to plants that were infested for 2 days with only 20 spider mites. This suggests that the enemy-free period might only provide a limited window of opportunity for T. urticae because relatively low numbers of T. urticae per plant can attract predators. Leaf damage also increased as a function of mite-days until the entire leaf was blanched. T. urticae populations decreased at this time, but predator response to volatiles dropped before the entire leaf was blanched and before the T. urticae population decreased. This result supports our hypothesis that predator response to plant volatiles is linked to and limited by the degree of leaf damage, and that the quantitative response to T. urticae populations occurs only within a range when plant quality has not been severely compromised.     

Responses of a predatory bug to a mixture of herbivore-induced plant volatiles from multiple plant species

The attractiveness of herbivore-induced plant volatiles (HIPVs) from a specific plant species to natural enemies has been well established. However, under natural conditions and polycultural agriculture systems, the interactions among trophic levels are thought to be more complex. For instance, complex mixtures of volatiles emitted from diverse host plant species infested by polyphagous herbivores might affect responses of natural enemies. In this study, we investigated whether a mixture of HIPVs emitted from herbivore-damaged multiple host plant species affect responses of a predatory bug. Therefore, we report (1) olfactory responses of the predatory bug (Orius strigicollis) to volatiles emitted from cotton bollworm (Helicoverpa armigera) first instar larvae-damaged multiple plant species (tomato, French bean and sweet corn), (2) chemical analyses of volatiles emitted from the three plant species exposed to different treatments and (3) olfactory responses of the predators to a reconstituted HIPV blend from multiple plant species based on chemical analyses. O. strigicollis significantly preferred volatiles emanating from H. armigera-damaged multiple plant species to volatiles emanating from a single plant species. In all the three plant species, H. armigera-damaged seedlings emitted significantly a greater amount of volatiles as well as a larger number of volatile compounds than an undamaged or a mechanically injured seedling. The predators preferred the reconstituted HIPVs from multiple plant species to the reconstituted HIPVs from a single plant species. Thus, the mixture of HIPVs from multiple plant species enhanced the attractiveness to the predators.     

New evidence for a multi-functional role of herbivore-induced plant volatiles in defense against herbivores

A diverse, often species-specific, array of herbivore-induced plant volatiles (HIPVs) are commonly emitted from plants after herbivore attack. Although research in the last 3 decades indicates a multi-functional role of these HIPVs, the evolutionary rationale underpinning HIPV emissions remains an open question. Many studies have documented that HIPVs can attract natural enemies, and some studies indicate that neighboring plants may eavesdrop their undamaged neighbors and induce or prime their own defenses prior to herbivore attack. Both of these ecological roles for HIPVs are risky strategies for the emitting plant. In a recent paper, we reported that most branches within a blueberry bush share limited vascular connectivity, which restricts the systemic movement of internal signals. Blueberry branches circumvent this limitation by responding to HIPVs emitted from neighboring branches of the same plant: exposure to HIPVs increases levels of defensive signaling hormones, changes their defensive status, and makes undamaged branches more resistant to herbivores. Similar findings have been reported recently for sagebrush, poplar and lima beans, where intra-plant communication played a role in activating or priming defenses against herbivores. Thus, there is increasing evidence that intra-plant communication occurs in a wide range of taxonomically unrelated plant species. While the degree to which this phenomenon increases a plant’s fitness remains to be determined in most cases, we here argue that withinplant signaling provides more adaptive benefit for HIPV emissions than does between-plant signaling or attraction of predators. That is, the emission of HIPVs might have evolved primarily to protect undamaged parts of the plant against potential enemies, and neighboring plants and predators of herbivores later co-opted such HIPV signals for their own benefit.Key words: intra-plant signaling, plantplant communication, eavesdropping, systemic wound signals, plant defense, tri-trophic interactionsPlants often emit a unique blend of volatiles in response to herbivore attack. The emission of these herbivore-induced plant volatiles (HIPVs) is an active response to herbivore feeding, producing a blend of volatiles that is distinct from those emitted following mechanical injury alone.¹ Their emission can be variable; while some compounds follow a diurnal pattern with increasing amounts during the time of high photosynthesis,^2,3 others are emitted primarily at night.⁴ In some cases, the HIPV blend produced also differs depending on the species of herbivore feeding on the plant.⁵ This specificity is thought to be due to chemicals in the herbivore’s regurgitant, such as the fatty-acid amino-acid conjugate volicitin, that activate the emission of volatiles in plants.^6,7 Furthermore, HIPVs are emitted not only from the site of damage, but also at times from systemically undamaged parts of the plant.⁸ This and other systemic responses are, however, restricted within a plant such that only parts of the plant that share vascular connections with the damaged tissue receive wound signals and have the potential to respond.^9,10The ecological role of HIPVs has been a subject of fascination and the evolutionary advantage gained for plants by emitting HIPVs remains an unresolved topic of discussion. While some HIPV compounds, and some of their precursors, have sufficient volatility that their release is essentially inevitable after synthesis,¹¹ most tend to be tightly regulated. Assuming that HIPV emissions evolved as a result of trophic interactions among plants, herbivores, and natural enemies, there are four general ecological roles that HIPVs may play: (1) a direct negative effect on the herbivore, (2) a signal to alert natural enemies of the herbivore, (3) a warning signal to nearby undamaged plants, and (4) a systemic warning signal within the damaged plant (Fig. 1). The first two potential roles involve the manipulation of animal behavior, while the last two may alter plant “behavior”.Open in a separate windowFigure 1Herbivore-induced plant volatiles (HIPVs) play multiple roles in interactions among plants, herbivores, and natural enemies (possible interactions are depicted by arrows). Some of them benefit the HIPV-emitting plant (Emitter); these positive interactions include repellent effects on herbivores, attraction of natural enemies of herbivores, activation or priming of defenses in unwounded parts within the emitting plant (within-plant signaling), and growth inhibitory effects on neighboring plants (Receiver) through allelopathy. On the other hand, HIPVs may negatively affect the emitting plant by attracting herbivores or natural enemies (e.g., certain parasitoids) that result in increased damage. Finally, neighboring plants may “eavesdrop” from the emitting plant by responding to HIPVs (between-plant signaling). This latter interaction may be negative to the emitter if it is outcompeted by neighbors who receive wound signals, but beneficial to the receiving plant. Drawing by Robert Holdcraft.Scents can have a demonstrable effect on animal behavior. With respect to plant-herbivore interactions, scents can provide information about the status of a plant to herbivores and their natural enemies. For example, HIPVs may repel adults moths searching for oviposition sites,³ which has been interpreted from the perspective of either a plant minimizing damage or, perhaps more realistically, an adult moth searching for an undamaged, high quality resource for her offspring. Conversely, HIPV-emitting plants may increase their chance of being injured if herbivores are attracted to these volatiles.¹² The more commonly accepted role of HIPVs in manipulating animal behavior is to attract natural enemies of the herbivores. This tri-trophic “cry for help”¹³ has a potential evolutionary benefit for both the plant emitting the volatiles and the natural enemies responding to this emission.^14–16 Although this idea makes sense in an evolutionary perspective, only a few studies have documented the occurrence of this phenomenon in natural systems.¹⁷ Indeed, the effectiveness of a cry for help depends on the presence of a helper and, equally importantly, the ability of the helper to increase plant fitness. In the case of predator attraction, the herbivore may be removed from the plant and consumed, thereby reducing damage for the emitting plant.¹⁸ However, insect herbivores infected by parasitoids, which also use HIPV cues to locate hosts,¹⁹ may also consume less plant material²⁰ but may also in some cases consume more plant material than unparasitized insect herbivores.²¹ Since there is currently no evidence that plants can modify HIPV blends to attract selectively predators versus parasitoids, an answered cry for help may not reliably decrease the total amount of damage to an emitting plant. Thus, the fact that natural enemies respond to HIPVs does not imply that these volatiles evolved for this purpose or that there is an adaptive advantage for a plant to use HIPVs to attract natural enemies. Rather, natural enemies of insect herbivores may have learned to co-opt the HIPV signal emitted by plants and, by doing so, increased their fitness irrespective of the ultimate fitness outcome to the plant.Though more controversial, scents can also have an effect on plant behavior.²² Early work suggested that HIPVs from wounded willows,²³ poplars²⁴ and sugar maples²⁴ could trigger defense responses from other neighboring conspecifics. More recent studies have shown that this signaling can occur between different species of plants.²⁵ While these results are intriguing, they appear to have little adaptive function from the perspective of an emitting plant, which could be facilitating the fitness of potential resource competitors. Further, unless the individual within the same plant species shared some degree of kinship,²⁶ an emitting plant would also be at a disadvantage by providing an HIPV wound signal to a conspecific that, in theory, occupies the same competitive niche space. On the other hand, unwounded conspecific should benefit from being able to ‘eavesdrop’ by detecting HIPVs from wounded plants as they share the same herbivore complex and thus are vulnerable to attack. Moreover, from a heterospecific receiver’s perspective, the benefits of eavesdropping can be confounded by the potential of mounting defenses against a signal generated by incompatible herbivores feeding on a different plant species.²⁷ So, eavesdropping may be adaptive for a receiving plant if it realizes increased fitness relative to a conspecific that did not receive the signal. The emitting plant derives no apparent adaptive benefit of using HIPVs to warn neighboring plants. However, the emitting plant may benefit if their HIPVs have inhibitory allelopathic activity on neighboring plants.²⁸Our recent work¹ highlighted another scenario by which an HIPV-emitting plant would derive a direct benefit from the emissions: when HIPVs act as systemic wound signals within damaged plants. We showed that branches of blueberry shrubs lack effective vascular connections and thus cannot transmit wound signals among branches via the vasculature. To compensate, HIPVs can be transmitted among branches and, in so doing, overcome the vascular constraints of the branching life history strategy. Exposure to HIPVs increased levels of defensive signaling hormones in undamaged branches, changed their defensive chemical status, and made them more resistant to herbivores.¹ This idea that HIPVs may function in intra-plant communication to activate or prime defenses in other parts of the emitting plant against future attack was first suggested separately by Farmer²⁹ and Orians.⁹ The hypothesis was first tested with mechanically clipped wild sagebrush,³⁰ and it was further tested with insect herbivores of wild lima bean³¹ and hybrid poplar.³² Under this scenario, the emitting plant derives a direct benefit from the HIPVs, providing an unambiguous fitness advantage.So, what is the most beneficial factor to a plant for emitting volatiles in response to herbivore feeding? In terms of maximizing the potential benefit and minimizing the potential risk to the emitting plant, the function of HIPVs in mediating systemic wound signaling clearly provides the greatest potential adaptive advantage. Thus, we propose that the primary adaptive benefit for the evolution of HIPVs is to signal and protect unwounded parts of the attacked plant with high risk of infestation against herbivores. Later, these volatiles provided cues that led to adaptive fitness advantages for neighboring plants and natural enemies of herbivores, which may or may not benefit the HIPV-emitting plant. Indeed, ecologically adaptive advantages have emerged and contribute to a diverse, multi-functional chemical ecology mediated by HIPVs.     

Herbivore-induced plant volatiles mediate host selection by a root herbivore

In response to herbivore attack, plants mobilize chemical defenses and release distinct bouquets of volatiles. Aboveground herbivores are known to use changes in leaf volatile patterns to make foraging decisions, but it remains unclear whether belowground herbivores also use volatiles to select suitable host plants. We therefore investigated how above- and belowground infestation affects the performance of the root feeder Diabrotica virgifera virgifera, and whether the larvae of this specialized beetle are able to use volatile cues to assess from a distance whether a potential host plant is already under herbivore attack. Diabrotica virgifera larvae showed stronger growth on roots previously attacked by conspecific larvae, but performed more poorly on roots of plants whose leaves had been attacked by larvae of the moth Spodoptera littoralis. Fittingly, D. virgifera larvae were attracted to plants that were infested with conspecifics, whereas they avoided plants that were attacked by S. littoralis. We identified (E)-β-caryophyllene, which is induced by D. virgifera, and ethylene, which is suppressed by S. littoralis, as two signals used by D. virgifera larvae to locate plants that are most suitable for their development. Our study demonstrates that soil-dwelling insects can use herbivore-induced changes in root volatile emissions to identify suitable host plants.     

Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey

We investigated how the plant‐inhabiting, anthocorid predator, Anthocoris nemoralis, copes with variation in prey, host plant and associated herbivore‐induced plant volatiles and in particular whether the preference for these plant odours is innate or acquired. We found a marked difference between the olfactory response of orchard‐caught predators and that of their first generation reared on flour moth eggs in the laboratory, i.e. under conditions free of herbivory‐induced volatiles. Whereas the orchard‐caught predators preferred odour from psyllid‐infested pear leaves, when offered against clean air in a Y‐tube olfactometer, the laboratory‐reared first generation of (naive) predators did not. The same difference was found when a single component (methyl salicylate) of the herbivore‐induced plant volatiles was offered against clean air. After experiencing methyl salicylate with prey, however, the laboratory‐reared predators showed a pronounced preference for this volatile. This acquired preference did not depend on whether the volatile had been experienced in the juvenile period or in the adult phase, but it did depend on whether it had been offered in presence or absence of prey. In the first case, they were attracted to the plant volatile in subsequent olfactometer experiments, but when the volatile had been offered during a period of prey deprivation, the predators were not attracted. We conclude that associative learning is the most likely mechanism underlying acquired odour preference.     

Biological activity and specificity of Miridae-induced plant volatiles

The ability of zoophytophagous predators to produce defensive plant responses due to their phytophagous behavior has been recently demonstrated. In the case of tomatoes, the mirids Nesidiocoris tenuis and Macrolophus pygmaeus are able to attract or repel pests and/or natural enemies in different ways. Nevertheless, the herbivore-induced plant volatiles (HIPVs) released by the phytophagy of both mirids, which are responsible for these behaviors, are unknown. In this work, the HIPVs produced by the plant feeding of N. tenuis and M. pygmaeus were characterized. In addition, the role of each HIPV in the repellence or attraction of two tomato pests, Bemisia tabaci and Tuta absoluta, and of the natural enemy Encarsia formosa was evaluated. Six green leaf volatiles (GLVs) plus methyl salicylate and octyl acetate clearly stood out as major differential peaks on the chromatogram in a directed analysis. The six GLV and methyl salicylate were repellent for B. tabaci and attractive to E. formosa, whereas they showed no effect on T. absoluta. Octyl acetate, which was significantly present only in the M. pygmaeus-punctured plants, was significantly attractive to T. absoluta, repellent to E. formosa and indifferent to B. tabaci. Unlike the remaining HIPVs, octyl acetate was emitted directly by M. pygmaeus and not by the plant. Our results showed that mirid herbivory could modulate the pest and natural plant enemy locations, since tomato plants release a blend of volatiles in response to this activity. These results could serve as a basis for future development of plant protection.