Role Of Herbivore-induced Plant Volatiles Research Articles

The Role of Herbivore-Induced Plant Volatiles in Tri-trophic Interactions and Pest Management

In agricultural ecosystems, the tri trophic interactions between plants, herbivores and their natural enemies are crucial for maintaining ecological balance and crop health. Natural enemies of pests predominantly regulate herbivore populations, emphasizing the importance of these interactions. Plants exhibit both induced and constitutive defences, Plants use herbivore-induced plant volatiles (HIPVs) as a key mechanism to attract natural enemies that defend them against the herbivores. HIPVs are chemical signals emitted in response to herbivore damage and can attract predators and parasitoids, indirectly they protect the plants. This review explores the role of HIPVs in plant defense, focusing on their evolutionary, chemical and practical aspects. with HIPVs acting as indirect defenses by recruiting natural enemies. The interaction between physical traits, chemical signals and semiochemicals, including volatile organic compounds (VOCs), significantly influences these interactions. Olfactometers, such as the Y-tube and four-arm designs, have been proven to be pivotal in studying insect responses to these volatile compounds, providing insights into their behavior and effectiveness in pest management. Despite advances in understanding HIPVs, research indicates variability in volatile emissions and their effectiveness across different herbivore species and developmental stages. Further studies are needed to improve the specificity of HIPV research, incorporating field-based analyses to capture natural environmental complexities. Future research should focus on optimizing HIPV applications in pest management, understanding spatial and temporal scales of HIPV interactions, and addressing the influence of environmental factors on HIPV efficacy.

Tritrophic Interactions among Arthropod Natural Enemies, Herbivores and Plants Considering Volatile Blends at Different Scale Levels.

Herbivore-induced plant volatiles (HIPVs) are released by plants upon damaged or disturbance by phytophagous insects. Plants emit HIPV signals not merely in reaction to tissue damage, but also in response to herbivore salivary secretions, oviposition, and excrement. Although certain volatile chemicals are retained in plant tissues and released rapidly upon damaged, others are synthesized de novo in response to herbivore feeding and emitted not only from damaged tissue but also from nearby by undamaged leaves. HIPVs can be used by predators and parasitoids to locate herbivores at different spatial scales. The HIPV-emitting spatial pattern is dynamic and heterogeneous in nature and influenced by the concentration, chemical makeup, breakdown of the emitted mixes and environmental elements (e.g., turbulence, wind and vegetation) which affect the foraging of biocontrol agents. In addition, sensory capability to detect volatiles and the physical ability to move towards the source were also different between natural enemy individuals. The impacts of HIPVs on arthropod natural enemies have been partially studied at spatial scales, that is why the functions of HIPVs is still subject under much debate. In this review, we summarized the current knowledge and loopholes regarding the role of HIPVs in tritrophic interactions at multiple scale levels. Therefore, we contend that closing these loopholes will make it much easier to use HIPVs for sustainable pest management in agriculture.

The Role of Herbivore-induced Plant Volatiles in Trophic Interactions: The Swiss Connection.

It is increasingly evident that plants actively respond to the threats and challenges that they come to face while growing. This is particularly manifested in the dynamic responses to insect herbivory, especially in terms of the volatile compounds that the attacked plants emit. Indeed, many plants respond to insect-inflicted damage with the synthesis and release of volatile organic compounds. These emissions, commonly referred to as herbivore-induced plant volatiles (HIPVs), play important roles in the interactions between the emitting plants and their biotic environment. The odorous signal can be picked up and exploited by various organisms: neighbouring plants, herbivores and their natural enemies, such as predators and parasitoid wasps. Coincidence or not, scientists currently working in Switzerland have made numerous key contributions to the work in this field. By highlighting their work, we attempt to give a somewhat historic overview of this field of research.

Identification of Semiochemicals from Cowpea, Vigna unguiculata, for Low-input Management of the Legume Pod Borer, Maruca vitrata

Cowpea, Vigna unguiculata L. Walp. (Fabaceae), is one of the most important food legumes grown on the African continent, as it provides an affordable source of dietary protein. Yields of cowpea are significantly reduced through damage by legume pod-borer, Maruca vitrata (Lepidoptera: Crambidae), caterpillars to flowers, tender leaves and pods. Semiochemical-based strategies are considered as environmentally benign and affordable for pest management, particularly on smallholder farms. In this study, we investigated the importance of cowpea flower volatiles as host location cues for egg-laying M. vitrata, and herbivore-induced plant volatiles (HIPVs) as M. vitrata repellents and natural enemy (Apanteles taragamae and Phanerotoma syleptae parasitoid) attractants. In oviposition choice assays, M. vitrata laid more eggs on flowering cowpea plants than non-flowering plants. Coupled gas chromatography-electrophysiology (GC-EAG) analysis using the antennae of female M. vitrata and an extract of flower volatiles collected by dynamic headspace collection revealed the presence of five EAG-active components that were identified by coupled GC-mass spectrometry (GC-MS) analysis as benzaldehyde, benzyl alcohol, acetophenone, a vinylbenzaldehyde isomer and (E)-cinnamaldehyde. A synthetic blend of the identified compounds, prepared using 3-vinylbenzaldehyde, induced M. vitrata to lay as many eggs on non-flowering cowpea as on flowering plants. The moths also preferred laying eggs on intact plants compared to M. vitrata-infested plants. As the emission of EAG-active floral compounds was determined to be lower in the headspace of infested cowpea flowers, the role of HIPVs emitted by M. vitrata-damaged leaves was also investigated. Of the compounds induced by larval damage, (E)-DMNT, indole, n-hexyl acetate, 1-octen-3-ol and linalool were shown by GC-EAG to possess electrophysiological activity. A synthetic blend of the EAG-active compounds, using racemic 1-octen-3-ol and linalool, significantly reduced egg numbers on flowering cowpea. Larval and egg parasitoids, i.e. A. taragamae and Ph. syleptae, respectively, of M. vitrata both preferred the Y-tube olfactometer arm treated with synthetic (E)-DMNT, whereas preference for racemic linalool and (E)-nerolidol was dose-dependent in A. taragamae. Our results provide the platform for the development of future semiochemical-based pest management strategies against M. vitrata on smallholder farms in West Africa.

Herbivore-induced plant volatiles enhance field-level parasitism of the mirid bug Apolygus lucorum

In China, the braconid wasp Peristenus spretus Chen & van Achterberg (Hymenoptera: Braconidae) is a native endoparasitoid of the mirid bug Apolygus lucorum (Meyer-Dür) (Hemiptera: Miridae). Castor bean (Ricinus communis L.) is a preferred host plant of A. lucorum, and P. spretus adults are attracted to its herbivore-damaged flowering plants. Here, we used headspace collection to sample the volatiles emitted by A. lucorum-damaged flowering R. communis plants, and employed gas chromatography-electroantennography (GC-EAD) to identify two electrophysiologically-active compounds. Active compounds were identified as m-cymene and 4′-ethyl-acetophenone. Electrophysiological activities were confirmed by EAG, with a gradient of five doses of each compound eliciting significant antennal responses. Next, in Y-tube olfactometer bioassays, female P. spretus were attracted to two synthetic volatile compounds at two different concentrations (10 mg/ml and 100 mg/ml). Under field conditions, A. lucorum parasitism rates – as recorded in volatile-baited barrel traps – for the two compounds were significantly higher than those for mineral oil (control). Our findings emphasize the important role of herbivore-induced plant volatiles in the P. spretus host selection process, and provide a potential way to enhance in-field parasitoid populations and improve biological control of A. lucorum.

The role of herbivore-induced plant volatiles (HIPVs) as indirect plant defense mechanism in a diverse plant and herbivore species; a review

When plants are attacked by herbivores, they release plant volatiles called herbivore-induced plant volatiles (HIPVs) to the environment to communicate with higher trophic levels. HIPVs play different ecological roles such as plant-plant interaction, plant-herbivore interaction, tritrophic interaction and other related interactions. Attractiveness of HIPVs to natural enemies in a tritrophic interaction varies depending on species diversity. Under natural and multiple cropping systems, tritrophic interaction is expected to be more complex than single tritrophic interaction with one species per trophic level. In complex tritrophic interaction, diversity of different trophic levels affects attractiveness of HIPVs to natural enemies. From plant diversity point of view, HIPVs mixture emanating from herbivore-damaged multiple plant species are reported to affect behavioral responses and foraging behavior of natural enemies under laboratory and field conditions. Similarly, from herbivore diversity point of view, in nature, plants are commonly attacked by more than one herbivore species. Constituents of HIPVs vary between plants infested by multiple and single herbivore species and this affects the behavioral responses and foraging behavior of natural enemies. This paper reviews recent findings on the role of HIPVs as indirect plant defense in systems with simple tritrophic interaction, and in diverse plants species and diverse herbivore species.

Electrophysiological and Oviposition Responses of Tuta absoluta Females to Herbivore-Induced Volatiles in Tomato Plants.

In response to attack by herbivorous insects, plants produce semiochemicals for intra- and interspecific communication. The perception of these semiochemicals by conspecifics of the herbivore defines their choice for oviposition and feeding. We aimed to investigate the role of herbivore-induced plant volatiles (HIPVs) by Tuta absoluta larvae on the oviposition choice of conspecific females on tomato plants. We performed two- choice and non-choice bioassays with plants damaged by larvae feeding and intact control plants. We also collected headspace volatiles of those plants and tested the response of female antennae on those blends with Gas Chromatography- Electro-Antennographical Detection (GC-EAD). In total 55 compounds were collected from the headspace of T. absoluta larvae-infested plants. Our results show that female moths preferred to oviposit on intact control plants instead of damaged ones. Herbivory induced the emission of hexanal, (Ζ)-3-hexen-1-ol, (E)-β-ocimene, linalool, (Z)-3-hexenyl butanoate, methyl salicylate, indole, nerolidol, guaidiene-6,9, β-pinene, β-myrcene, α-terpinene, hexenyl hexanoate, β-elemene, β-caryophyllene and (Ε-Ε)- 4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), one unidentified sesquiterpene and three unknown compounds. In Electroantennographic (EAG) assays, the antennae of T. absoluta females responded to hexanal, (Ζ)-3-hexen-1-ol, methyl salicylate and indole. The antennae of T. absoluta females exhibited a dose-response in EAG studies with authentic samples. Strong EAG responses were obtained for compounds induced on damaged tomato plants, as well as in nonanal, a compound emitted by both infested and control plants. These compounds could be utilized in integrated pest management of T. absoluta.

Tritrophic Interactions Mediated by Herbivore-Induced Plant Volatiles: Mechanisms, Ecological Relevance, and Application Potential.

Tritrophic interactions between plants, herbivores, and their natural enemies are an integral part of all terrestrial ecosystems. Herbivore-induced plant volatiles (HIPVs) play a key role in these interactions, as they can attract predators and parasitoids to herbivore-attacked plants. Thirty years after this discovery, the ecological importance of the phenomena is widely recognized. However, the primary function of HIPVs is still subject to much debate, as is the possibility of using these plant-produced cues in crop protection. In this review, we summarize the current knowledge on the role of HIPVs in tritrophic interactions from an ecological as well as a mechanistic perspective. This overview focuses on the main gaps in our knowledge of tritrophic interactions, and we argue that filling these gaps will greatly facilitate efforts to exploit HIPVs for pest control.

Herbivore induced plant volatiles represents a favorable host to onion thrips (Thrips tabaci)

Onion thrips, Thrips tabacis Lindeman (Thysanoptera: Thripidae) is an important pest of horticulture crops throughout the globe. However, there is a paucity of studies on its behavioral ecology in relation to herbivore induced plant volatiles (HIPVs). An attempt was made to study behaviour of T. tabaci towards HIPVs and healthy plant volatiles. Olfactometer bioassays revealed that T. tabaci significantly preferred HIPVs from conspecific infested onion to volatiles from healthy onion plants. Gas chromatography-Mass spectrometry (GC-MS) analysis of HIPVs and volatiles from healthy onion plants revealed substantial changes in their volatile profiles. Our study provides empirical data on signals HIPVs may provide herbivores and suggests that the role of HIPVs, mostly generalized as defense, may vary based on the interaction and must be studied closely to understand their ecological roles. It also provides basis for the development of kairomone based management strategies against this devastating pest.

The timing of herbivore-induced volatile emission in black poplar (Populus nigra) and the influence of herbivore age and identity affect the value of individual volatiles as cues for herbivore enemies.

BackgroundThe role of herbivore-induced plant volatiles as signals mediating the attraction of herbivore enemies is a well-known phenomenon. Studies with short-lived herbaceous plant species have shown that various biotic and abiotic factors can strongly affect the quantity, composition and timing of volatile emission dynamics. However, there is little knowledge on how these factors influence the volatile emission of long-lived woody perennials.The aim of this study was to investigate the temporal dynamics of herbivore-induced volatile emission of black poplar (Populus nigra) through several day-night cycles following the onset of herbivory. We also determined the influence of different herbivore species, caterpillars of the gypsy moth (Lymantria dispar) and poplar hawkmoth (Laothoe populi), and different herbivore developmental stages on emission.ResultsThe emission dynamics of major groups of volatile compounds differed strikingly in response to the timing of herbivory and the day-night cycle. The emission of aldoximes, salicyl aldehyde, and to a lesser extent, green leaf volatiles began shortly after herbivore attack and ceased quickly after herbivore removal, irrespective of the day-night cycle. However, the emission of most terpenes showed a more delayed reaction to the start and end of herbivory, and emission was significantly greater during the day compared to the night. The identity of the caterpillar species caused only slight changes in emission, but variation in developmental stage had a strong impact on volatile emission with early instar L. dispar inducing more nitrogenous volatiles and terpenoids than late instar caterpillars of the same species.ConclusionsThe results indicate that only a few of the many herbivore-induced black poplar volatiles are released in tight correlation with the timing of herbivory. These may represent the most reliable cues for herbivore enemies and, interestingly, have been shown in a recent study to be the best attractants for an herbivore enemy that parasitizes gypsy moth larvae feeding on black poplar.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0304-5) contains supplementary material, which is available to authorized users.

To be in time: egg deposition enhances plant-mediated detection of young caterpillars by parasitoids.

Animals use information from their environment while foraging for food or prey. When parasitic wasps forage for hosts, they use plant volatiles induced by herbivore activities such as feeding and oviposition. Little information is available on how wasps exploit specific plant volatiles over time, and which compounds indicate changes in host quality. In experiments investigating the role of herbivore-induced plant volatiles in wasp foraging, induction of plant response is usually achieved by placing larvae on clean plants instead of allowing the natural sequence of events: to let eggs deposited by the herbivore develop into larvae. We compared the attraction of the parasitoid Cotesia glomerata to volatiles emitted by black mustard (Brassica nigra) plants induced by eggs and successive larval stages of the Large Cabbage White butterfly (Pieris brassicae) to the attraction of this parasitoid to black mustard plant volatiles induced only by larval feeding in a wind tunnel setup. We show that wasps are attracted to plants infested with eggs just before and shortly after larval hatching. However, wasp preference changed at later time points towards plants induced only by larval feeding. These temporal changes in parasitoid attraction matched with changes in the chemical compositions of the blends of plant volatiles. Previous studies have shown that host quality/suitability decreases with caterpillar age and that P. brassicae oviposition induces plant defences that negatively affect subsequently feeding caterpillars. We investigated parasitoid performance in hosts of different ages. Wasp performance was positively correlated with preference. Moreover, parasitism success decreased with time and host stage. In conclusion, the behaviour of Cotesia glomerata is fine-tuned to exploit volatiles induced by eggs and early host stages that benefit parasitoid fitness.

Herbivore‐induced plant volatiles provide associational resistance against an ovipositing herbivore

SummaryPlants produce herbivore‐induced plant volatiles (HIPVs) in response to damage by herbivores. AlthoughHIPVs are known to enhance plant resistance by affecting herbivore host plant preferences and by attracting natural enemies, little is known about the role ofHIPVs on the resistance of neighbouring plants and the mechanism behind this associational resistance.This study examined the effect ofHIPVs from herbivore‐damaged host plants (alfalfa (Medicago sativa), clover (Trifolium alexandrinum) and cotton (Gossypium hirsutum)) on oviposition byEgyptian cotton leafworm (Spodoptera littoralis) (Lepidoptera:Noctuidae) on neighbouring, undamaged host plants.There was a significant reduction in oviposition byS. littoralison undamaged plants adjacent to herbivore‐damaged cotton plants under both field and laboratory conditions. The results showed that the associational resistance byHIPVs depends on direct effects on oviposition behaviour inS. littoralis. There were also indications that other mechanisms may be involved.Associational resistance viaHIPVs was not observed for all plant species tested. Emission ofHIPVs from damaged cotton increased the resistance of undamaged cotton and alfalfa plants to oviposition byS. littoralis, butHIPVs from damaged alfalfa and clover neighbours did not provide resistance to undamaged cotton plants.Synthesis. Our results suggest that the presence ofHIPV‐emitting plant neighbours can reduce herbivory on undamaged plants and enhance plant resistance by affecting oviposition behaviour in insect herbivores.

Smelling the Wood from the Trees: Non-Linear Parasitoid Responses to Volatile Attractants Produced by Wild and Cultivated Cabbage

Despite a large number of studies on herbivore-induced plant volatiles (HIPVs), little is known about which specific compounds are used by natural enemies to locate prey- or host- infested plants. In addition, the role of HIPVs in attracting natural enemies has been restricted largely to agricultural systems. Differences in volatile blends emitted by cultivars and plants that originate from wild populations may be attributed to potentially contrasting selection regimes: natural selection among the wild types and artificial selection among cultivars. A more realistic understanding of these interactions in a broader ecological and evolutionary framework should include studies that involve insect herbivores, parasitoids, and wild plants on which they naturally interact in the field. We compared the attractiveness of HIPVs emitted by wild and cultivated cabbage to the parasitoid Cotesia rubecula, and determined the chemical composition of the HIPV blends to elucidate which compounds are involved in parasitoid attraction. Wild and cultivated cabbage differed significantly in their volatile emissions. Cotesia rubecula was differentially attracted to the wild cabbage populations and preferred wild over cultivated cabbage. Isothiocyanates, which were only emitted by the wild cabbages, may be the key components that explain the preference for wild over cultivated cabbage, whereas terpenes may be important for the differential attraction among the wild populations. Volatile analysis revealed that parasitoid attraction cannot be explained by simple linear relationships. Our results suggest that unraveling which compound(s) are innately attractive to parasitoids of cabbage pests should include wild Brassicaceae.

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 within-plant 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.

Herbivore-Induced Volatiles in the Perennial Shrub, Vaccinium corymbosum, and Their Role in Inter-branch Signaling

Herbivore feeding activates plant defenses at the site of damage as well as systemically. Systemic defenses can be induced internally by signals transported via phloem or xylem, or externally transmitted by volatiles emitted from the damaged tissues. We investigated the role of herbivore-induced plant volatiles (HIPVs) in activating a defense response between branches in blueberry plants. Blueberries are perennial shrubs that grow by initiating adventitious shoots from a basal crown, which produce new lateral branches. This type of growth constrains vascular connections between shoots and branches within plants. While we found that leaves within a branch were highly connected, vascular connectivity was limited between branches within shoots and absent between branches from different shoots. Larval feeding by gypsy moth, exogenous methyl jasmonate, and mechanical damage differentially induced volatile emissions in blueberry plants, and there was a positive correlation between amount of insect damage and volatile emission rates. Herbivore damage did not affect systemic defense induction when we isolated systemic branches from external exposure to HIPVs. Thus, internal signals were not capable of triggering systemic defenses among branches. However, exposure of branches to HIPVs from an adjacent branch decreased larval consumption by 70% compared to those exposed to volatiles from undamaged branches. This reduction in leaf consumption did not result in decreased volatile emissions, indicating that leaves became more responsive to herbivory (or "primed") after being exposed to HIPVs. Chemical profiles of leaves damaged by gypsy moth caterpillars, exposed to HIPVs, or non-damaged controls revealed that HIPV-exposed leaves had greater chemical similarities to damaged leaves than to control leaves. Insect-damaged leaves and young HIPV-exposed leaves had higher amounts of endogenous cis-jasmonic acid compared to undamaged and non-exposed leaves, respectively. Our results show that exposure to HIPVs triggered systemic induction of direct defenses against gypsy moth and primed volatile emissions, which can be an indirect defense. Blueberry plants appear to rely on HIPVs as external signals for inter-branch communication.

Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods

The relatively new research field of Chemical Ecology has, over the last two decades, revealed an important role of plant-produced volatile organic compounds (VOCs) in mediating interactions between plants and other organisms. Of particular interest are the volatile blends that plants actively emit in response to herbivore damage. Various efforts are underway to pinpoint the bioactive compounds in these complex blends, but this has proven to be exceedingly difficult. Here we give a short overview on the role of herbivore-induced plant volatiles in interactions between plants and other organisms and we review methods that are currently employed to collect and identify key volatile compounds mediating these interactions. Our perspective on future directions of this fascinating research field places special emphasis on the need for an interdisciplinary approach. Joint efforts by chemists and biologists should not only facilitate the elucidation of crucial compounds, but can also be expected to lead to an exploitation of this knowledge, whereby ecological interactions may be chemically manipulated in order to protect crops and the environment.

The Role of Methyl Salicylate in Prey Searching Behavior of the Predatory Mite Phytoseiulus persimilis

Many carnivorous arthropods use herbivore-induced plant volatiles to locate their prey. These plant volatiles are blends of up to hundreds of compounds. It is often unknown which compounds in such a complex volatile blend represent the signal to the foraging carnivore. We studied the role of methyl salicylate (MeSA) as part of the volatile blend in the foraging behavior of the predatory mite Phytoseiulus persimilis by using a Y-tube olfactometer. MeSA is one of the compounds released by lima bean, infested with Tetranychus urticae--a prey species of the predatory mite. MeSA attracted satiated predatory mites in a dose-dependent way with optimum attraction at a dose of 0.2 microg. Predatory mites did not discriminate between a prey-induced lima bean volatile blend (that contains MeSA) and a prey-induced volatile blend to which an extra amount of synthetic MeSA had been added. However, they preferred a MeSA-containing volatile blend (induced by T. urticae) to an otherwise similar but MeSA-free blend (induced by jasmonic acid). Adding synthetic MeSA to the MeSA-free blend significantly increased the mites' choice for this odor, suggesting an important role for MeSA. This study is a new step toward unraveling the role of herbivore-induced plant volatiles in the foraging behavior of predatory arthropods.