Herbivore-Induced Plant Volatiles Mediate In-Flight Host Discrimination by Parasitoids

Herbivore feeding induces plants to emit volatiles that are detectable and reliable cues for foraging parasitoids, which allows them to perform oriented host searching. We investigated whether these plant volatiles play a role in avoiding parasitoid competition by discriminating parasitized from unparasitized hosts in flight. In a wind tunnel set-up, we used mechanically damaged plants treated with regurgitant containing elicitors to simulate and standardize herbivore feeding. The solitary parasitoid Cotesia rubecula discriminated among volatile blends from Brussels sprouts plants treated with regurgitant of unparasitized Pieris rapae or P. brassicae caterpillars over blends emitted by plants treated with regurgitant of parasitized caterpillars. The gregarious Cotesia glomerata discriminated between volatiles induced by regurgitant from parasitized and unparasitized caterpillars of its major host species, P. brassicae. Gas chromatography-mass spectrometry analysis of headspace odors revealed that cabbage plants treated with regurgitant of parasitized P. brassicae caterpillars emitted lower amounts of volatiles than plants treated with unparasitized caterpillars. We demonstrate (1) that parasitoids can detect, in flight, whether their hosts contain competitors, and (2) that plants reduce the production of specific herbivore-induced volatiles after a successful recruitment of their bodyguards. As the induced volatiles bear biosynthetic and ecological costs to plants, downregulation of their production has adaptive value. These findings add a new level of intricacy to plant–parasitoid interactions.     

Does Aphid Infestation Interfere with Indirect Plant Defense against Lepidopteran Caterpillars in Wild Cabbage?

Attraction of parasitoids to plant volatiles induced by multiple herbivory depends on the specific combinations of attacking herbivore species, especially when their feeding modes activate different defense signalling pathways as has been reported for phloem feeding aphids and tissue feeding caterpillars. We studied the effects of pre-infestation with non-host aphids (Brevicoryne brassicae) for two different time periods on the ability of two parasitoid species to discriminate between volatiles emitted by plants infested by host caterpillars alone and those emitted by plants infested with host caterpillars plus aphids. Using plants originating from three chemically distinct wild cabbage (Brassica oleracea) populations, Diadegma semiclausum switched preference for dually infested plants to preference for plants infested with Plutella xylostella hosts alone when the duration of pre-aphid infestation doubled from 7 to 14 days. Microplitis mediator, a parasitoid of Mamestra brassicae caterpillars, preferred dually-infested plants irrespective of aphid-infestation duration. Separation of the volatile blends emitted by plants infested with hosts plus aphids or with hosts only was poor, based on multivariate statistics. However, emission rates of individual compounds were often reduced in plants infested with aphids plus hosts compared to those emitted by plants infested with hosts alone. This effect depended on host caterpillar species and plant population and was little affected by aphid infestation duration. Thus, the interactive effect of aphids and hosts on plant volatile production and parasitoid attraction can be dynamic and parasitoid specific. The characteristics of the multi-component volatile blends that determine parasitoid attraction are too complex to be deduced from simple correlative statistical analyses.     

The Impact of Herbivore-Induced Plant Volatiles on Parasitoid Foraging Success: A General Deterministic Model

Parasitoids respond to volatiles that plants produce when injured by herbivores. A considerable body of literature addresses the chemical pathways of herbivore-induced volatile production. However, there is almost no theory or data on how timing of volatile release in relationship to host availability for parasitization impacts the utility of these cues to parasitoids and on the extent that this volatile release timing might increase or decrease the percent of herbivores that become parasitized. This kind of information is critical in judging the benefits that might accrue from a breeding program aimed at enhancing herbivore-responsive volatile production. We developed a general model to begin examining this issue by using available parameters from two tritrophic systems. The model uses herbivore oviposition, development, and mortality rates, linked to a range of plant volatile induction and cessation periods for calculating the proportion of plants in a field that are (1) not producing volatiles but occupied by suitable herbivore hosts, (2) producing volatiles and occupied by suitable herbivore hosts, (3) producing volatiles but not occupied by suitable herbivore hosts, and (4) not producing volatiles and not occupied by suitable herbivore hosts. The impact of the plant volatiles on parasitoid foraging success is then determined by comparing the expected number of hosts parasitized when the parasitoid focuses solely on the volatile-producing plants to when it forages randomly among all plants. Under some conditions, parasitoids can attack three times more herbivores if they focus on volatile-producing plants. However, when we simulate plants that take several days to cease volatile production after pupation or death of the herbivore, parasitization rate does not increase when parasitoids use volatiles as cues. The utility of the volatile cues is consistently greater when a smaller proportion of plants is occupied by herbivores, indicating that their usefulness may be reduced to zero in fields saturated with volatiles.     

Chemical Ecology of the host searching behavior in an Egg Parasitoid: are Common Chemical Cues exploited to locate hosts in Taxonomically Distant Plant Species?

Parasitoids are known to exploit volatile cues emitted by plants after herbivore attack to locate their hosts. Feeding and oviposition of a polyphagous herbivore can induce the emission of odor blends that differ among distant plant species, and parasitoids have evolved an incredible ability to discriminate them and locate their hosts relying on olfactive cues. We evaluated the host searching behavior of the egg parasitoid Cosmocomoidea annulicornis (Ogloblin) (Hymenoptera: Mymaridae) in response to odors emitted by two taxonomically distant host plants, citrus and Johnson grass, after infestation by the sharpshooter Tapajosa rubromarginata (Signoret) (Hemiptera: Cicadellidae), vector of Citrus Variegated Chlorosis. Olfactory response of female parasitoids toward plants with no herbivore damage and plants with feeding damage, oviposition damage, and parasitized eggs was tested in a Y-tube olfactometer. In addition, volatiles released by the two host plant species constitutively and under herbivore attack were characterized. Females of C. annulicornis were able to detect and significantly preferred plants with host eggs, irrespectively of plant species. However, wasps were unable to discriminate between plants with healthy eggs and those with eggs previously parasitized by conspecifics. Analysis of plant volatiles induced after sharpshooter attack showed only two common volatiles between the two plant species, indole and β-caryophyllene. Our results suggest that this parasitoid wasp uses common chemical cues released by many different plants after herbivory at long range and, once on the plant, other more specific chemical cues could trigger the final decision to oviposit.

     

Fungal Infection Reduces Herbivore-Induced Plant Volatiles of Maize but does not Affect Naïve Parasitoids

Plants attacked by insects release volatile compounds that attract the herbivores' natural enemies. This so-called indirect defense is plastic and may be affected by an array of biotic and abiotic factors. We investigated the effect of fungal infection as a biotic stress agent on the emission of herbivore-induced volatiles and the possible consequences for the attraction of two parasitoid species. Maize seedlings that were simultaneously attacked by the fungus Setosphaeria turcica and larvae of Spodoptera littoralis emitted a blend of volatiles that was qualitatively similar to the blend emitted by maize that was damaged by only the herbivore, but there was a clear quantitative difference. When simultaneously challenged by fungus and herbivore, the maize plants emitted in total 47% less of the volatiles. Emissions of green leaf volatiles were unaffected. In a six-arm olfactometer, the parasitoids Cotesia marginiventris and Microplitis rufiventris responded equally well to odors of herbivore-damaged and fungus- and herbivore-damaged maize plants. Healthy and fungus-infected plants were not attractive. An additional experiment showed that the performance of S. littoralis caterpillars was not affected by the presence of the pathogen, nor was there an effect on larvae of M. rufiventris developing inside the caterpillars. Our results confirm previous indications that naïve wasps may respond primarily to the green leaf volatiles.     

Herbivore-Induced Plant Volatiles Can Serve as Host Location Cues for a Generalist and a Specialist Egg Parasitoid

Herbivore-induced plant volatiles are important host finding cues for larval parasitoids, and similarly, insect oviposition might elicit the release of plant volatiles functioning as host finding cues for egg parasitoids. We hypothesized that egg parasitoids also might utilize HIPVs of emerging larvae to locate plants with host eggs. We, therefore, assessed the olfactory response of two egg parasitoids, a generalist, Trichogramma pretiosum (Tricogrammatidae), and a specialist, Telenomus remus (Scelionidae) to HIPVs. We used a Y-tube olfactometer to tests the wasps’ responses to volatiles released by young maize plants that were treated with regurgitant from caterpillars of the moth Spodoptera frugiperda (Noctuidae) or were directly attacked by the caterpillars. The results show that the generalist egg parasitoid Tr. pretiosum is innately attracted by volatiles from freshly-damaged plants 0–1 and 2–3 h after regurgitant treatment. During this interval, the volatile blend consisted of green leaf volatiles (GLVs) and a blend of aromatic compounds, mono- and homoterpenes, respectively. Behavioral assays with synthetic GLVs confirmed their attractiveness to Tr. pretiosum. The generalist learned the more complex volatile blends released 6–7 h after induction, which consisted mainly of sesquiterpenes. The specialist T. remus on the other hand was attracted only to volatiles emitted from fresh and old damage after associating these volatiles with oviposition. Taken together, these results strengthen the emerging pattern that egg and larval parasitoids behave in a similar way in that generalists can respond innately to HIPVs, while specialists seems to rely more on associative learning.     

Effect of the Presence of a Nonhost Herbivore on the Response of the Aphid Parasitoid <Emphasis Type="Italic">Diaeretiella rapae</Emphasis> to Host-infested Cabbage Plants

The vast majority of studies of plant indirect defense strategies have considered simple tritrophic systems that involve plant responses to attack by a single herbivore species. However, responses by predators and parasitoids to specific, herbivore-induced, volatile blends could be compromised when two or more different herbivores are feeding on the same plant. In Y-tube olfactometer studies, we investigated the responses of an aphid parasitoid, Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae), to odors from cabbage plants infested with the peach-potato aphid Myzus persicae (Sulzer) (Homoptera: Aphididae), in both the presence and absence of a lepidopteran caterpillar, Plutella xylostella L. (Lepidoptera: Plutellidae). Female parasitoids chose aphid-infested plants over uninfested plants but did not distinguish between caterpillar-infested and uninfested plants. When given a choice between odors from an aphid-infested plant and those from a plant infested with diamondback moth larvae, they significantly chose the former. Furthermore, the parasitoids responded equally to odors from a plant infested with aphids only and those from a plant infested with both aphids and caterpillars. The results support the hypothesis that the aphid and the caterpillar induce different changes in the volatile profile of cabbage plants and that D. rapae females readily distinguish between the two. Furthermore, the changes to the plant volatile profile induced by the caterpillar damage did not hinder the responses of the parasitoid to aphid-induced signals.     

Impact of Herbivore-induced Plant Volatiles on Parasitoid Foraging Success: A Spatial Simulation of the <Emphasis Type="Italic">Cotesia rubecula,Pieris rapae,</Emphasis> and <Emphasis Type="Italic">Brassica oleracea</Emphasis> System

Many parasitoids are known to use herbivore-induced plant volatiles as cues to locate hosts. However, data are lacking on how much of an advantage a parasitoid can gain from following these plant cues and which factors can limit the value of these cues to the parasitoid. In this study, we simulate the Cotesia rubecula-Pieris rapae-Brassica oleracea system, and ask how many more hosts can a parasitoid attack in a single day of foraging by following plant signals versus randomly foraging. We vary herbivore density, plant response time, parasitoid flight distance, and available host stages to see under which conditions parasitoids benefit from herbivore-induced plant cues. In most of the parameter combinations studied, parasitoids that responded to cues attacked more hosts than those that foraged randomly. Parasitoids following plant cues attacked up to ten times more hosts when they were able to successfully attack herbivores older than first instar; however, if parasitoids were limited to first instar hosts, those following plant cues were at a disadvantage when plants took longer than a day to respond to herbivory. At low herbivore densities, only parasitoids with a larger foraging radius could take advantage of plant cues. Although preference for herbivore-induced volatiles was not always beneficial for a parasitoid, under the most likely natural conditions, the model predicts that C. rubecula gains fitness from following plant cues.     

Induction of volatile emissions in maize by different larval instars of Spodoptera littoralis

Maize plants under attack by caterpillars emit a specific blend of volatiles that is highly attractive to parasitic wasps. The release of these signals is induced by elicitors in the caterpillar regurgitant. Studies suggest that plants respond differently to different herbivore species and even to different herbivore stages, thus providing parasitoids and predators with specific signals. We tested if this is the case for different larval instars of the noctuid moth Spodoptera littoralis when they feed on maize plants. Cut maize plants were incubated in diluted regurgitant from second, third, or fifth instar caterpillars. There were no differences in total amount released after these treatments, but there were small differences in the release of the minor compounds phenethyl acetate and -humulene. Regurgitant of all three instars contained the elicitor volicitin. To test the effect of actual feeding by the larvae, potted plants were infested with caterpillars of one of the three instars, and volatiles were collected the following day. The intensity of the emissions was correlated with the number of larvae feeding on a plant, and with the amount of damage inflicted, but was independent of the instar that caused the damage. We also used artificial damage to mimic the manner of feeding of each instar to test the importance of physical aspects of damages for the odor emission. The emission was highly variable, but no differences were found among the different types of damage. In olfactometer tests, Microplitis rufiventris, a parasitoid that can only successfully parasitize second and early third instar S. littoralis, did not differentiate among the odors of maize plants attacked by different instar larvae. The odor analyses as well as the parasitoid's responses indicate that maize odors induced by S. littoralis provide parasitoids with poor information on the larval developmental stage. We discuss the results in the context of variability and lack of specificity in odorous plant signals.     

Volatile Stimuli Related to Feeding Activity of Nonprey Caterpillars, Spodoptera exigua, Affect Olfactory Response of the Predatory Mite Phytoseiulus persimilis

The effect of volatiles related to feeding activity of nonprey caterpillars, Spodoptera exigua, on the olfactory response of the predatory mites Phytoseiulus persimilis was examined in a Y-tube olfactometer. At a low caterpillar density (20 caterpillars on 10 Lima bean leaves), the predators were significantly more attracted to volatiles from infested leaves on which the caterpillars and their products were present or from infested leaves from which the caterpillars and their products had been removed when compared to volatiles from uninfested leaves. The predators, however, significantly avoided odors from 20 caterpillars and their products (mainly feces) removed from bean leaves. In contrast, at a higher caterpillar density (100 caterpillars on 10 Lima bean leaves), the predators avoided volatiles from caterpillar-infested bean leaves. Volatiles from infested leaves from which the caterpillars and their products had been removed were not preferred over volatiles from uninfested leaves. Volatiles from feces collected from 100 caterpillars were strongly avoided by the predators, while the behavior of the predatory mites was not affected by volatiles from 100 caterpillars removed from a plant. The data show that carnivorous arthropods may avoid nonprofitable herbivores. This avoidance seems to result from an interference of volatiles from herbivore products with the attraction to herbivore-induced plant volatiles.     

Olfactory Responses of Parasitoid Apoanagyrus lopezi to Odor of Plants, Mealybugs, and Plant–Mealybug Complexes

Apoanagyrus (Epidinocarsis) lopezi De Santis is an endoparasitoid used in the biological control of the cassava mealybug Phenacoccus manihoti Matile-Ferrero in Africa. The response of naive and mated females of A. lopezi to odors from cassava plant (var. Zanaga), parasitized or unparasitized mealybugs, and plant–mealybug host complexes with or without feeding hosts was investigated in a Y-tube olfactometer. Dual-choice tests revealed that mealybug-infested plants and mealybug-damaged plants were the major sources of volatiles that attract female parasitoids to the microhabitat of its hosts. The emission of volatile chemicals appears not to be limited to the infested plant part but to occur systemically throughout the plant. On their own, unparasitized mealybugs were more attractive than uninfested plants or parasitized mealybugs alone. Parasitization of P. manihoti by A. lopezi decreased the response of parasitoids to mealybugs or mealybug–plant complexes. Plants infested with unparasitized hosts attracted more female parasitoids than plants infested with parasitized mealybugs. These results indicate that, in the long-range host-searching process, females of A. lopezi respond mainly to mealybug-induced synomones, and specific host-derived cues play a minor role.     

Oral Secretions Affect HIPVs Induced by Generalist (<Emphasis Type="Italic">Mythimna loreyi</Emphasis>) and Specialist (<Emphasis Type="Italic">Parnara guttata</Emphasis>) Herbivores in Rice

Plants synthesize variable mixtures of herbivore-induced plant volatiles (HIPVs) as part of their evolutionary conserved defense. To elucidate the impact of chewing herbivores with different level of adaptation on HIPV profiles in rice, we measured HIPVs released from rice seedlings challenged by either the generalist herbivore Mythimna loreyi (MYL) or the specialist Parnara guttata (PAG). Both herbivores markedly elicited the emission of HIPVs, mainly on the second and third days after attack compared to control plants. In addition, side-by-side HIPV comparisons using MYL and PAG caterpillars revealed that generalist feeding induced comparably more HIPVs relative to specialist, particularly on day two as highlighted by multivariate analysis (PLS-DA) of emitted HIPVs, and further confirmed in mimicked herbivory experiments. Here, mechanically wounded plants treated with water (WW) released more VOCs than untreated controls, and on top of this, oral secretions (OS) from both herbivores showed differential effects on volatile emissions from the wounded plants. Similar to actual herbivory, MYL OS promoted higher amounts of HIPVs relative to PAG OS, thus supporting disparate induction of rice indirect defenses in response to generalist and specialist herbivores, which could be due to the differential composition of their OS. (196 words).     

Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L

When attacked by herbivorous insects, many plants emit volatile compounds that are used as cues by predators and parasitoids foraging for prey or hosts. While such interactions have been demonstrated in several host–plant complexes, in most studies, the herbivores involved are leaf-feeding arthropods. We studied the long-range plant volatiles involved in host location in a system based on a very different interaction since the herbivore is a fly whose larvae feed on the roots of cole plants in the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae). The parasitoid studied is Trybliographa rapae Westwood (Hymenoptera: Figitidae), a specialist larval endoparasitoid of D. radicum. Using a four-arm olfactometer, the attraction of naive T. rapae females toward uninfested and infested turnip plants was investigated. T. rapae females were not attracted to volatiles emanating from uninfested plants, whether presented as whole plants, roots, or leaves. In contrast, they were highly attracted to volatiles emitted by roots infested with D. radicum larvae, by undamaged parts of infested roots, and by undamaged leaves of infested plants. The production of parasitoid-attracting volatiles appeared to be systemic in this particular tritrophic system. The possible factors triggering this volatile emission were also investigated. Volatiles from leaves of water-stressed plants and artificially damaged plants were not attractive to T. rapae females, while volatiles emitted by leaves of artificially damaged plants treated with crushed D. radicum larvae were highly attractive. However, T. rapae females were not attracted to volatiles emitted by artificially damaged plants treated only with crushed salivary glands from D. radicum larvae. These results demonstrate the systemic production of herbivore-induced volatiles in this host-plant complex. Although the emission of parasitoid attracting volatiles is induced by factors present in the herbivorous host, their exact origin remains unclear. The probable nature of the volatiles involved and the possible origin of the elicitor of volatiles release are discussed.     

Defense Suppression through Interplant Communication Depends on the Attacking Herbivore Species

In response to herbivory, plants emit volatile compounds that play important roles in plant defense. Herbivore-induced plant volatiles (HIPVs) can deter herbivores, recruit natural enemies, and warn other plants of possible herbivore attack. Following HIPV detection, neighboring plants often respond by enhancing their anti-herbivore defenses, but a recent study found that herbivores can manipulate HIPV-interplant communication for their own benefit and suppress defenses in neighboring plants. Herbivores induce species-specific blends of HIPVs and how these different blends affect the specificity of plant defense responses remains unclear. Here we assessed how HIPVs from zucchini plants (Cucurbita pepo) challenged with different herbivore species affect resistance in neighboring plants. Volatile “emitter” plants were damaged by one of three herbivore species: saltmarsh caterpillars (Estigmene acrea), squash bugs (Anasa tristis), or striped cucumber beetles (Acalymma vittatum), or were left as undamaged controls. Neighboring “receiver” plants were exposed to HIPVs or control volatiles and then challenged by the associated herbivore species. As measures of plant resistance, we quantified herbivore feeding damage and defense-related phytohormones in receivers. We found that the three herbivore species induced different HIPV blends from squash plants. HIPVs induced by saltmarsh caterpillars suppressed defenses in receivers, leading to greater herbivory and lower defense induction compared to controls. In contrast, HIPVs induced by cucumber beetles and squash bugs did not affect plant resistance to subsequent herbivory in receivers. Our study shows that herbivore species identity affects volatile-mediated interplant communication in zucchini, revealing a new example of herbivore defense suppression through volatile cues.

     

Systemically Induced Plant Volatiles Emitted at the Time of “Danger”

Feeding by Pieris brassicae caterpillars on the lower leaves of Brussels sprouts (Brassica oleracea var. gemmifera) plants triggers the release of volatiles from upper leaves. The volatiles are attractive for a natural antagonist of the herbivore, the parasitoid Cotesia glomerata. Parasitoids are attracted only if additional damage is inflicted on the systemically induced upper leaves and only after at least three days of herbivore feeding on the lower leaves. Upon termination of caterpillar feeding, the systemic signal is emitted for a maximum of one more day. Systemic induction did not occur at low levels of herbivore infestation. Systemically induced leaves emitted green leaf volatiles, cyclic monoterpenoids, and sesquiterpenes. GC-MS profiles of systemically induced and herbivore-infested leaves did not differ for most compounds, although herbivore infested plants did emit higher amounts of green leaf volatiles. Emission of systemically induced volatiles in Brussels sprouts might function as an induced defense that is activated only when needed, i.e., at the time of caterpillar attack. This way, plants may adopt a flexible management of inducible defensive resources to minimize costs of defense and to maximize fitness in response to unpredictable herbivore attack.     

Identification of Key Plant-Associated Volatiles Emitted by <Emphasis Type="Italic">Heliothis virescens</Emphasis> Larvae that Attract the Parasitoid, <Emphasis Type="Italic">Microplitis croceipes</Emphasis>: Implications for Parasitoid Perception of Odor Blends

Herbivores emit plant-associated volatile organic compounds (VOCs) after feeding on plants. These plant-associated VOCs can be used by parasitoids to locate their hosts. It is hypothesized that certain compounds play key roles in the attractiveness of host-associated odor blends. The larval parasitoid, Microplitis croceipes (Hymenoptera: Braconidae) and its herbivore host, Heliothis virescens (Lepidoptera: Noctuidae), a major pest of cotton plant were used as model species to identify key compounds mediating attraction of parasitoids to hosts. Comparative GC/MS analyses of cotton-fed vs. artificial diet-fed hosts indicated that 12 of 17 compounds in the headspace of H. virescens larvae were exclusive to plant-fed hosts, and thus considered to be plant-associated. In order to identify key attractive compounds, a full blend of 15 commercially available synthetic compounds was modified by removing each of the 10 plant-associated compounds emitted by host larvae. In Y-tube olfactometer bioassays testing parasitoid responses to modified blends, 1-octen-3-ol, decanal, (E)-β-caryophyllene, α-humulene, α-farnesene, and β-pinene were identified as key compounds contributing to attractiveness of the natural blend of VOCs emitted by cotton-fed hosts. The results showed that while various host-associated compounds act in concert to serve as useful host location cues, only a fraction of the natural blend mediates attraction in parasitoids. Furthermore, the role of a compound is better assessed in the context of other compounds, and odor blends are better perceived as a whole rather than as individual components.     

Modifications of the Chemical Profile of Hosts after Parasitism Allow Parasitoid Females to Assess the Time Elapsed Since the First Attack

In solitary parasitoids, only one adult can emerge from a given host. In some of these species, when several eggs are laid on the same host, supernumerary individuals are eliminated by lethal larval fights. In the solitary parasitoid Anisopteromalus calandrae, the probability of a second larva winning the fight depends on the time elapsed since the first oviposition. The older the first egg is at the moment a second egg is laid, the less chance the second egg has of winning the competition. As a consequence, females of this species lay their eggs preferentially on recently parasitized hosts rather than on hosts parasitized by an egg about to hatch. Anisopteromalus calandrae females parasitize bruchid larvae located in cowpea seeds. In a series of choice test experiments using an artificial seed system, we demonstrated that the cue that allows parasitoid females to differentiate between hosts parasitized for different lengths of time comes from the host and not from the artificial seed or the previously laid egg. This cue is perceived at short range, indicating that the chemicals involved are probably partly volatile. Interestingly, although parasitism stops host development, cuticular profiles continue to evolve, but in a different way from those of unparasitized hosts. This difference in the host’s cuticular profile after parasitism, therefore, probably underlies the parasitoid female’s discrimination.     

Response of a Predatory ant to Volatiles Emitted by Aphid- and Caterpillar-Infested Cucumber and Potato Plants

In response to herbivory by insects, various plants produce volatiles that attract enemies of the herbivores. Although ants are important components of natural and agro-ecosystems, the importance of herbivore-induced plant volatiles (HIPVs) as cues for ants for finding food sources have received little attention. We investigated responses of the ant Formica pratensis to volatiles emitted by uninfested and insect-infested cucumber (Cucumis sativus) and potato (Solanum tuberosum) plants. Cucumber plants were infested by the phloem-feeding aphid Aphis gossypii, the leaf chewer Mamestra brassicae or simultaneously by both insects. Potato plants were infested by either Aphis gossypii, by the leaf chewer Chrysodeixis chalcites or both. In olfactometer experiments, ants preferred volatile blends emitted by cucumber plants infested with M. brassicae caterpillars alone or combined with A. gossypii to volatiles of undamaged plants or plants damaged by A. gossypii only. No preference was recorded in choice tests between volatiles released by aphid-infested plants over undamaged plants. Volatiles emitted by potato plants infested by either C. chalcites or A. gossypii were preferred by ants over volatiles released by undamaged plants. Ants did not discriminate between potato plants infested with aphids and caterpillars over plants infested with aphids only. Plant headspace composition showed qualitative and/or quantitative differences between herbivore treatments. Multivariate analysis revealed clear separation between uninfested and infested plants and among herbivore treatments. The importance of HIPVs in indirect plant defence by ants is discussed in the context of the ecology of ant-plant interactions and possible roles of ants in pest management.     

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.     

The Role of Fresh <Emphasis Type="Italic">versus</Emphasis> Old Leaf Damage in the Attraction of Parasitic Wasps to Herbivore-Induced Maize Volatiles

The odor produced by a plant under herbivore attack is often used by parasitic wasps to locate hosts. Any type of surface damage commonly causes plant leaves to release so-called green leaf volatiles, whereas blends of inducible compounds are more specific for herbivore attack and can vary considerably among plant genotypes. We compared the responses of naïve and experienced parasitoids of the species Cotesia marginiventris and Microplitis rufiventris to volatiles from maize leaves with fresh damage (mainly green leaf volatiles) vs. old damage (mainly terpenoids) in a six-arm olfactometer. These braconid wasps are both solitary endoparasitoids of lepidopteran larvae, but differ in geographical origin and host range. In choice experiments with odor blends from maize plants with fresh damage vs. blends from plants with old damage, inexperienced C. marginiventris showed a preference for the volatiles from freshly damaged leaves. No such preference was observed for inexperienced M. rufiventris. After an oviposition experience in hosts feeding on maize plants, C. marginiventris females were more attracted by a mixture of volatiles from fresh and old damage. Apparently, C. marginiventris has an innate preference for the odor of freshly damaged leaves, and this preference shifts in favor of a blend containing a mixture of green leaf volatiles plus terpenoids, after experiencing the latter blend in association with hosts. M. rufiventris responded poorly after experience and preferred fresh damage odors. Possibly, after associative learning, this species uses cues that are more directly related with the host presence, such as volatiles from host feces, which were not present in the odor sources offered in the olfactometer. The results demonstrate the complexity of the use of plant volatiles by parasitoids and show that different parasitoid species have evolved different strategies to exploit these signals.