Egg parasitoid attraction toward induced plant volatiles is disrupted by a non-host herbivore attacking above or belowground plant organs (original) (raw)
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Attraction of egg-killing parasitoids toward induced plant volatiles in a multi-herbivore context
Oecologia, 2015
by S. exigua eggs, indicating the specificity of the plant responses toward lepidopteran herbivores. The results of the chemical analysis revealed significant differences between the volatile blends emitted by plants in response to attack by P. brassicae and S. exigua eggs which were in agreement with the behavioural observations. We investigated the attraction of Trichogramma wasps toward P. brassicae egg-induced volatiles in plants simultaneously attacked by larvae and nymphs of different non-hosts. The two chewing caterpillars P. brassicae and S. exigua, but not the phloem-feeding aphid B. brassicae, can disrupt the attraction of Trichogramma species toward P. brassicae egg-induced volatiles. Indirect plant defenses are discussed in the context of multiple herbivory by evaluating the importance of origin, dietary specialization and feeding guild of different attackers on the recruitment of eggkilling parasitoids.
PeerJ, 2017
Several phases of herbivorous insect attack including feeding and oviposition are known to induce plant defenses. Plants emit volatiles induced by herbivores to recruit insect parasitoids as an indirect defense strategy. So far, volatiles induced by herbivore walking and their putative role in the foraging behavior of egg parasitoids have not been investigated. In this paper we studied the response of the egg parasitoid Trissolcus basalis toward volatiles emitted by Vicia faba plants as consequence of the walking activity of the host Nezara viridula. Olfactometer bioassays were carried out to evaluate wasp responses to plants in which the abaxial or the adaxial surfaces were subjected to walking or/and oviposition. Results showed that host female walking on the abaxial but not on the adaxial surface caused a repellence effect in T. basalis 24 h after plant treatment. The emission of active volatiles also occurred when the leaf was turned upside-down, indicating a specificity of stre...
Journal of Chemical Ecology, 2011
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, monoand 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.
Plant Volatiles Induced by Herbivore Egg Deposition Affect Insects of Different Trophic Levels
PLoS ONE, 2012
Plants release volatiles induced by herbivore feeding that may affect the diversity and composition of plant-associated arthropod communities. However, the specificity and role of plant volatiles induced during the early phase of attack, i.e. egg deposition by herbivorous insects, and their consequences on insects of different trophic levels remain poorly explored. In olfactometer and wind tunnel setups , we investigated behavioural responses of a specialist cabbage butterfly (Pieris brassicae) and two of its parasitic wasps (Trichogramma brassicae and Cotesia glomerata) to volatiles of a wild crucifer (Brassica nigra) induced by oviposition of the specialist butterfly and an additional generalist moth (Mamestra brassicae). Gravid butterflies were repelled by volatiles from plants induced by cabbage white butterfly eggs, probably as a means of avoiding competition, whereas both parasitic wasp species were attracted. In contrast, volatiles from plants induced by eggs of the generalist moth did neither repel nor attract any of the tested community members. Analysis of the plant's volatile metabolomic profile by gas chromatography-mass spectrometry and the structure of the plant-egg interface by scanning electron microscopy confirmed that the plant responds differently to egg deposition by the two lepidopteran species. Our findings imply that prior to actual feeding damage, egg deposition can induce specific plant responses that significantly influence various members of higher trophic levels.
Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host
PLoS Biology, 2012
Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids. Citation: Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE, et al. (2012) Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host. PLoS Biol 10(11): e1001435.
Is Attraction Fatal? The Effects of Herbivore-Induced Plant Volatiles on Herbivore Parasitism
Ecology, 2002
We investigated the relationship between parasitoid attraction to herbivoreinduced plant volatiles and larval parasitism rates of two closely related heliothine, noctuid moths. Heliothis subflexa Guenee is a specialist on plants in the genus Physalis, while Heliothis virescens Fabricius is an extreme generalist. In North America, these species serve as the only known hosts for the specialist parasitoid Cardiochiles nigriceps Vierick; oviposition into Helicoverpa zea, a non-host, does occur but results in lethal encapsulation of C. nigriceps' eggs. Heliothis virescens larvae are parasitised by C. nigriceps far more frequently than are H. subflexa larvae. Parasitoid attraction to volatiles emitted by tobacco in response to herbivory by H. virescens has previously been demonstrated. Using field experiments, we examined the possibility that pre-detection defenses against parasitoid attraction to herbivore-induced plant volatiles are responsible for H. subflexa's relatively low rates of parasitism by C. nigriceps. Herbivore-damaged plants were significantly more attractive to C. nigriceps than were larvae, larval frass, larval saliva, or damaged leaves alone. Plant species affected parasitoid attraction: tobacco was the most preferred plant species, followed by Physalis angulata, and then cotton. The parasitoid was also more attracted to host species (H. subflexa and H. virescens) than to the non-host species, H. zea. There was an interaction between plant species and herbivore species: each plant species was most attractive when infested by its typical herbivore (e.g., H. virescens on tobacco). We compared these data with those of a previously published experiment on field parasitism of H. virescens and H. subflexa, conducted at the same time and place. Our results indicate that differences in parasitoid attraction to herbivore-induced plant volatiles do not contribute to H. subflexa's relatively low parasitism rate. For the generalist, H. virescens, rates of attraction correspond with rates of parasitism; for the specialist, H. subflexa, they do not. Attraction to H. subflexa on P. angulata is greater than to H. virescens on P. angulata, yet parasitism of H. subflexa is much less than parasitism of H. virescens. These results indicate that pre-detection defenses are not responsible for H. subflexa's low parasitism on P. angulata.
Journal of Chemical Ecology, 2008
Volatiles emitted by plants in response to feeding by Lygus species were tested in neurophysiological, behavioral, and parasitism trials with Anaphes iole, an egg parasitoid of Lygus. Electroantennogram analyses indicated that A. iole antennae responded to most herbivore-induced plant volatiles (HIPVs) tested and that females were usually more responsive than males. Antennal responses to (Z)-3hexenyl acetate and methyl salicylate were among the strongest. Behavioral assays in a four-arm olfactometer demonstrated that response of female wasps to (Z)-3hexenyl acetate varied greatly depending on preconditioning regime. Preconditioning wasps to complex host-plant odors led to stronger preference than did a single preconditioning stimulus, i.e., (Z)-3-hexenyl acetate. In a horizontal wind tunnel, female wasps were attracted by methyl salicylate and α-farnesene. Parasitism of Lygus lineolaris eggs by A. iole in a cotton field was greater when the eggs were associated with (Z)-3-hexenyl acetate or αfarnesene than with controls. Overall, the results of this study show that A. iole can perceive a variety of plant volatiles released after its host damages plants, that the degree of associative learning in A. iole can be manipulated based on preconditioning regime, and that single synthetic HIPVs are attractive to A. iole and can be used to increase attack rates on host eggs. Therefore, it appears that HIPVs have potential for use in suppression of Lygus population densities.
Herbivore-Induced Plant Volatiles Mediate In-Flight Host Discrimination by Parasitoids
Journal of Chemical Ecology, 2005
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 herbivoreinduced 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 plantYparasitoid interactions.
The parasitoid wasp Apanteles taragamae is a promising candidate for the biological control of the legume pod borer Maruca vitrata, which recently has been introduced into Benin. The effects of volatiles from cowpea and peabush flowers and Maruca vitrata larvae on host selection behavior of the parasitoid Apanteles taragamae were investigated under laboratory conditions by using a Ytube olfactometer. Naïve and oviposition-experienced female wasps were given a choice between several odor sources that included (1) uninfested, (2) Maruca vitratainfested, and (3) mechanically damaged cowpea flowers, as well as (4) stem portions of peabush plants carrying leaves and flowers, (5) healthy M. vitrata larvae, and moribund (6), and live virus-infected M. vitrata larvae. Responses of naïve and oviposition-experienced female wasps did not differ for any of the odor source combinations. Wasps were significantly attracted to floral volatiles produced by cowpea flowers that had been infested with M. vitrata larvae and from which the larvae had been removed. Apanteles taragamae females also were attracted to Maruca vitrata-infested flowers after removal of both the larvae and their feces. Female wasps discriminated between volatiles from previously infested flowers and mechanically damaged flowers. Uninfested cowpea flowers attracted only oviposition-experienced wasps that had received a rewarding experience (i.e. the parasitization of two M. vitrata larvae feeding on cowpea flowers) before the olfactometer test. Wasps also were attracted to uninfested leaves and flowers of peabush. Moreover, they were also attracted to healthy and live virus-infected M. vitrata larvae, but not when the latter were moribund. Our data show that, similarly to what has been extensively been reported for foliar volatiles, flowers of plants also emit parasitoidattracting volatiles in response to being infested with an herbivore.