Plant-natural enemy association in the tritrophic system,Cotesia rubecula-Pieris rapae-brassiceae (cruciferae): I. Sources of infochemicals

The role of airborne infochemicals in host selection by the parasitoidCotesia rubecula (Marshal) (Hymenoptera: Braconidae) was examined in a wind tunnel. To elucidate the role of volatile chemicals in attractingC. rubecula to cabbage infested by the host [Pieris rapae L. (Lepidoptera: Pieridae)], the potential sources of volatiles related toP. rapae infestation on cabbage were tested individually. The responses of females to nonhost plant species, bean and geranium, as well as to frass of a nonhost lepidopteran were also examined.C. rubecula was attracted to cabbage previously infested byP. rapae and to frass and regurgitate ofP. rapae. No attraction was observed to larvae ofP. rapae alone. Females were also attracted to mechanically damaged cabbage, cabbage previously infested byPlutella xylostella L. (Lepidoptera: Plutellidae) (a nonhost lepidopteran herbivore), and cabbage previously infested by snails (a nonhost, noninsect herbivore). Intact cabbage, bean, and geranium plants elicited no attraction. A low frequency of attraction was observed to mechanically damaged bean and geranium. Attraction was also observed to frass ofP. xylostella. Volatiles from cabbage related to damage, and volatiles from frass and regurgitate of the host seem to play an important role in guidingC. rubecula to plants infested by its host.     

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.     

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.     

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.     

Rejection of host plant by larvae of cabbage butterfly: Diet-dependent sensitivity to an antifeedant

Garden nasturtium,Tropaeolum majus (Tropaeolaceae), is an acceptable host plant for the cabbage butterfly,Pieris rapae. Eggs are readily laid on the plant and hatching larvae feed and develop into normal pupae and adults. However, when second- to fifth-instar larvae were transferred from cabbage to nasturtium, they refused to feed and starved to death. Similar results were obtained when larvae were transferred from other host plants to nasturtium. However, larvae that were reared on nasturtium readily accepted cabbage as a new host plant. We have demonstrated the presence of strong antifeedants in nasturtium foliage and identified the most prominent active compound as chlorogenic acid. However, larvae reared on nasturtium had limited sensitivity, and larvae reared on a wheat germ diet were completely insensitive to the antifeedants. Larvae apparently develop sensitivity to the deterrent as a result of feeding on other host plants, whereas continuous exposure to the deterrent causes habituation or suppression of sensitivity development. The results demonstrate that dietary experience can dramatically affect the response of an insect to a potentially antifeedant compound in a plant.     

Plant-natural enemy association in the tritrophic systemCotesia rubecula-Pieris rapae-brassicaceae (cruciferae): II. Preference ofC. rubecula for landing and searching

The responses of the parasitoidCotesia rubecula to differently damaged cabbages were recorded during a series of choice tests. To determine if flyingC. rubecula can discriminate differences in the blend of volatiles emitted by cabbages damaged by different causes and how plant volatiles released from a distant source affect the searching behavior ofC. rubecula once searching on a plant, wasps were presented with a choice of plants located one behind the other and separated by a distance of 15 cm. The sources of damage were: cabbage damaged by the host (Pieris rapae), by a nonhost lepidopteran herbivore (Plutella xylostella), by a nonhost, noninsect herbivore (snail), and by mechanical means. The results showed that the site of first landing and the time spent searching on the leaves was influenced by the type of damage inflicted on plants. Wasps preferred to land on cabbages damaged by host and nonhost species of Lepidoptera over those damaged by snails and mechanical means. No preference was observed for first landing between cabbages damaged by the two species of Lepidoptera or between cabbages damaged by snails and mechanical means. Cabbage damaged byP. rapae was searched most intensively, followed by cabbage damaged byP. xylostella, cabbage damaged by snails, and cabbage damaged by mechanical means.C. rubecula differentiates between the volatile blends emitted by differently damaged cabbages, and it is attracted to volatiles related to recent lepidopteran damage. Wasps searched longer on freshly damaged than on leaves with older damage.     

Role of volatile inforchemicals emitted by feces of larvae in host-searching behavior of parasitoidCotesia rubecula (Hymenoptera: Braconidae): A behavioral and chemical study

The role of volatile infochemicals emitted by feces of larvae in the host-searching behavior of the parasitoidCotesia rubecula was evaluated during single- and dual-choice tests inside a wind tunnel. The following treatments were tested: feces produced by second and fourth instars ofPieris rapae (preferred host), second instars ofP. brassicae (inferior host), second instars ofP. napi (nonhost), and wet feces of second instars ofP. rapae. During a single-choice situation females ofC. rubecula oriented to all types of feces tested. When a preference was to be made,C. rubecula preferred feces of second instars ofP. rapae over that of fourth, feces ofP. rapae over that ofP. brassicae, feces ofP. napi over that ofP. brassicae, and wet over normal host feces. No preference was exhibited between feces of second instars ofP. napi and that of second instars ofP. rapae. The relative importance of infochemicals from host feces versus plant damage caused by host larvae to the searching behavior ofC. rubecula was also evaluated. Plant damage was more important to the searching females than host feces when feces were present in specific concentrations in relation to damage. The volatiles released by normal and wet feces of second instars ofP. rapae, wet feces of fourth instars ofP. rapae, and normal and wet feces ofP. brassicae were collected and identified. Overall, 85 chemical compounds were recorded belonging to the following chemical groups: alcohols, ketones, aldehydes, esters, isothiocyanates, sulfides, nitriles, furanoids, terpenoids and pyridines. The blend of chemicals emitted by feces of different instars ofP. rapae and different species ofPieris exhibited an instar and species specificity in both quantity and quality. Wetting of normal feces increased the amount of volatile chemicals released, and it was also responsible for the appearance of new compounds. The role of feces of larvae in the host-seeking behavior ofC. rubecula is discussed.     

Role of the Lipoxygenase/lyase Pathway of Host-food Plants in the Host Searching Behavior of Two Parasitoid Species, Cotesia glomerata and Cotesia plutellae

To elucidate the role of the plant lipoxygenase (LOX)/lyase pathway for host search behavior of two parasitic wasps attacking herbivorous larvae, an Arabidopsis mutant (all84) was isolated with a mutation somewhere in the LOX/lyase pathway. Detached leaves of the mutant were shown to release less (Z)-3-hexenal, a first green leaf volatile (GLV) product of the LOX/lyase pathway. The braconid larval parasitoids studied, Cotesia glomerata and Cotesia plutella, differ in their ability to discriminate among plant volatiles induced by feeding of lepidopteran hosts and nonhosts: C. plutella only responds to plant volatiles induced by hosts (Plutella larvae), whereas the response by the more generalist C. glomerata is not host specific. The Arabidopsis mutant all84 infested by Pieris larvae was less attractive to C. glomerata than Arabidopsis wild type (wt) infested by the host larvae. C. glomerata was attracted by two of the GLV biosynthesized through the LOX/lyase pathway, (E)-2-hexenal and (Z)-3-hexenyl acetate. However, attraction of C. plutellae to volatiles from Plutella-infested all84 plants did not differ from attraction to host-infested wt Arabidopsis. Both wasp species were arrested to the respective host-infested edge of the wt leaf by showing characteristic antennal searching behavior on the edge. In C. glomerata, the duration of this searching behavior at the infested leaf edge was significantly shorter on all84 plants than on wt plants. By contrast, the duration of the searching behavior of C. plutellae on the host-infested leaf edge of all84 was not significantly different from that on the wt leaf. These data suggest that the LOX/lyase pathway is directly involved in the production of attractants and arrestants important for host search behavior of the more generalist C. glomerata, but not for the specialist C. plutellae.     

<Emphasis Type="Italic">Barbarea vulgaris</Emphasis> Glucosinolate Phenotypes Differentially Affect Performance and Preference of Two Different Species of Lepidopteran Herbivores

The composition of secondary metabolites and the nutritional value of a plant both determine herbivore preference and performance. The genetically determined glucosinolate pattern of Barbarea vulgaris can be dominated by either glucobarbarin (BAR-type) or by gluconasturtiin (NAS-type). Because of the structural differences, these glucosinolates may have different effects on herbivores. We compared the two Barbarea chemotypes with regards to the preference and performance of two lepidopteran herbivores, using Mamestra brassicae as a generalist and Pieris rapae as a specialist. The generalist and specialist herbivores did not prefer either chemotype for oviposition. However, larvae of the generalist M. brassicae preferred to feed and performed best on NAS-type plants. On NAS-type plants, 100% of the M. brassicae larvae survived while growing exponentially, whereas on BAR-type plants, M. brassicae larvae showed little growth and a mortality of 37.5%. In contrast to M. brassicae, the larval preference and performance of the specialist P. rapae was unaffected by plant chemotype. Total levels of glucosinolates, water soluble sugars, and amino acids of B. vulgaris could not explain the poor preference and performance of M. brassicae on BAR-type plants. Our results suggest that difference in glucosinolate chemical structure is responsible for the differential effects of the B. vulgaris chemotypes on the generalist herbivore. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Jasmonic Acid-Induced Changes in <Emphasis Type="BoldItalic">Brassica oleracea</Emphasis> Affect Oviposition Preference of Two Specialist Herbivores

Jasmonic acid (JA) is a key hormone involved in plant defense responses. The effect of JA treatment of cabbage plants on their acceptability for oviposition by two species of cabbage white butterflies, Pieris rapae and P. brassicae, was investigated. Both butterfly species laid fewer eggs on leaves of JA-treated plants compared to control plants. We show that this is due to processes in the plant after JA treatment rather than an effect of JA itself. The oviposition preference for control plants is adaptive, as development time from larval hatch until pupation of P. rapae caterpillars was longer on JA-treated plants. Total glucosinolate content in leaf surface extracts was similar for control and treated plants; however, two of the five glucosinolates were present in lower amounts in leaf surface extracts of JA-treated plants. When the butterflies were offered a choice between the purified glucosinolate fraction isolated from leaf surface extracts of JA-treated plants and that from control plants, they did not discriminate. Changes in leaf surface glucosinolate profile, therefore, do not seem to explain the change in oviposition preference of the butterflies after JA treatment, suggesting that as yet unknown infochemicals are involved.     

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.     

A chemical basis for differential acceptance ofErysimum cheiranthoides by twoPieris species

Wormseed mustard,Erysimum cheiranthoides, is unacceptable as a host for the cabbage butterfly,Pieris rapae. However, it is preferred for oviposition byPieris napi oleracea in the greenhouse. Isolation and identification of the oviposition stimulants toP. napi oleracea were accomplished by C₁₈ open-column chromatography, TLC, ion-exchange chromatography, HPLC, UV, and NMR spectroscopy. Glucoiberin and glucocheirolin were identified as the most active stimulants. The extracted glucoiberin was as stimulatory as glucocheirolin, although its concentration in theErysimum plants was about 10 times lower than that of glucocheirolin. These glucosinolates were only weak stimulants toP. rapae. Furthermore,P. rapae was strongly deterred by the cardenolides, erysimoside and erychroside, fromE. cheiranthoides, andP. napi oleracea was less sensitive to these compounds. No other deterrent toP. napi oleracea was detected in this plant species. The results explain the differential acceptance ofE. cheiranthoides by these twoPieris species.     

Olfactory responses of the parasitoidDiaeretiella rapae (Hymenoptera: Aphidiidae) to odor of plants,aphids, and plant-aphid complexes

Diaeretiella rapae (M'Intosh) (Hymenoptera: Aphidiidae) is a parasitoid of several aphid species, including the Russian wheat aphid (RWA),Diuraphis noxia (Mordvilko), and the cabbage aphid (CA).Brevicoryne brassicae (L.). The response of matedD. rapae females to odors from wheat, cabbage, and plant-host complexes was investigated using a four-choice olfactometer. Experienced parasitoids, but not inexperienced females, responded positively to odors of the wheat-RWA complex in a no-choice test. In choice tests, experienced parasitoids did not respond to odors of uninfested cabbage and wheat leaves, but did respond positively to aphid-infested plants and to aphids alone. The response ofD. rapae to the cabbage-CA complex and to CA alone was significantly greater than to the wheat-RWA complex and RWA alone, suggesting an innate odor preference for crucifer-feeding aphids.     

Chemical and experiential basis for rejection ofTropaeolum majus byPieris rapae larvae

Rejection of nasturtium,Tropaeolum majus, by cabbage-reared larvae ofPieris rapae has been explained by the presence of feeding deterrents in the nastrutium foliage. Sensitivity to the deterrents develops as neonate larvae feed on cabbage. The most prominent deterrent compound, which is present in nasturtium at a concentration of 40 mg/100 g fresh leaves, was identified as chlorogenic acid. When neonate larvae were fed on a cabbage leaf treated with high concentrations of deterrent-containing extracts of nasturtium foliage, they remained insensitive to the deterrents, so they accepted nasturtium when transferred as second instars. When neonate larvae were reared on a cabbage leaf treated with 0.1 mg chlorogenic acid, ca. 35% of the second instars accepted nasturtium. Similar dietary exposure of neonates to the subunits of chlorogenic acid, caffeic acid and quinic, acid resulted in much less or no effect on the rejection behavior of second instars. The results suggest that the combined effects of specific chemical constituents of nasturtium can explain the rejection of this plant by larvae ofP. rapae, but if larvae are continuously exposed to these compounds immediately after hatching, they apparently become habituated to the feeding deterrents. The lack of activity of the subunits of chlorogenic acid suggests that specific structural features are necessary for a dietary constituent to cause such habituation or suppression of sensitivity development.     

Induction of parasitoid attracting synomone in brussels sprouts plants by feeding ofPieris brassicae larvae: Role of mechanical damage and herbivore elicitor

Induction of plant defense in response to herbivory includes the emission of synomones that attract the natural enemies of herbivores. We investigated whether mechanical damage to Brussels sprouts leaves (Brassica oleracea var.gemmifera) is sufficient to obtain attraction of the parasitoidCotesia glomerata or whether feeding byPieris brassicae caterpillars elicits the release of synomones not produced by mechanically damaged leaves. The response of the parasitoidCotesia glomerata to different types of simulated herbivory was observed. Flight-chamber dual-choice tests showed that mechanically damaged cabbage leaves were less attractive than herbivore-damaged leaves and mechanically damaged leaves treated with larval regurgitant. Chemical analysis of the headspace of undamaged, artificially damaged, caterpillar-infested, and caterpillar regurgitant-treated leaves showed that the plant responds to damage with an increased release of volatiles. Greenleaf volatiles and several terpenoids are the major components of cabbage leaf headspace. Terpenoids are emitted in analogous amounts in all treatments, including undamaged leaves. On the other hand, if the plant is infested by caterpillars or if caterpillar regurgitant is applied to damaged leaves, the emission of green-leaf volatiles is highly enhanced. Our data are in contrast with the induction of more specific synomones in other plant species, such as Lima bean and corn.     

Herbivore-Induced Volatile Production by Arabidopsis thaliana Leads to Attraction of the Parasitoid Cotesia rubecula: Chemical, Behavioral, and Gene-Expression Analysis

Many plant species defend themselves against herbivorous insects indirectly by producing volatiles in response to herbivory. These volatiles attract carnivorous enemies of the herbivores. Research on the model plant Arabidopsis thaliana (L.) Heynh. has contributed considerably to the unraveling of signal transduction pathways involved in direct plant defense mechanisms against pathogens. Here, we demonstrate that Arabidopsis is also a good candidate for studying signal transduction pathways involved in indirect defense mechanisms by showing that: (1) Adult females of Cotesia rubecula, a specialist parasitic wasp of Pieris rapae caterpillars, are attracted to P. rapae-infested Arabidopsis plants. (2) Arabidopsis infested by P. rapae emits volatiles from several major biosynthetic pathways, including terpenoids and green leaf volatiles. The blends from herbivore-infested and artificially damaged plants are similar. However, differences can be found with respect to a few components of the blend, such as two nitriles and the monoterpene myrcene, that were produced exclusively by caterpillar-infested plants, and methyl salicylate, that was produced in larger amounts by caterpillar-infested plants. (3) Genes from major biosynthetic pathways involved in volatile production are induced by caterpillar feeding. These include AtTPS10, encoding a terpene synthase involved in myrcene production, AtPAL1, encoding phenylalanine ammonia-lyase involved in methyl salicylate production, and AtLOX2 and AtHPL, encoding lipoxygenase and hydroperoxide lyase, respectively, both involved in the production of green leaf volatiles. AtAOS, encoding allene oxide synthase, involved in the production of jasmonic acid, also was induced by herbivory.     

Differences in Volatile Profiles of Turnip Plants Subjected to Single and Dual Herbivory Above- and Belowground

Plants attacked by herbivorous insects emit volatile organic compounds that are used by natural enemies to locate their host or prey. The composition of the blend is often complex and specific. It may vary qualitatively and quantitatively according to plant and herbivore species, thus providing specific information for carnivorous arthropods. Most studies have focused on simple interactions that involve one species per trophic level, and typically have investigated the aboveground parts of plants. These investigations need to be extended to more complex networks that involve multiple herbivory above- and belowground. A previous study examined whether the presence of the leaf herbivore Pieris brassicae on turnip plants (Brassica rapa subsp. rapa) influences the response of Trybliographa rapae, a specialist parasitoid of the root feeder Delia radicum. It showed that the parasitoid was not attracted by volatiles emitted by plants under simultaneous attack. Here, we analyzed differences in the herbivore induced plant volatile (HIPV) mixtures that emanate from such infested plants by using Orthogonal Partial Least Squares-Discriminant Analysis (OPLS-DA). This multivariate model focuses on the differences between odor blends, and highlights the relative importance of each compound in an HIPV blend. Dual infestation resulted in several HIPVs that were present in both isolated infestation types. However, HIPVs collected from simultaneously infested plants were not the simple combination of volatiles from isolated forms of above- and belowground herbivory. Only a few specific compounds characterized the odor blend of each type of damaged plant. Indeed, some compounds were specifically induced by root herbivory (4-methyltridecane and salicylaldehyde) or shoot herbivory (methylsalicylate), whereas hexylacetate, a green leaf volatile, was specifically induced after dual herbivory. It remains to be determined whether or not these minor quantitative variations, within the background of more commonly induced odors, are involved in the reduced attraction of the root feeder’s parasitoid. The mechanisms involved in the specific modification of the odor blends emitted by dual infested turnip plants are discussed in the light of interferences between biosynthetic pathways linked to plant responses to shoot or root herbivory.     

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.     

Volatile Emissions Triggered by Multiple Herbivore Damage: Beet Armyworm and Whitefly Feeding on Cotton Plants

Plants are commonly attacked by more than one species of herbivore, potentially causing the induction of multiple, and possibly competing, plant defense systems. In the present paper, we determined the interaction between feeding by the phloem feeder silverleaf whitefly (SWF), Bemisia tabaci Gennadius (B-biotype = B. argentifolii Bellows and Perring), and the leaf-chewing beet armyworm (BAW), Spodoptera exigua Hübner, with regard to the induction of volatile compounds from cotton plants. Compared to undamaged control plants, infestation with SWF did not induce volatile emissions or affect the number and density of pigment glands that store volatile and nonvolatile terpenoid compounds, whereas infestation by BAW strongly induced plant volatile emission. When challenged by the two insect herbivores simultaneously, volatile emission was significantly less than for plants infested with only BAW. Our results suggest that tritrophic level interactions between cotton, BAW, and natural enemies of BAW, that are known to be mediated by plant volatile emissions, may be perturbed by simultaneous infestation by SWF. Possible mechanisms by which the presence of whiteflies may attenuate volatile emissions from caterpillar-damaged cotton plants are discussed.     

Relative importance of infochemicals from first and second trophic level in long-range host location by the larval parasitoidCotesia glomerata

Recently parasitoids were hypothesized to encounter a reliability-detectability problem relating to chemical stimuli from the first and second trophic level, when searching for hosts. The relative role of infochemicals originating from the host,Pieris brassicae (second trophic level), and its food plant, cabbage (first trophic level), have been investigated with respect to long-range host location by the larval parasitoidCotesia glomerata. Flight-chamber dual choice tests showed that uninfested cabbage plants are least attractive to female wasps. Host larvae and their feces were more attractive than clean plants but far less attractive than artificially damaged and herbivore-damaged plants. The plant-host complex, with host larvae actively feeding on the plant, was the most attractive odor source for the parasitoids. The data indicate that one of the solutionsC. glomerata uses to solve the reliability-detectability problem is to respond to infochemicals that are emitted from herbivore-damaged plants. Whether these infochemicals are herbivore-induced synomones that are produced by the plant remains to be demonstrated. Infochemicals emitted by the herbivore or its by-products are of little importance in the foraging behavior ofC. glomerata.