Recognition of aphid parasitoids by honeydew-collecting ants: The role of cuticular lipids in a chemical mimicry system

The aphidiid waspLysiphlebus cardui parasitizes in ant-attendedAphis fabae cirsiiacanthoidis colonies without causing aggressive behavior in the antLasius niger. By contrast,Trioxys angelicae, another aphidiid parasitoid of aphids, is rapidly recognized and vigorously attacked by the ants.L. niger workers also responded differently to dead individuals ofL. cardui andT. angelicae. DeadL. cardui parasitoids were often ignored when encountered byL. niger, whereas deadT. angelicae individuals were immediately grasped by ants that discovered them. However, hexane-washed parasitoids caused a similar reaction pattern in the ants, in that both aphidiid species were tolerated in the aphid colony. Lure experiments demonstrated that chemical stimuli on the cuticle are major cues for the ants to distinguish between the parasitoids. The hexane extract ofL. cardui transferred to washed individuals ofT. angelicae resulted in ant responses characteristic towardsL. cardui, andL. niger workers displayed the typical removal pattern they normally showed towardsT. angelicae whenT. angelicae extract was applied toL. cardui individuals. Both parasitoid species treated with the hexane extract ofA. fabae cirsiiacanthoidis were similarily treated by the ants as were aphid control individuals. The suggestion that the aphidiid waspL. cardui uses chemical mimicry is discussed.     

Attack Rate and Success of the Parasitoid Diaeretiella rapae on Specialist and Generalist Feeding Aphids

Lipaphis erysimi (Kaltenbach) is a specialist crucifer feeding aphid and Myzus persicae (Sulzer) is a generalist feeding aphid. The foraging behavior of Diaeretiella rapae (McIntosh), a parasitoid with the ability to parasitize both of these species, was assessed using a series of attack rate and success bioassays, with turnip, Brassica rapa var rapifera, as the host plant. The attack rate of D. rapae was significantly greater on L. erysimi than on M. persicae when aphids were feeding on turnip leaf discs in Petri dishes, irrespective of the aphid species upon which the parasitoids were originally reared. Attack rate bioassays with leaf discs absent, using both satiated and starved aphids, revealed that background chemistry and internal aphid chemistry may have small effects on attack rate. Excision of D. rapae pupae from mummy cases and subsequent use of the fully developed adults in attack rate bioassays showed that cues received by D. rapae at the time of adult emergence provide cues that prime D. rapae to attack L. erysimi at a greater rate than M. persicae. However, the relative success of D. rapae on these two aphid species, in terms of the percentage of attacks resulting in a successful adult parasitoid, was not significantly different.     

Caterpillar Footprints as Host Location Kairomones for <Emphasis Type="Italic">Cotesia marginiventris</Emphasis>: Persistence and Chemical Nature

Herbivores walking over the epicuticular wax layer of a plant may leave tracks that disclose their presence to hunting predators or parasitoids. The braconid wasp Cotesia marginiventris is a solitary parasitoid of young noctuid caterpillars. It can locate potential hosts from a distance by orienting toward the scent of herbivore-damaged plants. Upon landing on the caterpillars’ food plant, the female parasitoid searches for further cues (kairomones) that confirm the presence of a suitable host. In a previous study, we showed that C. marginiventris recognizes the chemical footprints of absent Spodoptera frugiperda caterpillars on a leaf. Here, we report on the persistence and chemical nature of this host location kairomone. In a series of behavioral assays, we confirmed that caterpillars of S. frugiperda leave chemical tracks that elicit characteristic antennation behavior in C. marginiventris for up to 2 days. Both hexane extracts of caterpillar footprints and of the larvae’s ventral cuticle induced antennation and contained almost identical long-chain hydrocarbons, thus suggesting the prolegs and claspers as the kairomones’ main source. A series of linear C₂₁ to C₃₂ alkanes accounted for ca 90% of all identified compounds. Female wasps showed significant antennation responses on leaves treated with a reconstructed blend of these n-alkanes. However, wasp responses were relatively weak. Therefore, we presume that minor compounds, such as monomethyl-branched alkanes, which were also found, may contribute additionally to host recognition.     

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.     

Role of cuticular hydrocarbons of aphid parasitoids in their relationship to aphid-attending ants

Lysiphlebus cardui, the dominant aphidiid parasitoid of the black bean aphid,Aphis fabae cirsiiacanthoidis (Afc), on creeping thistle, is able to forage in ant-attended aphid colonies without being attacked by ants. Several behavioral observations and experimental studies led to the hypothesis thatL. cardui mimics the cuticular hydrocarbon profile of its host aphid. Chemical analysis of the cuticular extracts revealed that bothL. cardui and Afc exclusively possess saturated hydrocarbons:n-alkanes, monomethyl (MMA), dimethyl (DMA), and trimethyl alkanes (TMA). Comparison of the hydrocarbon profiles of parasitoid and aphid showed great qualitative resemblance between parasitoid and host:L. cardui possesses almost all host-specific compounds in addition to species-specific hydrocarbons of mainly higher molecular weight (>C₃₀). However, there is a lesser quantitative correspondence between parasitoid and host aphid. Furthermore, we analyzed the cuticular hydrocarbon profile of another parasitoid of Afc,Trioxys angelicae. This aphidiid species is vigorously attacked and finally killed by honeydewcollecting ants when encountered in aphid colonies. Its cuticular hydrocarbon profile is characterized by the presence of large amounts of (Z)-11-alkenes of chain lenghts C₂₇, C₂₉, C₃₁, and C₃₃, in addition to alkanes and presumably trienes. The role of the unsaturated hydrocarbons onT. angelicae as recognition cues for aphid-attending ants is discussed.     

A Comparison of Semiochemically Mediated Interactions Involving Specialist and Generalist <Emphasis Type="Italic">Brassica</Emphasis>-feeding Aphids and the Braconid Parasitoid <Emphasis Type="Italic">Diaeretiella rapae</Emphasis>

Diaeretiella rapae, a parasitoid that predominately specializes in the parasitism of Brassica-feeding aphids, attacks Lipaphis erysimi, a specialist feeding aphid of the Brassicaceae and other families in the Capparales, at a greater rate than the generalist-feeding aphid, Myzus persicae. In this study, we investigated the orientation behavior of D. rapae to the volatile chemicals produced when these two aphid species feed on turnip (Brassica rapa var rapifera). We showed no significant preference orientation behavior to either aphid/turnip complex over the other. Isothiocyanates are among the compounds emitted by plants of the Brassicaceae in response to insect feeding damage, including by aphids. We assessed parasitoid orientation behavior in response to laboratory-formulated isothiocyanates. We tested two formulations and discovered significant orientation toward 3-butenyl isothiocyanate. We also assessed plant and aphid glucosinolate content, and showed large levels of glucosinolate concentration in L. erysimi, whereas there was little change in plant content in response to aphid feeding. Our results suggest that during the process of host location, similar cues may be utilized for locating L. erysimi and M. persicae, whereas the acceptance of hosts and their suitability may involve aspects of nonvolatile aphid chemistry.     

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.

     

Mechanisms of behavioral alterations of parasitoids reared in artificial systems

A high quality of mass reared parasitoids is required for successful biological control of pest insects. Although the phenomenon of behavioral deterioration of parasitoids due to rearing in artificial conditions is well known, its significance is often underestimated, and the underlying mechanisms are poorly investigated. We quantified behavioral alterations of parasitoids reared in an artificial system vs. a natural system and elucidated some of the mechanisms involved. The model systems consisted of apple fruits (natural system) or an artificial diet devoid of apple (artificial system), the herbivore Cydia pomonella, and its larval parasitoid Hyssopus pallidus, a candidate biological control agent. Two parasitoid strains, one reared for 30 generations in the natural system and one in the artificial system, were compared by using the females' ability to respond to frass from codling moth caterpillars fed on apple fruits (apple-frass). The searching response of parasitoids reared in the artificial system compared to those reared in the natural system was reduced by an average of 53.2%. Gas chromatography–mass spectrometry (GC-MS) analyses of the two types of caterpillars' food and of the two corresponding types of frass showed that 15 compounds were present only in apple fruits and apple-frass, three compounds only in artificial diet and artificial-diet-frass, while four compounds were present in both frass types but not in the food sources. This suggests the presence of a food-derived and a host-derived component in the frass. Results from both bioassays and chemical analyses indicate that the kairomonal activity of the frass is due to both apple fruit and host components. The reduced response of parasitoids reared in artificial conditions might, therefore, be due to a lack of recognition of the apple fruit component. In a further experiment, the two parasitoid strains were reared in the opposite system for one generation. While the response to the host frass was significantly reduced in parasitoids that emerged from the artificial system, it was fully restored in parasitoids that emerged from the natural system. This indicates that the behavioral alteration was related to a learning process during ontogenesis rather than to a selection exhibited over generations.     

Host Sex Discrimination by an Egg Parasitoid on Brassica Leaves

Egg parasitoids are able to find their hosts by exploiting their chemical footprints as host location cues. In nature, the apolar epicuticular wax layer of plants that consists of several classes of hydrocarbons serves as the substrate that retains these contact kairomones. However, experiments on chemical footprints generally have used filter paper as substrate to study insect behavior. Here, we explored the ability of Trissolcus basalis (Scelionidae) females to discriminate between footprint cues left by male and female Nezara viridula (Pentatomidae) on leaves of their host plant Brassica oleracea (broccoli). Furthermore, we analyzed the chemical composition of the outermost wax layer of broccoli leaves to evaluate the degree of overlap in insect and plant cuticular hydrocarbons that could lead to masking effects in the detection of footprint cues. Our results showed that B. oleracea epicuticular wax retains the chemical footprints of adult bugs and allows T. basalis females to differentiate hosts of different sex. Traces of female bugs elicited more extensive searching behavior in egg parasitoids than traces of males. The application of n-nonadecane, a compound specific to male N. viridula, on the tarsi of female bugs prevented parasitoid females from distinguishing between host male and host female footprints. Analyses of B. oleracea leaves revealed that epicuticular waxes were mainly composed of linear alkanes, ketones, and secondary alcohols. Alkanes were dominated by n-nonacosane (nC29) and n-hentriacontane (nC31), while male-specific n-nonadecane (nC19) was absent. The ecological significance of these results for parasitoid host location behavior is discussed.     

Herbivore-Mediated Effects of Glucosinolates on Different Natural Enemies of a Specialist Aphid

The cabbage aphid Brevicoryne brassicae is a specialist herbivore that sequesters glucosinolates from its host plant as a defense against its predators. It is unknown to what extent parasitoids are affected by this sequestration. We investigated herbivore-mediated effects of glucosinolates on the parasitoid wasp Diaeretiella rapae and the predator Episyrphus balteatus. We reared B. brassicae on three ecotypes of Arabidopsis thaliana that differ in glucosinolate content and on one genetically transformed line with modified concentrations of aliphatic glucosinolates. We tested aphid performance and the performance and behavior of both natural enemies. We correlated this with phloem and aphid glucosinolate concentrations and emission of volatiles. Brevicoryne brassicae performance correlated positively with concentrations of both aliphatic and indole glucosinolates in the phloem. Aphids selectively sequestered glucosinolates. Glucosinolate concentration in B. brassicae correlated negatively with performance of the predator, but positively with performance of the parasitoid, possibly because the aphids with the highest glucosinolate concentrations had a higher body weight. Both natural enemies showed a positive performance-preference correlation. The predator preferred the ecotype with the lowest emission of volatile glucosinolate breakdown products in each test combination, whereas the parasitoid wasp preferred the A. thaliana ecotype with the highest emission of these volatiles. The study shows that there are differential herbivore-mediated effects of glucosinolates on a predator and a parasitoid of a specialist aphid that selectively sequesters glucosinolates from its host plant.     

Semiochemicals for use with parasitoids: Status and future

Allelochemicals are known to serve important roles at all steps in the host-searching sequence of parasitoids. We discuss the various roles of these allelochemics and the type of information needed to develop their use in pest control, which to date has been very limited. Rapid advancements are being made with respect to airborne chemicals and longer-range foraging behavior. Moreover, recent discoveries have shown that genetic diversity in parasitoid populations and phenotypic plasticity of individuals, together with their physiological state, often result in substantial variations in the response to chemical cues. Successful application of semiochemical-parasitoid systems will require management of these intrinsic parasitoid variables as well as management of the foraging environment. We illustrate emerging technology for such an application. For the immediate future, the development of this technology will allow us to: (1) define the genetic and phenotypic foraging profiles important to consistent and efficient parasitoid foraging, and (2) establish the proper propagation and release procedures and monitoring bioassays necessary to ensure appropriate behavioral and physiological qualities of released organisms. For the long term, we envision technology for comprehensively manipulating the pest/crop environment in ways that would provide foraging stimuli and other needs important to retention and efficiency of parasitoids.     

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.     

Comparative Innate Responses of the Aphid Parasitoid <Emphasis Type="Italic">Diaeretiella rapae</Emphasis> to Alkenyl Glucosinolate Derived Isothiocyanates,Nitriles, and Epithionitriles

Cruciferous plants (Brassicaceae) are characterized by the accumulation of a group of secondary metabolites known as glucosinolates that, following attack by pathogens or herbivores, may be hydrolyzed to one of a number of products including isothiocyanates and nitriles. Despite the range of hydrolysis products that may be produced, the toxicity of glucosinolates to pathogens and herbivores may be explained largely by the production of isothiocyanates. Isothiocyanates are also known to provide an indirect defense by acting as host finding cues for parasitoids of insect herbivores that attack crucifers. It has been speculated that nitriles may provide a similar indirect defense. Here, we investigate the olfactory perception and orientation behavior of the aphid parasitoid Diaeretiella rapae, to a range of alkenylglucosinolate hydrolysis products, including isothiocyanates, nitriles, and epithionitriles. Electroantennogram responses indicated peripheral odor perception in D. rapae females to all 3-butenylglucosinolate hydrolysis products tested. By contrast, of the 2-propenylglucosinolate hydrolysis products tested, only the isothiocyanate elicited significant responses. Despite showing peripheral olfactory detection of a range of 3-butenylglucosinolate hydrolysis products, naïve females oriented only to the isothiocyanate. Similarly, parasitoids oriented to 3-isothiocyanatoprop-1-ene, but not to the corresponding nitrile or epithionitrile. However, by rearing D. rapae either on Brassica nigra, characterized by the accumulation of 2-propenylglucosinolate, or Brassica rapa var rapifera, characterized by the accumulation of 3-butenylglucosinolate, altered the innate response of parasitoids to 3-isothiocyanatoprop-1-ene and 4-isothiocyanatobut-1-ene. These results are discussed in relation to the defensive roles of glucosinolate hydrolysis products and the influence of the host plant on aphid parasitoid behavior.     

Response to walnut olfactory and visual cues by the parasitic wasp Diachasmimorpha juglandis

Diachasmimorpha juglandis is a specialist parasitoid attacking fly larvae in the genus Rhagoletis that feed exclusively on walnut fruit husks. In a free-foraging assay comparing response to uninfested, infested, and mechanically damaged fruits, we first determined that D. juglandis use host feeding damage on the fruit as a cue for host presence. In another free-foraging assay that used artificial walnut models and wind tunnel experiments, D. juglandis distinguished infested from uninfested fruits by using either olfactory or visual cues separately. However, the response rate of wasps in the wind tunnel was raised considerably when visual cues were also available. We analyzed the volatile compounds emitted by cohorts of uninfested, mechanically damaged, and infested fruits 1, 3, 5, 8, and 10 days after oviposition by flies into the infested fruits. Total volatile emissions did not differ significantly among treatments, but quantitative changes in volatiles distinguished infested fruits from uninfested and damaged fruits. The fact that parasitoids did not distinguish between infested and damaged fruits in assays where damage was visible indicates that they rely on visual cues when those are available.     

The Role of Honeydew in Host Searching of Aphid Hyperparasitoids

Foraging in many insect parasitoids is mediated by chemicals associated with hosts. For example, honeydew, the feces of feeding aphids, induces and/or prolongs searching behavior of aphid parasitoids. In the laboratory, we tested if aphid hyperparasitoids, which belong to a higher trophic level, also rely on aphid honeydew to locate their hosts. We used the potato aphid. Macrosiphum euphorbiae, the primary parasitoid, Aphidius nigripes, and four hyperparasitoids, Asaphes suspensus, Dendrocerus carpenteri. Alloxysta victrix, and Syrphophagus aphidivorus that possess different biological attributes and host ranges. We determined if foraging hyperparasitoid females could discriminate between (i) honeydew from a host and a non-aphid host (the potato aphid and the soft brown scale, Coccus hesperidum), and (ii) honeydew from healthy aphids and those parasitized by A. nigripes. Females of A. suspensus did not react to any of the honeydew treatments. While the presence of non-aphid honeydew did not modify the behavior of A. victrix, D. carpenteri, and S. aphidivorus females, they exhibited an increase in searching time and path length but not walking speed when in the presence of honeydew from aphids. However, there were no changes in host searching behaviors, such as antennation or ovipositor probing that have been reported for primary aphid parasitoids. There was no difference in the response of hyperparasitoid females to honeydew from healthy and parasitized aphids. These results indicate that hyperparasitoids may use aphid honeydew, a conspicuous cue from the second trophic level, as an infochemical to locate their hosts.     

Chemical cues from Murgantia histrionica eliciting host location and recognition in the egg parasitoid Trissolcus brochymenae

Host location and recognition by the egg parasitoid Trissolcus brochymenae were analyzed in terms of response to kairomones from several stages of its host, Murgantia histrionica. In a Y-tube olfactometer, parasitoid females responded by increasing residence time and/or reducing linear speed to chemical cues from gravid females, virgin females and males, fifth and third instars, and eggs. In an open arena, T. brochymenae females also responded to patches contaminated by chemicals from the host in the same stages, sexes, and/or physiological conditions as those tested in the olfactometer. The parasitoid displayed arrestment behavior, increased residence time, changed walking pattern, and intense substrate examination. When host egg clusters or glass dummies with a chemical egg extract were placed on the host-contaminated open arena, these elicited an orientation response in the parasitoid. In addition, the chemical egg extract without dummies elicited the same response, whereas dummies without extract did not influence parasitoid behavior. In a closed arena, the parasitoid females recognized and attempted to probe glass beads treated with chemical extracts of host eggs. There were no significant differences compared with their response to the host eggs, and they did not respond to untreated beads. Host recognition was elicited by chemicals from the follicular secretion used by the host to glue the eggs on the substrate. These results are discussed in relation to the level of the host selection sequence influenced by these cues.     

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.     

Specific foraging kairomones used by a generalist parasitoid

In general, it is assumed that generalist natural enemies do not innately use specific cues for the location of their host or prey species. This hypothesis was tested using naïve females of the generalist parasitoid Lariophagus distinguendus Förster and two of its hosts, larvae of the lesser grain borer Rhyzopertha dominica (F.) and of the granary weevil Sitophilus granarius L., feeding in wheat grains. In a four-chamber olfactometer, female parasitoids were attracted to volatiles emanating from the feces of both host species. Chemical analysis of the volatiles from the feces of R. dominica revealed the presence of dominicalure 1 and 2, the species specific aggregation pheromones of R. dominica. The main compounds in the volatiles from feces of S. granarius were identified as chemicals related to mites that are associated with hosts of L. distinguendus. Because these mites are not specific for S. granarius but also co-occur with other hosts, the mite chemicals have to be considered as general cues. In bioassays, synthetic dominicalure was attractive to naïve L. distinguendus, explaining the attraction of feces volatiles from R. dominica. Synthetic mite chemicals and sitophilate, the aggregation pheromone of S. granarius, had no effect on naïve parasitoids. It remains to be determined which innate chemical cues from feces of S. granarius are used by L. distinguendus. In contrast to our initial hypothesis, the generalist L. distinguendus is innately using specific cues for foraging. Two ideas are provided to explain this result.     

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.     

Body Odors of Parasitized Caterpillars Give Away the Presence of Parasitoid Larvae to Their Primary Hyperparasitoid Enemies

Foraging success of parasitoids depends on the utilization of reliable information on the presence of their often, inconspicuous hosts. These parasitic wasps use herbivore-induced plant volatiles (HIPVs) that provide reliable cues on host presence. However, host searching of hyperparasitoids, a group of parasitoids that parasitize the larvae and pupae of other parasitoids, is more constrained. Their hosts do not feed on plants, and often are even concealed inside the body of the herbivore host. Hyperparasitoids recently have been found to use HIPVs of plants damaged by herbivore hosts in which the parasitoid larvae develop. However, hyperparasitoids that search for these parasitoid larvae may be confronted with healthy and parasitized caterpillars on the same plant, further complicating their host location. In this study, we addressed whether the primary hyperparasitoid Baryscapus galactopus uses caterpillar body odors to discriminate between unparasitized herbivores and herbivores carrying larvae of parasitoid hosts. We show that the hyperparasitoids made faster first contact and spent a longer mounting time with parasitized caterpillars. Moreover, although the three parasitoid hosts conferred different fitness values for the development of B. galactopus, the hyperparasitoids showed similar behavioral responses to caterpillar hosts carrying different primary parasitoid hosts. In addition, a two-chamber olfactometer assay revealed that volatiles emitted by parasitized caterpillars were more attractive to the hyperparasitoids than those emitted by unparasitized caterpillars. Analysis of volatiles revealed that body odors of parasitized caterpillars differ from unparasitized caterpillars, allowing the hyperparasitoids to detect their parasitoid host.