Cotesia Glomerata Research Articles

Associative learning of host presence in non‐host environments influences parasitoid foraging

1. Parasitoids are known to utilise learning of herbivore‐induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non‐suitable herbivores (non‐hosts). Simultaneous infestation of plants by hosts and non‐hosts has been found to result in induction of HIPVs that differ from host‐infested plants. Each non‐host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non‐host herbivore also contain the host.2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non‐hosts in the laboratory and in semi‐field experiments.3. In two‐choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant–host–non‐host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non‐host caterpillar Mamestra brassicae or the non‐host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non‐host caterpillars or aphids in a semi‐field situation.4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.

Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning

Invasive insect herbivores have the potential to interfere with native multitrophic interactions by affecting the chemical cues emitted by plants and disrupting the attraction of natural enemies mediated by herbivore-induced plant volatiles (HIPVs). In a previous study, we found that the presence of the exotic herbivore Spodoptera littoralis on Brassica rapa plants infested by the native herbivore Pieris brassicae makes these dually-infested plants unattractive to the main parasitoid of P. brassicae, the braconid wasp Cotesia glomerata. Here we show that this interference by S. littoralis is strongly dependent on the relative densities of the two herbivores. Parasitoids were only deterred by dually-infested plants when there were more S. littoralis larvae than P. brassicae larvae on a plant. Furthermore, the blend of HIPVs emitted by dually-infested plants differed the most from HIPVs emitted by Pieris-infested plants when S. littoralis density exceeded P. brassicae density. We further found that associative learning by the parasitoid affected its preferences: attraction to dually-infested plants increased after parasitoids were presented a P. brassicae caterpillar (rewarding experience) in presence of the odor of a dually-infested plant, but not when presented a S. littoralis caterpillar (non-rewarding experience). A non-rewarding experience prior to the bioassays resulted in a general decrease in parasitoid motivation to respond to plant odors. We conclude that herbivore density and associative learning may play an important role in the foraging behavior of natural enemies in communities, and such effects should not be overlooked when investigating the ecological impact of exotic species on native food webs.

The spitting image of plant defenses: Effects of plant secondary chemistry on the efficacy of caterpillar regurgitant as an anti-predator defense.

In the arms race between plants, herbivores, and their natural enemies, specialized herbivores may use plant defenses for their own benefit, and variation in plant traits may affect the benefits that herbivores derive from these defenses. Pieris brassicae is a specialist herbivore of plants containing glucosinolates, a specific class of defensive secondary metabolites. Caterpillars of P. brassicae are known to actively spit on attacking natural enemies, including their main parasitoid, the braconid wasp Cotesia glomerata. Here, we tested the hypothesis that variation in the secondary metabolites of host plants affects the efficacy of caterpillar regurgitant as an anti‐predator defense. Using a total of 10 host plants with different glucosinolate profiles, we first studied natural regurgitation events of caterpillars on parasitoids. We then studied manual applications of water or regurgitant on parasitoids during parasitization events. Results from natural regurgitation events revealed that parasitoids spent more time grooming after attack when foraging on radish and nasturtium than on Brassica spp., and when the regurgitant came in contact with the wings rather than any other body part. Results from manual applications of regurgitant showed that all parameters of parasitoid behavior (initial attack duration, attack interruption, grooming time, and likelihood of a second attack) were more affected when regurgitant was applied rather than water. The proportion of parasitoids re‐attacking a caterpillar within 15 min was the lowest when regurgitant originated from radish‐fed caterpillars. However, we found no correlation between glucosinolate content and regurgitant effects, and parasitoid behavior was equally affected when regurgitant originated from a glucosinolate‐deficient Arabidopsis thaliana mutant line. In conclusion, host plant affects to a certain extent the efficacy of spit from P. brassicae caterpillars as a defense against parasitoids, but this is not due to glucosinolate content. The nature of the defensive compounds present in the spit remains to be determined, and the ecological relevance of this anti‐predator defense needs to be further evaluated in the field.

Take-off mechanisms in parasitoid wasps.

High-speed video analyses of the natural behaviour of parasitoid wasps revealed three strategies used to launch the insects into the air. Which strategy is the most energy efficient? In Pteromalus puparum, 92% of take-offs by were propelled entirely by movements of the middle and hind legs, which were depressed at their coxo-trochanteral and extended at their femoro-tibial joints. The front legs left the ground first, followed by the hind legs, so that the middle legs provided the final propulsion. Second, in other species of a similar mass, Cotesia glomerata and Leptopilina boulardi, all take-offs were propelled by a mean of 2.8 and 3.8wingbeats, respectively, with little or no contribution from the legs. The first strategy resulted in take-off times that were four times shorter (5 versus 22.8 ms) and take-off velocities that were four times faster (0.8 versus 0.2 m s-1). Calculations from the kinematics indicate that propulsion by the legs was the most energy-efficient strategy, because more energy is put into propulsion of the body, whereas in take-off propelled by repetitive wing movements energy is lost to generating these movements and moving the air. In heavier species such as Netelia testacea and Amblyteles armatorius, take-off was propelled by the combined movements of the middle and hind legs and wingbeats. In A. armatorius, this resulted in the longest mean take-off time of 33.8 ms but an intermediate take-off velocity of 0.4 m s-1 In all three strategies the performance could be explained without invoking energy storage and power amplification mechanisms.

Eco-toxicological risk and impact of pesticides on important parasitoids of cabbage butterflies in cruciferous ecosystem

Eco-toxicological risk and impact of pesticides was estimated on three important parasitoids of butterflies viz., Hyposoter ebeninus, Cotesia glomerata and Pteromalus puparum. Four commonly used pesticides were evaluated using standard protocol (of IOBC/WPRS-group). In laboratory tests, the survival of the female wasps decreased significantly on fresh contact and ingestion of deltamethrin, spinosad and azadirachtin; whereas Bacillus thuringiensis var kurstaki (Btk) was found harmless pesticide. Under semi-field conditions, parasitoid mortality decreased significantly on fresh contact with the pesticides. Although, at 72 h after treatment, spinosad and deltamethrin were found harmful (Class-IV) and azadirachtin was moderately harmful (Class-III), whereas Btk was harmless (Class-I). Furthermore, 15-day-old residues of pesticides (except deltamethrin) were harmless to all parasitoid species under semi-field conditions. Notably, adult emergence and pupal duration in pesticide-treated cocoons were not significantly affected; however, their survival decreased after emergence except in Btk. The contact and oral toxicity trends of the pesticides were almost similar for three species of parasitoid females and pupae; however little variability was observed in toxicity to the host caterpillars parasitized by H. ebeninus (HCPHE) and C. glomerata (HCPCG). In semi-field tests, fresh residues of all the pesticides were harmful to HCPHE and HCPCG. However, action of Btk was slightly delayed and toxicity was rather low for HCPCG. In 15-day-old residues, deltamethrin and azadirachtin were slightly harmful to the parasitized caterpillars, whereas those of Btk and spinosad were harmless. Since, Btk appeared to be safe for parasitoids; it could be used for managing cabbage butterflies in brassicaceous crops.

Combined use of herbivore‐induced plant volatiles and sex pheromones for mate location in braconid parasitoids

Herbivore-induced plant volatiles (HIPVs) are important cues for female parasitic wasps to find hosts. Here, we investigated the possibility that HIPVs may also serve parasitoids as cues to locate mates. To test this, the odour preferences of four braconid wasps - the gregarious parasitoid Cotesia glomerata (L.) and the solitary parasitoids Cotesia marginiventris (Cresson), Microplitis rufiventris Kokujev and Microplitis mediator (Haliday) - were studied in olfactometers. Each species showed attraction to pheromones but in somewhat different ways. Males of the two Cotesia species were attracted to virgin females, whereas females of M. rufiventris were attracted to virgin males. Male and female M. mediator exhibited attraction to both sexes. Importantly, female and male wasps of all four species were strongly attracted by HIPVs, independent of mating status. In most cases, male wasps were also attracted to intact plants. The wasps preferred the combination of HIPVs and pheromones over plant odours alone, except M. mediator, which appears to mainly use HIPVs for mate location. We discuss the ecological contexts in which the combined use of pheromones and HIPVs by parasitoids can be expected. To our knowledge, this is the first study to show that braconid parasitoids use HIPVs and pheromones in combination to locate mates.

Herbivore species identity rather than diversity of the non‐host community determines foraging behaviour of the parasitoid wasp C otesia glomerata

Extensive research has been conducted to reveal how species diversity affects ecosystem functions and services. Yet, consequences of diversity loss for ecosystems as a whole as well as for single community members are still difficult to predict. Arthropod communities typically are species-rich, and their species interactions, such as those between herbivores and their predators or parasitoids, may be particularly sensitive to changes in community composition. Parasitoids forage for herbivorous hosts by using herbivore-induced plant volatiles (indirect cues) and cues produced by their host (direct cues). However, in addition to hosts, non-suitable herbivores are present in a parasitoid's environment which may complicate the foraging process for the parasitoid. Therefore, ecosystem changes in the diversity of herbivores may affect the foraging efficiency of parasitoids. The effect of herbivore diversity may be mediated by either species numbers per se, by specific species traits, or by both. To investigate how diversity and identity of non-host herbivores influence the behaviour of parasitoids, we created environments with different levels of non-host diversity. On individual plants in these environments, we complemented host herbivores with 1–4 non-host herbivore species. We subsequently studied the behaviour of the gregarious endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) while foraging for its gregarious host Pieris brassicae L. (Lepidoptera: Pieridae). Neither non-host species diversity nor non-host identity influenced the preference of the parasitoid for herbivore-infested plants. However, after landing on the plant, non-host species identity did affect parasitoid behaviour, whereas non-host diversity did not. One of the non-host species, Trichoplusia ni Hubner (Lepidoptera: Noctuidae), reduced the time the parasitoid spent on the plant as well as the number of hosts it parasitized. We conclude that non-host herbivore species identity has a larger influence on C. glomerata foraging behaviour than non-host species diversity. Our study shows the importance of species identity over species diversity in a multitrophic interaction of plants, herbivores, and parasitoids.

Integrating Insect Life History and Food Plant Phenology: Flexible Maternal Choice Is Adaptive.

Experience of insect herbivores and their natural enemies in the natal habitat is considered to affect their likelihood of accepting a similar habitat or plant/host during dispersal. Growing phenology of food plants and the number of generations in the insects further determines lability of insect behavioural responses at eclosion. We studied the effect of rearing history on oviposition preference in a multivoltine herbivore (Pieris brassicae), and foraging behaviour in the endoparasitoid wasp (Cotesia glomerata) a specialist enemy of P. brassicae. Different generations of the insects are obligatorily associated with different plants in the Brassicaceae, e.g., Brassica rapa, Brassica nigra and Sinapis arvensis, exhibiting different seasonal phenologies in The Netherlands. Food plant preference of adults was examined when the insects had been reared on each of the three plant species for one generation. Rearing history only marginally affected oviposition preference of P. brassicae butterflies, but they never preferred the plant on which they had been reared. C. glomerata had a clear preference for host-infested B. rapa plants, irrespective of rearing history. Higher levels of the glucosinolate breakdown product 3-butenyl isothiocyanate in the headspace of B. rapa plants could explain enhanced attractiveness. Our results reveal the potential importance of flexible plant choice for female multivoltine insects in nature.

Feeding guild of non-host community members affects host-foraging efficiency of a parasitic wasp.

Interactions between predator and prey, or parasitoid and host, are shaped by trait- and density-mediated processes involving other community members. Parasitoids that lay their eggs in herbivorous insects locate their hosts through infochemicals such as herbivore-induced plant volatiles (HIPVs) and host-produced kairomones. Hosts are frequently accompanied by non-host herbivores that are unsuitable for the parasitoid. These non-hosts may interfere with host location primarily through trait-mediated processes, by their own infochemicals, and their induction of the emission of plant volatiles. Although it is known that single non-hosts can interfere with parasitoid host location, it is still unknown whether the observed effects are due to species specific characteristics or to the feeding habits of the non-host herbivores. Here we addressed whether the feeding guild of non-host herbivores differentially affects foraging of the parasitoid Cotesia glomerata for its common host, caterpillars of Pieris brassicae feeding on Brassica oleracea plants. We used different phloem-feeding and leaf-chewing non-hosts to study their effects on host location by the parasitoid when searching for host-infested plants based on HIPVs and when searching for hosts on the plant using infochemicals. To evaluate the ultimate effect of these two phases in host location, we studied parasitism efficiency of parasitoids in small plant communities under field-tent conditions. We show that leaf-chewing non-hosts primarily affected host location through trait-mediated effects via plant volatiles, whereas phloem-feeding non-hosts exerted trait-mediated effects by affecting foraging efficiency of the parasitoid on the plant. These trait-mediated effects resulted in associational susceptibility of hosts in environments with phloem feeders and associational resistance in environments with non-host leaf chewers.

Density‐mediated indirect interactions alter host foraging behaviour of parasitoids without altering foraging efficiency

1. Foraging decisions of parasitoids are influenced by host density via density-mediated indirect interactions. However, in the parasitoid's environment, non-suitable herbivores are also present. These non-hosts also occur in different densities, which can affect a parasitoid's foraging behaviour. 2. The influence of non-host densities can be expressed during the first phase of the foraging process, when parasitoids use plant volatiles to locate plants infested by their host. They may also play a role during the second phase, when parasitoids use infochemicals from the host and plant to locate, recognise and accept the host. 3. By using laboratory and field setups, it was studied whether the density of non-host herbivores influences these two phases of the foraging behaviour of the parasitoid Cotesia glomerata as well as the parasitoid's efficiency to find its host, Pieris brassicae caterpillars. 4. The findings show that a high non-host density, regardless of the species used, negatively affected parasitoid preference for host-infested plants, but that the behaviour on the plant and the total host-finding efficiency of the parasitoids were not influenced by non-host density. 5. These results are discussed in the context of density-mediated indirect interactions.

Development of a solitary koinobiont hyperparasitoid in different instars of its primary and secondary hosts

Parasitoid wasps are excellent organisms for studying the allocation of host resources to different fitness functions such as adult body mass and development time. Koinobiont parasitoids attack hosts that continue feeding and growing during parasitism, whereas idiobiont parasitoids attack non-growing host stages or paralyzed hosts. Many adult female koinobionts attack a broad range of host stages and are therefore faced with a different set of dynamic challenges compared with idiobionts, where host resources are largely static. Thus far studies on solitary koinobionts have been almost exclusively based on primary parasitoids, yet it is known that many of these are in turn attacked by both koinobiont and idiobiont hyperparasitoids. Here we compare parasitism and development of a primary koinobiont hyperparasitoid, Mesochorus gemellus (Hymenoptera: Ichneumonidae) in larvae of the gregarious primary koinobiont parasitoid, Cotesia glomerata (Hymenoptera: Braconidae) developing in the secondary herbivore host, Pieris brassicae (Lepidoptera: Pieridae). As far as we know this is the first study to examine development of a solitary primary hyperparasitoid in different stages of its secondary herbivore host. Pieris brassicae caterpillars were parasitized as L1 by C. glomerata and then these parasitized caterpillars were presented in separate cohorts to M. gemellus as L3, L4 or L5 instar P. brassicae. Different instars of the secondary hosts were used as proxies for different developmental stages of the primary host, C. glomerata. Larvae of C. glomerata in L5 P. brassicae were significantly longer than those in L3 and L4 caterpillars. Irrespective of secondary host instar, every parasitoid cluster was hyperparasitized by M. gemellus but all only produced male progeny. Male development time decreased with host stage attacked, whereas adult male body mass did not, which shows that M. gemellus is able to optimally exploit older host larvae in terms of adult size despite their decreasing mass during the pupal stage. Across a range of cocoon masses, hyperparasitoid adult male body mass was approximately 84% as large as primary parasitoids, revealing that M. gemellus is almost as efficient at exploiting host resources as secondary (pupal) hyperparasitoids.

Powdery mildew suppresses herbivore-induced plant volatiles and interferes with parasitoid attraction in Brassica rapa.

The co-occurrence of different antagonists on a plant can greatly affect infochemicals with ecological consequences for higher trophic levels. Here we investigated how the presence of a plant pathogen, the powdery mildew Erysiphe cruciferarum, on Brassica rapa affects (1) plant volatiles emitted in response to damage by a specialist herbivore, Pieris brassicae; (2) the attraction of the parasitic wasp Cotesia glomerata and (3) the performance of P. brassicae and C. glomerata. Plant volatiles were significantly induced by herbivory in both healthy and mildew-infected plants, but were quantitatively 41% lower for mildew-infected plants compared to healthy plants. Parasitoids strongly preferred Pieris-infested plants to dually-infested (Pieris + mildew) plants, and preferred dually infested plants over only mildew-infected plants. The performance of P. brassicae was unaffected by powdery mildew, but C. glomerata cocoon mass was reduced when parasitized caterpillars developed on mildew-infected plants. Thus, avoidance of mildew-infested plants may be adaptive for C. glomerata parasitoids, whereas P. brassicae caterpillars may suffer less parasitism on mildew-infected plants in nature. From a pest management standpoint, the concurrent presence of multiple plant antagonists can affect the efficiency of specific natural enemies, which may in turn have a negative impact on the regulation of pest populations.

Elevated Ozone Modulates Herbivore-Induced Volatile Emissions of Brassica nigra and Alters a Tritrophic Interaction.

Plants damaged by herbivores emit volatile organic compounds (VOCs) that are used by parasitoids for host location. In nature, however, plants are exposed to multiple abiotic and biotic stresses of varying intensities, which may affect tritrophic interactions. Here, we studied the effects of ozone exposure and feeding by Pieris brassicae larvae on the VOCs emitted by Brassica nigra and the effects on oriented flight of the parasitoid Cotesia glomerata. We also investigated the oriented flight of C. glomerata in a wind-tunnel with elevated ozone levels. Herbivore-feeding induced the emission of several VOCs, while ozone alone had no significant effect. However, exposure to 120ppb ozone, followed by 24hr of herbivore-feeding, induced higher emissions of all VOCs as compared to herbivore-feeding alone. In accordance, herbivore-damaged plants elicited more oriented flights than undamaged plants, whereas plants exposed to 120ppb ozone and 24hr of herbivore-feeding elicited more oriented flights than plants subjected to herbivore-feeding alone. Ozone enrichment of the wind-tunnel air appeared to negatively affect orientation of parasitoids at 70ppb, but not at 120ppb. These results suggest that the combination of ozone and P. brassicae-feeding modulates VOC emissions, which significantly influence foraging efficiency of C. glomerata.

Plant Quantity Affects Development and Survival of a Gregarious Insect Herbivore and Its Endoparasitoid Wasp.

Virtually all studies of plant-herbivore-natural enemy interactions focus on plant quality as the major constraint on development and survival. However, for many gregarious feeding insect herbivores that feed on small or ephemeral plants, the quantity of resources is much more limiting, yet this area has received virtually no attention. Here, in both lab and semi-field experiments using tents containing variably sized clusters of food plants, we studied the effects of periodic food deprivation in a tri-trophic system where quantitative constraints are profoundly important on insect performance. The large cabbage white Pieris brassicae, is a specialist herbivore of relatively small wild brassicaceous plants that grow in variable densities, with black mustard (Brassica nigra) being one of the most important. Larvae of P. brassicae are in turn attacked by a specialist endoparasitoid wasp, Cotesia glomerata. Increasing the length of food deprivation of newly molted final instar caterpillars significantly decreased herbivore and parasitoid survival and biomass, but shortened their development time. Moreover, the ability of caterpillars to recover when provided with food again was correlated with the length of the food deprivation period. In outdoor tents with natural vegetation, we created conditions similar to those faced by P. brassicae in nature by manipulating plant density. Low densities of B. nigra lead to potential starvation of P. brassicae broods and their parasitoids, replicating nutritional conditions of the lab experiments. The ability of both unparasitized and parasitized caterpillars to find corner plants was similar but decreased with central plant density. Survival of both the herbivore and parasitoid increased with plant density and was higher for unparasitized than for parasitized caterpillars. Our results, in comparison with previous studies, reveal that quantitative constraints are far more important that qualitative constraints on the performance of gregarious insect herbivores and their gregarious parasitoids in nature.

The Gastropod Menace: Slugs on Brassica Plants Affect Caterpillar Survival through Consumption and Interference with Parasitoid Attraction.

Terrestrial molluscs and insect herbivores play a major role as plant consumers in a number of ecosystems, but their direct and indirect interactions have hardly been explored. The omnivorous nature of slugs makes them potential disrupters of predator-prey relationships, as a direct threat to small insects and through indirect, plant-mediated effects. Here, we examined the effects of the presence of two species of slugs, Arion rufus (native) and A. vulgaris (invasive) on the survivorship of young Pieris brassicae caterpillars when feeding on Brassica rapa plants, and on plant attractiveness to the main natural enemy of P. brassicae, the parasitoid Cotesia glomerata. In two separate predation experiments, caterpillar mortality was significantly higher on plants co-infested with A. rufus or A. vulgaris. Moreover, caterpillar mortality correlated positively with slug mass and leaf consumption by A. vulgaris. At the third trophic level, plants infested with slugs and plants co-infested with slugs and caterpillars were far less attractive to parasitoids than plants damaged by caterpillars only, independently of slug species. Chemical analyses confirmed that volatile emissions, which provide foraging cues for parasitoids, were strongly reduced in co-infested plants. Our study shows that the presence of slugs has the potential to affect insect populations, directly via consumptive effects, and indirectly via changes in plant volatiles that result in a reduced attraction of natural enemies. The fitness cost for P. brassicae imposed by increased mortality in presence of slugs may be counterbalanced by the benefit of escaping its parasitoids.

Oviposition preference of cabbage white butterflies in the framework of costs and benefits of interspecific herbivore associations.

When deciding where to oviposit, herbivorous insects consider: (i) the plant’s value as a food source, (ii) the risks of competing with con- and heterospecific herbivores, and (iii) the risks of parasitism and predation on the host plant. The presence of con- and/or heterospecific competitors would further affect the oviposition preference, because the preceding herbivores induce direct/indirect defences in plants against forthcoming herbivores, and thereby alter oviposition decisions. In previous studies, the abovementioned factors have not been studied in an integrative manner. We performed here a case study of this by assessing the oviposition preferences of a small white butterfly, Pieris rapae, for plants occupied by combinations of conspecific larvae, heterospecific larvae (Plutella xylostella), specialist parasitoids of Pi. rapae (Cotesia glomerata) and generalist predators (ants). We previously reported that the females showed equal preference for Pl. xylostella-infested and uninfested plants. Here, we showed that Pi. rapae females preferred uninfested plants to conspecific-infested ones, and Pl. xylostella-infested plants to Pi. rapae-infested ones. We discuss these oviposition preferences of Pi. rapae females in the framework of costs and benefits of interspecific herbivore associations from the above point of view.

Volatile-mediated foraging behaviour of three parasitoid species under conditions of dual insect herbivore attack

Infochemicals play an important role in structuring intra- and interspecific interactions. Many parasitoid wasp species rely on herbivory or oviposition-induced plant volatiles (HIPVs/OIPVs) to locate their herbivorous hosts, and must cope with variation in the volatile blends due to factors such as plant/host species, herbivore density or attack by several herbivores. However, little is known about how dual herbivory or changes in herbivore density affect multiple parasitoid species, each attacking a different herbivore, in the same system. In a natural system, we investigated the effect of dual attack on the ability of three parasitoid species to differentiate between volatiles induced by hosts and those induced by a combination of hosts and nonhosts. Black mustard, Brassica nigra, plants were infested with eggs or caterpillars of Pieris brassicae, alone or in combination with different densities of Brevicoryne brassicae aphids. We determined the ability of three different parasitoid species that parasitize either P. brassicae eggs (Trichogramma brassicae), caterpillars (Cotesia glomerata) or B. brassicae aphids (Diaeretiella rapae) to discriminate between the induced volatiles, and analysed the plant volatile blends. Dual infestation did not affect the parasitoid species equally and aphid infestation altered, in a density-dependent manner, the volatile-mediated foraging of all three parasitoid species. Chemical analyses of the volatile blends revealed nonlinear emission patterns in relation to aphid density in both plants attacked by aphids alone and in plants attacked by a combination of aphids and caterpillars. Simple correlations between behaviour and volatile emissions in pairwise comparisons suggest the importance of certain volatiles explaining attraction, whereas dose-response type analyses reveal that these simple correlation analyses provide an incomplete picture.

Differentially expressed genes linked to natural variation in long-term memory formation in Cotesia parasitic wasps.

Even though learning and memory are universal traits in the Animal Kingdom, closely related species reveal substantial variation in learning rate and memory dynamics. To determine the genetic background of this natural variation, we studied two congeneric parasitic wasp species, Cotesia glomerata and C. rubecula, which lay their eggs in caterpillars of the large and small cabbage white butterfly. A successful egg laying event serves as an unconditioned stimulus (US) in a classical conditioning paradigm, where plant odors become associated with the encounter of a suitable host caterpillar. Depending on the host species, the number of conditioning trials and the parasitic wasp species, three different types of transcription-dependent long-term memory (LTM) and one type of transcription-independent, anesthesia-resistant memory (ARM) can be distinguished. To identify transcripts underlying these differences in memory formation, we isolated mRNA from parasitic wasp heads at three different time points between induction and consolidation of each of the four memory types, and for each sample three biological replicates, where after strand-specific paired-end 100 bp deep sequencing. Transcriptomes were assembled de novo and differential expression was determined for each memory type and time point after conditioning, compared to unconditioned wasps. Most differentially expressed (DE) genes and antisense transcripts were only DE in one of the LTM types. Among the DE genes that were DE in two or more LTM types, were many protein kinases and phosphatases, small GTPases, receptors and ion channels. Some genes were DE in opposing directions between any of the LTM memory types and ARM, suggesting that ARM in Cotesia requires the transcription of genes inhibiting LTM or vice versa. We discuss our findings in the context of neuronal functioning, including RNA splicing and transport, epigenetic regulation, neurotransmitter/peptide synthesis and antisense transcription. In conclusion, these brain transcriptomes provide candidate genes that may be involved in the observed natural variation in LTM in closely related Cotesia parasitic wasp species.

Toxicity of Lavandula angustifolia oil constituents and spray formulations to insecticide‐susceptible and pyrethroid‐resistant Plutella xylostella and its endoparasitoid Cotesia glomerata

Plutella xylostella is one of the most serious insect pests of cruciferous crops. This study was conducted to determine the toxicity of 21 constituents from Lavandula angustifolia essential oil (LA-EO) and another 16 previously known LA-EO constituents and the toxicity of six experimental spray formulations containing the oil (1-6 g L(-1) sprays) to susceptible KS-PX and pyrethroid-resistant JJ-PX P. xylostella larvae, as well as to its endoparasitoid Cotesia glomerata adults. Linalool and linalool oxide (LC50 = 0.016 mg cm(-3) ) were the most toxic fumigant compounds and were 10.7-fold less toxic than dichlorvos to KS-PX larvae. Either residual or fumigant toxicity of these compounds was almost identical against larvae from either of the two strains. Against C. glomerata, dichlorvos (LC50 = 7 × 10(-6) mg cm(-3) ) was the most toxic insecticide. LA-EO was ∼1430 times less toxic than dichlorvos. The oil applied as 6 g L(-1) spray and emamectin benzoate 21.5 g L(-1) emulsifiable concentrate provided 100% mortality against larvae from either of the two strains. Reasonable P. xylostella control in greenhouses can be achieved by a spray formulation containing the 6 g L(-1) oil as potential contact-action fumigant. © 2015 Society of Chemical Industry.

Habitat complexity reduces parasitoid foraging efficiency, but does not prevent orientation towards learned host plant odours.

It is well known that many parasitic wasps use herbivore-induced plant odours (HIPVs) to locate their inconspicuous host insects, and are often able to distinguish between slight differences in plant odour composition. However, few studies have examined parasitoid foraging behaviour under (semi-)field conditions. In nature, food plants of parasitoid hosts are often embedded in non-host-plant assemblages that confer both structural and chemical complexity. By releasing both naïve and experienced Cotesia glomerata females in outdoor tents, we studied how natural vegetation surrounding Pieris brassicae-infested Sinapis arvensis and Barbarea vulgaris plants influences their foraging efficiency as well as their ability to specifically orient towards the HIPVs of the host plant species on which they previously had a positive oviposition experience. Natural background vegetation reduced the host-encounter rate of naïve C. glomerata females by 47 %. While associative learning of host plant HIPVs 1 day prior to foraging caused a 28 % increase in the overall foraging efficiency of C. glomerata, it did not reduce the negative influence of natural background vegetation. At the same time, however, females foraging in natural vegetation attacked more host patches on host-plant species on which they previously had a positive oviposition experience. We conclude that, even though the presence of natural vegetation reduces the foraging efficiency of C. glomerata, it does not prevent experienced female wasps from specifically orienting towards the host-plant species from which they had learned the HIPVs.