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Knowledge about the orientation mechanisms used by two important predaceous mirids (Macrolophus pygmaeus Rambour and Nesidiocoris tenuis (Reuter)) in finding their prey (whitefly Bemisia tabaci (Gennadius) and the tomato borer Tuta absoluta (Meyrick)) is limited. In a Y-tube olfactometer, we tested the behavioral responses of naïve and experienced predators to uninfested plants, herbivore-induced plant volatiles (HIPVs) from plants infested with T. absoluta and/or B. tabaci, the sex pheromone of T. absoluta, and volatiles produced by plants injured by the predators. Nesidiocoris tenuis responds to volatiles produced by uninfested plants only after experience with the plant, whereas naïve and experienced M. pygmaeus show positive chemotaxis. Both predators are attracted to volatiles from prey-infested plants, and we provide the first evidence that experience affects this response in M. pygmaeus. Infestation of the same plant by both prey species elicited similar responses by the two predators as plants infested by either herbivore singly. Neither predator responded to sex pheromones of T. absoluta. Macrolophus pygmaeus avoided plants injured by conspecifics, while N. tenuis females were attracted by such plants. The implications of these results for augmentative biological control are discussed.

Root herbivores can influence both the performance and the behaviour of parasitoids of aboveground insect herbivores through changes in aboveground plant quality and in the composition of the plant's odour blend. Here we show that root herbivory by Delia radicum larvae did not influence the innate preferences for plant odours of the two closely related parasitoid species Cotesia glomerata and C. rubecula, but did affect their learned preferences, and did so in an opposite direction. While C. glomerata learned to prefer the odour of plants with intact roots, C. rubecula learned to prefer the odour of root-infested plants. The learned preference of C. glomerata for the odour of plants with intact roots matches our previously published result of its better performance when developing in P. brassicae hosts feeding on this plant type. In contrast, the relatively stronger learned preference of C. rubecula for the odour of root-infested plants cannot be merely explained by its performance, as the results of our present study indicate that D. radicum root herbivory did not influence the performance of C. rubecula nor of its host P. rapae. Our results stress the importance of assessing the influence of root herbivores on both innate and learned responses of parasitoids to plant odours.

We studied the formation of protein synthesis-dependent long-term memory (LTM) in the parasitic wasp Nasonia vitripennis Walker (Hymenoptera: Pteromalidae), a parasitoid of fly pupae. Female wasps were trained in one of five different training procedures in the presence of hosts and the odour cinnamon. Six days later the reaction of the wasps towards the odour was tested in a static four-chamber olfactometer. When wasps were trained by a single drilling experience we could not find any reaction to cinnamon after 6 days. In contrast, when wasps were trained either via drilling plus host feeding, three drilling events (spaced training), 1 h training, or 24 h training including oviposition, they significantly preferred cinnamon 6 days later. Wasps which were injected the transcription inhibitor actinomycin D after a 1-h training to block protein synthesis showed normal memory retention up to 3 days, but did not react to cinnamon after 4 and 6 days. Control experiments showed no influence of actinomycin D on the natural behaviour and the general odour discrimination ability of N. vitripennis. This demonstrates that protein synthesis-dependent LTM has been formed. To our knowledge this is the first time that LTM formation after drilling plus host feeding but without oviposition is demonstrated in a parasitic wasp. These results were combined with additional findings about anaesthesia-sensitive memory, anaesthesia-resistant memory, and intermediate memory to develop a multiphase model of memory dynamics in N. vitripennis and to discuss ecological adaptations of memory formation in N. vitripennis and other parasitic wasp species.

Plants can accumulate and release defensive chemicals by activating various signaling pathways when they are damaged by herbivores or pathogens. The jasmonic acid pathway is activated after damage by chewing herbivores. Here we used jasmonic acid (JA) as an exogenous elicitor to induce feral cabbage plants. In this study, the effects of root JA (RJA) and shoot JA (SJA) induction on the foraging behavior of , a parasitoid of the large cabbage white butterfly , was investigated under semi-field conditions. In all combinations of differently induced plants (RJA, SJA and control plants), the percentages of shoot induced plants that were visited by at least one wasp were significantly higher than those of controls or root induced plants during 3 h of foraging. Consequently, parasitism rates of on shoot-JA induced plants were significantly higher than on plants induced with JA to the roots or control plants in all tests. However, this behavioral preference was not reflected in the allocation of offspring. The clutch sizes of eggs on control, root induced and shoot induced plants were not significantly different from each other in two-choice or three-choice experiments, but did differ with clutch size in the two-choice experiment of uninduced control plants versus SJA. This semi-field study helps to further understand the choice behavior and preferences of parasitoids in natural multitrophic communities in which plants induced with root or shoot herbivores occur together.

Parasitic wasps employ a wide range of chemical cues to find their hosts. Very recently, we discovered how 2 closely related egg parasitoids, Trichogramma brassicae and Trichogramma evanescens, exploit the anti-aphrodisiac pheromone benzyl cyanide of one of their hosts, the gregarious large cabbage white butterfly Pieris brassicae that deposits a clutch of more than 20 eggs per oviposition bout. The pheromone is transferred by male butterflies to females during mating to enforce female monogamy. On detecting the anti-aphrodisiac, the tiny parasitic wasps ride on a mated female butterfly to a host plant and then parasitize her freshly laid eggs. The present study demonstrates that both wasp species similarly exploit the anti-aphrodisiac mixture of methyl salicylate and indole of another host, the more common solitary small cabbage white butterfly Pieris rapae that deposits only one egg at a time. Interestingly, this behavior is innate in T. brassicae, whereas T. evanescens learns it after one successful ride on a mated female butterfly. Moreover, we show that the wasps only respond to the anti-aphrodisiacs of the 2 cabbage white butterflies when the ubiquitous compounds are part of a complete mated female odor blend. Obviously, parasitic wasps use the sophisticated espionage-and-ride strategy to find eggs of different gregarious and solitary host species. From the wasps' perspective there seems to be a trade-off between the abundance and egg-laying behavior of the butterflies. Our findings suggest that Pieris butterflies are under strong selective pressure to minimize the use of an anti-aphrodisiac. Copyright 2010, Oxford University Press.

Summary 1Plant species employ several direct and indirect defence strategies to protect themselves against insect herbivores. Most studies, however, have focused on shoot-induced responses. Much less is known about interactions between below- and above-ground herbivores and how these may affect their respective parasitoids. 2Here, we quantify the impact of below-ground induced responses vs. that of above-ground induced responses in a feral Brassica on the performance of Pieris brassicae and its endoparasitoid Cotesia glomerata. Jasmonic acid (JA) was applied to induce the plants above- or below-ground. The glucosinolate, sugar and amino acid levels of the leaves were analysed. 3Pieris brassicae larvae grew significantly slower on shoot JA-induced (SJA) plants than on root JA-induced (RJA) and control plants, which were treated with acidic water. On RJA and control plants they showed similar developmental trajectories. Pupal masses, survival till eclosion and egg load, however, were similar on all plants. 4The development of C. glomerata larvae on SJA plants was significantly longer than that on RJA and control plants. In contrast, the parasitoid's pupal stage lasted longer in hosts feeding on control plants. The total developmental times eventually were similar in all groups. However, the masses of male and female C. glomerata adults that developed hosts on control and RJA plants were significantly larger than those from hosts on SJA plants. JA application increased total glucosinolate contents and decreased the sugars and total amino acids levels independent of whether JA was applied. However, the trajectories of herbivore-induced glucosinolate levels differed between RJA and SJA plants. 5These results show that the differential effects of above- and below-ground-induced responses on herbivores also affect higher trophic levels in a nonlinear fashion via differential changes in host plant quality. In particular, the indirect effects that below-ground herbivores have on the performance of above-ground parasitoids may exceed the direct effects of plant chemistry on herbivore performance. Consequently, above-ground and below-ground interactions mediated by induced plant responses have the potential to mediate insect community structure and function in complex ways.

Long-term memory (LTM) formation usually requires repeated, spaced learning events and is achieved by the synthesis of specific proteins. Other memory forms require a single learning experience and are independent of protein synthesis. We investigated in two closely related parasitic wasp species,Cotesia glomerataandCotesia rubecula, whether natural differences in foraging behaviour are correlated with differences in LTM acquisition and formation. These parasitic wasp species lay their eggs in young caterpillars of pierid butterflies and can learn to associate plant odours with a successful egg laying experience on caterpillars on the odour-producing plant. We used a classical conditioning set-up, while interfering with LTM formation through translation or transcription inhibitors. We show here thatC. rubeculaformed LTM after three spaced learning trials, whereasC. glomeratarequired only a single trial for LTM formation. After three spaced learning trials, LTM formation was complete within 4 h inC. glomerata, whereas inC. rubecula, LTM formation took 3 days. Linking neurobiology with ecology, we argue that this species-specific difference in LTM acquisition and formation is adaptive given the extreme differences in both the number of foraging decisions of the two wasp species and in the spatial distributions of their respective hosts in nature.

Classical optimal-foraging theory predicts that a parasitoid is less likely to leave a patch after a host encounter when the host distribution is aggregated, whereas a parasitoid is more likely to leave after a host encounter when the host distribution is regular. Field data on host distributions in the area of origin of the whitefly parasitoid Encarsia formosa showed that whiteflies aggregate at several spatial scales. However, infested leaves most likely contained a single host. This suggests that a host encounter is not enough to decide when to leave. We therefore tested the effect of host distribution and parasitoid experience on patch-leaving behavior. Each parasitoid was observed for several consecutive days in a three-dimensional arena with leaflets containing on average one host per leaflet in an either regular or aggregated host distribution. A proportional hazards model showed that a host encounter decreased the leaving tendency on a leaflet with one host when the time since the latest host encounter was short, but increased the leaving tendency when the time since the latest host encounter was long, independent of host distribution. We conclude that a parasitoid can switch from decreasing to increasing its tendency to leave a patch after a host encounter. We propose two hypotheses that may explain the evolution of such a switching mechanism. [KEYWORDS: optimal foraging ; patch-leaving behavior ; host distribution ; Encarsia formosa ; whitefly]

We studied the formation of protein synthesis-dependent long-term memory (LTM) in the parasitic wasp Nasonia vitripennis Walker (Hymenoptera: Pteromalidae), a parasitoid of fly pupae. Female wasps were trained in one of five different training procedures in the presence of hosts and the odour cinnamon. Six days later the reaction of the wasps towards the odour was tested in a static four-chamber olfactometer. When wasps were trained by a single drilling experience we could not find any reaction to cinnamon after 6 days. In contrast, when wasps were trained either via drilling plus host feeding, three drilling events (spaced training), 1 h training, or 24 h training including oviposition, they significantly preferred cinnamon 6 days later. Wasps which were injected the transcription inhibitor actinomycin D after a 1-h training to block protein synthesis showed normal memory retention up to 3 days, but did not react to cinnamon after 4 and 6 days. Control experiments showed no influence of actinomycin D on the natural behaviour and the general odour discrimination ability of N. vitripennis. This demonstrates that protein synthesis-dependent LTM has been formed. To our knowledge this is the first time that LTM formation after drilling plus host feeding but without oviposition is demonstrated in a parasitic wasp. These results were combined with additional findings about anaesthesia-sensitive memory, anaesthesia-resistant memory, and intermediate memory to develop a multiphase model of memory dynamics in N. vitripennis and to discuss ecological adaptations of memory formation in N. vitripennis and other parasitic wasp species.

Plants can accumulate and release defensive chemicals by activating various signaling pathways when they are damaged by herbivores or pathogens. The jasmonic acid pathway is activated after damage by chewing herbivores. Here we used jasmonic acid (JA) as an exogenous elicitor to induce feral cabbage plants. In this study, the effects of root JA (RJA) and shoot JA (SJA) induction on the foraging behavior of , a parasitoid of the large cabbage white butterfly , was investigated under semi-field conditions. In all combinations of differently induced plants (RJA, SJA and control plants), the percentages of shoot induced plants that were visited by at least one wasp were significantly higher than those of controls or root induced plants during 3 h of foraging. Consequently, parasitism rates of on shoot-JA induced plants were significantly higher than on plants induced with JA to the roots or control plants in all tests. However, this behavioral preference was not reflected in the allocation of offspring. The clutch sizes of eggs on control, root induced and shoot induced plants were not significantly different from each other in two-choice or three-choice experiments, but did differ with clutch size in the two-choice experiment of uninduced control plants versus SJA. This semi-field study helps to further understand the choice behavior and preferences of parasitoids in natural multitrophic communities in which plants induced with root or shoot herbivores occur together.

Herbivore-induced plant volatiles (HIPV) provide important information that influences host location behaviour for insect natural enemies, such as parasitoid wasps, that develop in the bodies of herbivorous insects. The dietary breadth of both the parasitoid and its host may affect the extent to which a searching parasitoid relies on HIPV. Specialist species are expected to rely on specific volatile cues to which they respond innately, whereas generalists are expected to show a higher degree of phenotypic plasticity that depends on foraging experience in the parasitoid. We compared the response to HIPV emitted by different plant species damaged by host and nonhost caterpillars for two congeneric parasitoid species, the specialist Diadegma semiclausum and the generalist Diadegma fenestrale, attacking caterpillars of the diamondback moth, Plutella xylostella. For the three tested plant species, Brassica oleracea, a feral Brassica population and Sinapis alba, both parasitoid species preferred volatiles from host-infested plants over those produced by undamaged plants. However, both parasitoid species only distinguished between volatiles induced by host and nonhosts when the caterpillars had been feeding on B. oleracea, the plant on which they had been reared. Chemical analysis of the volatile blends could not explain volatile preferences of the parasitoids. Despite the difference in their dietary breadth, the two parasitoids responded similarly to HIPV and experience treatments. A flexible response to a wide array of volatile blends by parasitoids is probably important in nature, given that different generations of the host and the parasitoid probably develop on different food plants.

Despite a large number of studies on herbivore-induced plant volatiles (HIPVs), little is known about which specific compounds are used by natural enemies to locate prey- or host- infested plants. In addition, the role of HIPVs in attracting natural enemies has been restricted largely to agricultural systems. Differences in volatile blends emitted by cultivars and plants that originate from wild populations may be attributed to potentially contrasting selection regimes: natural selection among the wild types and artificial selection among cultivars. A more realistic understanding of these interactions in a broader ecological and evolutionary framework should include studies that involve insect herbivores, parasitoids, and wild plants on which they naturally interact in the field. We compared the attractiveness of HIPVs emitted by wild and cultivated cabbage to the parasitoid Cotesia rubecula, and determined the chemical composition of the HIPV blends to elucidate which compounds are involved in parasitoid attraction. Wild and cultivated cabbage differed significantly in their volatile emissions. Cotesia rubecula was differentially attracted to the wild cabbage populations and preferred wild over cultivated cabbage. Isothiocyanates, which were only emitted by the wild cabbages, may be the key components that explain the preference for wild over cultivated cabbage, whereas terpenes may be important for the differential attraction among the wild populations. Volatile analysis revealed that parasitoid attraction cannot be explained by simple linear relationships. Our results suggest that unraveling which compound(s) are innately attractive to parasitoids of cabbage pests should include wild Brassicaceae.

Although the neural and genetic pathways underlying learning and memory formation seem strikingly similar among species of distant animal phyla, several more subtle inter- and intraspecific differences become evident from studies on model organisms. The true significance of such variation can only be understood when integrating this with information on the ecological relevance. Here, we argue that parasitoid wasps provide an excellent opportunity for multi-disciplinary studies that integrate ultimate and proximate approaches. These insects display interspecific variation in learning rate and memory dynamics that reflects natural variation in a daunting foraging task that largely determines their fitness: finding the inconspicuous hosts to which they will assign their offspring to develop. We review bioassays used for oviposition learning, the ecological factors that are considered to underlie the observed differences in learning rate and memory dynamics, and the opportunities for convergence of ecology and neuroscience that are offered by using parasitoid wasps as model species. We advocate that variation in learning and memory traits has evolved to suit an insect's lifestyle within its ecological niche.

International audience; 1. Belowground herbivory has recently been shown to disrupt the host location behaviour of aboveground parasitoids and thereby impact plants indirect defences. Reverse interactions, on the other hand, have received little attention so far. 2. Lab and field studies were conducted to examine whether the presence of the leaf herbivore Pieris brassicae Linnaeus on brassicaceous plants influences the response of Trybliographa rapae Westwood, a specialist parasitoid of the root feeder Delia radicum Linnaeus. 3. The present results show that the attraction of the parasitoid towards host-infested plants disappeared when these plants were also infested by P. brassicae. This absence of attraction was observed both when the complete odour blend or only undamaged leaves from damaged plants were offered, emphasising the role of systemically induced volatiles for host location in T. rapae. 4. Furthermore, the field study revealed that parasitism levels dropped from 30% on root-infested plants to 4% on double-infested plants. 5. The present study is the first to confirm that reduced attraction to host-infested plants as a result of simultaneous attack by below- and aboveground herbivores translates into lower levels of parasitism in the field.

It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical- and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata, a parasitoid of the leaf herbivore Pieris brassicae, mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.

Communication signals inducing aggregative behaviour profoundly affect a variety of ecological interactions, partly because they can be exploited by every member of the foodweb. To develop an evolutionary argument for the use of signals inducing aggregative behaviour in animals, the intricate role of aggregation pheromones in the ecology of Drosophila is discussed as a case study. Costs and benefits for the use of aggregation pheromone depend largely on the local characteristics of the environment, they involve various multitrophic interactions, and payoffs and penalties are density dependent. Plasticity in the use of pheromone is predicted and indeed found. For every ecological system, informational cues accompany food web interactions, and this affects the optimal strategy for individuals in their release of and response to such cues.

The profiles of pyrrolizidine alkaloids (PAs) in the two highly polyphagous arctiids Estigmene acrea and Grammia geneura and their potential PA sources in southeastern Arizona were compiled. One of four species of Boraginaceae, Plagiobothrys arizonicus, contained PAs; this is the first PA record for this plant species. The principle PA sources are Senecio longilobus (Asteraceae) and Crotalaria pumila (Fabaceae). The known PA pattern of S. longilobus was extended; the species was found to contain six closely related PAs of the senecionine type. Three novel PAs of the monocrotaline type, named pumilines A–C, were isolated and characterized from C. pumila, a species not studied before. The pumilines are the major PAs in the seeds, while in the vegetative organs they are accompanied by the simple necine derivatives supinidine and as the dominant compound subulacine (1,2-epoxytrachelanthamidine). In both plant species, the PAs are stored as N-oxides, except C. pumila seeds, which accumulate the free bases. Great variation in PA composition was observed between local populations of C. pumila. The PA profiles were established for larvae and adults of E. acrea that as larvae had fed on an artificial diet supplemented with crotalaria-powder and of G. geneura fed with S. longilobus. In both experiments, the larvae had a free choice between the respective PA source and diet or food plants free of PAs. The profiles compiled for the two species reflect the alkaloid profiles of their PA sources with one exception, subulacine could never be detected in E. acrea. Besides acquired PAs, insect PAs synthesized from acquired necine bases and necic acids of insect origin were detected in the two arctiid species. These insect PAs that do not occur in the larval food sources accounted for some 40–70% (E. acrea) and 17–37% (G. geneura) of total PAs extracted from the insects. A number of novel insect PAs were identified. Plant-acquired and insect PAs were found to accumulate as N-oxides. The results are discussed in relation to specific biochemical, electrophysiological, and behavioral mechanisms involved in PA sequestration by arctiids.