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There is increasing evidence that plant-associated microorganisms play important roles in defending plants against insect herbivores through both direct and indirect mechanisms. While previous research has shown that these microbes can modify the behaviour and performance of insect herbivores and their natural enemies, little is known about their effect on egg parasitoids which utilize oviposition-induced plant volatiles to locate their hosts. In this study, we investigated how root inoculation of sweet pepper (Capsicum annuum) with the plant-beneficial fungi Beauveria bassiana ARSEF 3097 or Trichoderma harzianum T22 influences the olfactory behaviour of the egg parasitoid Trissolcus basalis following egg deposition by its host Nezara viridula. Olfactometer assays showed that inoculation by T. harzianum significantly enhanced the attraction of the egg parasitoid, while B. bassiana had the opposite effect. However, no variation was observed in the chemical composition of plant volatiles. Additionally, fitness-related traits of the parasitoids (wasp body size) were not altered by any of the two fungi, suggesting that fungal inoculation did not indirectly affect host quality. Altogether, our results indicate that plant inoculation with T. harzianum T22 can be used to enhance attraction of egg parasitoids, which could be a promising strategy in manipulating early plant responses against pest species and improving sustainable crop protection. From a more fundamental point of view, our findings highlight the importance of taking into account the role of microorganisms when studying the intricate interactions between plants, herbivores and their associated egg parasitoids.

Plants can detect neighbouring plants through a reduction in the ratio between red and far-red light (R:FR). This provides a signal of plant–plant competition and induces rapid plant growth while inhibiting defence against biotic stress, two interlinked responses designated as the shade avoidance syndrome (SAS). Consequently, the SAS can influence plant–herbivore interactions that could cascade to higher trophic levels. However, little is known about how the expression of the SAS can influence tritrophic interactions. We investigated whether changes in R:FR affect the emission of herbivore-induced plant volatiles (HIPVs), and whether these changes influence the attraction of the zoophytophagous predator Macrolophus pygmaeus. We also studied how the expression of the SAS and subsequent inhibition of plant defences affects the reproduction of M. pygmaeus in both the presence and absence of the greenhouse whitefly (WF) (Trialeurodes vaporariorum) as arthropod prey. The results show that changes in R:FR have little effect on HIPV emissions and predator attraction. However, a reduction in R:FR leads to increased reproduction of both the predator and the WFs. We discuss that shade avoidance responses can increase the population development of M. pygmaeus through a combination of reduced plant defences and increased herbivore densities.

Soil composition and herbivory are two environmental factors that can affect plant traits including flower traits, thus potentially affecting plant-pollinator interactions. Importantly, soil composition and herbivory may interact in these effects, with consequences for plant fitness. We assessed the main effects of aboveground insect herbivory and soil amendment with exuviae of three different insect species on visual and olfactory traits of Brassica nigra plants, including interactive effects. We combined various methodological approaches including gas chromatography/mass spectrometry, spectroscopy and machine learning to evaluate changes in flower morphology, colour and the emission of volatile organic compounds (VOCs). Soil amended with insect exuviae increased the total number of flowers per plant and VOC emission, whereas herbivory reduced petal area and VOC emission. Soil amendment and herbivory interacted in their effect on the floral reflectance spectrum of the base part of petals and the emission of 10 VOCs. These findings demonstrate the effects of insect exuviae as soil amendment on plant traits involved in reproduction, with a potential for enhanced reproductive success by increasing the strength of signals attracting pollinators and by mitigating the negative effects of herbivory.

Microorganisms living in and on macroorganisms may produce microbial volatile compounds (mVOCs) that characterise organismal odours. The mVOCs might thereby provide a reliable cue to carnivorous enemies in locating their host or prey. Parasitism by parasitoid wasps might alter the microbiome of their caterpillar host, affecting organismal odours and interactions with insects of higher trophic levels such as hyperparasitoids. Hyperparasitoids parasitise larvae or pupae of parasitoids, which are often concealed or inconspicuous. Odours of parasitised caterpillars aid them to locate their host, but the origin of these odours and its relationship to the caterpillar microbiome are unknown. Here, we analysed the odours and microbiome of the large cabbage white caterpillar Pieris brassicae in relation to parasitism by its endoparasitoid Cotesia glomerata. We identified how bacterial presence in and on the caterpillars is correlated with caterpillar odours and tested the attractiveness of parasitised and unparasitised caterpillars to the hyperparasitoid Baryscapus galactopus. We manipulated the presence of the external microbiome and the transient internal microbiome of caterpillars to identify the microbial origin of odours. We found that parasitism by C. glomerata led to the production of five characteristic volatile products and significantly affected the internal and external microbiome of the caterpillar, which were both found to have a significant correlation with caterpillar odours. The preference of the hyperparasitoid was correlated with the presence of the external microbiome. Likely, the changes in external microbiome and body odour after parasitism were driven by the resident internal microbiome of caterpillars, where the bacterium Wolbachia sp. was only present after parasitism. Micro-injection of Wolbachia in unparasitised caterpillars increased hyperparasitoid attraction to the caterpillars compared to untreated caterpillars, while no differences were found c

Soil composition and herbivory are two environmental factors that can affect plant traits including flower traits, thus potentially affecting plant–pollinator interactions. Importantly, soil composition and herbivory may interact in these effects, with consequences for plant fitness. We assessed the main effects of aboveground insect herbivory and soil amendment with exuviae of three different insect species on visual and olfactory traits of Brassica nigra plants, including interactive effects. We combined various methodological approaches including gas chromatography/mass spectrometry, spectroscopy and machine learning to evaluate changes in flower morphology, colour and the emission of volatile organic compounds (VOCs). Soil amended with insect exuviae increased the total number of flowers per plant and VOC emission, whereas herbivory reduced petal area and VOC emission. Soil amendment and herbivory interacted in their effect on the floral reflectance spectrum of the base part of petals and the emission of 10 VOCs. These findings demonstrate the effects of insect exuviae as soil amendment on plant traits involved in reproduction, with a potential for enhanced reproductive success by increasing the strength of signals attracting pollinators and by mitigating the negative effects of herbivory.

The use of light-emitting diode (LED) lights in horticulture allows growers to adjust the light spectrum to optimize crop production and quality. However, changes in light quality can also influence plant–arthropod interactions, with possible consequences for pest management. The addition of far-red light has been shown to interfere with plant immunity, thereby increasing plant susceptibility to biotic stress and increasing pest performance. Far-red light also influences plant emission of volatile organic compounds (VOCs) and might thus influence tritrophic interactions with biological control agents. We investigated how far-red light influences the VOC-mediated attraction of the predatory mite Phytoseiulus persimilis to tomato plants infested with Tetranychus urticae, and its ability to control T. urticae populations. RESULTS: Far-red light significantly influences herbivore-induced VOC emissions of tomato plants, characterized by a change in relative abundance of terpenoids, but this did not influence the attraction of P. persimilis to herbivore-induced plants. Supplemental far-red light led to an increased population growth of T. urticae and increased numbers of P. persimilis. This resulted in a stronger suppression of T. urticae populations under supplemental far-red light, to similar T. urticae numbers as in control conditions without supplemental far-red light. CONCLUSION: We conclude that supplemental far-red light can change herbivore-induced VOC emissions but does not interfere with the attraction of the predator P. persimilis. Moreover, far-red light stimulates biological control of spider mites in glasshouse tomatoes due to increased population build-up of the biocontrol agent.

Biological control using plant-beneficial fungi has gained considerable interest as a sustainable method for pest management, by priming the plant for enhanced defense against pathogens and insect herbivores. However, despite promising outcomes, little is known about how different fungal strains mediate these beneficial effects. In this study, we evaluated whether inoculation of tomato seeds with the plant-beneficial fungi Beauveria bassiana ARSEF 3097, Metarhizium brunneum ARSEF 1095 and Trichoderma harzianum T22 affected the plant’s volatile organic compound (VOC) profile and the host-choice behavior of Nesidiocoris tenuis, an emerging pest species in NW-European tomato cultivation, and the related zoophytophagous biocontrol agent Macrolophus pygmaeus. Results indicated that fungal inoculation did not significantly alter the VOC composition of tomato plants. However, in a two-choice cage assay where female insects were given the option to select between control plants and fungus-inoculated plants, N. tenuis preferred control plants over M. brunneum-inoculated plants. Nearly 72% of all N. tenuis individuals tested chose the control treatment. In all other combinations tested, no significant differences were found for none of the insects. We conclude that inoculation of tomato with plant-beneficial fungi had limited effects on plant volatile composition and host-choice behavior of insects. However, the observation that N. tenuis was deterred from the crop when inoculated with M. brunneum and attracted to non-inoculated plants may provide new opportunities for future biocontrol based on a push-pull strategy.

•Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. •We assessed the phenotypic integration of CCDs in a meta-analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. •Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs. •We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals.

Anthropophilic mosquitoes are effective vectors of human disease because of their biting preferences. To find their host, these mosquitoes are guided by human odours, primarily produced by human skin bacteria. By analysing the skin bacterial and skin volatile profiles of humans, bonobos, chimpanzees, gorillas, lemurs and cows, we investigated whether primates that are more closely related to humans have a skin bacterial community and odour profile that is similar to that of humans. We then investigated whether this affected discrimination between humans and closely related primates by anthropophilic and zoophilic mosquitoes that search for hosts. Humans had a lower skin bacterial diversity than the other animals and their skin bacterial composition was more similar to that in other primates than it was to the skin bacteria of cows. Like the skin bacterial profiles, the volatile profiles of the animal groups were clearly different from each other. The volatile profiles of cows and lemurs were more closely related to the human profiles than expected. Human volatiles were indeed preferred above cow volatiles by anthropophilic mosquitoes and no preference was observed when tested against non-human primate odour, except for bonobo volatiles, which were preferred over human volatiles. Unravelling the differences between mosquito hosts and their effect on host selection is important for a better understanding of cross-species transmission of vector-borne diseases.

Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta‐analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs. We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals.

Plants release a variety of volatile organic compounds that play multiple roles in the interactions with other plants and animals. Natural enemies of plant-feeding insects use these volatiles as cues to find their prey or host. Here, we report differences between the volatile blends of tomato plants infested with the whitefly Bemisia tabaci or the tomato borer Tuta absoluta. We compared the volatile emission of: (1) clean tomato plants; (2) tomato plants infested with T. absoluta larvae; and (3) tomato plants infested with B. tabaci adults, nymphs, and eggs. A total of 80 volatiles were recorded of which 10 occurred consistently only in the headspace of T. absoluta-infested plants. Many of the compounds detected in the headspace of the two herbivory treatments were emitted at different rates. Plants damaged by T. absoluta emitted at least 10 times higher levels of many compounds compared to plants damaged by B. tabaci and intact plants. The multivariate separation of T. absoluta-infested plants from those infested with B. tabaci was due largely to the chorismate-derived compounds as well as volatile metabolites of C18-fatty acids and branched chain amino acids that had higher emission rates from T. absoluta-infested plants, whereas the cyclic sesquiterpenes α- and β-copaene, valencene, and aristolochene were emitted at significantly higher levels from B. tabaci-infested plants. Our findings imply that feeding by T. absoluta and B. tabaci induced emission of volatile blends that differ quantitatively and qualitatively, providing a chemical basis for the recently documented behavioral discrimination by two generalist predatory mirid species, natural enemies of T. absoluta and B. tabaci employed in biological control.

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.

Mosquitoes display biting preferences among different sites of the human body. In addition to height or convection currents, body odour may play a role in the selection of these biting sites. Previous studies have shown that skin emanations are important host-finding cues for mosquitoes. In this study, skin emanations were collected from armpits, hands and feet; the volatile profiles were analysed and tested for their attractiveness to the malaria mosquito Anopheles coluzzii. Skin emanations collected from armpits were less attractive to An. coluzzii compared to hands or/and feet. The difference may have been caused by deodorant residues, which were found in the armpit samples and not in those of hands and feet. In a subsequent experiment, volunteers were asked to avoid using skincare products for five days, and thereafter, no differences in attractiveness of the body parts to mosquitoes were found. The detected deodorant compound isopropyl tetradecanoate inhibited mosquito landings in a repellent bioassay. It is concluded that the volatiles emanated from different body parts induced comparable levels of attraction in mosquitoes, and that skincare products may reduce a person' s attractiveness to mosquitoes.

Foraging success of predators profoundly depends on reliable and detectable cues indicating the presence of their often inconspicuous prey. Carnivorous insects rely on chemical cues to optimize foraging efficiency. Hyperparasitoids that lay their eggs in the larvae or pupae of parasitic wasps may find their parasitoid hosts developing in different herbivores. They can use herbivore-induced plant volatiles (HIPVs) to locate parasitized caterpillars. Because different herbivore species induce different HIPV emission from plants, hyperparasitoids may have to deal with large variation in volatile information that indicates host presence. In this study, we used an ecogenomics approach to first address whether parasitized caterpillars of two herbivore species (Pieris rapae and P. brassicae) induce similar transcriptional and metabolomic responses in wild Brassica oleracea plants and, second, whether hyperparasitoids Lysibia nana are able to discriminate between these induced plant responses to locate their parasitoid host in different herbivores under both laboratory and field conditions. Our study revealed that both herbivore identity and parasitism affect plant transcriptional and metabolic responses to herbivory. We also found that hyperparasitoids are able to respond to HIPVs released by wild B. oleracea under both laboratory and field conditions. In addition, we observed stronger attraction of hyperparasitoids to HIPVs when plants were infested with parasitized caterpillars. However, hyperparasitoids were equally attracted to plants infested by either herbivore species. Our results indicate that parasitism plays a major role in HIPV-mediated plant–hyperparasitoid interactions. Furthermore, these findings also indicate that plant trait-mediated indirect interaction networks play important roles in community-wide species interactions.