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There is increasing evidence that microorganisms emit a wide range of volatile compounds (mVOCs, microbial volatile organic compounds) that act as insect semiochemicals, and therefore play an important role in insect behaviour. Although it is generally believed that phylogenetically closely related microbes tend to have similar phenotypic characteristics and therefore may elicit similar responses in insects, currently little is known about whether the evolutionary history and phylogenetic relationships among microorganisms have an impact on insect‐microbe interactions. In this study, we tested the hypothesis that phylogenetic relationships among 40 Bacillus strains isolated from diverse environmental sources predicted mVOC composition and the olfactory response of the generalist aphid parasitoid Aphidius colemani . Results revealed that phylogenetically closely related Bacillus strains emitted similar blends of mVOCs and elicited a comparable olfactory response of A. colemani in Y‐tube olfactometer bioassays, varying between attraction and repellence. Analysis of the chemical composition of the mVOC blends showed that all Bacillus strains produced a highly similar set of volatiles, but often in different concentrations and ratios. Benzaldehyde was produced in relatively high concentrations by strains that repel A. colemani , while attractive mVOC blends contained relatively higher amounts of acetoin, 2,3‐butanediol, 2,3‐butanedione, eucalyptol and isoamylamine. Overall, these results indicate that bacterial phylogeny had a strong impact on mVOC compositions and as a result on the olfactory responses of insects.

To locate mating partners and essential resources such as food, oviposition sites and shelter, insects rely to a large extent on chemical cues. While most research has focused on cues derived from plants and insects, there is mounting evidence that indicates that micro‐organisms emit volatile compounds that may play an important role in insect behaviour. In this study, we assessed how volatile compounds emitted by phylogenetically diverse bacteria affected the olfactory response of the primary parasitoid Aphidius colemani and one of its secondary parasitoids, Dendrocerus aphidum. Olfactory responses were evaluated for volatile blends emitted by bacteria isolated from diverse sources from the parasitoid's habitat, including aphids, aphid mummies and honeydew, and from the parasitoids themselves. Results revealed that A. colemani showed a wide variation in response to bacterial volatiles, ranging from significant attraction over no response to significant repellence. Our results further showed that the olfactory response of A. colemani to bacterial volatile emissions was different from that of D. aphidum. Gas chromatography‐mass spectrometry analysis of the volatile blends revealed that bacterial strains repellent to A. colemani produced significantly higher amounts of esters, organic acids, aromatics and cycloalkanes than attractive strains. Strains repellent to D. aphidum produced significantly higher amounts of alcohols and ketones, whereas the strains attractive to D. aphidum produced higher amounts of the monoterpenes limonene, linalool and geraniol. Overall, our results indicate that bacterial volatiles can have an important impact on insect olfactory responses, and should therefore be considered as an additional, so far often overlooked factor in studying multitrophic interactions between plants and insects. A free Plain Language Summary can be found within the Supporting Information of this article. ispartof: FUNCTIONAL ECOLOGY vol:34 issue:2 pages:507-520 status: published

Understanding how animals learn is crucial to interpreting animal behaviour. Flower-visiting insects, such as bees and parasitoids, are excellent animal models to study visual and olfactory learning, including memory phenomena. The diversity of resources flower-visiting insects exploit predisposes them to learn and remember the colours, shapes and odours associated with rewarding experiences (e.g. flowers), allowing them to focus on the most rewarding resources. Recent research has shown that nectar-living microbes release volatile organic compounds (VOCs) that contribute to overall flower scent. Nevertheless, little is known about the extent to which nectar microbiota mediate insect learning of floral preferences. In this study, we investigated whether VOCs produced by nectar microbes serve as a learning cue to parasitoids and how long any developed preference is maintained. Experiments were performed using the generalist aphid parasitoid Aphidius ervi and three nectar yeasts, including the nectar specialist Metschnikowia reukaufii and the generalist species Hanseniaspora uvarum and Sporobolomyces roseus. Results showed that naive parasitoids had an innate preference for nectar fermented by the nectar specialist M. reukaufii, but not by the other two yeasts which had either a neutral (H. uvarum) or deterrent (S. roseus) effect. When parasitoids were conditioned with yeast-fermented nectar, they were strongly attracted to their odours 2 and 24 h after conditioning, but not after 48 h. Furthermore, when parasitoids were conditioned to one yeast-fermented nectar, they also showed increased attraction to other yeast-fermented nectars. This generalization suggests that their learning ability may have broader ecological consequences. However, this generalized response to other yeast VOCs lasted for only 2 h. We conclude that parasitoids show conditioned responses to the scent of yeast-fermented nectar, and yeasts, therefore, may play an important but understudied role in shaping their foraging behaviour.

BACKGROUND\ud Recent studies have shown that microorganisms emit volatile compounds that affect insect behaviour. However, it remains largely unclear whether microbes can be exploited as a source of attractants to improve biological control of insect pests. In this study, we used a combination of coupled gas chromatography‐electroantennography (GC–EAG) and Y‐tube olfactometer bioassays to identify attractive compounds in the volatile extracts of three bacterial strains that are associated with the habitat of the generalist aphid parasitoid Aphidius colemani, and to create mixtures of synthetic compounds to find attractive blends for A. colemani. Subsequently, the most attractive blend was evaluated in two‐choice cage experiments under greenhouse conditions.\ud \ud RESULTS\ud GC–EAG analysis revealed 20 compounds that were linked to behaviourally attractive bacterial strains. A mixture of two EAG‐active compounds, styrene and benzaldehyde applied at a respective dose of 1 μg and 10 ng, was more attractive than the single compounds or the culture medium of the bacteria in Y‐tube olfactometer bioassays. Application of this synthetic mixture under greenhouse conditions resulted in significant attraction of the parasitoids, and outperformed application of the bacterial culture medium.\ud \ud CONCLUSION\ud Compounds isolated from bacterial blends were capable of attracting parasitoids both in laboratory and greenhouse assays, indicating that microbial cultures are an effective source of insect attractants. This opens new opportunities to attract and retain natural enemies of pest species and to enhance biological pest control.

Summary 1.Nectar is a crucial energy resource that strongly mediates the interactions between plants and animal pollinators or plant defenders. Previous research has shown that nectar is commonly colonized by microorganisms, most commonly bacteria and yeasts, which can have a strong impact on nectar chemistry. However, at present little is known about the effects of microorganisms on the fitness of animals feeding on nectar. 2.We used three nectar bacteria representing different metabolic groups (Asaia sp., Lactococcus sp. and Rosenbergiella sp.) and the common generalist aphid parasitoid Aphidius ervi (Haliday) (Hymenoptera: Braconidae) to test the hypothesis that different nectar-dwelling bacteria affect nectar consumption and insect longevity differently by altering the chemistry of nectar. 3.Bacteria significantly affected nectar chemistry by altering its acidity, sugar and amino acids composition/concentration and by adding compounds synthesized by the microbes. Although inoculation with bacteria did not affect nectar consumption, a significant difference in insect longevity was observed. The impact on longevity was species specific, with Lactococcus being beneficial and Asaia having a detrimental effect.​ 4.Bacteria have a strong impact on nectar chemistry and changes in nectar chemistry may not only influence the foraging behavior of flower-visiting animals and impact on plant fitness, but also influence the fitness of nectar-consuming organisms. As effects were species dependent, changes in nectar chemistry induced by different bacteria may have contrasting effects on the interactions between plants and insects. It is therefore essential to know how different microbes alter nectar chemistry to understand the relationships between plants, nectar-inhabiting microbes and nectar-consuming animals. This article is protected by copyright. All rights reserved.

Aphid parasitoids are commonly used in the biological control of aphids. However, their success in biological control largely depends on the availability of carbohydrate-rich food as an energy source for maintenance and reproduction. Therefore, as these resources have become rare in modern agricultural systems, external sugar sources like flowering plants or artificial sugar solutions are more and more used to provide the biocontrol agents with the necessary sugars. When developing such artificial food sources, it is essential to carefully select the sugars that best support the target parasitoids without benefiting non-target insects, such as pest insects or hyperparasitoids. Here, we investigated the gustatory response and longevity of two commonly used aphid parasitoids (Aphidius colemani and Aphidius matricariae) and their hyperparasitoid Dendrocerus aphidum when provided with one of eight plant- and/or insect-derived sugars (fructose, galactose, glucose, melibiose, melezitose, rhamnose, sucrose and trehalose). Our results showed that the studied insect species consumed the largest amounts of sugars that are most commonly found in honeydew (sucrose, fructose, glucose and melezitose) and also survived best when feeding on these sugars. Both Aphidius spp. survived well on melibiose, whereas D. aphidum performed poorly on this sugar. When melibiose was offered in a mixture with glucose, a significant reduction in longevity was observed for D. aphidum when compared to glucose only, while this was less pronounced for Aphidius spp. This knowledge can be exploited in tailoring food sources to selectively support Aphidius parasitoids, enhancing the biological control of aphids.

To meet their carbohydrate requirements, adult parasitoids exploit a broad range of sugar resources, including floral and extrafloral nectar and honeydew. Although honeydew might be the predominant sugar source, especially in agricultural systems, it often is nutritionally inferior to sugar sources like nectar. Given its broad availability, it may be expected that sugar-feeding insects have evolved specialized adaptations to deal with this typically inferior sugar source. This would apply especially to organisms that have a close association with honeydew producers. Here, we hypothesized that parasitoids of honeydew-producing insects should show a pronounced response to sugars, such as fructose, sucrose, melezitose, and trehalose, and to a lesser extent glucose. To test this hypothesis, we investigated sugar consumption, feeding behavior and survival of the aphid parasitoid Aphidius ervi on several sugars (equiweight solutions). Our results show that A. ervi adults consumed typical honeydew sugars (sucrose, fructose, trehalose, and melezitose) the most, while consuming considerably less glucose or melibiose. Rhamnose, which does not occur in aphid honeydew, was not, or was only marginally, consumed. When different sugars were provided at the same time, A. ervi adults preferred sucrose or fructose over glucose or melezitose. Furthermore, pre-exposure to sucrose or fructose significantly reduced subsequent intake of glucose, suggesting an acquired distaste for glucose after being previously exposed to highly preferred sugars such as sucrose and fructose. Altogether, this study shows that A. ervi adults prefer sugars (fructose, melezitose, trehalose, and sucrose) that are overrepresented in aphid honeydew and show a lower preference to one (glucose) that is underrepresented in honeydew.