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Animals such as bumblebees use chemosensory cues to both locate and evaluate essential resources. Increasingly, it is recognized that microbes can alter the quality of foraged resources and produce metabolites that may act as foraging cues. The distinct nature of these chemosensory cues however and their use in animal foraging remain poorly understood. Here, we test the hypothesis that species of nectar-inhabiting microbes differentially influence pollinator attraction and feeding via microbial metabolites produced in nectar. We first examined the electrophysiological potential for bumblebee (Bombus impatiens) antennal olfactory neurons to respond to microbial volatile organic compounds (mVOCs), followed by an olfactory preference test. We also assessed gustatory preferences for microbial-altered nectar through both no-choice and choice feeding assays. Antennal olfactory neurons responded to some mVOCs, and bees preferred nectar solutions inoculated with the bacterium Asaia astilbes over the yeast Metschnikowia reukaufii based on volatiles alone. However, B. impatiens foragers consumed significantly more Metschnikowia-inoculated nectar, suggesting distinct roles for mVOCs and non-volatile metabolites in mediating both attraction and feeding decisions. Collectively, our results suggest that microbial metabolites have significant potential to shape interspecific, plant-pollinator signalling, with consequences for forager learning, economics and floral host reproduction.

The plant microbiome can influence plant phenotype in diverse ways, yet microbial contribution to plant volatile phenotype remains poorly understood. We examine the presence of fungi and bacteria in the nectar of a coflowering plant community, characterize the volatiles produced by common nectar microbes and examine their influence on pollinator preference. Nectar was sampled for the presence of nectar-inhabiting microbes. We characterized the headspace of four common fungi and bacteria in a nectar analog. We examined electrophysiological and behavioral responses of honey bees to microbial volatiles. Floral headspace samples collected in the field were surveyed for the presence of microbial volatiles. Microbes commonly inhabit floral nectar and the common species differ in volatile profiles. Honey bees detected most microbial volatiles tested and distinguished among solutions based on volatiles only. Floral headspace samples contained microbial-associated volatiles, with 2-ethyl-1-hexanol and 2-nonanone - both detected by bees - more often detected when fungi were abundant. Nectar-inhabiting microorganisms produce volatile compounds, which can differentially affect honey bee preference. The yeast Metschnikowia reukaufii produced distinctive compounds and was the most attractive of all microbes compared. The variable presence of microbes may provide volatile cues that influence plant-pollinator interactions.

Nectar microbe-produced volatiles can contribute to floral blends and modify pollinator preference for flowers. Identifying and describing the compounds that may underlie this effect is a key goal. Semi-quantitative or quantitative data is often critical for chemical ecology investigations, given that biotic responses (i.e., insects or plants) can fluctuate with concentration, relative ratios, or composition of the emitted volatile profiles. However, field-based, in situ microbial volatile detection and quantification is difficult due to the small scale of the nectar microhabitat. Laboratory-based inoculations of bulk synthetic nectars are useful for screening weakly-abundant and difficult to analyze volatiles, which may be crucial in eliciting responses. Despite the limitations of this approach, it allows rapid identification of target molecules for further validation with bioassays. Targeted analytical methods to identify or quantify semiochemicals may then be developed and validated for field tests. Here, we report the first quantitative assessment of microbe volatile emission in laboratory-based tests with synthetic nectar. We also review briefly solid-phase microextraction collection and gas-chromatography data interpretation. Nectar microbe interactions with plants and insects offer opportunities for agricultural improvement, and a selection of potential uses are highlighted.

Insect pests cause serious economic, yield, and food safety problems to managed crops worldwide. Compounding these problems, insect pests often vector pathogenic or toxigenic microbes to plants. Previous work has considered plant-insect and plant-microbe interactions separately. Although insects are well-understood to use plant volatiles to locate hosts, microorganisms can produce distinct and abundant volatile compounds that in some cases strongly attract insects. In this paper, we focus on the microbial contribution to plant volatile blends, highlighting the compounds emitted and the potential for variation in microbial emission. We suggest that these aspects of microbial volatile emission may make these compounds ideal for use in agricultural applications, as they may be more specific or enhance methods currently used in insect control or monitoring. Our survey of microbial volatiles in insect-plant interactions suggests that these emissions not only signal host suitability but may indicate a distinctive time frame for optimal conditions for both insect and microbe. Exploitation of these host-specific microbe semiochemicals may provide important microbe- and host-based attractants and a basis for future plant-insect-microbe chemical ecology investigations.

BACKGROUND: Spotted‐wing drosophila, Drosophila suzukii, is a serious pest of thin‐skinned fruits. Alternative methods to control this pest are needed to reduce insecticide use, including new repellents. Previous research demonstrated that D. suzukii adults use odor cues to avoid blueberries infected with the fungal pathogen Colletotrichum fioriniae, which causes the disease anthracnose. To identify novel D. suzukii repellents, we investigated the volatile emission from experimentally‐infected fruit, which were inoculated with C. fioriniae isolates in the laboratory, and from field‐collected fruit, which were naturally infected and harvested from a field. We then tested the pathogen‐induced volatiles on D. suzukii adult behavior. RESULTS: Volatile emission was similar between all five C. fioriniae strains, with good agreement between experimentally‐infected and field‐collected berries. In total, 14 volatiles were found to be more abundant in infected versus uninfected fruit headspace. In multiple‐choice bioassays, nine of the 14 volatiles elicited repellency responses from adult D. suzukii. These nine volatiles were further evaluated in dual choice assays, where all nine reduced fly capture by 43–96% compared to the control. The most repellent compounds tested were the esters ethyl butanoate and ethyl (E)‐but‐2‐enoate, which were more or equally repellent to the known D. suzukii repellents 1‐octen‐3‐ol, geosmin, and 2‐pentylfuran. Dose–response assays identified concentration‐dependent effects on D. suzukii repellency and oviposition when applied individually and consistent aversion observed across doses of a 1:1 blend. CONCLUSION: We report two repellents from C. fioriniae‐infected blueberries that could be useful semiochemicals for the behavioral manipulation of D. suzukii in the field. © 2023 Society of Chemical Industry. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA. [ABSTRACT FROM AUTHOR]

Flowering crops are heavily managed during bloom to both promote pollination and prevent disease. Disease management practices can alter the floral microbiome, including pathogens and nontarget microbes. However, whether agrochemical presence or altered microbiome composition affect pollinator foraging and pollination services is unclear.We assessed effects of orchard management tactics and landscape context on the flower microbiome in almond, Prunus dulcis. Fourteen orchards (five conventional, four organic and five conventional with habitat augmentation) were sampled at early and peak bloom to characterize bacterial and fungal communities associated with floral tissues. The surveys were complemented by an artificial flower experiment to assess effects of fungicides and microbes on honey bee foraging. Finally, a field trial was conducted to test effects of fungicides and microbes on pollination.As bloom progressed, bacterial and fungal abundance and diversity increased across all floral tissue types and management strategies. The magnitude by which microbial abundance and diversity were affected varied, with proximity to apiaries and orchard management having notable effects on bacteria and fungi respectively.Experiments revealed that fungicides reduced nectar removal by honey bees; however, neither fungicide nor microbe treatments affected pollination, as measured through pollen tube initiation and growth.Synthesis and applications. Our results reveal that microbiota associated with flowers of a pollinator‐dependent crop are temporally dynamic and sensitive to management practices. However, pollination services in almond may be resilient to both agrochemical disturbance and microbial augmentation of flowers, the latter of which may become more prominent as microbial solutions to disease management are embraced in agroecosystems. [ABSTRACT FROM AUTHOR]