Nectar, the main floral reward for pollinators, varies greatly in composition and concentration. The assumption that nectar quality is equivalent to its sugar (energy) concentration is too simple. Diverse non-sugar components, especially amino acids and secondary metabolites, play various roles in nutrition and health of pollinators. Many nectar compounds have indirect effects by altering the foraging behaviour of pollinators or protecting them from disease. This review also emphasizes the water component of nectar, often ignored because of evaporative losses and difficulties in sampling small nectar volumes. Nectar properties vary with environmental factors, pollinator visits and microbial contamination. Pollination mutualisms depend on the ability of insect and vertebrate pollinators to cope with and benefit from the variation and diversity in nectar chemistry. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.

Sweet solutions: nectar chemistry and quality

Floral nectar is prone to colonization by nectar-adapted yeasts and bacteria via air-, rain-, and animal-mediated dispersal. Upon colonization, microbes can modify nectar chemical constituents that are plant-provisioned or impart their own through secretion of metabolic by-products or antibiotics into the nectar environment. Such modifications can have consequences for pollinator perception of nectar quality, as microbial metabolism can leave a distinct imprint on olfactory and gustatory cues that inform foraging decisions. Furthermore, direct interactions between pollinators and nectar microbes, as well as consumption of modified nectar, have the potential to affect pollinator health both positively and negatively. Here, we discuss and integrate recent findings from research on plant–microbe–pollinator interactions and their consequences for pollinator health. We then explore future avenues of research that could shed light on the myriad ways in which nectar microbes can affect pollinator health, including the taxonomic diversity of vertebrate and invertebrate pollinators that rely on this reward. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.

Potential effects of nectar microbes on pollinator health

There is a global industry built upon the production of ‘bioinoculants’, which include both bacteria and fungi. The recent increase in bioinoculant uptake by land users coincides with a drive for more sustainable land use practises. But are bioinoculants sustainable? These microbes are believed to improve plant performance, but knowledge of their effect on resident microbial communities is scant. Without a clear understanding of how they affect soil microbial communities, their utility is unclear. To assess how different inoculation practises may affect bioinoculant effects on soil microbial communities, we surveyed the existing literature. Our results show that bioinoculants significantly affect soil microbial diversity and that these effects are mediated by inoculant type, diversity, and disturbance regime. Further, these changes to soil microbes affect plant outcomes. Knowledge that these products may influence crop performance indirectly through changes to soil microbial diversity attests to the importance of considering the soil microbiome when assessing both bioinoculant efficacy and threats to soil ecosystems.

Do Bioinoculants Affect Resident Microbial Communities? A Meta-Analysis

Floral nectar often contains pollen and microorganisms, which may change nectar's chemical composition, and in turn impact pollinator affinity. However, their individual and combined effects remain understudied. Here we examined the impacts of the nectar specialist yeast, Metschnikowia reukaufii, and the addition of sunflower (Hellianthus annus) pollen. Pollen grains remained intact, yet still increased yeast growth and amino acid concentrations in nectar, whereas yeast depleted amino acids. Pollen, but not yeast, changed nectar sugar concentrations by converting sucrose to its monomers. Both pollen and yeast contributed emissions from nectar, though yeast volatiles were more abundant than pollen volatiles. Yeast volatile emission was positively correlated with pollen concentration and cell density, and yeast depleted a subset of pollen-derived volatiles. Honey bees avoided foraging on yeast-inoculated nectar and foraged equally among uninoculated nectars regardless of pollen content, underscoring the importance of microbial metabolites in mediating pollinator foraging. This article is protected by copyright. All rights reserved.

Pollen and yeast change nectar aroma and nutritional content alone and together, but honey bee foraging reflects only the avoidance of yeast

Priority effects, where arrival order and initial relative abundance modulate local species interactions, can exert taxonomic, functional, and evolutionary influences on ecological communities by driving them to alternative states. It remains unclear if these wide-ranging consequences of priority effects can be explained systematically by a common underlying factor. Here, we identify such a factor in an empirical system. In a series of field and laboratory studies, we focus on how pH affects nectar-colonizing microbes and their interactions with plants and pollinators. In a field survey, we found that nectar microbial communities in a hummingbird-pollinated shrub, Diplacus (formerly Mimulus) aurantiacus, exhibited abundance patterns indicative of alternative stable states that emerge through domination by either bacteria or yeasts within individual flowers. In addition, nectar pH varied among D. aurantiacus flowers in a manner that is consistent with the existence of these alternative stable states. In laboratory experiments, Acinetobacter nectaris, the bacterium most commonly found in D. aurantiacus nectar, exerted a strongly negative priority effect against Metschnikowia reukaufii, the most common nectar-specialist yeast, by reducing nectar pH. This priority effect likely explains the mutually exclusive pattern of dominance found in the field survey. Furthermore, experimental evolution simulating hummingbird-assisted dispersal between flowers revealed that M. reukaufii could evolve rapidly to improve resistance against the priority effect if constantly exposed to A. nectaris-induced pH reduction. Finally, in a field experiment, we found that low nectar pH could reduce nectar consumption by hummingbirds, suggesting functional consequences of the pH-driven priority effect for plant reproduction. Taken together, these results show that it is possible to identify an overarching factor that governs the eco-evolutionary dynamics of priority effects across multiple levels of biological organization. 

Wide-ranging consequences of priority effects governed by an overarching factor

Nectar bacteria stimulate pollen germination and bursting to enhance microbial fitness.

Culturable bacteria are more common than fungi in floral nectar and are more easily dispersed by thrips, a ubiquitous flower visitor.

For many flower visitors, pollen is the primary source of non-carbon nutrition, but pollen has physical defenses that make it difficult for consumers to access nutrients. Nectar-dwelling microbes are nearly ubiquitous among flowers and can reach high densities, despite the fact that floral nectar is nitrogen limited, containing only very low concentrations of non-carbon nutrients. Pollen contains trace micronutrients and high protein content but is protected by a recalcitrant outer shell. Here, we report that a common genus of nectar-dwelling bacteria, Acinetobacter, exploits pollen nutrition by inducing pollen germination and bursting. We use time course germination assays to quantify the effect of Acinetobacter species on pollen germination and pollen bursting. Inoculation with Acinetobacter species resulted in increased germination rates within 15 minutes, and bursting by 45 minutes, as compared to uninoculated pollen. The pollen germination and bursting phenotype is density-dependent, with lower concentrations of A. pollinis SCC477 resulting in a longer lag time before the spike in germination, which is then closely followed by a spike in bursting. Lastly, A. pollinis grows to nearly twice the density with germinable pollen vs ungerminable pollen, indicating that their ability to induce and exploit germination plays an important role in rapid growth. To our knowledge, this is the first direct test of non-plant biological induction of pollen germination, as well as the first evidence of induced germination as a method of nutrient procurement, as the microbes appear to hijack the pollens normally tightly controlled germination mechanisms for their benefit. Our results suggest that further study of microbe-pollen interactions may inform many aspects of pollination ecology, including microbial ecology in flowers, the mechanisms of pollinator nutrient acquisition from pollen, and cues of pollen germination for plant reproduction.

https://biorxiv.org/content/10.1101/2021.01.07.425766v1.full.pdf

Nectar bacteria stimulate pollen germination and bursting to enhance their fitness

Dispersal, particularly variation in dispersal ability among taxa, affects community assembly in individual communities and biodiversity maintenance within metacommunities. Although fungi and bacteria frequently coexist, their relative dispersal abilities are poorly understood. Here, we compare the incidence and abundance of culturable flower-inhabiting bacteria and fungi among individual flowers. Using collections that span two coflowering communities across two years, we assess viable bacterial and fungal incidence and abundance within individual flower samples, and examine patterns across plant species that differ in flower traits. Our results demonstrate that bacteria can be detected in more flowers and in greater numerical abundance than fungi, particularly in flowers with more exposed corollas. For fungi, however, flowers with long corollas were equally likely as exposed flowers to contain cells, and hosted higher numbers of fungal cells, primarily yeasts. Across all flowers, bacteria and fungal incidence was positively related, but within flowers containing microbes, bacterial and fungal incidence was negatively related, suggesting shared dispersal routes but competition among microbes within flowers. The difference in dispersal abilities of bacteria and fungi identified here may have broad relevance for community assembly of microbes and plant-pollinator interactions.

/pdf/fungi-are-more-dispersal-limited-than-bacteria-among-flowers-4qrhn177f6.pdf

Fungi are more dispersal-limited than bacteria among flowers

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Nectar bacteria stimulate pollen germination and bursting to enhance microbial fitness.

Culturable bacteria are more common than fungi in floral nectar and are more easily dispersed by thrips, a ubiquitous flower visitor.

Nectar bacteria stimulate pollen germination and bursting to enhance their fitness

Fungi are more dispersal-limited than bacteria among flowers