Nectar‐inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator

Rering, Caitlin C.; Beck, John J.; Hall, Griffin W.; McCartney, Mitchell M.; Vannette, Rachel L.

doi:10.1111/nph.14809

Cited by 181 publications

(203 citation statements)

References 69 publications

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“…, Rering et al. , Adler et al. , McFrederick and Rehan , Russell and Ashman ), consequences of pollinator behavior extend beyond plant fertilization to patterns of microbial transmission.…”

Section: Discussionmentioning

confidence: 99%

Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

et al. 2019

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Dispersal is central to the ecology and evolution of spatially structured communities. While flower microbial communities are spatially structured among floral organs, how dispersal vectors distribute microbes among floral organs is unknown. Pollinators are recognized as key microbial vectors, but effects of their different foraging behaviors on transfer dynamics among flowers or different floral organs are not known. We asked how foraging behaviors of a model pollinator (Bombus impatiens) affect acquisition and dispersal of microbes among flower organs. We used monkeyflowers (Mimulus guttatus) to examine dispersal within a natural context and artificial flowers to test how common bee foraging behaviors (nectaring, buzzing, or scrabbling) shaped dispersal of a green fluorescent protein‐labeled bacteria, Pseudomonas fluorescens. Bees acquired 1% of a flower's microbes and dispersed 31% of acquired microbes to the next flower. All bees acquired microbes, and 85% and 76% of bees dispersed microbes to live and artificial flowers, respectively. Microbes acquired from the corolla were mainly deposited on the corolla, followed by the stamens, and least on the nectary/pistil. Bee foraging behavior affected acquisition, with scrabbling for pollen resulting in 23% more microbes acquired than nectaring, and with buzzing for pollen resulting in a 79% slower rate of microbial acquisition relative to scrabbling. Bee foraging behavior also affected deposition but depended on the floral organ: Scrabbling and buzzing for pollen led to greater deposition than nectaring for corolla and stamen but not nectary. Our results have implications for transmission of beneficial and pathogenic microbes among plants and pollinators, and thus the ecology and evolution of floral microbial communities.

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“…, Rering et al. , Adler et al. , McFrederick and Rehan , Russell and Ashman ), consequences of pollinator behavior extend beyond plant fertilization to patterns of microbial transmission.…”

Section: Discussionmentioning

confidence: 99%

Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

et al. 2019

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“…, Rering et al. ). Most insect pollinators are well equipped to detect and recognize microbial infestation of food sources (Fouks and Lattorff ), and yeasts have been hypothesized to provide an honest signal (via volatiles) to plant visitors of sugar‐rich microsites (Madden et al.…”

Section: Introductionmentioning

confidence: 99%

“…Bumble bees might preferentially visit yeast‐containing nectar, because they can detect these flowers more easily, or find them more rewarding due to the increased temperature of the nectar (Herrera and Pozo ) or their more complex olfactory display (Rering et al. ).…”

Section: Introductionmentioning

confidence: 99%

The impact of yeast presence in nectar on bumble bee behavior and fitness

Pozo

Kemenade

Oystaeyen³

et al. 2019

Ecological Monographs

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The presence of yeasts in pollen and floral nectar is rather the norm than the exception. Due to the metabolic activities of yeasts, sugar and amino acid composition of nectar often drastically change and may negatively impact the nutritional value of nectar for pollinators and hence insect fitness. On the other hand, the presence of yeasts in floral nectar may also increase its nutritional value due to yeast's probiotic effect and the release of yeast's metabolites. In this study, we investigated whether the presence of defined flower‐ and insect‐associated yeasts affected individual and colony fitness of the bumble bee pollinator Bombus terrestris. Specifically, we tested whether the presence of yeasts in nectar affected bumble bee foraging behavior and nectar consumption, individual growth and colony development, larval and queen mortality, and mating success. Quantitative analyses of sugar and amino acid profiles showed that nectar yeasts significantly affected the chemical composition of nectar. However, dual‐choice experiments indicated that yeast inoculation did not significantly affect foraging behavior or consumption rates. Nest development, on the other hand, was significantly affected by the presence of yeasts, but effects largely depended on species identity, with Candida bombiphila, Metschnikowia gruessii, and Rhodotorula mucilaginosa having the largest positive impact on colony growth. Interestingly, the effects at the colony level were more pronounced than at the individual level. In vitro growth tests further showed that yeasts have the potential to suppress the growth of the bumble bee gut pathogen Crithidia bombi. Overall, these results demonstrate that nectar‐inhabiting yeasts can have diverse effects on bumble bee fitness and therefore may mediate plant–pollinator mutualisms.

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“…Flowers are multi‐purpose reproductive structures and microbial communities of flowers can have a large impact on plant fitness by directly affecting the survival and reproduction of the plant (e.g., Alexander & Antonovics, ), or through effects on pollination (Herrera, Pozo, & Medrano, ; Rering, Beck, Hall, McCartney, & Vannette, ; Schaeffer, Mei, Andicoechea, Manson, & Irwin, ; Schaeffer, Phillips, Duryea, Andicoechea, & Irwin, ; Vannette, Gauthier, & Fukami, ). Understanding microbial community assembly in flowers can highlight important, and underappreciated, ecological processes affecting floral evolution and plant‐pollinator interactions.…”

Section: Introductionmentioning

confidence: 99%

Floral organs act as environmental filters and interact with pollinators to structure the yellow monkeyflower (Mimulus guttatus) floral microbiome

Gómez

Ashman

2019

Molecular Ecology

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Assembly of microbial communities is the result of neutral and selective processes. However, the relative importance of these processes is still debated. Microbial communities of flowers, in particular, have gained recent attention because of their potential impact to plant fitness and plant‐pollinator interactions. However, the role of selection and dispersal in the assembly of these communities remains poorly understood. Here, we evaluated the role of pollinator‐mediated dispersal on the contribution of neutral and selective processes in the assembly of floral microbiomes of the yellow monkeyflower (Mimulus guttatus). We sampled floral organs from flowers in the presence and absence of pollinators within five different serpentine seeps in CA and obtained 16S amplicon data on the epiphytic bacterial communities. Consistent with strong microenvironment selection within flowers we observed significant differences in community composition across floral organs and only a small effect of geographic distance. Pollinator exposure affected the contribution of environmental selection and depended on the rate and intimacy of interactions with flower visitors. This study provides evidence of the importance of dispersal and within‐flower heterogeneity in shaping epiphytic bacterial communities of flowers, and highlights the complex interplay between pollinator behaviour, environmental selection and additional abiotic factors in shaping the epiphytic bacterial communities of flowers.

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Nectar‐inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator

Cited by 181 publications

References 69 publications

Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

The impact of yeast presence in nectar on bumble bee behavior and fitness

Floral organs act as environmental filters and interact with pollinators to structure the yellow monkeyflower (Mimulus guttatus) floral microbiome

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