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

Abstract

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.

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

“…Despite the fact that medium and large bees (the most common pollinators in our observations) can travel large distances (on the scale of kilometers), they tend to visit more nearby flowers in a single trip (Brunet, Zhao, & Clayton, ; Castilla et al, ). Moreover, controlled experiments in the laboratory have shown that bees tend to collect only a small fraction of the whole flower microbiome in a visit, but they deposit most of the bacteria in their next visits (Russell et al, ). This is consistent with our data, where pollinators probably introduced new taxa in the local environments without affecting overall diversity.…”

“…Each floral organ is likely to create unique conditions for the establishment of bacteria (Aleklett, Hart, & Shade, 2014;Junker & Keller, 2015). Pollinators that transport microbes have different behaviours on flowers and could create varying opportunities for contact with floral structures (Laverty & Plowright, 1988;Russell, Rebolleda-Gómez, Shaible, & Ashman, 2019). Yet we have a poor understanding of the extent to which floral organs and their interaction with pollinators creates heterogeneity in microbial communities within flowers.…”

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

“…Pollinators that transport microbes have different behaviors on flowers and could create varying 49 opportunities for contact with floral structures (Laverty & Plowright 1988;Russell et al 2019). 50…”

“…pollinators are likely to have sustained engagement with the stamens and alter the microbial 513 environment of these organs by removing pollen. In a recent paper, Russell et al (2019) showed 514 that in flowers of M. guttaus scrabbling (one of the common behaviors to forage pollen in bees) 515 results in a larger deposition of microbes than other behaviors, and in artificial flowers this 516 behavior leads to the largest deposition of bacteria on the stamen. Here, we showed that 517 differences in bacterial community composition in the stamens across pollinator treatments 518 increased with increased pollination rates.…”

Towards a better understanding of the role of nectar-inhabiting yeasts in plant–animal interactions

“…to feed on nectar, seek shelter or use these as mating/nesting places), pollen can get attached to their body surfaces and subsequently be spread to new flowers [1,4]. Pollinators and non-pollinating visitors are not sterile but carry diverse microbial communities, particularly consisting of bacteria and fungi, that may disperse to nectar and the surface of other floral parts such as the corolla, stamens, and pistil when visiting flowers [5][6][7][8][9][10][11]. The dispersal of microbes from flower to flower by animal vectors is a dynamic process that keeps ongoing during the flower lifetime [6,9,10].…”