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.