Exosymbiotic microbes within fermented pollen provisions are as important for the development of solitary bees as the pollen itself

Abstract

Developing bees derive significant benefits from the microbes present within their guts and fermenting pollen provisions. External microbial symbionts (exosymbionts) associated with larval diets may be particularly important for solitary bees that suffer reduced fitness when denied microbe‐colonized pollen. To investigate whether this phenomenon is generalizable across foraging strategy, we examined the effects of exosymbiont presence/absence across two solitary bee species, a pollen specialist and generalist. Larvae from each species were reared on either microbe‐rich natural or microbe‐deficient sterilized pollen provisions allocated by a female forager belonging to their own species (conspecific‐sourced pollen) or that of another species (heterospecific‐sourced pollen). Our results reveal that the presence of pollen‐associated microbes was critical for the survival of both the generalist and specialist larvae, regardless of whether the pollen was sourced from a conspecific or heterospecific forager. Given the positive effects of exosymbiotic microbes for larval fitness, we then examined if the magnitude of this benefit varied based on whether the microbes were provisioned by a conspecific forager (the mother bee) or a heterospecific forager. In this second study, generalist larvae were reared only on microbe‐rich pollen provisions, but importantly, the sources (conspecific versus heterospecific) of the microbes and pollen were experimentally manipulated. Bee fitness metrics indicated that microbial and pollen sourcing both had significant impacts on larval performance, and the effect sizes of each were similar. Moreover, the effects of conspecific‐sourced microbes and conspecific‐sourced pollen were strongly positive, while that of heterospecific‐sourced microbes and heterospecific‐sourced pollen, strongly negative. Our findings imply that not only is the presence of exosymbionts critical for both specialist and generalist solitary bees, but more notably, that the composition of the specific microbial community within larval pollen provisions may be as critical for bee development as the composition of the pollen itself.

Bee microbiomes in a changing climate: investigating the effects of temperature on solitary bee life history and health

“…Although our sterilization method eliminated Arsenophonus and other bacteria from microbe-deficient pollen, larvae reared on sterile provisions had comparable survivorship to bees consuming microbe-rich diets. These results contradict previous research strongly suggesting that larval survivorship depends on the presence of microbes in larval food [12][13][14]. Preliminary data from a recent in vitro study, however, also indicates that provision microbes can have adverse consequences for solitary bee fitness: the addition of Apilactobacillus micheneri (previously Lactobacillus) in the diet of megachilid larvae increased mortality [79], an unexpected result given the frequent detection in solitary bees [66,80,81] and known functions of lactobacilli in eusocial bees (e.g., preventing the spoilage of stored pollen and defense against pathogens) [82,83].…”

“…We also found contradictory evidence regarding the importance of the provision microbiota for larval health: immature bees reared on pollen without microbes weighed more than those feeding on microbe-rich provisions. Past studies found that larvae acquire fatty and amino acids from microbial prey within provisions, resulting in heavier bees than those reared on sterile pollen [12][13][14]. These opposing results may be explained by differences in pollen sterilization methods: in choice assays, EO exposure does not affect the palatability of pollen to bumblebees [28], but it is unknown whether soaking provisions in ethanol [12][13][14] affects pollen consumption in solitary bees, perhaps leading to differences in biomass, fat content, and trophic positions.…”

“…Solitary bees are thought to derive benefits from the provision microbiota, either as dietary resources or by pre-digesting pollen [12][13][14]16]. Differences in thermal optima between larvae and symbionts have unknown consequences for developing solitary bees.…”

“…Past studies found that larvae acquire fatty and amino acids from microbial prey within provisions, resulting in heavier bees than those reared on sterile pollen [12][13][14]. These opposing results may be explained by differences in pollen sterilization methods: in choice assays, EO exposure does not affect the palatability of pollen to bumblebees [28], but it is unknown whether soaking provisions in ethanol [12][13][14] affects pollen consumption in solitary bees, perhaps leading to differences in biomass, fat content, and trophic positions. Of note, while not statistically significant, bumblebees consumed less pollen per day when fed EO exposed pollen compared to the no treatment control [28].…”

Microbiome and floral associations of a wild bee using biodiversity survey collections

“…Removing these symbionts can lead to dysbiosis, the lack of beneficial relationships between microbes and their host (Belizário & Faintuch, 2018; Ye et al, 2021). With their absence potentially resulting in declines in growth rate, survivorship, and fitness (Dharampal et al, 2019, 2020, 2022), fostering beneficial microbial communities is one method to support bee health.…”