Bees just wanna have fungi: a review of bee associations with nonpathogenic fungi

Abstract

Bee-fungus associations are common, and while most studies focus on entomopathogens, emerging evidence suggests that bees associate with a variety of symbiotic fungi that can influence bee behavior and health. Here, we review nonpathogenic fungal taxa associated with different bee species and bee-related habitats. We synthesize results of studies examining fungal effects on bee behavior, development, survival, and fitness. We find that fungal communities differ across habitats, with some groups restricted mostly to flowers (Metschnikowia), while others are present almost exclusively in stored provisions (Zygosaccharomyces). Starmerella yeasts are found in multiple habitats in association with many bee species. Bee species differ widely in the abundance and identity of fungi hosted. Functional studies suggest that yeasts affect bee foraging, development, and pathogen interactions, though few bee and fungal taxa have been examined in this context. Rarely, fungi are obligately beneficial symbionts of bees, whereas most are facultative bee associates with unknown or ecologically contextual effects. Fungicides can reduce fungal abundance and alter fungal communities associated with bees, potentially disrupting bee-fungi associations. We recommend that future study focus on fungi associated with non-honeybee species and examine multiple bee life stages to document fungal composition, abundance, and mechanistic effects on bees.

Keywords: Starmerella; Anthophila; microbiome; provision; symbiosis; yeast.

Figure 1.

Occurrence of the top 14 fungal genera associated with bee species represented in this review, including fungi isolated in association with bee bodies or provisions. For each study, the top three fungal genera are represented. Fungal occurrence is represented as presence or absence, and so is biased toward bee species that are overrepresented in studies (Apis mellifera). The number of studies representing each bee species is included following species names.

Figure 2.

Composition of fungal communities associated with different bee habitats, including flowers (whole flowers, pollen, and nectar), bee nest provisions (stored pollen and nectar, propolis, and corbicular pollen), and the bee body [adult (external, whole body, and gastrointestinal tract), larvae, and pupae]. The top 14 fungal genera by frequency of detection are represented.

Figure 3.

Plots showing variation in taxa recovered using different methods in current studies of bee–fungi associations. (A) Number of studies of specific habitats considered in this study in association with bees, (B) number of studies employing various detection and identification methods of fungal communities, and (C) differences in fungal communities across detection methods. Detection methods included are culture-based isolation followed by morphological and physiological identification, culture-based isolation followed by sequencing-based identification, and culture-independent community identification (amplicon sequencing). ‘Other’ detection methods include API test strips, RNA transcriptomics, microscopy, and taxa-specific PCR. The top 14 fungal genera are represented.