Omnivory in bees: Elevated trophic positions among all major bee families

Authors: Steffan, Shawn; GAINES-DAY, HANNAH - University Of Wisconsin; DHARAMPAL, PRARTHANA - University Of Wisconsin; CHIKARAISHI, YOSHITO - Hokkaido University; TAKIZAWA, YUKO - Hokkaido University; DANFORTH, BRYAN - Cornell University

Submitted to: The American Naturalist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/7/2019
Publication Date: 5/15/2019
Citation: Steffan, S.A., Gaines-Day, H.R., Dharampal, P., Chikaraishi, Y., Takizawa, Y., Danforth, B.N. 2019. Omnivory in bees: Elevated trophic positions among all major bee families. The American Naturalist. 194(3). https://doi.org/10.1086/704281.
DOI: https://doi.org/10.1086/704281

Interpretive Summary: The clear pattern of rampant omnivory across all bee families evidenced in this study, potentially reconstructs our current knowledge of the trophic tendencies of this major insect group. Although bees are considered exclusively pollen-eating herbivores, the ubiquity of mutualistic microbes within their pollen provision diet strongly suggests that they consume considerable amounts of microbial protein. Empirical data presented here provides the first quantitative evidence that larval bees obtain significant amounts, if not the majority, of their proteins from microbial meat, rather than plant matter alone. While their diet of both plant and microbe-derived protein makes them omnivores, it would appear that microbes (and not the bees) are the main herbivores in this plant-insect-microbe symbiosis. Impact: Aside from being important dietary components for larval bees, the pollen microbiome performs multiple support services for innumerable native bees, including pollen preservation, and resistance against parasites and pathogens. However, the growing use of fungicides can eliminate key elements of these microbial symbionts, such as yeasts, and in so doing allow pathogenic microbes to infiltrate the unoccupied niches. The adverse effects of such community shifts are exacerbated by the high specificity, and strong dependence of bees on the pollen microbiome. Our work establishes a foundation for future studies looking at how native bee health can be sustained by preserving their microbial symbionts.

Technical Abstract: As pollen- and nectar-foragers, bees have long been considered strictly herbivorous. Their pollen-provisions, however, are host to diverse microbial communities, which develop within the pollen as it is consumed by bee larvae. Among social bee species, pollen-provisions are generally aged 1-4 days before being consumed by larvae, while solitary bees may ferment their pollen-provisions for weeks. In both cases, microbes consume the pollen-provision, converting it into a complex of plant and microbial components. In turn, bee larvae consume the entire pollen complex, including the microbes suffused throughout it, ingesting proteins from both plant and microbial sources. Since microbes are analogous to metazoan consumers within trophic hierarchies, the pollen-eating microbes are, functionally, strict herbivores. Larval bees should register trophically as omnivores when they consume such pollen-microbe complexes. We tested this hypothesis using compound-specific isotopic analysis to measure bee trophic position across all major bee families. Our findings indicated that bee trophic identity was consistently, significantly higher than that of a strict herbivore (trophic level 2.0), providing the first quantitative evidence that omnivory is common among bees, and that microbe-derived protein represents a major component of bee nutrition.