Honey bee colony performance and health are intimately linked to the foraging environment. Recent evidence suggests that the US Conservation Reserve Program (CRP) has a positive impact on environmental suitability for supporting honey bee apiaries. However, relatively little is known about the influence of habitat conservation efforts on honey bee colony health. Identifying specific factors that influence bee health at the colony level incorporates longitudinal monitoring of physiology across diverse environments. Using a pooled-sampling method to overcome individual variation, we monitored colony-level molecular biomarkers during critical pre- and post-winter time points. Major categories of colony health (nutrition, oxidative stress resistance, and immunity) were impacted by apiary site. In general, apiaries within foraging distance of CRP lands showed improved performance and higher gene expression of vitellogenin (vg), a nutritionally regulated protein with central storage and regulatory functions. Mirroring vg levels, gene transcripts encoding antioxidant enzymes and immune-related proteins were typically higher in colonies exposed to CRP environments. Our study highlights the potential of CRP lands to improve pollinator health and the utility of colony-level molecular diagnostics to assess environmental suitability for honey bees.

Carbohydrate-active enzymes play an important role in the honey bee (Apis mellifera) due to its dietary specialization on plant-based nutrition. Secretory glycoside hydrolases (GHs) produced in worker head glands aid in the processing of floral nectar into honey and are expressed in accordance with age-based division of labor. Pollen utilization by the honey bee has been investigated in considerable detail, but little is known about the metabolic fate of indigestible carbohydrates and glycosides in pollen biomass. Here, we demonstrate that pollen consumption stimulates the hydrolysis of sugars that are toxic to the bee (xylose, arabinose, mannose). GHs produced in the head accumulate in the midgut and persist in the hindgut that harbors a core microbial community composed of approximately 10 bacterial cells. Pollen consumption significantly impacted total and specific bacterial abundance in the digestive tract. Bacterial isolates representing major fermentative gut phylotypes exhibited primarily membrane-bound GH activities that may function in tandem with soluble host enzymes retained in the hindgut. Additionally, we found that plant-originating β-galactosidase activity in pollen may be sufficient, in some cases, for probable physiological activity in the gut. These findings emphasize the potential relative contributions of host, bacteria, and pollen enzyme activities to carbohydrate breakdown, which may be tied to gut microbiome dynamics and associated host nutrition.