Bioindication of radioactive contamination by honey bees in the Bryansk and Rostov regions: Foraging dynamics of 137Cs and 40K in the plant–bee–bee product pathway

Although some studies have investigated the accumulation of radionuclides in honey, other bee products such as wax and bee bread remain insufficiently studied, particularly in terms of seasonal and intra-seasonal dynamics. Spatial patterns of contamination within the foraging area of honey bees, as well as the role of botanical composition of nectar sources, also remain poorly understood. This study examines the dynamics of ¹³⁷Cs and ⁴⁰K accumulation along the pathway plant-bee-bee product on radioactively contaminated territories in the Bryansk Region during different periods of the honey flow. The results are compared with data collected at low-contamination sites in the Rostov Region. Samples of honey, capping wax, and nectariferous plants were collected in the villages of Vereshchaki and Katichi (Bryansk Region), as well as in the stanitsa of Vyoshenskaya (Rostov Region). The equivalent gamma-dose rate was also measured in the vicinity of the Bryansk apiaries. The activity concentrations of ¹³⁷Cs and ⁴⁰K in plants and bee products were determined using gamma spectrometry. Statistically significant differences in the activity concentration of ¹³⁷Cs in honey samples from the Bryansk and Rostov regions were identified during different phases of the honey flow. In honey collected from contaminated areas (soil contamination density of ¹³⁷Cs ranging from 185 to 555 kBq/m²), the mean activity concentration of ¹³⁷Cs was 44 ± 24 Bq/kg (range: 21-89 Bq/kg), significantly exceeding that of the control group. In capping wax, the mean activity concentration reached 56 ± 33 Bq/kg (range: 29-115 Bq/kg). Pollen analysis and direct foraging tracking linked notably elevated ¹³⁷Cs activity concentrations in honey to nectar from Brassica spp. (rapeseed, field mustard), Phacelia tanacetifolia, Melilotus spp. (white/yellow sweet clover), Trifolium spp. (white/yellow clover), Centaurea spp. (cornflower, false-phrygian knapweed), Symphytum officinale (common comfrey), Filipendula ulmaria (meadowsweet), Calluna vulgaris (common heather), and Solidago virgaurea (European goldenrod), indicating the species-specific ability of these plants to accumulate radiocaesium and their potential as bioindicators of localized contamination hotspots. No statistically significant differences in the activity concentrations of ⁴⁰K in honey were observed between the regions. Higher variability and greater accumulation of radionuclides were found in capping wax compared to honey, likely due to biophysical filtration processes and differences in the physicochemical properties of honey and wax matrices. Transfer factors for ¹³⁷Cs and ⁴⁰K along the pathway nectariferous plant-honey/wax were calculated. For ¹³⁷Cs, arithmetic mean activity concentrations were used in the control group (homogeneous contamination), while weighted means were applied in the experimental groups (heterogeneous contamination) to account for spatial variability. A marked difference was found in ¹³⁷Cs concentrations in plants between the experimental groups (237 Bq/kg) and the control group (45 Bq/kg), while the transfer factors for ¹³⁷Cs remained consistent: 0.16-0.19 for honey and 0.24-0.44 for wax, suggesting the stability of these indicators under varying contamination conditions. The weighting of plant sample contributions was based on a digital area estimation of bee foraging zones, using pixel-wise analysis of masked regions on satellite imagery. Transfer factors for ⁴⁰K were calculated using pooled samples due to its uniform distribution across all settlements, yielding values of 0.05 for honey and 0.19 for wax. Partitioning analysis in a modern hive system was conducted, reflecting the mass-based distribution of radionuclides within the trophic system of honey bees. These results advance understanding of radionuclide distribution in agroecosystems and confirm the effectiveness of using honey bees and bee products as bioindicators of radioactive contamination across territories with both high and low contamination densities.