Associations Between Land Use, Climate, and Pathogen Prevalence in Honey Bee Colonies

Honey bees (Apis mellifera) are key pollinators in agricultural ecosystems that face increasing pressure from pathogens and environmental change. However, how these environmental factors interact remains incompletely understood. To assess associations between climate, landscape composition, and pathogen occurrence in real agroecosystems, we monitored honey bee colonies across 30 apiaries in southern Italy over two years, in summer and autumn. Molecular screening revealed widespread multi-pathogen exposure, with two viruses, Black Queen Cell Virus (BQCV) and Deformed Wing Virus (DWV), and gut trypanosomatid parasite (Lotmaria passim) being the most frequently detected. In contrast, Nosema ceranae, along with Bee Macula-like Virus (BeeMLV) and Acute Bee Paralysis Virus (ABPV), occurred at lower but still notable frequencies. Infections were generally more frequent in adult foragers than in in-hive bees and larvae, and overall pathogen occurrence tended to be higher in summer than in autumn. Higher humidity was associated with higher overall pathogen occurrence and coinfection levels, whereas higher temperature showed a weaker association with these outcomes. Associations between landscape composition and pathogen occurrence differed across pathogens: a higher proportion of semi-natural habitats was associated with lower viral occurrence, particularly BQCV and DWV; however, N. ceranae was more frequently detected under the same landscape conditions. In contrast, L. passim showed context-dependent responses, with landscape effects emerging only through interactions with humidity and temperature. Pathogen coinfections were more occurrent under warm, humid conditions, although this pattern was partially buffered in landscapes richer in semi-natural habitats. Together, these results indicate that, within the studied apiaries, honey bee pathogen occurrence was associated with climate, season, and land use. These findings suggest that environmental context should be considered when interpreting honey bee health monitoring data in heterogeneous agricultural landscapes, with potential implications for apiary management.