Interactions of husbandry, landscape, and immunity in regulating viral loads for managed honey bees

The western honey bee, Apis mellifera, continues to experience widespread die-offs that threaten their critical ecological and agricultural roles. Given the recognized impact of viruses on the increased mortality rates, it is imperative to understand the forces shaping viral infections. In this study, we explore how hive husbandry, landscape, and immunity influence viral loads in managed bees. We characterized 43 apiaries across Central Florida for eight husbandry interventions, five landscape variables, transcription of four immune genes, and infection intensities of four viruses: Black Queen cell virus (BQCV), deformed wing virus type A (DWV-A), Lake Sinai virus (LSV-2), and Israeli acute paralysis virus (IAPV). We found that colonies surrounded by more floral resources and fresh water bodies were associated with increased viral loads and increased viral coinfections. We speculate that increased floral resources increased pollinator abundance, thereby increasing transmission rates and viral richness. We further speculate that increased open water similarly increased pollinator abundance and/or exposure to immunity-altering pesticides. Last, we show that husbandry interventions aimed at reducing Varroa destructor mites can have positive and negative off-target viral impacts. Our data underscore the importance of landscape, immunity, and husbandry in honey bee disease dynamics and highlight the complexity of their interactions.