Species traits, landscape quality and floral resource overlap with honeybees determine virus transmission in plant-pollinator networks

Abstract

Emerging infectious diseases pose a threat to pollinators. Virus transmission among pollinators via flowers may be reinforced by anthropogenic land-use change and concomitant alteration of plant–pollinator interactions. Here, we examine how species’ traits and roles in flower-visitation networks and landscape-scale factors drive key honeybee viruses—black queen cell virus (BQCV) and deformed wing virus—in 19 wild bee and hoverfly species, across 12 landscapes varying in pollinator-friendly (flower-rich) habitat. Viral loads were on average more than ten times higher in managed honeybees than in wild pollinators. Viral loads in wild pollinators were higher when floral resource use overlapped with honeybees, suggesting these as reservoir hosts, and increased with pollinator abundance and viral loads in honeybees. Viral prevalence decreased with the amount of pollinator-friendly habitat in a landscape, which was partly driven by reduced floral resource overlap with honeybees. Black queen cell virus loads decreased with a wild pollinator’s centrality in the network and the proportion of visited dish-shaped flowers. Our findings highlight the complex interplay of resource overlap with honeybees, species traits and roles in flower-visitation networks and flower-rich pollinator habitat shaping virus transmission.