Resident viruses, but not honeybee-associated viruses, impair solitary bee fitness in the field

Viruses can impact individual host fitness and host population dynamics, especially following viral host shifts. The decline of bee populations over the last decades may be linked to viruses spilling over from honeybees. However, evidence for the impact of spillover or resident viruses on solitary bee fitness remains scarce. Here, by assessing solitary bee (Osmia cornuta) foraging, offspring sex ratio, survival, and body mass across seven locations in northern Switzerland, we show that resident viruses – but not honeybee-associated viruses –impact tokens of fitness in the field. Viral loads of Osmia-resident Ganda bee virus (GABV) and Scaldis River bee virus (SRBV), honeybee-associated viruses (black queen cell virus (BQCV) and deformed wing virus B (DWV-B) were quantified in foraging females. Prevalence and loads of GABV and SRBV were higher than BQCV and DWV-B. Further, females with high SRBV or GABV loads had reduced offspring survival or lower male offspring body mass, respectively, while honeybee-associated viruses had no impact on tokens of O. cornuta fitness. We demonstrate that viruses can negatively affect solitary bee fitness, but the degree of impact seems to vary with viral type. This calls for further research to unravel the dynamics of multi-host pathogens in pollinator communities.

Methods
Solitary bee Osmia cornuta trap nests were placed in seven apple orchards in northern Switzerland and supplied with O. cornuta cocoons at the time when the apple started blooming. To track individual O. cornuta female nesting activity, foraging performance and different aspects of reproductive success (survival, sex ratio, and body mass of offspring), we individually tagged females, videoed their foraging activity at their individual nests and used machine learning-based software for automated analysis of the videos ("Bee Tracker", Knauer et al. 2022, doi:10.1002/ece3.8575). After video recording at all sites was completed (12 days after the confirmed start of nesting), we collected all tagged females at night when the females were resting in their nests and freeze-killed the bees for later analysis of viruses. After overwintering, each offspring (cocoon) of an identified nest from a tagged female was transferred into a separate labelled 2-mL Eppendorf® tube with a small hole to allow air exchange. We recorded whether or not the offspring successfully hatched (survival, i.e., alive vs. dead), determined its sex morphologically (i.e., female or male), and measured its body mass (in mg). From the videos, we further extracted the foraging trip duration of the tagged females (in min).