An invasive ant increases deformed wing virus loads in honey bees

Abstract

The majority of invasive species are best known for their effects as predators. However, many introduced predators may also be substantial reservoirs for pathogens. Honey bee-associated viruses are found in various arthropod species including invasive ants. We examined how the globally invasive Argentine ant ( Linepithema humile ), which can reach high densities and infest beehives, is associated with pathogen dynamics in honey bees. Viral loads of deformed wing virus (DWV), which has been linked to millions of beehive deaths around the globe, and black queen cell virus significantly increased in bees when invasive ants were present. Microsporidian and trypanosomatid infections, which are more bee-specific, were not affected by ant invasion. The bee virome in autumn revealed that DWV was the predominant virus with the highest infection levels and that no ant-associated viruses were infecting bees. Viral spillback from ants could increase infections in bees. In addition, ant attacks could pose a significant stressor to bee colonies that may affect virus susceptibility. These viral dynamics are a hidden effect of ant pests, which could have a significant impact on disease emergence in this economically important pollinator. Our study highlights a perhaps overlooked effect of species invasions: changes in pathogen dynamics.

Variable viral loads and immune response in an invasive ant's native and introduced ranges

“…Interestingly, some of the viruses present in high loads in some regions were detected, but were also less prevalent in other regions. Variations in infection patterns could be due to interactions within the pathogen communities (Lester et al., 2019; Viljakainen, Holmberg, et al., 2018), host social environment (Viljakainen, Jurvansuu, et al., 2018) or wider ecosystem interactions such as proximity with other host species as previously shown in Argentine ants (Dobelmann et al., 2020, 2023). Prospecting for natural enemies of invasive species has proven to be a promising tool to control the red imported fire ant, Solenopsis invicta (Oi et al., 2015; Valles et al., 2018), and the viruses we found in high loads might be associated with previously observed population declines (Cooling et al., 2012) and candidates to further investigate as potential biological control for the Argentine ant.…”

“…Social network plasticity is an effective component of social immunity (Stroeymeyt et al., 2018) and the Argentine ant does form large networks of nests, allowing for a high degree of plasticity. Furthermore, Argentine ants also carry viruses that can infect other insects (Baty et al., 2020; Dobelmann et al., 2020; Sébastien et al., 2015) and have been shown to be associated with elevated viral loads in cohabiting honey bees (Dobelmann et al., 2023). Interestingly, a recent study comparing viral communities in three sympatric ant species showed increased diversity and abundance in introduced species, including L. humile , which exhibited highest diversity, loads and overlap with other species (Viljakainen et al., 2023).…”