Flowers as viral hot spots: Honey bees (Apis mellifera) unevenly deposit viruses across plant species

Abstract

RNA viruses, once considered specific to honey bees, are suspected of spilling over from managed bees into wild pollinators; however, transmission routes are largely unknown. A widely accepted yet untested hypothesis states that flowers serve as bridges in the transmission of viruses between bees. Here, using a series of controlled experiments with captive bee colonies, we examined the role of flowers in bee virus transmission. We first examined if honey bees deposit viruses on flowers and whether bumble bees become infected after visiting contaminated flowers. We then examined whether plant species differ in their propensity to harbor viruses and if bee visitation rates increase the likelihood of virus deposition on flowers. Our experiment demonstrated, for the first time, that honey bees deposit viruses on flowers. However, the two viruses we examined, black queen cell virus (BQCV) and deformed wing virus (DWV), were not equally distributed across plant species, suggesting that differences in floral traits, virus ecology and/or foraging behavior may mediate the likelihood of deposition. Bumble bees did not become infected after visiting flowers previously visited by honey bees suggesting that transmission via flowers may be a rare occurrence and contingent on multiplicative factors and probabilities such as infectivity of virus strain across bee species, immunocompetence, virus virulence, virus load, and the probability a bumble bee will contact a virus particle on a flower. Our study is among the first to experimentally examine the role of flowers in bee virus transmission and uncovers promising avenues for future research.

Experimental infection of bumblebees with honeybee-associated viruses: no direct fitness costs but potential future threats to novel wild bee hosts

“…BQCV, DWV-A and DWV-B have been frequently detected in bumblebees (Bombus spp. ; [19,24,26,27,29,39,40] and other wild bee species collected from the field (reviewed in [25]), as well as in other insect species associated with honeybees or the flowers they visit (e.g. [54][55][56][57][58]).…”

“…are widespread wild bee species in northern temperate regions [36], yet many are decreasing in abundance or distribution, with parasites being a potential cause of their decline [37,38]. BQCV is the most prevalent virus in bumblebees [24,26,29,30], it exhibits broad tissue tropism in the American Bombus huntii [39,40], and its prevalence in Bombus spp. covaries with that in Apis.…”

Bee Viruses: Routes of Infection in Hymenoptera

“…Although no study to date has reported the presence of viruses in the feces of non-Apis species, one could expect that virus particles are shed via the feces, similar to how this happens in honey bees. Several studies have directly identified the role of shared flowers in the transmission of a number of bee pathogens, including viruses (Singh et al, 2010;Graystock et al, 2015;Adler et al, 2018;Alger et al, 2019). Therefore, infected bees visiting flowers can contaminate the flower surface, nectar and pollen with virus particles they shed via their feces.…”

“…Eusocial non-Apis species belong to the tribes Meliponini (stingless bees) and Bombini (bumble bees). Both tribes have a social structure similar to honey bees, with a single reproductive (Singh et al, 2010;Alger et al, 2019), depicted in the middle surrounded by a red dotted line. Inter-and intra-species transmission in non-social bees, depicted on the left side can occur through contact at nest aggregations or the reuse of virus-contaminated old nest cavities (Krunicì and Stanisavljevicì, 2006).…”

Mode of Transmission Determines the Virulence of Black Queen Cell Virus in Adult Honey Bees, Posing a Future Threat to Bees and Apiculture

“…One of the most prevalent honey bee viruses is Black queen cell virus (BQCV) [32][33][34], so-called because it kills developing queen honey bee larvae, whose necrotic remains blacken their pupal cells [35][36][37]. Nurse honey bees horizontally transfer BQCV from infected cells to healthy larvae in brood food [38], and queens may also vertically transmit it to eggs [9].…”