Condition-dependent virulence of slow bee paralysis virus in Bombus terrestris: are the impacts of honeybee viruses in wild pollinators underestimated?

Abstract

Slow bee paralysis virus (SBPV)—previously considered an obligate honeybee disease—is now known to be prevalent in bumblebee species. SBPV is highly virulent in honeybees in association with Varroa mites, but has been considered relatively benign otherwise. However, condition-dependent pathogens can appear asymptomatic under good, resource abundant conditions, and negative impacts on host fitness may only become apparent when under stressful or resource-limited conditions. We tested whether SBPV expresses condition-dependent virulence in its bumblebee host, Bombus terrestris, by orally inoculating bees with SBPV and recording longevity under satiated and starvation conditions. SBPV infection resulted in significant virulence under starvation conditions, with infected bees 1.6 times more likely to die at any given time point (a median of 2.3 h earlier than uninfected bees), whereas there was no effect under satiated conditions. This demonstrates clear condition-dependent virulence for SBPV in B. terrestris. Infections that appear asymptomatic in non-stressful laboratory assays may nevertheless have significant impacts under natural conditions in the wild. For multi-host pathogens such as SBPV, the use of sentinel host species in laboratory assays may further lead to the underestimation of pathogen impacts on other species in nature. In this case the impact of ‘honeybee viruses’ on wild pollinators may be underestimated, with detrimental effects on conservation and food security. Our results highlight the importance of multiple assays and multiple host species when testing for virulence, in order for laboratory studies to accurately inform conservation policy and mitigate disease impacts in wild pollinators.Electronic supplementary materialThe online version of this article (doi:10.1007/s00442-017-3851-2) contains supplementary material, which is available to authorized users.

Evidence for and against deformed wing virus spillover from honey bees to bumble bees: a reverse genetic analysis

“…For example, exposure to clothianidin-a neonicotinoid insecticide-was found to have a negative impact on honey bee immune status and promote DWV infection 54 . In Bombus terrestris condition mediated virulence of Slow bee paralysis virus upon starvation has been demonstrated 55 . Our study uses a reverse genetic approach to investigate pathogen spillover from honey bees to bumble bees.…”

Bumble bees in landscapes with abundant floral resources have lower pathogen loads

“…For example, honey bees fed diets lacking pollen had higher loads of viruses 21 and diets with low pollen species diversity increased honey bee mortality when bees were infected with Vairimorpha 22 . Caged bumble bees ( B. terrestris ) exhibited increased mortality from viruses only if starved 23 . Nutritional deprivation is likely to act through altering immune function, as immune genes are more highly expressed when forage is abundant 24 .…”

Exposure of Larvae of the Solitary Bee Osmia bicornis to the Honey Bee Pathogen Nosema ceranae Affects Life History

“…Bee population declines have been reported globally [2,4,5,6,7,8,9,10,11,12,13]. Causes for decline include land use changes, habitat loss, and fragmentation [14], pesticide use [15,16,17], pathogens, climate change, invasive species [12,18,19,20], or the interaction of several factors [18,21,22,23,24,25,26,27]. The importance and effectiveness of wild bee pollinators has increasingly been acknowledged in recent years [28].…”