Viruses occupy a large proportion of the pathogen communities within honey bee colonies, with more than 80 species detected in Apis mellifera. Honey bee viruses are globally distributed and several species have been linked to honey bee diseases that threaten colony health. However, less is known about the ecology and epidemiology of viruses within honey bee colonies, and in particular whether a link exists between virus temporal dynamics and seasonal variations and/or colony dynamics. Using a large-scale longitudinal survey conducted over three years, we report the prevalence and abundance of deformed wing virus, acute bee paralysis virus, black queen cell virus, chronic bee paralysis virus and sacbrood virus (DWV, ABPV complex, BQCV, CBPV and SBV) in more than 300 colonies located in two different environments of southern Europe (Provence in France, Piemonte in Italy), and exhibiting contrasted climatic conditions. Monthly measurements performed throughout the beekeeping seasons indicate distinct seasonal trends in prevalence and abundance of the five virus species: DWV, SBV and ABPV complex displayed marked seasonal variations, that were similar in both environments tested. We also highlight the link between seasonal virus dynamics and colony dynamics for SBV/BQCV, and parasite dynamics for DWV. This study improves our understanding of virus ecology within honey bee colonies.

Within the context of climate change, winter temperatures at high latitudes are predicted to rise faster than summer temperatures. This phenomenon is expected to negatively affect the diapause performance and survival of insects, since they largely rely on low temperatures to lower their metabolism and preserve energy. However, some insects like honeybees, remain relatively active during the winter and elevate their metabolic rate to produce endothermic heat when temperatures drop. Warming winters are thus expected to improve overwintering performance of honeybees. In order to verify this hypothesis, for two consecutive years, we exposed honeybee colonies to either a mild or cold winter. We then monitored the influence of wintering conditions on several parameters of honeybee overwintering physiology, such as levels of the cryoprotectant glycerol, expression levels of immune and antioxidant genes, and genes encoding multifunctional proteins, including vitellogenin, which promotes bee longevity. Winter conditions had no effect on the expression of antioxidant genes, and genes related to immunity were not consistently affected. However, mild winters were consistently associated with a lower investment in glycerol synthesis and a higher expression of fat body genes, especially apidaecin and vitellogenin. Finally, while we found that viral loads generally decreased through the winter, this trend was more pronounced under mild winter conditions. In conclusion, and without considering how warming temperatures might affect other aspects of honeybee biology before overwintering, our data suggest that warming temperatures will likely benefit honeybee vitality by notably reducing their viral loads over the winter.

Many of the physiological traits in insects are shaped by environmental temperatures, which can influence their interactions with pathogens. Therefore, quantifying the thermal responses of the host-pathogen system is crucial for better understanding and predicting their dynamics due to environmental changes. This is particularly important in honey bees, which are experiencing severe colony losses around the world, notably due to infection with the Deformed wing virus (DWV). To investigate the influence of temperature on the honey bee/DWV relationship we exposed adult bees to low or high temperatures and determined the effects on viral titers and bee survival. Emerging bees naturally infected with DWV were reared in vitro at different temperatures ranging from 15 degrees C to 37 degrees C. In addition, some bees reared at 37 degrees C were exposed daily to acute heat treatments (40 and 43 degrees C). High temperatures significantly decreased DWV titers close to the initial viral load at emergence but increased bee mortality. The lowest temperature resulted in higher mortality, but virus load was not significantly impacted. In conclusion, our results indicate that temperature could contribute to seasonal variations in viral loads but do not suggest temperature to be used as a tool to eliminate viruses, even given that high temperatures limit viral multiplication.

Honeybee colonies are increasingly exposed to environmental stress factors, which can lead to their decline or failure. However, there are major gaps in stressor risk assessment due to the difficulty of assessing the honeybee colony state and detecting abnormal events. Since stress factors usually induce a demographic disturbance in the colony (e.g. loss of foragers, early transition from nurse to forager state), we suggest that disturbances could be revealed indirectly by measuring the age- and task-related physiological state of bees, which can be referred to as biological age (an indicator of the changes in physiological state that occur throughout an individual lifespan). We therefore estimated the biological age of bees from the relationship between age and biomarkers of task specialization (vitellogenin and the adipokinetic hormone receptor). This relationship was determined from a calibrated sample set of known-age bees and mathematically modelled for biological age prediction. Then, we determined throughout the foraging season the evolution of the biological age of bees from colonies with low (conventional apiary) or high Varroa destructor infestation rates (organic apiary). We found that the biological age of bees from the conventional apiary progressively decreased from the spring (17 days) to the fall (6 days). However, in colonies from the organic apiary, the population aged from spring (13 days) to summer (18.5 days) and then rejuvenated in the fall (13 days) after Varroa treatment. Biological age was positively correlated with the amount of brood (open and closed cells) in the apiary with low Varroa pressure, and negatively correlated with Varroa infestation level in the apiary with high Varroa pressure. Altogether, these results show that the estimation of biological age is a useful and effective method for assessing colony demographic state and likely detrimental effects of stress factors.

Since climate change is expected to bring more severe and frequent extreme weather events such as heat waves, assessing the physiological and behavioural sensitivity of organisms to temperature becomes a priority. We therefore investigated the responses of honeybees, an important insect pollinator, to simulated heat waves (SHW). Honeybees are known to maintain strict brood thermoregulation, but the consequences at the colony and individual levels remain poorly understood. For the first time, we quantified and modelled colony real-time activity and found a 70% increase in foraging activity with SHW, which was likely due to the recruitment of previously inactive bees. Pollen and nectar foraging was not impacted, but an increase in water foragers was observed at the expense of empty bees. Contrary to individual energetic resources, vitellogenin levels increased with SHW, probably to protect bees against oxidative stress. Finally, though immune functions were not altered, we observed a significant decrease in deformed wing virus loads with SHW. In conclusion, we demonstrated that honeybees could remarkably adapt to heat waves without a cost at the individual level and on resource flow. However, the recruitment of backup foraging forces might be costly by lowering the colony buffering capacity against additional environmental pressures.

The prevalence of viruses in honey bee colonies can present seasonal variations. However, little is known about the effect of temperature on virus titers. Since in some organisms different viruses can be affected by high t emperatures, we tested whether increased rearing temperatures had an effect on virus titers in adult bees.