Nosema ceranae, Fipronil and their combination compromise honey bee reproduction via changes in male physiology

Abstract

The honey bee is threatened by biological agents and pesticides that can act in combination to induce synergistic effects on its physiology and lifespan. The synergistic effects of a parasite/pesticide combination have been demonstrated on workers and queens, but no studies have been performed on drones despite their essential contribution to colony sustainability by providing semen diversity and quality. The effects of the Nosema ceranae/fipronil combination on the life traits and physiology of mature drones were examined following exposure under semi-field conditions. The results showed that the microsporidia alone induced moderate and localized effects in the midgut, whereas fipronil alone induced moderate and generalized effects. The parasite/insecticide combination drastically affected both physiology and survival, exhibiting an important and significant generalized action that could jeopardize mating success. In terms of fertility, semen was strongly impacted regardless of stressor, suggesting that drone reproductive functions are very sensitive to stress factors. These findings suggest that drone health and fertility impairment might contribute to poorly mated queens, leading to the storage of poor quality semen and poor spermathecae diversity. Thus, the queens failures observed in recent years might result from the continuous exposure of drones to multiple environmental stressors.

Factors affecting the reproductive health of honey bee (Apis mellifera) drones—a review

“…Similar results were obtained for drones reared in laboratory conditions following exposure to fipronil in the sugar syrup, which experienced significantly lower sperm viability and concentration (Kairo et al 2017a). Interestingly, the same research group found that fipronil interacts with the microsporidian parasite Nosema ceranae and their interaction causes lower drone sperm viability and antioxidant activity compared to untreated drones (Kairo et al 2017b).…”

Non-detection of honeybee hive contamination following Vespula wasp baiting with protein containing fipronil

“…Second, residual wasp bait that is not taken by pest wasps becomes a dry solid within 3 days and is removed from the bait stations after 3–8 days without replacement. Consequently, the environmental exposure of bee colonies to the toxicant (or its environmental or metabolic breakdown products) and the period over which they could develop sub-lethal effects is shorter than indicated by published toxicity tests [ 36 , 40 , 52 – 53 ], although even brief periods of exposure can result in subtle sub-lethal effects with both immediate and delayed effects.…”

Understanding the Effects of Sublethal Pesticide Exposure on Honey Bees: A Role for Probiotics as Mediators of Environmental Stress

“…Drones are also affected by pesticides. Sublethal concentrations of neonicotinoids and phenylpyrazoles can reduce sperm viability (Kairo et al, 2016(Kairo et al, , 2017aStraub et al, 2016), which can hamper fertilization of queens and the production of diploid workers. Together, reduced sperm transfer and fertilization may limit the production of a genetically diverse workforce, which may compromise the division of labour (Jones et al, 2004) and response to disease (Sherman et al, 1988).…”