There is clear evidence for sublethal effects of neonicotinoid insecticides on non-target ecosystem service-providing insects. However, their possible impact on male insect reproduction is currently unknown, despite the key role of sex. Here, we show that two neonicotinoids (4.5 ppb thiamethoxam and 1.5 ppb clothianidin) significantly reduce the reproductive capacity of male honeybees (drones), Apis mellifera. Drones were obtained from colonies exposed to the neonicotinoid insecticides or controls, and subsequently maintained in laboratory cages until they reached sexual maturity. While no significant effects were observed for male teneral (newly emerged adult) body mass and sperm quantity, the data clearly showed reduced drone lifespan, as well as reduced sperm viability (percentage living versus dead) and living sperm quantity by 39%. Our results demonstrate for the first time that neonicotinoid insecticides can negatively affect male insect reproductive capacity, and provide a possible mechanistic explanation for managed honeybee queen failure and wild insect pollinator decline. The widespread prophylactic use of neonicotinoids may have previously overlooked inadvertent contraceptive effects on non-target insects, thereby limiting conservation efforts.

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Reproductive strategies can act as strong selective forces on reproductive traits of male insects, resulting in species-specific variation in sperm quantity and viability. For solitary bees, basic measures of sperm quantity and viability are scarce. Here we evaluated for the first time quantity and viability of sperm in male Osmia cornuta solitary bees at different times after emergence, and how they were affected by male body mass and environmental condition (laboratory or semi-field arena). Sperm viability immediately after adult emergence showed no significant difference compared to four day old individuals, suggesting that O . cornuta males are capable of mating immediately post emergence. However, sperm counts were significantly higher in four day old individuals from the semi-field arena when compared to newly emerged males. This might reflect a final phase of sperm maturation. Regardless of individual male age and body mass differences, O . cornuta males produced on average ~175’000 spermatozoa that were ~65% viable, which are both significantly lower compared to eusocial honeybees and bumblebees. Moreover, sperm quantity, but not viability, was positively correlated with male body mass four days after emergence, while no such relationship was detected immediately after emergence. Even though individuals maintained in semi-field conditions exhibited a significantly greater loss of body mass, experimental arena had no significant effect on male survival, sperm quality or total living sperm produced. This suggests that the proposed laboratory design provides a cost-efficient and simple experimental approach to assess sperm traits in solitary bees. In conclusion, our data suggest a reduced investment in both sperm quantity and quality by male O . cornuta , which appears to be adaptive in light of the life history of this solitary bee.