Effects of Varroa destructor on Apis mellifera capensis Drone Sperm Quality Characteristics and Colony Demographics

Varroa destructor (V. destructor) threatens honeybee colonies and negatively affects drone weight and survival. Therefore, this mite species poses a risk to the reproductive potential of drones, and subsequently colony health and performance. However, studies on the impact of V. destructor infestation on sperm characteristics are limited, and results appear to be inconclusive. This study aimed to investigate the effect of V. destructor infestation on multiple sperm quality characteristics that are regarded as important for successful fertilization. In this cross-sectional study, conducted in the Western Cape, South Africa, during the summer of 2021, 53 sexually mature Apis mellifera capensis (A.m. capensis) were harvested. Analysis of semen included functional (total motility, progressive motility and swimming speeds; kinematic parameters) and structural sperm parameters (sperm head, tail, total length) using a computer-aided sperm analysis system. Drone weight and demographic information of colonies were also assessed. Three infestation groups were compared, i.e., < 1% (n = 4 colonies) (median: 0.33%; range: 0.00-0.40%), 1%-2% (n = 2 colonies) (median: 1.07%; range: 1.00%-1.45%) and 10% (n = 2 colonies) (10.0% ± 0.00%). In this study, V. destructor infestation had minor, non-significant effects on drone weight (11% lower in highly infested drones; p = 0.123) and sperm concentration (p = 0.064). Sperm motility was, however, significantly affected by infestation levels, with the least infected drones producing sperm with significantly higher total motility (99.1% vs. 83.9% and 68.2%; p = 0.002), progressiveness, swimming speed and kinematics (VCL, VSL, VAP; p < 0.001). Sperm vitality was not affected by V. destructor infestation (p = 0.559). Infestation altered sperm structure with drones from highly infected colonies producing significantly longer sperm (tail: 227 ± 1.22 μm vs. 224 ± 2.31 μm; total length: 236 ± 1.23 μm vs. 233 ± 2.16 μm; p < 0.001). Furthermore, significant relationships were observed between V. destructor infestation and sperm functionality as well as sperm structure. Colony demographics was not negatively affected by V. destructor infestation level, but in contrast, significant relationships were found between colony demographics and sperm motility and kinematic parameters as well as sperm structure. Findings of this study suggest that V. destructor infestation may hinder drone reproductive potential through subtle alterations in sperm quality, particularly sperm motility and kinematics. This study further highlights the importance of sperm quality parameters as markers of the impact of V. destructor infestation on honeybee drone and colony reproduction and survival.