Neonicotinoid insecticides can serve as inadvertent insect contraceptives

Abstract

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.

Keywords: Apis mellifera; insecticide; pollination; reproduction; sperm; sub-lethal.

Figure 1.

Drone (male) honeybee teneral body mass. Comparison of drone honeybee (Apis mellifera) teneral body mass (mg) showed no significant difference between controls (N = 200) and neonicotinoid insecticides (N = 120) (p = 0.80). The boxplots show the inter-quartile range (box), the median (black line within box), data range (horizontal black lines from box), and outliers (black dots).

Figure 2.

Honeybee drone (male) and worker (female) cage mortality. Survival curves (Kaplan–Meier) indicate the cumulative survival (%) of honeybee (Apis mellifera) drones (N = 567) (a) and workers (N = 1120) (b) under neonicotinoid insecticide exposure compared with controls. A significant difference was only observed for the mortality of drones (p < 0.001). A significant difference between treatment groups is indicated by ***p < 0.001.

Figure 3.

Honeybee sperm assessment. Assessment of various sperm traits in male (drone) honeybees (Apis mellifera) under neonicotinoid insecticide (N = 90) exposure compared with controls (N = 145). (a) Comparison of sperm quantity showed no significant differences (p = 0.1375). (b) Percentage of viable sperm in honeybee drones showed significant differences (p = 0.03). (c) Total quantity of living sperm in honeybee drones showed a significant difference (p < 0.05). All boxplots show the inter-quartile range (box), the median (black line within box), data range (horizontal black lines from box), and outliers (black dots). A significant difference between treatment groups is indicated by *p < 0.05.