Drone exposure to the systemic insecticide Fipronil indirectly impairs queen reproductive potential

Abstract

A species that requires sexual reproduction but cannot reproduce is doomed to extinction. The important increasing loss of species emphasizes the ecological significance of elucidating the effects of environmental stressors, such as pesticides, on reproduction. Despite its special reproductive behavior, the honey bee was selected as a relevant and integrative environmental model because of its constant and diverse exposure to many stressors due to foraging activity. The widely used insecticide Fipronil, the use of which is controversial because of its adverse effects on honey bees, was chosen to expose captive drones in hives via syrup contaminated at 0.1 μg/L and gathered by foragers. Such environmental exposure led to decreased spermatozoa concentration and sperm viability coupled with an increased sperm metabolic rate, resulting in drone fertility impairment. Subsequently, unexposed queens inseminated with such sperm exhibited fewer spermatozoa with lower viability in their spermatheca, leaving no doubt about the detrimental consequences for the reproductive potential of queens, which are key for colony sustainability. These findings suggest that pesticides could contribute to declining honey bee populations through fertility impairment, as exemplified by Fipronil. More broadly, reproductive disorders should be taken into consideration when investigating the decline of other species.

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems

“…This confirmed earlier research by the same authors had shown that queens inseminated with sperm of fipronil exposed drones had less and less viable spermatozoa stored in their spermatheca (Kairo et al 2016). They found that several pesticides, among them fipronil, imidacloprid, and thiamethoxam, reduced sperm viability (in vitro sperm assay).…”

Assessment of the toxic effect of pesticides on honey bee drone fertility using laboratory and semifield approaches: A case study of fipronil

“…The amount of food collected in the feeders was measured daily to assess the effect of fipronil on worker feeding behavior. Regardless of the rearing method, fipronil did not affect the amount of syrup and pollen that was gathered by the bees (data not shown), as was previously observed in bees grown under semifield conditions [26]. A comparison of the amount of food that was gathered by workers between bees reared using different methods was not relevant because the feeding methods were different.…”

“…Hence, exposure to environmental stressors, such as biological or chemical agents, can have different effects on drone life traits and fertility depending on the approach used. To better explore this notion, at least with regard for chemical agents, in the present study, we reared drones with different methods using bees that were or were not exposed to a relevant concentration of the insecticide fipronil, which has been previously shown to have effects on drone fertility under semifield conditions and on the reproductive potential of the queen .…”

“…Because reproductive functions are highly important for colony growth and sustainability, scientists advise that they should be taken into consideration [19,20]. However, no standardized methods are available to assess the effects of plant protection products on reproduction, whereas an increasing amount of evidence indicates that fertility has been impaired in reproducers and that this has impacted honey bee decline [20][21][22][23][24][25][26].…”

Immunosuppression in Honeybee Queens by the Neonicotinoids Thiacloprid and Clothianidin

“…Although reports of colony losses due to high rates of queen failure exist, only few studies address direct or indirect physiological effects in queens caused by pesticide exposure 2, 5, 29, 30 . Most studies focused on only three neonicotinoid insecticides, clothianidin, imidacloprid, and thiamethoxam, which are currently subject to a moratorium in the European Union 31 .…”