Neonicotinoid insecticides severely affect honey bee queens

Queen health is crucial to colony survival of social bees. Recently, queen failure has been proposed to be a major driver of managed honey bee colony losses, yet few data exist concerning effects of environmental stressors on queens. Here we demonstrate for the first time that exposure to field realistic concentrations of neonicotinoid pesticides during development can severely affect queens of western honey bees (Apis mellifera). In pesticide-exposed queens, reproductive anatomy (ovaries) and physiology (spermathecal-stored sperm quality and quantity), rather than flight behaviour, were compromised and likely corresponded to reduced queen success (alive and producing worker offspring). This study highlights the detriments of neonicotinoids to queens of environmentally and economically important social bees, and further strengthens the need for stringent risk assessments to safeguard biodiversity and ecosystem services that are vulnerable to these substances

Neonicotinoid pesticides can reduce honeybee colony genetic diversity

Neonicotinoid insecticides can cause a variety of adverse sub-lethal effects in bees. In social species such as the honeybee, Apis mellifera, queens are essential for reproduction and colony functioning. Therefore, any negative effect of these agricultural chemicals on the mating success of queens may have serious consequences for the fitness of the entire colony. Queens were exposed to the common neonicotinoid pesticides thiamethoxam and clothianidin during their developmental stage. After mating, their spermathecae were dissected to count the number of stored spermatozoa. Furthermore, their worker offspring were genotyped with DNA microsatellites to determine the number of matings and the genotypic composition of the colony. Colonies providing the male mating partners were also inferred. Both neonicotinoid and control queens mated with drones originating from the same drone source colonies, and stored similar number of spermatozoa. However, queens reared in colonies exposed to both neonicotinoids experienced fewer matings. This resulted in a reduction of the genetic diversity in their colonies (i.e. higher intracolonial relatedness). As decreased genetic diversity among worker bees is known to negatively affect colony vitality, neonicotinoids may have a cryptic effect on colony health by reducing the mating frequency of queens

Data from: Neonicotinoid insecticides can serve as inadvertent insect contraceptives

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

Neonicotinoid insecticides can serve as inadvertent insect contraceptives

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 formanaged 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

Corrected Effective Mating inferred from offspring DNA genotyping of control and neonicotinoid honeybee queens (<i>Apis mellifera</i>).

<p><b>Boxplot shows inter-quartile range (box), median (black line within interquartile range), means (black asterisk); data range (dashed vertical lines).</b> Queens exposed to neonicotinoid pesticides during their developmental stage mated with fewer males, resulting in lower Effective Matings than control queens. *P≤0.1, **P≤0.05, ***P≤0.01 (comparison with Controls).</p

Corrected Relatedness inferred from offspring DNA genotyping of control and neonicotinoid honeybee queens (<i>Apis mellifera</i>).

<p><b>Boxplot shows inter-quartile range (box), median (black line within interquartile range), means (black asterisk); data range (dashed vertical lines).</b> Queens exposed to neonicotinoid pesticides during their developmental stage mates with fewer males, resulting in higher Corrected Relatedness among worker offspring than control queens. *P≤0.1, **P≤0.05, ***P≤0.01 (comparison with Controls).</p

Summary of statistical methods and results.

<p>Summary of statistical methods and results.</p

Effective Mating, Relatedness, Sperm Count and Paternity Skew in the control and neonicotinoid treated honeybee (<i>Apis mellifera</i>) queens.

<p>Effective Mating, Relatedness, Sperm Count and Paternity Skew in the control and neonicotinoid treated honeybee (<i>Apis mellifera</i>) queens.</p

Microsatellite markers for honeybee <i>Apis mellifera</i> genotyping.

<p>Microsatellite markers for honeybee <i>Apis mellifera</i> genotyping.</p

Frequency of control and neonicotinoid honeybee (<i>Apis mellifera</i>) queens mated by Drones Source Colony.

<p>Singletons that mated with different types of queen (i.e. control or neonicotinoid) were paired. Frequency of queens that mated with drones from each Drone Source Colony is represented in light grey and dark grey for the control and neonicotinoid queens, respectively.</p