Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder

Honey bee (Apis mellifera L.) colony collapse disorder (CCD) that appeared in 2005/2006 still lingers in many parts of the world.
Here we show that sub-lethal exposure of neonicotinoids, imidacloprid or clothianidin, affected the winterization of healthy colonies
that subsequently leads to CCD. We found honey bees in both control and neonicotinoid-treated groups progressed almost
identically through the summer and fall seasons and observed no acute morbidity or mortality in either group until the end of winter.
Bees from six of the twelve neonicotinoid-treated colonies had abandoned their hives, and were eventually dead with symptoms
resembling CCD. However, we observed a complete opposite phenomenon in the control colonies in which instead of abandonment,
they were re-populated quickly with new emerging bees. Only one of the six control colonies was lost due to Nosemalike
infection. The observations from this study may help to elucidate the mechanisms by which sub-lethal neonicotinoids exposure
caused honey bees to vanish from their hives.