Nicotine-like pesticides are likely to cause long-term damage to wild honey bee populations even though they might initially appear to be harmless, a new study has shown.
The bees counteract the immediate impact of neonicotinoid pesticides by producing more female workers at the expense of male drones, whose job is to breed.
With fewer males available for mating with queens, the long-term survival of the colony is put at risk, the research suggests.
The findings may help explain apparently conflicting evidence about the effect of the controversial chemicals on bee populations.
While work involving the artificial exposure of honey bees to the pesticides has indicated that the chemicals impair the insects' ability to forage for pollen and nectar, by and large this evidence has not been supported by wild bee studies.
The new research suggests that in the wild, the bees themselves help to cover up the evidence. Even though pesticide exposure led to "significant excess mortality" of free-ranging bees, colonies compensated for the loss by altering their demographics.
Writing in the journal Proceedings of the Royal Society B, the scientists led by Dr Mickael Henry, from the French INRA agricultural institute in Avignon, concluded: "The most exposed colonies modified the timing of their reproductive investment, delaying drone brood production in favour of increased worker brood production.
"We have now reconciled the conflicting laboratory and field assessments of neonicotinoid toxicity. It is thus urgent that risk assessors take into account the scientific evidence for behavioural disorders triggered by trace levels of neonicotinoids."
Because of the possible risk to bees, in 2013 the European Union banned the use of three neonicotinoids on flowering crops for two years.
But the move was highly controversial and opposed by the UK Government, which was nevertheless obliged to enforce the ban.
The French scientists studied 18 bee colonies exposed to oil seed rape grown from seeds treated with the neonicotinoid thiamethoxam.
During the study, bees were also found to have been unintentionally exposed to nectar contaminated with imidacloprid, another member of the same pesticide family.
Commenting on the new research, Dr Christopher Connolly, from the University of Dundee, said: "Although honeybee colonies may be able to maintain colony strength by switching their production from male (non-working) bees to female foragers, this may have serious implications to honeybee reproduction. Indeed, many beekeepers in the UK are reporting problems with the mating of new queens.
"In summary, this study identifies three new and important consequences of neonicotinoid exposure to honeybees; increased mortality of female foragers, an increasing vulnerability to the effects of neonicotinoids and a consequential reduction in the number of male bees that are required for mating of new queens and the long-term survival of honeybee colonies.
"It is important to remember that all other insect pollinators do not possess the enormous buffering capacity of honeybees and are therefore more acutely at risk to the impact of pesticides."
Dr Scott Hayward, from the University of Birmingham, said: "There have been multiple reports outlining the detrimental effects of neonics under lab exposures, but negative impacts from field investigations have been less clear cut. This research identifies a clear relationship between neonic exposure in the field and bee mortality. However, the findings are complicated somewhat by an unintended exposure to two different pesticides."
A Department for Environment, Food and Rural Affairs (Defra) spokesman said: "The EU Commission introduced precautionary restrictions on neonicotinoids from December 2013, which the UK has fully implemented.
"The Government makes decisions on pesticides based on the recommendations of senior scientists and independent experts who have looked at the best available scientific evidence.
"The Commission has now begun a review of the science relating to neonicotinoids and bees, and the UK will contribute fully to this review."