Bee deaths Pesticides used in farming are also killing worker bees and damaging their ability to gather food, meaning colonies that are vital for plant pollination are more likely to fail when they are used, according to a new study.
"Here we show that chronic exposure of bumblebees to two pesticides ... impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success," write Gill and team.
The United Nations has estimated that a third of all plant-based foods eaten by people depend on bee pollination and scientists have been baffled by plummeting numbers of bees, mainly in North America and Europe, in recent years.
Gill says previous studies have mostly examined the impact of pesticides on individual bees, but his study looked at the impact on bee colonies.
"Although field-level pesticide concentrations can have subtle or sublethal effects at the individual level, it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level," he and colleagues write.
Gill and colleagues exposed colonies of 40 bumblebees, which are bigger than the more common honeybee, to neonicotinoid and pyrethroid pesticides over four weeks at levels similar to those in fields.
Neonicotinoids are nicotine-like chemicals used to protect various crops from locusts, aphids and other pests.
The researchers found that the average number of bees lost in the experiment - both dead in the nesting box and failing to return - was about two-thirds of the total for bees exposed to a combination of the two pesticides against a third for a control, exposed to neither.
"Effects at the individual level can have a major knock-on effect at the colony level. That's the novelty of the study," says Gill.
The researchers also say the possible combinatorial effects of pesticide exposure have rarely been investigated.
In their study they found bumblebees exposed to a combination of neonicotinoid and pyrethroid pesticides were about half as successful at gathering pollen, used as food, compared to a control.
They also devoted more workers to collecting food, meaning fewer were raising larvae.
Australian bee expert Professor Boris Baer welcomes the new research.
"[The study] provides clear evidence for what has been widely suspected to be a major factor contributing towards bee decline: the action of pesticides commonly used intensively in modern agriculture," says Baer, from the Centre for Integrative Bee Research at the University of Western Australia.
"This research consolidates a further dimension to the acute bee and pollinator problem, and could well be an important milestone to understand the dramatic decline events we have observed over recent years, that are often referred to as Colony Collapse Disorder (CCD)."
Gill and colleagues say their findings underscore the importance of wider testing of pesticides to ensure they do not also target bees.
France banned a neonicotinoid pesticide made by Swiss agrochemicals group Syngenta in June, citing evidence of a threat to the country's bees. A report last month, however, said that the original research was flawed.
"My guess is that the decline of bees is like a jigsaw -there are probably a lot of pieces to put into place. This is probably a very important piece of that jigsaw," says Gill.
In a separate commentary in the same issue of Nature, Dr Juliet Osborne of the University of Exeter in England says the study underscored the need to understand all factors that may contribute to harm bees and to CCD.
"For example, we have as yet no convincing demonstration of the relative effects of pesticides on bee colonies compared to the effects of parasites, pathogens and foraging resources," she writes.
Other experts have hailed the study's innovation but note that bumblebees can not be directly compared with honeybees, as they are biologically different.
Still others emphasise more research is needed.
"It certainly wouldn't be fair to say that this research spells doom for wild bees," says Dr James Cresswell, also of the University of Exeter.