The decline of wild bees across England is linked to the use of controversial pesticides, according to scientists.
Species of wild bee exposed to oilseed rape crops treated with neonicotinoids suffered population decline of up to 30% between 2002 and 2011, the research led by the Centre for Ecology and Hydrology found.
The pesticide is the subject of an EU-wide two-year ban amid concerns over its harmful impact on bees, such as damaging their ability to forage and navigate, and colony growth.
The research looked at changes in occurrence of 62 species with oilseed rape cropping patterns across England between 1994 and 2011, examining data from 31,818 surveys across more than 4,000 square kilometres of land.
It found an average population decline across all species of 13%, of which more than half - 7% - was attributable to the use of neonicotinoids between 2002 and 2011, after the pesticide came into wide-scale commercial use.
Species which forage on oilseed rape were three times more seriously affected on average than those which did not.
Neonicotinoids caused declines of more than 20% for the five most seriously affected species, according to analysis of the data, provided by Fera Science - formerly the Food and Environmental Research Agency - and the Bees, Wasps and Ants Recording Scheme.
Dr Nick Isaac, who co-authored the paper, said the damaging effects of the pesticide reported in small-scale studies had been replicated.
"The negative effects that have been reported previously, they do scale up," he said. "They scale up to long-term, large-scale, multi-species impacts that are harmful."
Bees play an important role in agriculture, with their pollinating services worth around £600 million a year in the UK in boosting yields and the quality of seeds and fruits.
The research is the strongest evidence yet of harm caused by neonicotinoids, Friends of the Earth's nature campaigner Paul de Zylva said, as he urged the Government to continue the pesticide ban after Britain leaves the EU.
He said: "The study uses data from real field conditions over 17 years and adds a huge new peak to the existing mountain of evidence showing the risk these chemicals pose to our bees.
"If the Government genuinely wants to safeguard Britain's bees, it must keep the ban on neonicotinoid pesticides regardless of what happens with Brexit - and tighten the way pesticides are tested and licensed for use."
But the National Farmers' Union (NFU) said the research does not show the chemicals cause widespread decline in populations.
NFU bee health specialist Dr Chris Hartfield said: "This study is another interesting piece to an unsolved puzzle about how neonicotinoid seed treatments affect bees. It does not show that neonicotinoids are causing widespread declines in pollinator populations and it certainly does not show that neonicotinoid use has caused any extinction of bees in England."
Dr Hartfield, who said farmers are well aware of the importance of bees and would not want to cause them harm, called for more science-based regulation but warned against over-regulation of chemicals for fear of the effect on the farming industry's future.
"Without many of these (plant protection) products, our ability to produce wholesome, affordable food for the nation will continue to stagnate," he said.
He said there are still knowledge gaps and a "limited evidence base" to guide and inform policymakers on the issue.
Decline was measured in terms of how much less widespread the species was compared with a scenario when neonicotinoids were not harmful, the researchers said.
They added that the study showed a decline in the number of populations of bees, not a decline in the number of bees.
Among the worst-affected of wild bee species, the lime-loving furrow bee, saw a 23% decline in the number of populations, while Hawthorn mining bee populations declined by 18%.
Neonicotinoids are applied to the seed prior to planting and can be transported to all tissues of a crop, meaning they can be ingested by pollinators which feed on the nectar.
"As a flowering crop, oilseed rape is beneficial for pollinating insects," said Dr Ben Woodcock, lead author of the paper published in Nature Communications.
"This benefit however, appears to be more than nullified by the effect of neonicotinoid seed treatment on a range of wild bee species."
The moratorium on the pesticide could be lifted following a review by the European Food Standards Authority, which is expected to be completed in January and will be informed in part by the new paper.
But Dr Woodcock warned neonicotinoids should be considered as a "contributory factor" to decline in the number of populations of wild bee and said a "complex array of drivers" including habitat, climate change and disease were also important.
"It's not a simple case that pesticides are causing declines," he said. "It's likely that there's a whole series of interacting factors and while people like a one-shot solution, it's probably not the case in most situations."
A spokeswoman for the Department for Environment, Food and Rural Affairs said: "The use of neonicotinoids is restricted and we are committed to ensuring pesticides are available only when the scientific evidence shows they do not pose unacceptable risks to the environment.
"Bees and other pollinators are vital to the diversity of our environment and food production, which is why we are leading on a nationwide strategy to better protect them.
"We are encouraging farmers to provide the food and habitats pollinators need on their land, as well as promoting simple actions the public can take such as cutting grass less often and growing pollen-rich plants."