A controversial type of pesticide linked to declining global bee populations appears to scramble bees' sense of direction, making it hard for them to find home. Starved of foragers and the pollen they carry, colonies produce fewer queens, and eventually collapse.

The phenomenon is described in two new studies published March 29 in Science. While they don't conclusively explain global bee declines, which almost certainly involve a combination of factors, they establish neonicotinoids as a prime suspect.

"It's pretty damning," said David Goulson, a bee biologist at Scotland's University of Stirling. "It's clear evidence that they're likely to be having an effect on both honeybees and bumblebees."

Neonicotinoids emerged in the mid-1990s as a relatively less-toxic alternative to human-damaging pesticides. They soon became wildly popular, and were the fastest-growing class of pesticides in modern history. Their effects on non-pest insects, however, were unknown.

In the mid-2000s, beekeepers in the United States and elsewhere started to report sharp and inexplicable declines in honeybee populations. Researchers called the phenomenon colony collapse disorder. It was also found in bumblebees, and in some regions now threatens to extirpate bees altogether.

Many possible causes were suggested, from viruses and mites to industrial beekeeping practices and climate change. Pesticides, in particular neonicotinoids, also came under scrutiny.

Leaked internal reports by the Environmental Protection Agency showed that industry-run studies used to demonstrate some neonicotinoids' environmental safety were shoddy and unreliable. Other researchers found signs that neonicotinoids, while they didn't kill bees outright, affected their ability to learn and navigate.

Those results came from laboratory situations, with no guarantee of real-world applicability, but they were troubling.

"Bees' ability to navigate is very important. When they leave their nest, they fly miles to gather food. Anything that makes them even a little bit worse at navigating or learning could be a disaster in those circumstances," said Goulson. "The research suggested effects on their learning ability, but it was all done in confined situations. What we and the French group did is something more natural."

In the first study, led by biologist Mickaël Henry of INRA, a French agricultural research institute, free-roaming honeybees were tagged with RFID chips that allowed researchers to track their movements. When dosed with a neonicotinoid, bees were more than twice as likely as non-dosed controls to die outside their hives. They seemed to get lost.

When the researchers added their results to computer simulations of honeybee dynamics, the model populations crashed.

Penn State entomologist James Frazier, who was not involved in the study, called it "the best study to date" on neonicotinoids' real-world effects on foraging.

The result dovetailed with the findings of Goulson's group, who exposed developing bumblebees to varying neonicotinoid levels and set them loose to forage in an enclosed field. Measured after six weeks of growth, pesticide-dosed colonies were stunted, weighing about 10 percent less and producing 85 percent fewer queens.

"Nests have annual cycles. They start with a single queen, and the nest grows through the season. If it doesn't get big enough, it doesn't have the resources to pour into rearing queens," Goulson said. "The French study shows that exposure to neonicotinoids make honeybees less likely to find their nest. That's likely the mechanism that led to our nests growing more slowly."

However, biologist Jerry Bromenshenk of the University of Montana was critical of the results. Goulson's results were interesting but the researchers weren't careful enough in verifying the doses given to their bees, and Henry's group administered an unrealistically high dose, said Bromenshenk.

The latter's dosing "is not what I would consider to be a field-relevant, low dose," wrote Bromenshenk in an email, citing another recent study that used RFIDs to track bees given what he considers a more realistic dose. "At truly field representative, sublethal doses – no effect," Bromenshenk wrote.

Both Goulson and Mace Vaughan, pollinator program director at the Xerces Society, an invertebrate conservation group, said neonicotinoids won't be the only cause of colony collapse disorder.

"If it was as simple as that, the answer would have been discovered a long time ago," said Goulson. "I'm sure it's a combination of things. I'm sure that disease is a part of it, and maybe the two interact." He noted a study in which honeybees exposed to neonicotinoids were especially vulnerable to a common bee parasite. Another study found that neonicotinoids dramatically increase the toxicity of fungicides.

Vaughan raised the issue of industrial-scale beekeeping practices, which have also been linked to bee declines. "We've potentially created a situation where behavioral impacts, compounded with a lack of genetic diversity and the food they eat, results in something like colony collapse disorder," he said.

"My only caution is that farmers use neonicotinoids for a reason," said Goulson. "If they were banned, farmers would have to use something else. The question is, what would that be? Would it be better? Would it also have harmful effects?"

While it's unlikely that neonicotinoids will be banned outright in the United States, where they're now used on more than 100 million crop acres and an unknown area of home gardens and urban vegetation, Vaughn said they could be used differently.

"I would call for a ban on their use without a demonstrated pest threat. If you have corn rootworm, and need to address that, then use neonicotinoid-coated seeds," he said. "But if it's a vague threat that you haven't identified, you shouldn't be using them. Maybe it makes you a few bucks, and certainly makes the seed companies a lot of money, but it's potentially killing bees across the country."

Heather Pilatic of the Pesticide Action Network recommended a return to pest management strategies used widely through the 1990s, when the rise of pesticide-treated seeds and genetically modified crops allowed farmers to change their growing strategies.

"When you plant the same crop, year after year, you're creating the conditions for a pest infestation," Pilatic said. "In the mid-1990s, we were doing a really good job of pest management with corn in particular. With the introduction of treated seeds, and in particular of genetically engineered corn, it all unraveled. But we know how to do it. We were doing it 20 years ago."

Penn State's Frazier said that the Environmental Protection Agency, which recently received a 1.25 million-signature-strong petition to ban neonicotinoids, is slowly becoming better at risk assessment, though the agency is still heavily influenced by chemical companies and opaque in its workings.

The fundamental problem isn't neonicotinoids, but our society's relationship to chemicals, said Frazier. "We're making ourselves the guinea pigs," he said. "I don't think that's what a rational society should be doing."

Image: Jack Wolf/Flickr

Citations: "Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth and Queen Production." By Penelope R. Whitehorn, Stephanie O’Connor, Felix L. Wackers, Dave Goulson. Science, Vol. 335 No. 6076, March 30, 2012.

"A Common Pesticide Decreases Foraging Success and Survival in Honey Bees." By Mickaël Henry, Maxime Beguin, Fabrice Requier, Orianne Rollin, Jean‐François Odoux, Pierrick Aupinel, Jean Aptel, Sylvie Tchamitchian, Axel Decourtye. Science, Vol. 335 No. 6076, March 30, 2012.