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A great yellow bumblebee makes its rounds of flowers. Exposure to insect-killing pesticides caused bumblebee colony sizes to drop, and the colonies produced fewer queens than unexposed bees.© Science/AAAS

What does not kill them does not in fact make them stronger when it comes to bees and pesticides. Two unusual studies with free-flying bumblebees and honeybees find that survivable exposure to certain pesticides can lead to delayed downturns in bee royalty and a subtle erosion of workforces.

Pesticides appear as a suspect in widespread declines, sometimes subtle and sometimes dramatic, of the bees and other animals that pollinate crops and wild plants. And in one of the most dramatic still unsolved mysteries in those declines — why honeybee colonies suddenly collapse — one leading hypothesis combines chronic pesticide exposure with other stressors such as disease.

Both of the new studies, appearing online March 29 in Science, test the risks of foraging on flowers treated with common insect killers from the nicotine-inspired class called neonicotinoids. These pesticides course through the whole plant, killing aphids and a range of other nibbling and sipping pests, but also work their way into the nectar and pollen that bees collect.

To simulate pesticide exposures that bumblebees might encounter when a field of canola blooms, entomologist Dave Goulson, of the University of Stirling in Scotland, and his colleagues fed 50 Bombus terrestris lab colonies nonfatal doses of the pesticide imidacloprid. After two weeks of eating spiked pollen and sugar water, bees were set outside and allowed to forage around the Stirling campus at will. By season’s end, the pesticide-dosed colonies were an average of 8 percent to 12 percent smaller than 25 unexposed neighbor colonies.

More noticeably, the contaminated colonies managed to produce only about two young queens each. The other colonies averaged about 14. Pitiful production of new young queens bodes ill for bumblebees because all other colony members die at the end of the growing season. Young queens represent each group’s sole hopes for making new colonies the next year.

Ecotoxicologist David Fischer of Bayer CropScience, which markets imidacloprid products, notes that earlier research (with constrained rather than free-flying bees) did not find a drop in young queens. Goulson isn’t surprised that his bumblebees showed more of an impact. “Navigation isn’t important when you live in a box,” he says.

A drop in pollinator reproduction is the kind of finding that can get the attention of agencies regulating pesticide use, says Jeffery Pettis, research leader of the U.S. Department of Agriculture’s bee labs who works in Beltsville, Md. Worldwide, growers commonly use five neonicotinoid pesticides for flowering crops. Amid these and previous studies, concerns are growing that usage rules may need to be tightened.

Goulson’s study ranks as the first test in bumblebees of pesticide side effects under natural field conditions, says Guy Smagghe of Ghent University in Belgium, who also works with these bees. Goulson notes that although bumblebees don’t get the press that honeybees do, many wildflowers depend on them, as do such crops as tomatoes and peppers.

For honeybees, earlier tests have raised the possibility that chronic, nonfatal exposure to neonicotinoids impairs learning, memory and other capacities that bees need for good flower hunting. To set up a test with bees flying freely outdoors, a research team in France (with substantial graduate student labor) used dental cement to fasten electronic identifiers onto more than 600 individual bees. Feeding bees low doses of the pesticide thiamethoxam in sugar water provided a realistic exposure, says coauthor Mickaël Henry of the French National Institute for Agricultural Research in Avignon.

After sipping the pesticide-tainted solution, the honeybees were moved up to a kilometer from their hives and released to find their way home. Researchers challenged bees with both familiar territory and landscapes the bees had never seen. Automated counters at hives logged the returnees.

By comparing the homing success of dosed versus untreated hives, researchers concluded that pesticides doubled the risk on any given day that a forager would not make it home. Computer simulations suggest that the population drop substantially weakens a colony, Henry says.

Honeybee research on whether pesticide exposure interferes with daily foraging could be relevant to other species, Goulson says. “If that is also happening in bumblebees, which is a reasonable guess, that could precisely explain our results.” If exposed bumblebees aren’t as good at bringing home food, then colonies might not grow or reproduce as well.

Bayer CropScience’s Fischer, based in Research Triangle Park, N.C., questions the realism of the dosage. Researchers essentially fed bees all at one time the amount of pesticide they might encounter over a whole day.

For common pesticides now on the market, “there are obviously big question marks as to whether the safety testing that was done on these was really adequate,” Goulson says. Chronic effects may not show up without tests of free-ranging bees confronting real-world problems.

The new studies help to start filling in gaps in the research, but there’s even less known about the multitude of pollinating bees that don’t live in colonies, says entomologist Mace Vaughan in Portland, Ore., with the Xerces Society for Invertebrate Conservation. Most wild bees living around farms are solitary and thus especially vulnerable. “If an individual bee is lost, she cannot be replaced and her reproduction stops,” he says.

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