ABOVE: A bumblebee (Bombus impatiens) foraging outdoors and wearing a unique tracking tag

JAMES CRALL

Bumblebees exposed to the insecticide imidacloprid tend to contribute less to the welfare of their colony than untreated bees, according to a report in Science today (November 8). Inside their nests, bees chronically eating this common pesticide were less active, didn’t care for larvae as much or pitch in on maintaining the nest, and had fewer social interactions, the researchers found.

“It’s very fascinating and gives us a much greater understanding of the mechanism behind the patterns that we’ve seen of reduced [bee] colony growth and reproduction,” says biologist Maj Rundlöf of Lund University in Sweden who was not involved in the research.

Imidacloprid is one of a class of neonicotinoid neurotoxic insecticides that were developed during the 1980s and 1990s and are now “absolutely pervasive globally,” says biologist James Crall, a postdoc in the lab of Benjamin de Bivort at Harvard University, who led the research. In an agricultural context, neonicotinoids are most commonly applied to seeds in high concentrations, so that they pervade and protect the whole plant, explains Crall. “The problem with that is that it also gets into nectar and pollen on which bees and other beneficial insects feed,” he says.

Even though the levels of neonicotinoids in the wild to which bees are exposed are not immediately lethal, says Crall, “there’s a mounting body of pretty clear evidence that these low, sublethal levels of exposure . . . still impair long-term colony growth and performance and especially in bumblebees.”

Studies examining how nicotinoids might negatively affect bee colonies have largely focused on the insects’ foraging behaviors—visiting flowers, gathering pollen, and so on. But these activities are only half the story, says entomologist and ecologist Dara Stanley of University College Dublin who was not part of the research team. Inside the nest, bees also work to ensure that resources reach the growing larvae, the nest is maintained and cleaned, and temperatures are kept constant. All these things, as well as social interactions, are thought to promote the health of the colony as a whole.

Crall and colleagues’ work “is the first study that I have seen that has looked at behaviors within the hive itself,” Stanley says.

This intimate view of colony life was achieved with high performance cameras that were, for a period of almost two weeks, robotically maneuvered above 12 laboratory-housed nests—six with access to normal nectar and six to nectar laced with the pesticide. Stuck to the back of each bee in the 12 colonies was a tiny piece of paper with a visual code enabling continuous computerized monitoring of their individual positions and activities.

Automated tracking of nest workers in a bumblebee colony james crall





“The technology is quite groundbreaking, and what it allowed them to do was groundbreaking too,” says insect cognition researcher Elli Leadbeater of Royal Holloway, University of London, who was not involved in the research. “They can track what all their tagged bees are doing . . . and so really drill down on what it is that neonicotinoids are doing to bee colonies.”

Crall’s team observed that bees exposed to typical levels of imidacloprid found in the wild tended to be less active in the nest, spent less time nursing larvae, and had fewer social interactions than did control bees. These effects on activity were more exaggerated at night than during the day, says Crall, but as to why, “it’s currently a total mystery,” he says. It’s also unclear why, as the experiment progressed, daytime activity became increasingly normal.

Regardless of the reason behind this day-night difference, its very existence suggests that certain effects of pesticides may be context dependent, and may therefore be missed by looking solely at foraging, says Leadbeater.

In separate experiments, the team showed that imidacloprid-exposed bee colonies in outdoor nests were incapable of regulating nest temperature. Bumblebees are very good at maintaining the internal temperature of their nests to protect the growing larvae, explains Crall. And worker bees will often build a wax barrier to protect the nest from cold. While eight of nine control colonies built such barriers, none of the pesticide-exposed colonies did, the team found—consistent with the reduced activity of the pesticide-exposed bees observed under laboratory conditions.

The team’s computerized in-nest monitoring system could be used to study the potential effects of a wide range of existing and novel insecticides, says Crall. But, even without further research, this study “definitely strengthens the arguments for the restriction of some of the neonicotinoids that have such impactful effects,” says Rundlöf.

Earlier this year, the European Union banned the use of certain neonicotinoids, including imidacloprid, on all outdoor crops. In the US and elsewhere, however, the use of these pesticides remains widespread.

J.D. Crall et al., “Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation,” Science, 362:683-86, 2018.