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"In sublethal doses, however, research has shown that imidacloprid and other neonicotinoids, such as fipronil, can impair honeybees' memory and learning, as well as their motor activity and navigation. When foraging for food and collecting nectar, honeybees memorize the smells of flowers and create a kind of olfactory map for subsequent trips.
However, in laboratory and field studies, honeybees exposed to imidacloprid seem to wander off, which may explain, say scientists, why hives all over the world are turning up empty.
Recent studies have reported on the "anomalous flying behavior" of imidacloprid-treated bees where the workaholic insects simply fall to the grass or appear unable to fly toward the hive.
In 2003, a French television documentary team filmed honeybee activity after exposure to imidacloprid. Clumsy and uncoordinated, their legs trembling, the bees looked like drunks unable to find the key to the front door of their hive. Others had trouble leaving the hive, seemed disoriented, and when they were eventually able to make their way out, soon disappeared, never to return.
The possibility that neonicotinoids are at the heart of the bee die-off implies a far more complex problem because of the widespread use of pesticides. Every year these chemicals are applied to hundreds of millions of acres of agricultural lands, gardens, golf courses and public and private lawns across the United States. Their use on major crops nearly tripled between 1964 and 1982, from 233 million pounds to 612 million pounds of active ingredients. And since then, their use has exploded. By 1999, the U.S. Environmental Protection Agency reported 5 billion pounds of pesticides used on U.S. crops, forests, lawns, flowers, homes and buildings.
Because of imidacloprid's emergence as a primary player in pest management, a painful paradox has developed in relation to the recent debate. Neonicotinoids are needed by farmers and growers to maintain the health of crops, many of which also require pollination by honeybees.
"Neonicotinoids are now the best aphid insecticide we have," said Peter Shearer, a specialist in fruit tree entomology with the Rutgers Agricultural and Extension Center in Bridgeton, N.J. "It's very important to our pests that have shown resistance to other chemicals. It's very important to eggplants, potatoes, tomatoes."
Shearer notes that apple farmers, for instance, don't use Provado, which has imidacloprid as an active ingredient, until after the bees, which are used for pollination, are removed from the orchards.
So it doesn't seem to be a logical route of bee die-off," he said. "It would have to last 11 months."
However, Shearer also acknowledges that some published studies indicate that imidacloprid can persist on both vegetation and in the soil for weeks, months and perhaps years.
In France, there have been inconsistent results since the bans on imidacloprid went into effect. In 2005, for the first time in a dozen years, the French honey harvest improved, but only in certain regions, according to the country´s beekeeping federation.
Some U.S. entomologists, who recently have been analyzing dead bees, have found a remarkably high number of viruses and fungal diseases in the carcasses, leading them to suspect there may be other culprits besides neonicotinoids.
A 2004 University of North Carolina study, for instance, found that some neonicotinoids, in combination with certain fungicides, increased the toxicity of the "neonics" to honeybees a thousand-fold.
"I don't think there is one smoking gun," said Hayes. "When neonicotinoids are used on termites, they can't remember how to get home, they stop eating and then the fungus takes over and kills them. That's one of the ways imidacloprid works on termites - it makes them vulnerable to other natural organisms. So if you look at what's happening to honeybees, that's pretty scary."
Last week the five-state Mid-Atlantic Apiculture Research and Extension Consortium released a progress report on colony collapse disorder. Its findings included "the high prevalence of fungi in adult bees" which seemed "indicative of stress or a compromised immune system; these symptoms have never been previously reported."
Another entomologist at the Rutgers center, Gerald Ghidiu, knows there is no simple answer to the problem.
They've been looking at this since the late 1990s," said the vegetable specialist. "They've done quite a few studies and they still can't find the direct link. Seventy-five percent of the vegetable crops in Arizona gets imidacloprid, but they have no problems with the honeybees right now. So why isn't it straight across the board? Everyone is in the dark over this."
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