Controversy Deepens Over Pesticides and Bee Collapse
By Brandon Keim
April 6, 2012
A controversial new study of honeybee deaths has
deepened a bitter dispute over whether the developed
world's most popular pesticides are causing an
Researchers led by biologist Chensheng Lu of Harvard
University report a direct link between hive health and
dietary exposure to imidacloprid, a so-called
neonicotinoid pesticide linked to colony collapse
disorder, the mysterious and massive die-off of bees
across North America and Europe.
The study isn't without critics, who say doses used in
the study may be unrealistically high. But the level of
a realistic dose is also a matter of controversy, and
even critics say the findings are troubling.
"Our result replicates colony collapse disorder as a
result of pesticide exposures," said Lu, who specializes
in environmental exposures to pesticides. "We need to
look at our agriculture policy and see if what we're
doing now is sustainable."
Developed in the 1990s as a relatively less-toxic
alternative to pesticides that seriously harmed human
health, neonicotinoids soon became the world's fastest-
growing pesticide class and an integral part of
industrial agricultural strategy. In the United States
alone, neonicotinoid-treated corn now covers a total
area slightly smaller than the state of Montana.
Like earlier pesticides, neonicotinoids disrupt insects'
central nervous systems. But unlike earlier pesticides,
which affected insects during and immediately after
spraying, neonicotinoids spread through the vascular
tissues of plants. They're toxic through entire growing
seasons, including flowering times when bees consume
The first reports of colony collapse disorder came in
the mid-2000s from commercial beekeepers, who depending
on region have experienced colony losses ranging from 30
to 90 percent. Commercial pollination costs have since
skyrocketed, and as wild bees are also afflicted, even
naturally occurring pollination is threatened.
Measuring bee declines, however, proved much easier than
explaining them. Among a lineup of potential culprits
including fungus, mites, viruses, bacteria and
pesticides, studies failed to find an obvious, smoking-
gun cause - but, piece by piece, evidence against
neonicotinoids has steadily accumulated.
Honeybees are clearly exposed to them throughout the
year and through multiple environmental routes. At
certain times, especially in spring, death often follows
exposure, and even non-lethal exposures may disrupt bee
learning and navigation. Neonicotinoids also appear to
make bees especially vulnerable to certain parasites and
may interact similarly with other stressors.
'These pesticides are everywhere, every year. We've
never used pesticides in the way we're using them now.'
Some European countries, including France, Germany and
Italy, have even banned neonicotinoids, though pesticide
companies vehemently defend their ecological safety and
say concerns are based on inconclusive and premature
Lu's study, released April 5 and scheduled for
publication in the June Bulletin of Insectology,
attempts to replicate the life history of commercial
bees, which are often fed dietary supplements of high-
fructose corn syrup that may contain neonicotinoid
residues that survive processing.
"We tried to mimic commercial beekeepers' practices. I
believe one reason that commercial beekeepers are
experiencing the most severe colony collapse disorder is
because of the link between high-fructose corn syrup and
neonicotinoids," Lu said.
In the spring of 2010, the researchers set up four
groups of commercially purchased colonies. Each
contained five hives, and during the summer months were
fed a diet containing either no imidacloprid, what Lu
considered a small dose of 20 parts per billion, or a
much higher dose of 400 parts per billion.
Colony collapse disorder is characterized in part by
bees abandoning their hives during winter, and that's
precisely what Lu's team reported in 15 of 16
imidacloprid-receiving hives. While other colony
collapse disorder symptoms, such as queens that stay in
the hive while workers flee, were not reported, Lu
considers the experimentally induced collapse to be
Reaction to the study was swift and varied.
Bayer, the chemical and pharmaceutical giant that
manufactures imidacloprid, issued a formal statement
denouncing the findings as "spectacularly incorrect" and
"based on artificial and unrealistic study parameters
that are wildly inconsistent with actual field
conditions insecticide use."
But Jeffery Pettis, a bee biologist at the United States
Department of Agriculture, called the results
"tantalizing but not conclusive." With only four
colonies used per dose level, the study's statistical
significance is limited, "but I would love to see this
study replicated such that the trends . they observed
could be actually validated," wrote Pettis in an email.
Among Bayer's criticisms is that imidacloprid, a first-
generation neonicotinoid, is little-used in the United
States. It's largely been replaced by newer formulations
- but these, said pesticide expert Charles Benbrook of
The Organic Center, an organic food research
consultancy, are chemically similar to imidacloprid.
"Virtually all our corn seed has been treated with a
very similar neonicotinoid," said Benbrook. If the study
had been conducted with clothianidin, another
controversial neonicotinoid, "they'd almost certainly
have found the same thing."
According to Bayer, "analysis from actual field grown
corn samples have shown no detectable imidacloprid
residues" in high-fructose corn syrup. But Benbrook said
that extensive testing by the Organic Center found
traces of imidacloprid, but they were impossible to
"It's very difficult to test for this particular
chemical in high-fructose corn syrup. A lot of labs have
spent lots of time trying to do it, but high-fructose
corn syrup is a very sticky, dense matrix that basically
gums up the testing machines," said Benbrook. "That's
why relatively little is known about imidacloprid in
high-fructose corn syrup."
Separate from the corn syrup issue is how the
experiment's imidacloprid doses compared to real-world
neonicotinoid exposures from pollen and crop residues.
Bee biologist Dave Goulson of Scotland's University of
Stirling, co-author of a recent paper on neonicotinoids
and hive health, said the doses "seem to be
unrealistically high," a critique echoed by Bayer.
But Pettis said the study's lower dose ranges, which
were sufficient to destroy the colonies, "were what bees
could encounter in the environment." His take was echoed
by biologist Christian Krupke of Purdue University, who
said the doses "are certainly within the range that bees
may encounter in the field."
One way in which bees are regularly exposed to
neonicotinoids is through drops of sap that form on the
edge of plants. Studies of these droplets have found
neonicotinoid levels even higher than those used in the
new study, and the droplets can be fatal to bees (see
Another major route of exposure is through dust emitted
by air-powered seed planters. Several years before the
emergence of colony collapse disorder, neonicotinoid
manufacturers started to coat seeds in the pesticides,
vastly increasing the amount used in fields. The
coatings are partially pulverized inside seed planters
and emitted in plumes that appear to be highly toxic.
Neonicotinoids also remain biologically active in soil
for years and perhaps decades, and it's possible that
they seep into roots and throughout plants in ways that
haven't yet been measured, said Krupke.
The Environmental Protection Agency is currently
evaluating the safety of neonicotinoids, and more than
1.25 million people have signed petitions requesting a
ban. In parts of Europe that have already banned
neonicotinoids, colony collapse disorder may have
slowed, though Krupke said these reports are too
anecdotal to consider scientifically reliable.
"If the relationship was as easy as that, we'd have
noticed it long ago. There are areas where
neonicotinoids are used, but you don't have colony
loss," Krupke said. "But what these studies are showing
is that because neonicotinoids are absolutely
ubiquitous, and we're seeing sub-lethal effects, is that
they're stressors. They've softened up the bees for
Pesticide risk analysis in the United States has focused
too much on whether chemicals are immediately, obviously
toxic, said Krupke. "Our way of thinking is
fundamentally flawed," he said. "We need to look at sub-
lethal effects, and for a longer time period. These
pesticides are everywhere, every year. We've never used
pesticides in the way we're using them now, where we
charge up a plant and it expresses pesticides all year
Lu described standing in front of the dosed beehives
used in his experiment, and referenced Silent Spring, an
influential work that lamented the unintended
consequences of bird-killing pesticides.
"The hives were dead silent," he said. "I kind of ask
myself: Is this the repeat of Silent Spring? What else
do we need to prove that it's the pesticides causing
colony collapse disorder?"
Image: Maja Dumat/Flickr Video: A honeybee dies after
eating guttation droplets released by corn grown from
commercial imidacloprid-coated seeds. (Girolami et
al./Journal of Economic Entomology)
Citation: "In situ replication of honey bee colony
collapse disorder." By Chensheng Lu, Kenneth M. Warchol,
Richard A. Callahan. Bulletin of Insectology, June 2012.
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