(Fortune Magazine) -- It's a sweet time for honeybees in the rolling hills of eastern Pennsylvania, and the ones humming around Dennis vanEngelsdorp seem too preoccupied by the blooming knapweed nearby to sting him as he carefully lifts the top off their hive. VanEngelsdorp, Pennsylvania's state apiarist, spots signs of plenty within: honeycomb stocked with yellow pollen, neat rows of wax hexagons housing larval bees, and a fertile queen churning out eggs.
But something has gone terribly wrong in this little utopia in a box. "There should be a lot more workers than there are," he says. "This colony is in trouble."
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Pennsylvania apiarist Dennis vanEngelsdorp helped form a group trying to crack the case of the vanishing insects.
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A frame removed from a hive afflicted by colony collapse disorder (CCD). The 'smoker' on top is used to sedate the bees.
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David Hackenberg sounded the alarm about collapsing colonies.
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That pattern -- worker bees playing Amelia Earhart -- has become dismayingly familiar to the nation's beekeepers over the past year, as well as to growers whose crops are pollinated by honeybees. A third of our food, from apples to zucchinis, begins with floral sex acts abetted by honeybees trucked around the country on 18-wheelers.
The mysterious deaths of the honeybees
We wouldn't starve if the mysterious disappearance of bees, dubbed colony collapse disorder, or CCD, decimated hives worldwide. For one thing, wheat, corn, and other grains don't depend on insect pollination.
But in a honeybee-less world, almonds, blueberries, melons, cranberries, peaches, pumpkins, onions, squash, cucumbers, and scores of other fruits and vegetables would become as pricey as sumptuous old wine. Honeybees also pollinate alfalfa used to feed livestock, so meat and milk would get dearer as well. Ditto for farmed catfish, which are fed alfalfa too.
And jars of honey, of course, would become golden heirlooms to pass along to the grandkids. (Used for millennia as a wound dressing, honey contains potent antimicrobial compounds that enable it to last for decades in sealed containers.)
In late June, U.S. Agriculture Secretary Mike Johanns starkly warned that "if left unchecked, CCD has the potential to cause a $15 billion direct loss of crop production and $75 billion in indirect losses."
$9.3 billion worth of endangered crops
Late last year vanEngelsdorp, a strapping, 37-year-old Netherlands native with a thatch of blond hair and a close-cropped goatee, helped organize a group of bee experts to identify the killer. In recent months he's acted as the team's gumshoe, driving thousands of miles to collect bees and honeycomb samples from CCD-afflicted hives to analyze for clues.
Meanwhile, Pennsylvania State University entomologist Diana Cox-Foster has scoured bees from collapsed colonies for signs of disease-causing microbes. She's shown that the insects are chock-full of them, as if their immune systems are suppressed.
Now the entomologists, aided by Ian Lipkin, a Columbia University scientist known for cracking the case of the West Nile virus (he identified the mosquito-transmitted killer of birds and sometimes people), are closing in on possible culprits and reportedly have submitted a study identifying a virus associated with CCD to a scientific journal. The bug may have been introduced into the U.S. via imported bees or bee-related products, say researchers familiar with the study.
"If I were a betting man," says Dewey Caron, a University of Delaware entomologist who co-authored a recent report on CCD's toll, "I'd bet it's a virus that's fairly new or one that's mutated to become more virulent." Other pathogens, such as fungi, may have combined forces with the virus, he adds.
But merely showing that germs selectively turn up in cases of CCD, he cautions, won't necessarily nail the culprit, for it will leave a key question unanswered: Are such microbes the main killers, or has something else stomped bees' immune systems, making them vulnerable to the infections?
After all, the first report on AIDS focused on a strange outbreak of rare fungal pneumonia, "opportunistic" infections whose root cause was later identified as HIV, the human immunodeficiency virus.
A fight about fish farms
Fortunately, a bee apocalypse seems unlikely at this point. Beekeepers have recovered from CCD-like hits in the past -- major bee die-offs seem to occur about once a decade. Most beekeepers recently contacted by Fortune say hives generally appear normal of late.
Still, ominous reports of worker-scarce hives like the one vanEngelsdorp recently examined suggest that whatever causes CCD is still in circulation and may well decimate hives again when bees' floral support system drops away this fall.
If that happens, "it will be a lot worse than the first time, because [commercial beekeepers] have already spent a lot of their money" replacing lost bees, says Richard Adee, head of the country's largest beekeeping operation, Adee Honey Farms of Bruce, S.D., which, despite its name, is largely a pollination business.
The losses weren't insured, he adds: Because of all the unpredictable things that can kill bees, from mites to droughts, insurers have long refused to cover them. "We'll see a lot of guys just hang it up."
So that's the thing to worry about: While CCD isn't likely to obliterate honeybees, it may wipe out enough migratory beekeepers to precipitate a pollination crisis.
They're already thin on the ground -- a rare breed of truck drivers who also happen to be applied entomologists, amateur botanists, skilled nursemaids of cussed old machines, traveling salesmen, and Job-like nurturers of finicky, stinging insects that, when they're not mysteriously dying off, can suddenly swarm on you like something out of Hitchcock.
Commercial beekeepers make up only about 1% of the 135,000 owners of hives in the U.S., but they manage over 80% of the nation's 2.4 million honeybee colonies. If the waning number of hives in the U.S. is any indication, commercial beekeeping was already in a long-term decline before CCD struck -- in 1960 there were about five million hives, more than twice as many as there are today.
Meanwhile, demand for pollination services is growing, largely because of our love affair with the almond -- it's increasingly seen as a health food, and the FDA acknowledged in 2004 that there are data "suggesting" a daily dose of 1.5 ounces of almonds or other nuts, along with a low-fat diet, may lower the risk of heart disease. By 2012 nearly 90% of the hives now estimated to exist in the U.S. will be needed to pollinate California's almond groves each spring, according to the Almond Board of California.
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Commercial beekeeping has a lot in common with the disappearing family farm. The typical bee rancher is a salt-of-the-earth, 50-something, strong-armed guy who often sweats through the night forklifting hives filled with seriously annoyed bees onto a flatbed semi in order to rush them to his next customer's field 500 miles away, which just may be near a crop sprayed with insecticides that will kill 15% of his livestock as they wing around the area.
Cheap honey imported from China and Argentina has clobbered his profits, forcing him to work his bees ever harder as migratory pollinators. He loses lots of bees to "vampire" mites, hive-busting bears, human vandals, and sometimes to beekeepers gone bad, who steal hives by night and pollinate by day. His kids can see that there are much easier ways to make a living.
But for all that, he's never lost the sense of wonder that came over him the first time he heard the piping of a queen -- a kind of battle cry that newly emerged honeybee queens make before fighting to the death for hive supremacy. From outside a hive, it sounds like a child wistfully tooting a toy trumpet in a distant room.
If CCD flares up again, one of the casualties may be the Paul Revere of colony collapse, a lanky, 58-year-old beekeeper named David Hackenberg. The story of the disappearing bees began one afternoon last October when he and his son Davey pulled into one of their "bee yards" near Tampa to check on 400 hives they had placed there three weeks earlier.
The Hackenbergs' main center of operations is a farm near Lewisburg, Pa., but like most migratory beekeepers, they move their bees south each winter for a few months of R&R (rest and reproduction) before the rigors of spring pollination.
Hackenberg, a gregarious raconteur with a Walter Brennan voice, says the first sign of trouble was that "there were hardly any bees flying around the hives. It was kind of a weird sensation, no bees in the air. We got out our smokers" -- bellows grafted to tin cans that beekeepers use to waft bee-sedating smoke into hives before opening them - "and smoked a few hives, and suddenly I thought, 'Wait a minute, what are we smoking?'
"Next thing, I started jerking covers off hives ... It was like somebody took a sweeper and swept the bees right out of the boxes. I set there a minute scratching my head, then I literally got down on my hands and knees and started looking for dead bees. But there weren't any."
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Hackenberg spread the word about his vanished bees. Within days other beekeepers began reporting similar cases. Penn State's Cox-Foster, vanEngelsdorp, and other bee experts launched an investigation. After turning up more than a dozen cases of collapsing colonies across the country, the team issued a report in mid-December telling of beekeepers who'd lost up to 90% of their bees.
The "unprecedented losses," according to the report, had many keepers "openly wondering if the industry can survive."
By late spring CCD had made headlines around the world. Assorted phobia purveyors vied to adopt the die-off as a poster child for everything from cellphone emanations to God's Just Wrath. Internet bloggers thrilled themselves silly bandying about a sentence from Albert Einstein, which the great physicist apparently tossed off about 40 years after his death to the public-relations department of a French beekeeping group: "If the bee disappears from the surface of the earth, man will have no more than four years to live."
A survey sponsored by Bee Alert Technology, a Missoula, Mont., firm that sells hive-tracking devices and other bee wares, turned up reports of CCD in 35 states and Puerto Rico by early June.
Despite the widespread impression that CCD started with Hackenberg's losses last October in Florida, says Bee Alert CEO Jerry Bromenshenk, "our survey shows that it probably first began to show up the previous spring in Michigan, Wisconsin, and Iowa. By midsummer [last year] it was moving through the heartland," hitting hives in the Dakotas, then appearing widely a few months later in the South and on both coasts.
A survey led by vanEngelsdorp and Florida apiary inspector Jerry Hayes suggests that a quarter of U.S. beekeepers were struck by CCD between September 2006 and March 2007. Those hit by mysterious die-offs lost, on average, 45% of their hives.
The surveys failed to show patterns suggesting CCD's cause. But they provided alibis for some prime suspects, such as beekeeper enemy No. 1: blood-sucking Varroa destructor mites. (Picture a tick as big as a Frisbee glommed onto your back -- that's what Varroa is like for a bee.) Varroa both transmits harmful viruses to bees and suppresses their immune systems.
But CCD has been reported in many hives without significant mite problems, says Jeff Pettis, an entomologist at the U.S. Department of Agriculture's Bee Research Laboratory in Beltsville, Md.
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Another leading suspect -- stress on bees due to migratory pollination -- hasn't gotten off the hook so easily. Low honey prices coupled with rising pollination fees for certain crops have prompted migratory beekeepers to put their bees on the road more than ever during the past few years.
Some now truck hives coast to coast, beginning in February with California almonds, then moving on to crops in the East, such as Maine blueberries. That potentially exposes bees to ever more diseases and insecticides. And many of the crops, such as cranberries, don't provide adequate bee nutrition.
The insects aren't very good travelers either. When a truck carrying bees gets caught in a summer traffic jam, for instance, hives quickly overheat, despite the fact that the millions of workers inside them furiously fan their wings in an attempt to prevent it, says Wes Card, a beekeeper whose Merrimack Valley Apiaries in Billerica, Mass., pollinates crops from California to Maine.
"Then every minute counts," he adds, for unless the driver can quickly find a way to pull off the road and hose down the hives with cooling water, desperately hot queens emerge from their inner sanctums and typically wind up venturing into nearby colonies on the truck, where they are perceived as alien invaders and promptly killed. (Ironically, worker bees typically execute a condemned monarch by clustering around her and vibrating their wing muscles to generate heat, fatally raising her temperature -- beekeepers call it "balling the queen" because the executioners form a ball of bees.) A hot day can turn a load of hives into a costly mess within minutes.
Stress probably isn't the main culprit, though. In fact, the biggest commercial beekeepers -- those with over 500 hives, most of whom are migratory pollinators -- lost a smaller percentage of their hives when hit by CCD last winter than did hobbyist beekeepers, according to the survey co-authored by vanEngelsdorp.
Further, there's some evidence that CCD may antedate the modern stresses put on bees. Large numbers of honeybees have mysteriously vanished a number of times since the mid-19th century, suggesting that CCD may be just the latest episode in a "cycle of disappearance" caused by a mystery disease that periodically flares up like a deadly worldwide flu epidemic.
Still, entomologists who have personally observed the effects of CCD insist that it is unlike any bee die-off they've seen. The University of Delaware's Caron, one of the bee world's biggest names, says he was stunned when 11 of 12 hives in the school's apiary collapsed last winter, apparently because of CCD.
"Never in 40 years had I witnessed the symptoms I was seeing," he says.
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One of CCD's strangest symptoms, say bee experts, is a phenomenon that might be called the madness of the nurses. Nurse bees are workers that nurture a hive's preadult bees, called brood. Workers begin their adult lives as nurses, and only during the final third or so of their six-week lives do they become foragers, venturing outside the hive to collect nectar and pollen.
Researchers have discovered that the young nurses are maintained in a kind of immature, thickheaded state by chemical signals emanating from the queen. Nurses aren't supposed to leave the hive. They're not ready to cope with the big outside world, which requires a mature bee's smarts. Besides, with nurses on leave, the all-important brood would wither.
Yet empty hives struck by CCD are often found with intact brood, which means nurses were on the job shortly before all the bees flew off forever. Beekeepers find this gross dereliction of duty much weirder than the disappearance of foragers, which essentially work themselves to death and often die outside the hive.
Says Hackenberg: "Basically, I've never seen bees go off and leave brood. That's the real kicker."
To explain the psychotic behavior, some beekeepers, including Hackenberg, point the finger at an increasingly popular class of insecticides called neonicotinoids. The chemicals are widely used by farmers on fruits and vegetables that bees pollinate, as well as on corn and other crops often grown nearby.
Soon after Bayer (Charts), the German drug and chemicals concern, first put the products on the market in the early 1990s, they were implicated in a bee die-off in France, where their use was then sharply restricted. Since 2000, studies by French and Italian researchers have suggested that low, "sublethal" doses of the chemicals -- which bees might get from lingering traces of the insecticides in fields -- can mess up the insects' memories and navigational abilities, potentially making them get lost. Bayer has countered with its own studies, which it asserts demonstrate that the products, when properly used, don't pose significant risks.
Honeybees' exposure to trace amounts of neonicotinoids can't be ruled out, says Chris Mullin, a Penn State University entomologist investigating whether pesticides are involved in CCD.
But he and other CCD investigators doubt that neonicotinoids will turn out to be the primary culprits. For one thing, many other chemicals to which bees are exposed are nerve toxins that can make them act strange at low doses. And it's hard to reconcile the rapid, widespread appearance of CCD last year with the fact that numerous such chemicals have long been widely used.
Could infectious microbes induce the nurses' insanity?
The great corn gold rush
Maybe. Young workers with a disease caused by "sacbrood" virus tend to start foraging abnormally early in life, when their healthy peers are still nursing. And as if discombobulated in their new roles, they fail to collect pollen.
Although sacbrood virus has been detected in bees from some hives with CCD symptoms, as have a number of other viruses, it doesn't appear to be closely associated with the disorder. But its ability to warp young bees' behavior suggests that viruses may well induce nurses to do the unthinkable.
Another explanation may make more sense, though: Perhaps the nurses aren't really acting crazy when they fly away. Instead, their strange behavior may represent a perfectly natural attempt by doomed workers to protect their sisters from killer microbes.
After all, a hive's workers represent a famously close-knit sorority, geared by evolution to act strictly in the best interests of their colonies. (Male "drones" don't work, by the way. They loaf about the hive most of their lives, zip out about noon every day in hopes of mating on the wing with young queens, then immediately die after copulating, presumably happy.) Beekeepers have long known that sick bees generally leave the hive to die, minimizing the risk that they will infect others.
In his seminal 1879 tome The A B C of Bee Culture, Amos Ives Root, an early giant of U.S. beekeeping, marveled that "when a bee is crippled or diseased from any cause, he [sic] crawls away ... out of the hive, and rids the community of his presence as speedily as possible. If bees could reason, we would call this a lesson of heroic self-sacrifice for the good of the community."
Might a fast-spreading, immune-suppressing disease be making nurses so sick that their urge to stay put is overruled by the altruistic impetus to depart?
The organic milk price war
The effort to answer such questions has entered a new phase with the recent linking of specific infectious agents to CCD (the ones whose identities are expected to be disclosed soon in a scientific journal). Now Cox-Foster says she and colleagues are trying to reproduce CCD's effects on bee colonies by seeding healthy hives with the agents -- the biomedical equivalent of getting a killer to confess.
Meanwhile, scattered reports over the summer of hives with abnormally few workers and little stored honey have many bee people worried. A few beekeepers, frazzled by earlier heavy losses and worried that truly ruinous ones are on the way, have already bailed out.
CCD 2 would probably be a lot uglier for growers -- and for us fruit and veggie eaters -- than version one was. In fact, we got lucky the first time it hit: "A lot of the bees brought to California this year were total junk," their hives sparsely populated because of CCD and other problems, says Lyle Johnston, a Rocky Ford, Colo., beekeeper who arranges the placement of 50,000 hives owned by other keepers in almond groves each spring. "But we had the most perfect weather during the almond bloom that I can recall. It saved our butts," by enabling bees to take to the air more often than they usually do.
"We dodged the bullet with fruit, too, this year," says the University of Delaware's Caron. "We had weak bees, but the weather was exceptional during the apple, blueberry, and cranberry blooms."
Unfortunately, Caron and others note, by keeping crop prices low, the good weather may have actually discouraged legislators from funding studies on CCD. To beekeepers' dismay, the farm bill recently passed by the U.S. House of Representatives, which calls for $286 billion to be spent over the next five years on everything from school snacks to biofuels, earmarked no funds specifically for CCD research.
And the lucky run of weather probably won't last much longer. Extraordinarily dry weather through spring and early summer in California and the Southeast has stressed bees in those regions, potentially setting up many hives for collapse later in the year.
Despite making some progress, cash-strapped scientists looking into CCD aren't likely to identify what causes it -- and ways to fend it off -- before the high-risk season for bee die-offs arrives with the onset of cold weather.
So what to do in light of this new, unsolved, and probably ongoing threat to our food supply? Don't panic. But do take time to slowly savor your next sweet, spicy slice of cantaloupe, watermelon, apple, peach, or pear.
The pure pleasure of it may get a lot rarer.