We may not realize it, but we need honey bees. They are responsible for many of the fruits, vegetables, nuts and grains we consume daily. However, suddenly American beekeepers are finding their colony populations dwindling down.

This article originally appeared in PLoS Biology, the peer-reviewed biology journal of the Public Library of Science. It has been edited by the Blast Magazine staff for our readers. The full-text article is available here with all citations and references.

By Benjamin P. Oldroy

On February 22, 2007, many Americans woke up to media reports that something was awry with their honey bees. A significant proportion of American beekeepers were complaining of unusually high rates of colony loss as their bees broke from their overwintering clusters. Loss of some colonies (say 10%) in early spring is normal and occurs every year. In 2007, however, losses were particularly heavy and widespread—beekeepers in 22 states (including Hawaii) reported the problem. Some beekeepers lost nearly all of their colonies. And the problem is not just in the United States. Many European beekeepers complain of the same problem. Moreover, beekeepers and researchers do not understand the specific causes of the losses.

Is there a real problem?

Were the losses in 2007 within the normal range, or is there something new afoot in the bee industry? If there is something new, what is it?

Should beekeepers be worried?

Should we be worried?

The US House Agriculture Committee is sufficiently worried to be holding hearings into the matter, as well they might. Honey bees are essential pollinators: in 2000, the value of American crops pollinated by bees was estimated to be $14.6 billion.

Here, I try to get to the bottom of the unsolved mystery of colony collapse disorder (CCD)—the official description of a syndrome in which many bee colonies died in the winter and spring of 2006–2007.

What is CCD?

The syndrome is mysterious in that the main symptom is simply a low number of adult bees in the hive. (This is a bit like going to a previously well-populated hen house and finding hardly any hens.) There are no bodies, and although there are often many disease organisms present, no outward signs of disease, pests, or parasites exist. Often there is still food in the hive, and immature bees (brood) are present.

The cause of the loss of bees seems to be the sudden early death, in the field, of large numbers of adult workers.

Were the Losses Unusual?

Some winter losses are normal, and because the proportion of colonies dying varies enormously from year to year, it is difficult to say when a crisis is occurring and when losses are part of the normal continuum.

What is clear is that about one year in ten, apiarists suffer unusually heavy colony losses. This has been going on for a long time. In Ireland, there was a “great mortality of bees” in 950, and again in 992 and 1443. One of the most famous events was in the spring of 1906, when most beekeepers on the Isle of Wight (United Kingdom) lost all of their colonies. American beekeepers also suffer heavy losses periodically. There was an incident in 1995 in which Pennsylvania beekeepers lost 53% of colonies.

Often terms such as “disappearing disease” or “spring dwindling” are used to describe the syndrome in which large numbers of colonies die in spring due to a lack of adult bees. However in 2007, some beekeepers experienced 80–100% losses. This is certainly the extreme end of a continuum, so perhaps there is indeed some new factor in play.

What Are the Possible Causes?

Diseases and parasites

Honey bees are affected by a large number of parasites and pathogens. Mostly these have a set of well-defined symptoms that do not relate to CCD. For example, there are two major bacterial diseases that affect the brood: European Foul Brood and American Foul Brood.

The parasitic mite Varroa destructor infests brood cells and lives phoretically on adult bees. But heavy mite infections are obvious to professional beekeepers, especially by the stage where colonies are dying of the infestation. So in itself, Varroa infestation is unlikely to cause CCD.

A Tarsonemid mite Acarapis woodi can infest the trachea of adult bees and is now widespread in North America. Acarapis infections were once thought to be the cause of the famous Isle of Wight disease, with symptoms like CCD.

A protozoan, Nosema apis, infests the guts of adult bees, and when present in high numbers, causes dysentery and early senescence of adult workers. This is also unlikely to be the direct cause of CCD, because the dysentery is obvious and because just about all honey bee colonies are chronically infected with the parasite every spring, even when there are no colony losses.

More likely to play a role in CCD are a variety of viruses that affect adult bees (see table in gallery). Most adult honey bees carry symptomless viral infections. However, under conditions of stress caused by poor nutrition, inclement weather or parasitism, viral populations can increase and cause symptoms in adult bees.

In-hive chemicals

Like other ranchers, many commercial honey producers are compelled by economic necessity to treat their livestock with a cocktail of drugs and pesticides to keep them healthy.

Of particular relevance to CCD are the pesticides used to control parasites and pests.

Beekeepers may be increasing dose rates or trying cocktails of chemicals. Some chemicals, particularly fluvalinate, may accumulate in comb wax, perhaps exposing commercial honey bees to levels of chemical residue that are inimical to worker longevity.

Other beekeepers have tried more “organic” approaches, including fumigation with formic acid, oxalic acid, or essential oils. Although these approaches do not place insecticides in colonies, they may also be less effective at controlling mites, and can be directly toxic to the bees.

Agricultural insecticides

American agricultural systems are dependent on the use of pesticides. Where insecticides are used, honey bee losses are common, and where bees are required for pollination, careful management is required to minimize bee losses.

To maintain effectiveness, new insecticides are constantly in development. Sometimes whole new classes of compounds are developed. Before release, all new compounds go through a rigorous registration process that includes assessment of risk to nontarget organisms, including honey bees. Insecticides must be applied in a manner that is nonhazardous to bees and other beneficial organisms. But as with all risk assessment, it is difficult to foresee all possible consequences of wide-spread usage of a particular compound. Perhaps some new insecticide-related phenomenon is now manifesting as CCD.

Bee poisoning is not very likely in early spring in the northern US, where CCD was most widely reported. Moreover, symptoms of acute insecticide poisoning—large numbers of dead and dying bees at the entrance to colonies—are easy to spot.

Nonetheless, beekeepers and some scientists remain suspicious that not all new compounds are safe for bees. For instance, wide spread losses of colonies in France in recent years have been blamed on a nicotine-like insecticide. Because of its low mammalian toxicity, high effectiveness and high mobility in plant and mammalian tissue, it is often used as systemic insecticide for the control of sap-sucking insects in crops and blood-sucking insects in companion animals. Therein lies the possible problem for honey bees: when applied to plants the insecticide may end up in nectar or pollen.

There is considerable debate about the chances of this happening to a degree that bees are endangered. Some (mainly French) studies report residues of Imidacloprid in nectar and pollen at levels that are potentially dangerous to bees, while others (mainly North American) detected no residues. Moreover, when Imidacloprid was fed to colonies in syrup or pollen at amounts likely to be found in the field, development and survival of colonies was equivalent in treated and control colonies, and contact with the pollen of treated corn plants had no affect on bee longevity.

Can we discount the possibility of nicotine-like insecticides as a contributor to CCD? Not completely. When individual bees are exposed to sub-lethal (some would say miniscule) doses of Imidacloprid, their performance in associative learning and memory tests is impaired. Perhaps there is a certain level of exposure at which foragers have a higher chance of becoming disorientated and lost.

Genetically modified crops

Farmers now have access to varieties of such staple crops as corn, cotton, canola and soybeans, where the genome has been modified to express a bacterium-derived protein with strong insecticidal properties . Crops have also been modified to express herbicide resistance genes, or insect protease inhibitors.

Genetically modified (GM) crops offer important environmental benefits in that the need for the application of pesticides on these crops is much reduced. But do the GM crops expressing insecticides in every cell pose a threat to foraging bees? To date, there is no strong evidence that GM crops cause acute toxicity to honey bees. Furthermore, the involvement of GM crops in CCD seems less likely when we note that states like Illinois, with huge areas under GM crops, have not reported problems with CCD.

Changed cultural practices

The honey price is currently depressed. Urbanization and more intensive agricultural practices are reducing honey yields nation wide. These twin factors lead many beekeepers to seek alternative income streams beyond honey production.

Chief among these is the leasing of colonies for pollination, particularly almond pollination—a crop that is totally dependent on honey bee pollination.

Many crops cause nutritional stress to the bees, or the transport or staging of colonies in holding yards may cause stress. When bees are moved out of these crops, they must feed on high quality pollen to restore body protein levels. This can be achieved by trucking the bees to a location with excellent floral resources or by feeding them. Presumably this is not always done. Anecdotal evidence suggests that CCD is more common in businesses in which bees are trucked large distances and rented for pollination.

Bees also need to feed on high-quality pollen in fall in order to produce long-lived bees that can survive winter. In the US, goldenrod (Solidago virgaurea) is very important in this regard, and the flowering was poor in 2006 in the northeast. Perhaps this contributed to CCD in the following spring.

Cool brood

Remarkably, honey bees maintain the temperature of their brood nest within ± 0.5 °C of 34.5 °C, despite major fluctuations in ambient temperature. If the brood is incubated a little outside this range, the resulting adults are normal physically, but show deficiencies in learning and memory. Workers reared at suboptimal temperatures tend to get lost in the field, and can’t perform communication dances effectively. Although entirely a hypothesis, I suspect that if colonies were unable to maintain optimal brood nest temperatures, CCD-like symptoms would be apparent.

Putting It All Together

We have seen that a large number of factors can produce CCD-like symptoms. We have also seen that CCD is not new: CCD-like symptoms have been known to beekeepers for more than a hundred years but are sufficiently infrequent that when symptoms are severe, beekeepers become concerned that there is something new afflicting their bees.

Clearly CCD is a multifactorial syndrome. Some researchers have suggested that the bees are suffering immunosuppression. Certainly, expression of immune genes in insects is costly, and if bees are stressed by other causes, they may be less able to mount an effective immune response to pathogens. This idea is now eminently testable, because the honey bee genome has been sequenced, and this could be used to determine if the known immune genes are underexpressed in colonies suffering from CCD.

I suggest that another possible cause of CCD might simply be inadequate incubation of the brood. Thus any factor—infections, chronic exposure to insecticides, inadequate nutrition, migration in adult population, and inadequate regulation of brood temperature might cause CCD-like symptoms.

My hypothesis could be easily tested by removing brood from several colonies and incubating some of it at optimal temperature and some at suboptimal temperature. The brood would then be used to constitute new colonies in which some colonies comprise workers raised at low temperature and some comprise workers raised at optimal temperature. I predict that the colonies comprising workers reared at suboptimal temperature will show signs of CCD. Moreover, I would not be surprised if they showed higher levels of stress-related viral infections. These effects could act synergistically—more virus leads to shorter-lived, less efficient workers, that in turn leads to suboptimal temperature regulation, and more short-lived bees.

Dr. Benjamin P. Oldroyd is with the Behaviour and Genetics of Social Insects Laboratory in the School of Biological Sciences at the University of Sydney in New South Wales, Australia. E-mail him

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