European beekeepers observed similar phenomena in Belgium, France, the Netherlands, Greece, Italy, Portugal, and Spain, and initial reports have also come in from Switzerland and Germany, albeit to a lesser degree. Possible cases of CCD have also been reported in Taiwan since April 2007.
The cause or causes of the syndrome are not yet fully understood, although many authorities attribute the problem to biotic factors such as: Varroa mites and insect diseases (i.e., pathogens including Nosema apis and Israel acute paralysis virus). Other proposed causes include environmental change-related stresses, malnutrition and pesticides (e.g. neonicotinoids such as imidacloprid), and migratory beekeeping. More highly speculative possibilities have included both cell phone radiation and genetically modified (GM) crops with pest control characteristics, though experts point out no evidence exists for either assertion.
From 1971 to 2006, there was a dramatic reduction in the number of feral honeybees in the US (now almost absent); and a significant, though somewhat gradual decline in the number of colonies maintained by beekeepers. This decline includes the cumulative losses from all factors such as urbanization, pesticide use, tracheal and Varroa mites, and commercial beekeepers retiring and going out of business. However, late in the year 2006 and in early 2007 the rate of attrition was alleged to have reached new proportions, and the term "Colony Collapse Disorder" was proposed to describe this sudden rash of disappearances.
Limited occurrences resembling CCD have been documented as early as 1896, and this set of symptoms has in the past several decades been given many different names (disappearing disease, spring dwindle, May disease, autumn collapse, and fall dwindle disease). Most recently, a similar phenomenon in the winter of 2004/2005 occurred, and was attributed to Varroa mites (the "Vampire Mite" scare), though this was never ultimately confirmed. Nobody has been able to determine the cause of any past appearances of this syndrome. Upon recognition that the syndrome does not seem to be seasonally-restricted, and that it may not be a "disease" in the standard sense — that there may not be a specific causative agent — the syndrome was renamed.
There are also putative cases reported by the media from India, Brazil and parts of Europe. Since the beginning of the 1990s, France, Belgium, Italy, Germany, Switzerland, Spain, Greece, Slovenia and the Netherlands have been affected by honey bee disappearances, though this is not necessarily associated with CCD; Austria and United Kingdom (where it has been dubbed the "Mary Celeste" phenomenon, after a ship whose crew disappeared in 1872) have also reportedly been affected. It is far from certain that all or any of these reported non-US cases are indeed CCD: there has been considerable publicity, but only rarely was the phenomenon described in sufficient detail. In Germany, for example, where some of the first reports of CCD in Europe appeared, and where — according to the German national association of beekeepers — 40% of the honey bee colonies died, there has been no scientific confirmation; as of early May 2007, the German media were reporting that no confirmed CCD cases seemed to have occurred in Germany.
The exact mechanisms of CCD are still unknown. One report indicates a strong but possibly non-causal association between the syndrome and the presence of the Israel acute paralysis virus. Other factors may also be involved, however, and several have been proposed as causative agents; malnutrition, pesticides, pathogens, immunodeficiencies, mites, fungus, genetically modified (GM) crops, beekeeping practices (such as the use of antibiotics, or long-distance transportation of beehives) and electromagnetic radiation. Whether any single factor is responsible, or a combination of factors (acting independently in different areas affected by CCD, or acting in tandem), is still unknown. It is likewise still uncertain whether CCD is a genuinely new phenomenon, as opposed to a known phenomenon that previously only had a minor impact.
At present, the primary source of information, and presumed "lead" group investigating the phenomenon, is the Colony Collapse Disorder Working Group, based primarily at Penn State University. Their preliminary report pointed out some patterns, but drew no strong conclusions. A survey of beekeepers early in 2007 indicates that most hobbyist beekeepers believed that starvation was the leading cause of death in their colonies, while commercial beekeepers overwhelmingly believed that invertebrate pests (Varroa mites, honey bee tracheal mites, and/or small hive beetles) were the leading cause of colony mortality. A scholarly review in June 2007, similarly addressed numerous theories and possible contributing factors, but left the issue unresolved.
In July 2007, the USDA released its "CCD Action Plan", which outlines a strategy for addressing CCD consisting of four main components:
As of late 2007, there is still no consensus of opinion, and no definitive causes have emerged; the schedule of presentations for a planned national symposium on CCD, titled "Colony Collapse Disorder in Honey Bees: Insight Into Status, Potential Causes, and Preventive Measures," which is scheduled for December 11, 2007, at the meeting of the Entomological Society of America in San Diego, California, gives no indication of any major breakthroughs.
Some researchers have attributed the syndrome to the practice of feeding high fructose corn syrup (HFCS) to supplement winter stores. The variability of HFCS may be relevant to the apparent inconsistencies of results. European commentators have suggested a possible connection with HFCS produced from genetically modified corn. If this were the sole factor involved, however, this should also lead to the exclusive appearance of CCD in wintering colonies being fed HFCS, but many reports of CCD occur in other contexts, with beekeepers who do not use HFCS.
Some researchers have commented that the pathway of propagation functions in the manner of a contagious disease; however, there is some sentiment that the disorder may involve an immunosuppressive mechanism, potentially linked to the aforementioned "stress" leading to a weakened immune system. Specifically, according to researchers at Penn State: "The magnitude of detected infectious agents in the adult bees suggests some type of immunosuppression." These researchers initially suggested a connection between Varroa destructor mite infestation and CCD, suggesting that a combination of these bee mites, deformed wing virus (which the mites transmit) and bacteria work together to suppress immunity and may be one cause of CCD. This research group is reported to be focusing on a search for possible viral, bacterial, or fungal pathogens which may be involved.
When a colony is dying, for whatever cause, and there are other healthy colonies nearby (as is typical in a bee yard), those healthy colonies often enter the dying colony and rob its provisions for their own use. If the dying colony's provisions were contaminated (by natural or man-made toxins), the resulting pattern (of healthy colonies becoming sick when in proximity to a dying colony) might suggest to an observer that a contagious disease is involved. However, it is typical in CCD cases that provisions of dying colonies are not being robbed, suggesting that at least this particular mechanism (toxins being spread via robbing, thereby mimicking a disease) is not involved in CCD.
Additional evidence that CCD might be an infectious disease came from the following observation: the hives of colonies that had died from CCD could be reused with a healthy colony only if they were first treated with DNA-destroying radiation.
According to a 2007 article, the mites Varroa destructor remain the world's most destructive honey bee killer due in part to the viruses they carry, including Deformed Wing Virus and Acute bee paralysis virus, which have both been implicated in CCD. Affliction with Varroa mites also tends to weaken the immune system of the bees. As such, Varroa have been considered as a possible cause of CCD, though not all dying colonies contain these mites.
In September 2007, results of a large-scale statistical RNA sequencing study of afflicted and non-afflicted colonies were reported. RNA from all organisms in a colony was sequenced and compared with sequence databases to detect the presence of pathogens. The study used technology from 454 Life Sciences developed for human genome sequencing. All colonies were found to be infected with numerous pathogens, but only the Israel acute paralysis virus (IAPV) showed a significant association with CCD: the virus was found in 25 of the 30 tested CCD colonies, and only in one of the 21 tested non-CCD colonies. Scientists pointed out that this association was no proof of causation, and other factors may also be involved in the disease or the presence of IAPV may only be a marker signifying afflicted colonies and not the actual causative agent. To prove causation, experiments are planned to deliberately infect colonies with the virus.
The IAPV was discovered in 2004 and belongs to the Dicistroviridae. It causes paralysis in bees which then die outside of the hive. It can be transmitted by the mite Varroa destructor. These mites, however, were found in only half of the CCD colonies.
The virus was also found in samples of Australian honey bees. Australian honey bees have been imported into the U.S. since 2004 and until recently it was thought possible that this is how the virus originally reached North America. Recent findings, however, reveal the virus has been present in American bees since 2002.
Some have suggested that the syndrome may be an inability by beekeepers to correctly identify known diseases such as European foulbrood or the microsporidian fungus Nosema. The testing and diagnosis of samples from affected colonies (already performed) makes this highly unlikely, as the symptoms are fairly well-known and differ from what is classified as CCD. A high rate of Nosema infection was reported in samples of bees from Pennsylvania, but this pattern was not reported from samples elsewhere.
Mariano Higes, a scientist heading a team at a government-funded apiculture centre in Guadalajara, Spain, has reported that when hives of European honey bees were infected with Nosema ceranae, a recently described microsporidian fungus, the colonies were wiped out within eight days. Higes has extrapolated from this research to conclude that CCD is caused by N. ceranae. Higes and his team have worked on this problem since 2000, and claim to have ruled out many other potential causes. Various areas in Europe have reported this fungus, but no direct link to CCD has yet been established. Highly preliminary evidence of N. ceranae was recently reported in a few hives in the Merced Valley area of California (USA). The researcher did not, however, believe this was conclusive evidence of a link to CCD; "We don't want to give anybody the impression that this thing has been solved. A USDA bee scientist has similarly stated, "while the parasite Nosema ceranae may be a factor, it cannot be the sole cause. The fungus has been seen before, sometimes in colonies that were healthy. Likewise, a Washington State beekeeper familiar with N. ceranae in his own hives discounts it as being the cause of CCD. A study reported in September 2007 found that 100% of afflicted and 80% of non-afflicted colonies contained Nosema ceranae.
The primary antibiotic used against Nosema is Fumagillin, which has been used in a German research project to reduce the microsporidian's impact, and is mentioned as a possible remedy by the CCDWG.
It is particularly difficult to evaluate pesticide contributions to CCD for several reasons. First, the variety of pesticides in use in the different areas reporting CCD makes it difficult to test for all possible pesticides simultaneously. Second, many commercial beekeeping operations are mobile, transporting hives over large geographic distances over the course of a season, potentially exposing the colonies to different pesticides at each location. Third, the bees themselves place pollen and honey into long-term storage, effectively meaning that there may be a delay of anywhere from days to months before contaminated provisions are fed to the colony, negating any attempts to associate the appearance of symptoms with the actual time at which exposure to pesticides occurred. Pesticides used on bee forage are far more likely to enter the colony via the pollen stores rather than via nectar (because pollen is carried externally on the bees, while nectar is carried internally, and may kill the bee if too toxic), though not all potentially lethal chemicals, either natural or man-made, affect the adult bees — many primarily affect the brood, but brood die-off does not appear to be happening in CCD. Most significantly, brood are not fed honey, and adult bees consume relatively little pollen; accordingly, the pattern in CCD suggests that if contaminants or toxins from the environment are responsible, it is most likely to be via the honey, as it is the adults that are dying (or leaving), not the brood.
One recently published view is that bees are falling victim to new varieties of nicotine-based pesticides; beekeepers in Canada are also losing their bees and are blaming neonicotinoid pesticides. To date, most of the evaluation of possible roles of pesticides in CCD have relied on the use of surveys submitted by beekeepers, but it seems likely that direct testing of samples from affected colonies will be needed, especially given the possible role of systemic insecticides such as the neonicotinoid imidacloprid (which are applied to the soil and taken up into the plant's tissues, including pollen and nectar), which may be applied to a crop when the beekeeper is not present. The known effects of imidacloprid on insects, including honey bees, are consistent with the symptoms of CCD; for example, the effects of imidacloprid on termites include apparent failure of the immune system, and disorientation. In Europe the interaction of the phenomenon of "dying bees" with imidacloprid, has been discussed for quite some time now. It was a study from the "Comité Scientifique et Technique (CST)" which was in the center of discussion recently, which led to a partial ban of imidacloprid in France (known as Gaucho), primarily due to concern over potential effects on honey bees. Consequently when fipronil, a phenylpyrazole insecticide and in Europe mainly labeled "Regent", was used as a replacement, it was also found to be toxic to bees, and banned partially in France in 2004. In February 2007, about forty French deputies, led by UMP member Jacques Remiller, requested the creation of a Parliamentary Investigation Commission on Overmortality of Bees, underlining that the honey production was decreasing by 1,000 tons a year for a decade. As of August 2007, no investigations were yet opened. The imidacloprid pesticide Gaucho was banned, however, in 1999 by the French Minister of Agriculture Jean Glavany. Five other insecticides based on fipronil were also accused of killing bees. However, the scientific committees of the European Union are still of the opinion "that the available monitoring studies were mainly performed in France and EU-member-states should consider the relevance of these studies for the circumstances in their country.
In 2005, a team of scientists led by the National Institute of Beekeeping in Bologna, Italy, found that pollen obtained from seeds dressed with imidacloprid contains significant levels of the insecticide, and suggested that the polluted pollen might cause honey bee colony death. Analysis of maize and sunflower crops originating from seeds dressed with imidacloprid suggest that large amounts of the insecticide will be carried back to honey bee colonies. Sub-lethal doses of imidacloprid in sucrose solution have also been documented to affect homing and foraging activity of honeybees. Imidacloprid in sucrose solution fed to bees in the laboratory impaired their communication for a few hours. Sub-lethal doses of imidacloprid in laboratory and field experiment decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired. However, no detailed studies of toxicity or pesticide residue in remaining honey or pollen in CCD-affected colonies have been published so far, so, despite the similarity in symptoms, no connection of neonicotinoids to CCD has yet been confirmed.
Most beekeepers affected by CCD report that they use antibiotics and miticides in their colonies, though the lack of uniformity as to which particular chemicals are used makes it seem unlikely that any single such chemical is involved. However, it is possible that not all such chemicals in use have been tested for possible effects on honey bees, and could therefore potentially be contributing to the CCD phenomenon. Some reports indicate that organic beekeepers (who do not use antibiotics or miticides) are not affected by CCD, despite proximity to non-organic beekeepers that have been affected.
In 2006 the "Committee on Status and Trends of Pollinators" of the United States National Research Council published a report on the "Status of Pollinators in North America". It suggested that GMO, besides other factors, might contribute to pollinator decline because, according to one scientific review of "the small literature on this topic, ... in some cases, there are negative but sublethal effects attributable to consumption of transgenic pollens." The report goes on to say that, "These effects varied with the identity of the transgene and the amount of its expression, but in no case have any effects of transgenic crops on honey bee populations been documented.
The preliminary report of the Colony Collapse Disorder Working Group concluded that while there is no evidence of any lethal or sub-lethal effects from Bt crops on honey bees, further research should be conducted. On March 28, 2007, the "Mid-Atlantic Apiculture Research and Extension Consortium published a new "Summary of Research on the Non-Target Effects of Bt Corn Pollen on Honeybees", which states that according to "a field study… (soon to be published in the bee journal Apidologie) there is no evidence thus far of any lethal or sub-lethal effects of the currently used Bt proteins on honey bees", and, specifically regarding the possible causal connections between Bt pollen and CCD, stated "While this possibility has not been ruled out, the weight of evidence reported here argues strongly that the current use of Bt crops is not associated with CCD." They further noted that CCD cases "have occurred in Europe and areas of Canada where Bt crops were not grown."
Since US beekeeper Nephi Miller first began moving his hives to different areas of the country for the winter of 1908, migratory beekeeping has become widespread in America.
Bee rental for pollination is a crucial element of US agriculture, which could not produce anywhere near its current levels with native pollinators alone. US beekeepers collectively earn much more from renting their bees out for pollination than they do from honey production.
Researchers are concerned that trucking colonies around the country to pollinate crops, where they intermingle with other bees from all over, helps spread viruses and mites among colonies. Additionally, such continuous movement and re-settlement is considered by some a strain and disruption for the entire hive, possibly rendering it less resistant to all sorts of systemic disorder.
Beekeepers in Europe and Asia are generally far less mobile, with bee populations moving and mingling within a smaller geographic extent (although some keepers do move longer distances, it is much less common).
This wider spread and intermingling in the US has resulted in far greater losses from Varroa mite infections in recent years.
A few scientists have suggested that climate change can make bee hives more vulnerable to CCD, although it is not implicated as a direct cause of the disorder. "We see plants blooming at different times of the year," says amateur beekeeper Wayne Esaias, a researcher at the NASA Goddard Space Flight Center, "and that's why the nectar flows are so much earlier now. I need to underscore that I have no evidence that global warming is a key player in colony collapse disorder. But it might be a contributor, and changes like this might be upping the stress level of our bee populations.
The 2006 University of Landau pilot study was looking for non-thermal effects of radio frequency ("RF") on honey bees (Apis mellifera carnica) and suggested that when bee hives have DECT cordless phone base stations embedded in them, the close-range electromagnetic field ("EMF") may reduce the ability of bees to return to their hive; they also noticed a slight reduction in honeycomb weight in treated colonies. In the course of their study, one half of their colonies broke down, including some of their controls which did not have DECT base stations embedded in them.
The team's 2004 exploratory study on non-thermal effects on learning did not find any change in behavior due to RF exposure from the DECT base station operating at 1880-1900 MHz.
Like the links to CCD from variants (herbicides, genetically modified crops, etc), the link of either cordless or cellular phones, cell towers, interference by the High Frequency Active Auroral Research Program (HAARP) or Ground Wave Emergency Network (GWEN) to CCD is speculative.
Honey bees are not native to the Americas, therefore their necessity as pollinators in the US is limited to strictly agricultural/ornamental uses, as no native plants require honey bee pollination, except where concentrated in monoculture situations—where the pollination need is so great at bloom time that pollinators must be concentrated beyond the capacity of native bees (with current technology).
They are responsible for pollination of approximately one third of the United States' crop species, including such species as almonds, peaches, soybeans, apples, pears, cherries, raspberries, blackberries, cranberries, watermelons, cantaloupes, cucumbers and strawberries. Many but not all of these plants can be (and often are) pollinated by other insects in small holdings in the U.S., including other kinds of bees, but typically not on a commercial scale. While some farmers of a few kinds of native crops do bring in honey bees to help pollinate, none specifically need them, and when honey bees are absent from a region, there is a presumption that native pollinators may reclaim the niche, typically being better adapted to serve those plants (assuming that the plants normally occur in that specific area).
However, even though on a per-individual basis, many other species are actually more efficient at pollinating, on the 30% of crop types where honey bees are used, most native pollinators cannot be mass-utilized as easily or as effectively as honey bees—in many instances they will not visit the plants at all. Beehives can be moved from crop to crop as needed, and the bees will visit many plants in large numbers, compensating via sheer numbers for what they lack in efficiency. The commercial viability of these crops is therefore strongly tied to the beekeeping industry.