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Bee Colony Collapse Disorder
Colony collapse disorder (CCD) is a phenomenon in which worker bees from a beehive or European honey bee colony abruptly disappear. While such disappearances have occurred throughout the history of apiculture, the term colony collapse disorder was first applied to a drastic rise in the number of disappearances of Western honey bee colonies in North America in late 2006. Colony collapse is significant because many agricultural crops worldwide are pollinated by bees.
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 while the Northern Ireland Assembly received reports of a decline greater than 50%. Possible cases of CCD have also been reported in Taiwan since April 2007.
The cause or causes of the syndrome are not yet understood. In 2007, some authorities attributed 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, pesticides (e.g.. neonicotinoids such as clothianidin and imidacloprid), and migratory beekeeping. More speculative possibilities have included both cell phone radiation and genetically modified (GM) crops with pest control characteristics, though no evidence exists for either assertion.
It has also been suggested that it may be due to a combination of many factors and that no single factor is the cause. The most recent report (USDA - 2010) states that "based on an initial analysis of collected bee samples (CCD- and non-CCD affected), reports have noted the high number of viruses and other pathogens, pesticides, and parasites present in CCD colonies, and lower levels in non-CCD colonies. This work suggests that a combination of environmental stressors may set off a cascade of events and contribute to a colony where weakened worker bees are more susceptible to pests and pathogens."
Applying proteomics-based pathogen screening tools in 2010, researchers announced they had identified a co-infection of invertebrate iridescent virus type 6 (IIV-6) and Nosema ceranae in all CCD colonies sampled. The study is the first to conclude that co-factors, the virus and fungus, were present in all of the collapsed colonies studied. However, scientists in the project emphasize additional research is still needed to consider how environmental factors like temperatures, drought and pesticides might play a role, if any, in CCD. Furthermore, the methodology used in these proteomic experiments has recently been questioned
From 1972 to 2006, there was a dramatic reduction in the number of feral honey bees in the U.S. (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, in late 2006 and early 2007 the rate of attrition was alleged to have reached new proportions, and the term "colony collapse disorder" began to be used to describe this sudden rash of disappearances, (sometimes referred to as Spontanious Hive Collapse or the Mary Celeste Syndrome in the United Kingdom).
Losses had remained stable since the 1990s at 17%-20% per year attributable to a variety of factors, such as mites, diseases, and management stress. The first report of CCD was in mid-November 2006 by a Pennsylvania beekeeper overwintering in Florida. By February 2007, large commercial migratory beekeepers in several states had reported heavy losses associated with CCD. Their reports of losses varied widely, ranging from 30% to 90% of their bee colonies; in some cases beekeepers reported loss of nearly all of their colonies with surviving colonies so weakened that they might no longer be viable to pollinate or produce honey.
Losses were reported in migratory operations wintering in California, Florida, Oklahoma and Texas. In late February, some larger non-migratory beekeepers in the mid- Atlantic and Pacific Northwest regions also reported significant losses of more than 50%. Colony losses also were reported in five Canadian provinces, several European countries, and countries in South and Central America and Asia. In 2010 the USDA reported that data on overall honey bee losses for 2010 indicated an estimated 34 percent loss, which is statistically similar to losses reported in 2007, 2008, and 2009.
Limited occurrences resembling CCD have been documented as early as 1869 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 senseâ€”that there may not be a specific causative agentâ€”the syndrome was renamed.
 Signs and symptoms
A colony which has collapsed from CCD is generally characterized by all of these conditions occurring simultaneously:
Presence of capped brood in abandoned colonies. Bees normally will not abandon a hive until the capped brood have all hatched.
Presence of food stores, both honey and bee pollen:
i. which are not immediately robbed by other bees
ii. which when attacked by hive pests such as wax moth and small hive beetle, the attack is noticeably delayed.
Presence of the queen bee. If the queen is not present, the hive died because it was queenless, which is not considered CCD.
Precursor symptoms that may arise before the final colony collapse are:
Insufficient workforce to maintain the brood that is present
Workforce seems to be made up of young adult bees
The colony members are reluctant to consume provided feed, such as sugar syrup and protein supplement.
 Scope and distribution
 North America
The National Agriculture Statistics Service reported that there were 2.44 million honey-producing hives in the United States as of February 2008, down from 4.5 million in 1980, and 5.9 million in 1947, though these numbers underestimate the total number of managed hives as they exclude several thousand hives managed for pollination contracts only, and also do not include hives managed by beekeepers owning fewer than 5 hives. This under-representation may be offset by the practice of counting some hives more than once; hives that are moved to different states to produce honey are counted in each state's total and summed in total counts.
In the U.S., at least 24 different states as well as portions of Canada had reported at least one case of CCD in 2007. However, subsequent analysis revealed that in many cases beekeepers reporting significant losses of bees did not experience true CCD, but losses due to other causes. In a 2007 survey of 384 responding beekeepers from 13 states reporting the number of hives containing few or no bees in spring, 23.8% met the specified criterion for CCD (that 50% or more of their dead colonies were found without bees and/or with very few dead bees in the hive or apiary).
In the U.S., CCD-suffering operations had a total loss of 45% compared to the total loss of 25% of all colonies experienced by non-CCD suffering beekeepers in 2006-2007; however, non-CCD winter losses as high as 50% have occurred in some years and regions (e.g., 2000-2001 in Pennsylvania), though normal winter losses are typically considered to be in the range of 15-25%.
A 2007-2008 survey of over 19% of colonies revealed a total loss of 35.8%. Operations that pollinated almonds lost, on average, the same number of colonies as those that did not. The 37.9% of operations that reported having at least some of their colonies die with a complete lack of bees had a total loss of 40.8% of colonies compared to the 17.1% loss reported by beekeepers without this symptom. Large operations were more likely to have this symptom suggesting that a contagious condition may be a causal factor. Sixty percent of all colonies that were reported dead in this survey died without dead bees, and thus possibly suffered from CCD. In 2010 the USDA reported that data on overall honey bee losses for 2010 indicate an estimated 34 percent loss, which is statistically similar to losses reported in 2007, 2008, and 2009.
According to the European Food Safety Authority (EFSA), in 2007 the United Kingdom had 274,000 hives, Italy had 1,091,630, and France 1,283,810. In 2008 the British Bee Keepers Association reported that the bee population in the United Kingdom dropped by around 30% between 2007 and 2008, and an EFSA study revealed that in Italy the mortality rate was 40-50%. However EFSA officials point out that the figures are not very reliable because before the bees started dying there was no harmonisation in the way different countries collected statistics on their bee populations. At that time (2008) the reports blamed the high death rate on the varroa mite, two seasons of unusually wet European summers, and some pesticides.
In 2010, David Aston of the British Beekeepersâ€™ Association stated, "We still do not believe CCD (which is now better defined) is a cause of colony losses in the UK, however we are continuing to experience colony losses, many if not most of which can be explained". He feels that recent studies suggest "further evidence to the evolving picture that there are complex interactions taking place between a number of factors, pathogens, environmental, beekeeping practices and other stressors, which are causing honey bee losses described as CCD in the US".
In 2009, Tim Lovett, president of the British Beekeepers' Association, said: "Anecdotally, it is hugely variable. There are reports of some beekeepers losing almost a third of their hives and others losing none. John Chapple, chairman of the London Beekeepers' Association, put losses among his 150 members at between a fifth and a quarter. "There are still a lot of mysterious disappearances; we are no nearer to knowing what is causing them." The government's National Bee Unit continued to deny the existence of CCD in Britain; it attributes the heavy losses to the varroa mite and rainy summers that stop bees foraging for food.
Bee keepers in Scotland also reported losses for the past three years. Andrew Scarlett, a Perthshire-based bee farmer and honey packer, lost 80% of his 1,200 hives during the 2009 winter. He attributed the losses to a virulent bacterial infection that quickly spread because of a lack of bee inspectors, coupled with sustained poor weather that prevented honeybees from building up sufficient pollen and nectar stores.
In Germany, 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 was no scientific confirmation; as of early May 2007, the German media were reporting that no confirmed CCD cases seemed to have occurred in Germany.
 Possible causes
The mechanisms of CCD are still unknown, but many causes have been proposed as causative agents; malnutrition, pathogens, immunodeficiencies, mites, fungus, pesticides, beekeeping practices (such as the use of antibiotics, or long-distance transportation of beehives) and electromagnetic radiation. Whether any single factor or a combination of factors (acting independently in different areas affected by CCD, or acting in tandem) is responsible is still unknown, however most recent information suggests a combination of factors is most likely. 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 the presumed "lead" group investigating the phenomenon, is the Colony Collapse Disorder Working Group, based primarily at Pennsylvania State University. Their preliminary report pointed out some patterns but drew no strong conclusions. A survey of beekeepers early in 2007 indicated 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 factor, but left the issue unresolved.
In July 2007, the United States Department of Agriculture (USDA) released its "CCD Action Plan", which outlined a strategy for addressing CCD consisting of four main components:
survey and data collection;
analysis of samples;
hypothesis-driven research; and
mitigation and preventative action.
In July 2009, the first annual report of the U.S. Colony Collapse Disorder Steering Committee was published. It suggested that colony collapse may be caused by the interaction of many agents in combination.
Similarly, in 2009 the CCD Working Group published a comprehensive descriptive study that concluded: "Of the 61 variables quantified (including adult bee physiology, pathogen loads, and pesticide levels), no single factor was found with enough consistency to suggest one causal agent. Bees in CCD colonies had higher pathogen loads and were co-infected with more pathogens than control populations, suggesting either greater pathogen exposure or reduced defenses in CCD bees."
The second annual Steering Committee report was released in November 2010. The group reported that although many associations, including pesticides, parasites, and pathogens have been identified throughout the course of research, "it is becoming increasingly clear that no single factor alone is responsible for [CCD]". Their findings indicated an absence of damaging levels of the parasite Nosema or parasitic Varroa mites at the time of collapse.
They did find an association of sub-lethal effects of some pesticides with CCD, including two common miticides in particular, coumaphos and fluvalinate, which are pesticides registered for use by beekeepers to control varroa mites. It was reported that studies also identified sub-lethal effects of neonicotinoids and fungicides, pesticides that may impair the bee's immune system. It is hypothesized that these pesticides impair the beeâ€™s immune system, which leaves the bee more susceptible to bee viruses.
A large survey of healthy and CCD-affected colonies also revealed elevated levels of pesticides in wax and pollen, but the amounts of pesticides were similar in both failing and healthy hives. They also confirmed suspected links between CCD and poor colony health, inadequate diet, and long-distance transportation. Studies continue to show very high levels of pathogens in CCD-affected samples and lower pathogen levels in non-affected samples, consistent with the empirical observation that healthy honey bee colonies normally fend off pathogens. These observations have led to the hypothesis that bee declines are resulting from immune suppression.
One of the patterns reported by the group at Pennsylvania State was that all producers in a preliminary survey noted a period of "extraordinary stress" affecting the colonies in question prior to their die-off, most commonly involving poor nutrition and/or drought. This is the only factor that all of the cases of CCD had in common in this report; accordingly, there is at least some significant possibility that the phenomenon is correlated to nutritional stress and may not manifest in healthy, well-nourished colonies. This is similar to the findings of a later independent survey in which small-scale beekeeping operations (up to 500 colonies) in several states reported their belief that malnutrition and/or weak colonies was the factor responsible for their bees dying in over 50% of the cases, whether the losses were believed to be due to CCD or not.
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.
Other researchers state that colony collapse disorder is mainly a problem of feeding the bees a monoculture diet when they should receive food from a variety of sources/plants. In winter the bees are given a single food source such as corn syrup (high-fructose or other), sugar and pollen substitute. In summer they may only pollinate a single crop (e.g., almonds, cherries, or apples).
A study published in 2010 found that bees that were fed pollen from a variety of different plant species showed signs of having a healthier immune system than those eating pollen from a single species. Bees fed pollen from five species had higher levels of glucose oxidase than bees fed pollen from one species, even if the pollen had a higher protein content. The authors hypothesised that CCD may be linked to a loss of plant diversity.
 Pathogens and immunodeficiency theories
Further information: Pathogen, immunodeficiency, and diseases of the honey bee
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 Pennsylvania 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 is an infectious disease came from the following observations: 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, and the CCD Working Group report in 2010 indicated that CCD-exhibiting hives tended to occur in proximity to one another within apiaries.
 Varroa and Israel acute paralysis virus
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. Dr. Enesto Guzman, an entomological researcher at the University of Guelph in Canada, studied 413 Ontario bee colonies in 2007-08. About 27% of hives did not survive the winter, and the Varroa mite was identified as the cause in 85% of the cases. As such, Varroa mites 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 unafflicted 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 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.
Recent research (2009) has found that an indicator for an impaired protein production is common among all bees affected by CCD, a pattern consistent with IAPV infection. It is conjectured that Dicistroviridae, like the IAPV, cause degradation of the ribosomes, which are responsible for protein production of cells, and that this reduced ribosomal function weakens the bees, making them more vulnerable to factors that might not otherwise be lethal.
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 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. However, a 2009 comprehensive survey of CCD-affected bee populations in the United States suggested that CCD likely involves an interaction between pathogens and other stress factors. They reported that their survey found only about half of the colonies sampled, both in CCD and control populations, were infected with N. ceranae.
The primary antifungal agent 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. Higes also claims to have successfully cured colonies with fumagillin. A review of these results in the journal Nature described these results as promising, but cautioned "N. ceranae may not be to blame for all cases of colony collapse". 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.
In the United States, N. ceranae has been detected in honey bees from Nebraska, Wisconsin, Arkansas, New York and South Dakota using PCR of the 16S gene. In New York, N. ceranae was detected in 49 counties, and of the 1200 honey bee samples collected, 528 (44%) were positive for Nosema, from which, PCR analysis of 371 spore positive samples revealed 96% were N. ceranae, 3% had both N. ceranae and N. apis, and 1% had N. apis only.
 Viral and fungal combination
A University of Montana and Montana State University team of scientists headed by Jerry Bromenshenk and working with the US Armyâ€™s Edgewood Chemical Biological Center published a paper in October, 2010 saying that a new DNA virus, invertebrate iridescent virus or IIV6, and the fungus Nosema ceranae were found in every killed colony the group studied. In their study they found that neither agent alone seemed deadly, but a combination of the virus and N. ceranae was always 100% fatal. Bromenshenk said it is not yet clear whether one condition weakens the bees enough to be finished off by the second, or whether they somehow compound the otherâ€™s destructive power. â€œTheyâ€™re co-factors, thatâ€™s all we can say at the moment. Theyâ€™re both present in all these collapsed colonies.â€
Previous research, though not all, had already identified the fungus as part of the problem, and several RNA-based viruses had been detected as well. But the Army/Montana team, using a new software system developed by the military for analyzing proteins, uncovered a new DNA-based virus, and established a linkage to N. ceranae. Once the virus and the fungus were identified, the researchers tested bees in the lab. First they infected the bees with the fungus alone, and some died, though not as many as with CCD. Then they infected some with just the virus, with the same result.
When the combination of virus and fungus was used, the results appeared similar to CCD. The researchers say that the next step to test their theory will be to inoculate a colony with the two pathogens to see if it causes a colony collapse. â€œThe real closure of the circle for us is to take the two pathogens to inoculate a colony, see it collapse, then pull out the pathogens again."
Whether this identified bee virus and its potential interaction with Nosema species is the cause or marker of CCD, is unknown. Also still not explained is the reason that the bees are never found dead in the hives but fly off at the time of death. Bromenshenk theorizes that the viral-fungal combination disrupts memory or navigating skills and the bees simply get lost. Another possibility, he said, is a kind of insect insanity. Scientists in the project emphasize that their conclusions are not the final word. They suggest that more research is still needed to determine, for example, how further outbreaks might be prevented, and how much environmental factors like heat, cold or drought might play a role. The study did not look into the role that pesticides may play, if any.
Information about the study was released to the public in a front page article in The New York Times with the heading "Scientists and Soldiers Solve A Bee Mystery". A few days later an article was published in Fortune Magazine with the title, "What a scientist didn't tell the New York Times about his study on bee deaths". Professor of entomology at Penn State University James Frazier, who is currently researching the sublethal impact of pesticides on bees, said that while Bromenshenk's study generated some useful data, Bromenshenk has a conflict of interest as CEO of a company developing scanners to diagnose bee diseases. "He could benefit financially from that if this thing gets popularized," Frazier says, "so it's a difficult situation to deal with." He adds that his own research has shown that pesticides affect bees "absolutely, in multiple ways."
Recently, the methods used to interpret the mass spectrometry data in the Bromenshenk study have been called into question, raising doubts as to whether IIV6 was ever correctly identified in any of the samples examined.
Further information: Pesticide toxicity to bees, Imidacloprid effects on bee population, and Bees and toxic chemicals
One of the more common general hypotheses concerns pesticides (or, more specifically, insecticides), though several studies have found no common environmental factors between unrelated outbreaks studied. In 2010 in the United States, the Organic Consumers Association reported that bee colony losses were not occurring at organic beekeeping operations.
A 2010 survey reported 98 pesticides and metabolites detected in mixtures up to 214 ppm in bee pollen. It was disclosed that that figure represents over half of the maximum individual pesticide incidences ever reported for apiaries. It was suggested that "while exposure to many of these neurotoxicants elicits acute and sublethal reductions in honey bee fitness, the effects of these materials in combinations and their direct association with CCD or declining bee health remains to be determined."
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 (though possibly effects of contaminated pollen consumed by juveniles may only show after they have developed into adults).
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 "ComitÃ© Scientifique et Technique (CST)" which was in the center of discussion, which led to a partial ban of imidacloprid in France. The imidacloprid pesticide Gaucho was banned, in 1999 by the French Minister of Agriculture Jean Glavany, 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 honey production was decreasing by 1,000 tons a year for a decade. As of August 2007, no investigations were yet opened. 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".
Around the same time French beekeepers succeeded in banning neonicotinoids, the Clinton administration permitted pesticides which were previously banned, including imidacloprid. In 2004, the Bush Administration reduced regulations further and pesticide applications increased.
In 2005, a team of scientists led by the National Institute of Beekeeping in Bologna, Italy, found pollen obtained from seeds dressed with imidacloprid contains significant levels of the insecticide, and suggested the polluted pollen might cause honey bee colony death. Analysis of maize and sunflower crops originating from seeds dressed with imidacloprid suggest large amounts of the insecticide will be carried back to honey bee colonies. Sublethal doses of imidacloprid in sucrose solution have also been documented to affect homing and foraging activity of honey bees. Imidacloprid in sucrose solution fed to bees in the laboratory impaired their communication for a few hours. Sublethal doses of imidacloprid in laboratory and field experiment decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired.
Research in 2008 by scientists from Pennsylvania State University found high levels of the pesticides fluvalinate and coumaphos in samples of wax from hives, as well as lower levels of 70 other pesticides. These chemicals have been used to try to eradicate varroa mites, a bee pest that itself has been thought to be a cause of CCD. Researchers from Washington State University, under entomology professor Steve Sheppard in 2009, confirmed high levels of pesticide residue in hive wax and found an association between it and significantly reduced bee longevity.
The WSU work also focused on the impact of the microsporidian pathogen Nosema ceranae, the build-up of which was high in the majority of the bees tested, even after large doses of the antibiotic fumagillin. Penn State's Dr. Maryann Frazier said, "Pesticides alone have not shown they are the cause of CCD. We believe that it is a combination of a variety of factors, possibly including mites, viruses and pesticides."
Main article: Fipronil
Fipronil is another chemical sometimes blamed for the spread of colony collapse disorder among bees. It has been found by the Minutes-Association for Technical Coordination Fund in France that even at very low nonlethal doses for bees, the pesticide still impairs their ability to locate their hive, resulting in large numbers of forager bees lost with every pollen-finding expedition; other studies, however, have shown no acute effect on honey bees.
Fipronil is designed to eliminate insects similar to bees such as Vespula germanica and many other colonial pests by a process of toxic baiting, whereby one insect returning to the hive spreads the pesticide among the brood.
 Antibiotics and miticides
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.
 Genetically modified crops
Some genetically modified (GM) crops produce the natural insecticide Bt toxin, which has been hypothesised to affect bees. In the scant literature on the topic, there exists no evidence of any negative effects on honey bee populations. Furthermore, CCD cases are known in areas of Europe and Canada where Bt crops are not grown, such as Switzerland.
 Bee rentals and migratory beekeeping
Since U.S. 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 U.S. agriculture, which could not produce anywhere near its current levels with native pollinators alone. U.S. 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.
 U.S. bee rental travel extent
One major U.S. beekeeper reports moving his hives from Idaho to California in January, then to apple orchards in Washington in March, to North Dakota two months later, and then back to Idaho by Novemberâ€”a journey of several thousand kilometres. Others move from Florida to New Hampshire or to Texas; nearly all visit California for the almond bloom in January.
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 U.S. has resulted in far greater losses from Varroa mite infections in recent years.
 Electromagnetic radiation
Despite considerable discussion on the Internet and in the lay media, there have been almost no careful studies, published in peer reviewed scientific literature, on effects of electromagnetic field exposure on honey bees. One of the few peer-reviewed studies was published in 1981 by Gary and Westerdahl. The investigators found "no evidence that airborne invertebrates would be significantly affected during transient passage through microwaves associated with solar power satellite ground-based microwave receiving stations". No mechanism has been established by which weak radiofrequency energy can affect the behavior of insects, apart from heating effects. However, it is well-established that honey bees can detect weak static or low-frequency magnetic fields, which they use as one of several cues in navigation.
In 2004 an exploratory study was conducted on the non-thermal effects of electromagnetic exposure and learning. The investigators did not find any change in behavior due to RF exposure from the DECT base station operating at 1880-1900 MHz.
In 2006 investigators at the University of Landau did a pilot study on the 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. In April 2007, news of this study appeared in various media outlets, beginning with an article in The Independent, which stated that the subject of the study included mobile phones and had related them to CCD. Though Cellular phones were implicated by other media reports at the time, they were not covered in the study. Researchers involved have since stated that their research did not include findings on cell phones, or their relationship to CCD, and indicated that the Independent article had misinterpreted their results and created "a horror story".
In April 2011, a study conducted by a former investigator of the EPFL Ã‰cole Polytechnique FÃ©dÃ©rale de Lausanne appeared, which stated that active mobile phones placed directly inside a beehive can induce the worker piping signal (in natural conditions, worker piping either announces the swarming process of the bee colony or is a signal of a disturbed bee colony); the author mentioned that "phones are not present in the close vicinity of honeybees in real life" and did not demonstrate what negative effect, if any, worker piping might have within a colony, nor was any link to CCD demonstrated.
As of March 1, 2007 MAAREC offered the following tentative recommendations for beekeepers noticing the symptoms of CCD:
Do not combine collapsing colonies with strong colonies.
When a collapsed colony is found, store the equipment where you can use preventive measures to ensure that bees will not have access to it.
If you feed your bees sugar syrup, use Fumagillin.
If you are experiencing colony collapse and see a secondary infection, such as European Foulbrood, treat the colonies with Terramycin, not Tylan.
Another proposed remedy for farmers of pollinated crops is simply to switch from using beekeepers to the use of native bees, such as bumble bees and mason bees . Native bees can be helped to establish themselves by providing suitable nesting locations and some additional crops the bees could use to feed from (e.g. when the pollination season of the commercial crops on the farm has ended).
A British beekeeper successfully developed a strain of bees that are resistant to varroa mites. Russian honey bees also resist infestations of varroa mites but are still susceptible to other factors associated with colony collapse disorder, and have detrimental traits that limit their relevance in commercial apiculture.
In the United Kingdom, a national bee database was set up in March 2009 to monitor colony collapse as a result of a 15% reduction in the bee population that had taken place over the previous two years. In particular, the register, funded by the Department for the Environment and administered by the National Bee Unit, will be used to monitor health trends and help establish whether the honey industry is under threat from supposed colony collapse disorder. Britain's 20,000 beekeepers have been invited to participate. In October 2010, David Aston of the British Beekeepersâ€™ Association stated, â€˜We still do not believe CCD is a cause of colony losses in the UK, however we are continuing to experience colony losses, many if not most of which can be explained. The approach being taken in UK beekeeping is to raise the profile of integrated bee health management, in other words identifying and trying to eliminate factors which reduce the health status of a colony. This incorporates increasing the skill level of beekeepers through training and education, raising the profile of habitat destruction and its effect of forage (nectar and pollen) availability, and of course research on the incidence and distribution of diseases and conditions in the UK together with more applied research and development on providing solutions."
 Society and culture
See also: List of crop plants pollinated by bees
The phenomenon is particularly important for crops such as almond growing in California, where honey bees are the predominant pollinator and the crop value in 2006 was $1.5 billion. In 2000, the total U.S. crop value that was wholly dependent on honey bee pollination was estimated to exceed $15 billion.
Honey bees are not native to the Americas, therefore their necessity as pollinators in the U.S. is limited to strictly agricultural/ornamental uses, as no native plants require honey bee pollination, except where concentrated in monoculture situationsâ€”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 (e.g., squash bees on cucurbits), 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 beesâ€”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 saturation pollination for what they lack in efficiency. The commercial viability of these crops is therefore strongly tied to the beekeeping industry. In China, hand pollination of apple orchards is labor intensive, time consuming and costly.
A number of documentaries have been produced in which possible causes of CCD have been explored. "Silence of the Bees" (Oct. 2007) is a part of the Nature television series and covers several recent investigative discoveries. The 2009 documentary Vanishing of the Bees pointed to neonicotinoid pesticides as being the most likely culprit, though the experts interviewed concede that no firm data yet exists. The 2010 feature length documentary Queen of the Sun: What are the bees telling us? features interviews with beekeepers, scientists, farmers, and philosophers