The mechanisms of CCD are still unknown, but many causes are currently being considered, such as
pesticides,
mites, fungi, beekeeping practices (such as the use of
antibiotics or long-distance transportation of beehives), malnutrition, poor quality queens, starvation, other
pathogens, and
immunodeficiencies. The current scientific consensus is that no single factor is causing CCD, but that some of these factors in combination may lead to CCD either additively or synergistically. survey and data collection; analysis of samples; hypothesis-driven research; mitigation and preventive action. The first annual report of the U.S. Colony Collapse Disorder Steering Committee was published in 2009. It suggested CCD may be caused by the interaction of many agents in combination. The same year, 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." A 2015 review examined 170 studies on colony collapse disorder and stressors for bees, including
pathogens,
agrochemicals, declining
biodiversity,
climate change and more. The review concluded that "a strong argument can be made that it is the interaction among parasites, pesticides, and diet that lies at the heart of current bee health problems." potentially linked to "stress" leading to a weakened immune system. Specifically, according to research done in 2007 at the Pennsylvania State University: "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. Parasites, such as varroa mites
(Varroa destructor), honey bee tracheal mites
(Acarapis woodi), fungal, bacterial and viral diseases, and kleptoparasites such as small hive beetles (
Aethina tumida), are all problems that have been introduced within the last 20 years in the continental U.S., and are faced by beekeepers. and the CCD Working Group report in 2010 indicated that CCD-exhibiting hives tended to occur in proximity to one another within apiaries. Affliction with
Varroa mites also tends to weaken the
immune system of the bees. Dr. Ernesto Guzman, an entomological researcher at the
University of Guelph in Canada, studied 413
Ontario bee colonies in 2007–08. The presence of
Varroa mites within colonies before winter was observed to weaken the immune systems of bees and introduce viruses that led to colony death during the winter. About 27% of hives did not survive the winter, and the
Varroa mite was identified as the cause in 85% of the cases.
Varroa mites also affect the queen's ability to reproduce, which is detrimental to the survival of the hive.
Varroa destructor is a parasitic mite that colonizes beehives and preys on honey bees by consuming their
hemolymph.
Varroa mites parasitize all types of honey bees (workers, nurse bees, larvae) depending on their life cycle stage. During the phoretic stage,
Varroa prefer to attach to nurse bees as this results in higher fitness leading into the reproductive stage. The mites then feed on larvae during their reproductive stage and increased fitness leads to an increase in mite fecundity (number of female offspring). Due to
Varroas ability to feed on all types of honey bees, they are one of the biggest threats to colonies, especially over winter. In 2020 a group of scientists announced that they were in the early stages of field testing a bacterium with specifically genetically modified
plasmids that both suppressed infection with deformed wing virus but also effectively reduced
Varroa mite survival.
Israeli acute paralysis virus In 2004,
Israeli acute paralysis virus (IAPV) was discovered in
Israel and at one time it was considered the cause of CCD. It was named after the place it was first identified; its place of origin is unknown. 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. All colonies were found to be infected with numerous pathogens, but only the IAPV virus 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. Research in 2009 has found that an indicator for 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.
Nosema Some have suggested the syndrome may be an inability by beekeepers to correctly identify known diseases such as
European foulbrood or the
microsporidian fungus
Nosema apis. 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. indicating that CCD may be caused by
N. ceranae. A research team claim to have ruled out many other potential causes, however, a 2009 survey of US CCD-affected bee populations found only about half of the colonies sampled, both in CCD and control populations, were infected with
N. ceranae. Higes also claims to have successfully cured colonies with fumagillin. A review of these results 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. In 2007,
N. ceranae was reported in a few hives in California. 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".
N. ceranae has been detected in honey bees from several states using
PCR of the
16S gene. In New York,
N. ceranae was detected in 49 counties, and of the 1,200 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. The infection damages the bee's midgut, resulting in the necrosis of intestinal tissue. This impairs the bee's ability to digest food and absorb nutrients. When healthy bees are fed pollen filled with fungicides,
insecticides, and other agrochemicals—including imidacloprid—they are more likely to be infected by
N. ceranae, thereby suggesting a potential link to CCD.
Viral and fungal combination A University of Montana and Montana State University team of scientists headed by Jerry Bromenshenk and working with the US Army's
Edgewood Chemical Biological Center published a paper in October 2010 saying that a new
DNA virus,
invertebrate iridescent virus type 6 (IIV-6), and the fungus
Nosema ceranae were found in every killed colony the group studied. In their study, they found neither agent alone seemed deadly, but a combination of the virus and
N. ceranae was always 100% fatal. Information about the study was released to the public in a front-page article in
The New York Times. 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 was 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. A few months later, the methods used to interpret the mass spectrometry data in the Bromenshenk study were called into question, raising doubts as to whether IIV-6 was ever correctly identified in any of the samples examined.
Pesticides According to the USDA, pesticides may be contributing to CCD. Scientists have long been concerned that pesticides, including possibly some
fungicides, may have sublethal effects on bees, not killing them outright, but instead impairing their development and behavior. Maryann Frazier, Senior Extension Associate Emeritus for Entomology at
Penn State, 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."
Neonicotinoids A class of insecticides called
neonicotinoids has come under particular scrutiny. Neonicotinoids are
systemic pesticides, typically used as seed treatments to reduce the application of foliar pesticides as the plants grow. Despite gaps in the scientific evidence, regulators have restricted the use of neonicotinoids in Europe and elsewhere largely on the basis of concerns for bee health.
Evidence of risk to bees The use of neonicotinoid pesticides in the US increased after 2005, coincident with rising bee deaths. Most corn (maize) grown in the US is grown from seeds treated with neonicotinoids. Although maize is wind-pollinated, honey bees that happen to be foraging on the plants may be exposed to pesticide residues in the nectar and pollen. Honey bees may also be exposed by foraging on wild plants unintentionally exposed to nicotinoids. To date, most of the evaluations of possible roles of pesticides in CCD have relied on the use of surveys submitted by beekeepers, but direct testing of samples from affected colonies seems likely to be needed.
Laboratory studies Neonicotinoids may interfere with bees' natural homing abilities, causing them to become disoriented and preventing them from finding their way back to the hive. These impairments may result from the effects of neonicotinoids on the long-term and short-term memory of bees. Sublethal doses of imidacloprid in laboratory and
field experiments decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired. Exposure to Imidacloprid matched to field levels has been shown to reduce colony growth and new queen production. A 2012
in situ study suggested that exposure to sublethal levels of imidacloprid in
high-fructose corn syrup (HFCS), which is used to feed honey bees when forage is not available, caused bees to exhibit symptoms consistent with CCD. The control group fed HFCS without insecticide does not show such symptoms. A 2013 literature review concluded that neonicotinoids in the amounts typically used were harmful to bees and that alternatives were urgently needed. The doses taken up by bees were not lethal, but possible chronic problems could be caused by long-term exposure. A meta-analysis study published in February 2010 found evidence from laboratory studies showing sublethal effects of imidacloprid on honey bees, but a lack of evidence on the environmental relevance of these findings. Similarly, a 2012 review concluded that in a laboratory setting, both lethal and sub-lethal effects on foraging behavior, memory, and learning ability were observed in honey bees exposed to neonicotinoids, but that these effects were not seen in field studies with field-realistic dosages. In 2012 several studies were published showing that neonicotinoids had previously undetected routes of exposure affecting bees including through dust, pollen, and nectar. Research also showed environmental persistence in agricultural irrigation channels and soil. The machines that plant corn seeds coated with clothianidin and imidacloprid release certain amounts of the pesticide into the air, another possible route of exposure. This was the first field study to establish a link between neonicotinoids and CCD.
Regulatory policy In Europe, the interaction of the phenomenon of "dying bees" with imidacloprid has been discussed for quite some time. A study from the (CST) was at the center of discussion, and 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. While French beekeepers succeeded in banning neonicotinoids, the
Clinton administration permitted pesticides that were previously banned, including imidacloprid. In 2004, the
Bush administration reduced regulations further, and pesticide applications increased. In 2013, a formal review by the
European Food Safety Authority (EFSA), reported that some neonicotinoids posed an unacceptably high risk to bees, and identified several data gaps not previously considered. Their review concluded, "A high acute risk to honey bees was identified from exposure via dust drift for the seed treatment uses in maize,
oilseed rape and cereals. A high acute risk was also identified from exposure via residues in nectar and/or pollen." After the 2013 EFSA review, the
European Commission (EC) proposed a two-year ban on neonicotinoids. In April 2013, the
European Union voted for a two-year restriction on neonicotinoid insecticides. The ban restricted the use of imidacloprid, clothianidin, and thiamethoxam for use on crops that are attractive to bees. Eight nations voted against the motion, including the British government, which argued that the science was incomplete. The ban can be seen as an application of the "
precautionary principle", established at the 1992 Rio Conference on the Environment and Development, which advocated that "lack of full scientific certainty shall not be used as a reason for postponing cost-effective measures to prevent
environmental degradation." In 2013 beekeepers and environmentalists jointly filed a lawsuit blaming the United States
Environmental Protection Agency (EPA) for continuing to allow the use of neonicotinoids in the United States. The suit specifically asked for suspension of clothianidin and thiamethoxam. The EPA responded to the suit by pointing to research which found the
Varroa mite responsible for the decline in bees and showed that the role of neonicotinoids in CCD had been overstated. The Save America's Pollinators Act (H.R. 2692) was introduced in Congress in 2013, and reintroduced in 2015. The proposed act asked that neonicotinoids be suspended until a full review of their impacts had occurred.
Fipronil Fipronil is a
phenylpyrazole insecticide, with a broad-spectrum
systemic mode of action. Fipronil is designed to eliminate insects similar to bees, such as yellowjackets (
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. In May 2003, the French Directorate-General of Food at the Ministry of Agriculture determined that a case of mass bee mortality observed in southern France was related to acute fipronil toxicity. Toxicity was linked to defective seed treatment, which generated dust. In February 2003, the ministry decided to temporarily suspend the sale of BASF crop protection products containing fipronil in France, including the "Regent" brand. In 2010 fipronil was blamed for the spread of CCD among bees, in a study by the Minutes-Association for Technical Coordination Fund in France, which found that even at very low nonlethal doses, this pesticide impaired the ability to locate the hive, resulting in large numbers of foragers lost with every pollen-finding expedition, though no mention was made regarding any of the other symptoms of CCD; other studies, however, have shown no acute effect of fipronil on honey bees.
Fungicides In 2013, researchers collected pollen from hives and fed it to healthy bees. The pollen had an average of nine different pesticides and fungicides. Further, the researchers discovered that bees that ate pollen with fungicides were three times more likely to be infected by parasites. Their study shows that fungicides thought harmless to bees, may play a significant role in CCD. Their research also showed that spraying practices may need to be reviewed because the bees sampled by the authors foraged not from crops, but almost exclusively from weeds and wildflowers, suggesting that bees are more widely exposed to pesticides than thought.
Dennis vanEngelsdorp, an entomologist at the University of Maryland, has been quoted as saying "Fungicides, which we didn't expect to harm insects, seem to have a sub-lethal effect on bee health". He went on further to state this is important because fungicides are not heavily regulated.
Antibiotics A study at the University of Texas in Austin found that commonly used antibiotics found in beekeeping to prevent disease lower the gut microbial levels in honeybees, A widespread occurrence of viral infections within a beehive can lead to colony collapse. Researchers state that although the antibiotics are necessary, beekeepers should exercise caution when determining the amount and length of use. A widespread occurrence of viral infections within a beehive can lead to colony collapse.
Miticides Beekeepers use miticides to rid colonies of
Varroa infestations; however, treatment can lead to higher levels of viral infections in colonies. High doses of treatment or the use of miticides for an extended period can lead to immune suppression in honey bees, making them more susceptible to viruses. 2008 research by scientists from Pennsylvania State University found high levels of the miticides
fluvalinate and
coumaphos in samples of wax from hives, as well as lower levels of 70 other pesticides. A large 2010 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. Extreme rainfall and lack thereof can both limit the extent to which bees can forage, thereby reducing their numbers and health.
Bee rentals and migratory beekeeping Since U.S. beekeeper
Nephi Miller first began moving his hives to different areas of the country in 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 disorders. In addition to the concern surrounding viruses and mites in transporting bees across the country, the stress bees experience in transport is a potential mechanism involved in colony collapse disorder.
Selective commercial breeding and lost genetic diversity in industrial apiculture Most of the focus on CCD has been on environmental factors. CCD is a condition recognised for the greatest impact in regions of 'industrial' or agricultural use of commercially bred bee colonies. Natural breeding and colony reproduction of wild bees is a complex and highly selective process, leading to a
diverse genetic makeup in large within-colony populations of bees, which might not be reproduced in commercially bred colonies.
Malnutrition In 2007, one of the patterns reported by the CCD Study Group at Pennsylvania State was that all producers in a preliminary survey noted a period of "extraordinary stress" affecting the colonies in question before their die-off, most commonly involving poor nutrition and/or drought. At least one researcher has stated, however, that if this were the sole factor involved, this should have led to the exclusive appearance of CCD in wintering colonies being fed HFCS, but many reports of CCD had occurred in other contexts with beekeepers who had not used HFCS. Other researchers have speculated 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, these 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). The monoculture diet is thus attributed to bee rentals and migratory beekeeping. While it is claimed that single pollen diets are greatly inferior to mixed pollen diets, there are a few pollens, however, that are acceptable for honey bees to be introduced to exclusively, including
sweet clover and
mustard. 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. Researchers found a proper diet that does lead to a healthy honey bee population. "The authors recommended a diet containing 1000 ppm potassium, 500 ppm calcium, 300 ppm magnesium, and 50 ppm each of sodium, zinc, manganese, iron, and copper." A 2013 study found that
p-coumaric acid, which is normally present in honey, assists bees in detoxifying certain pesticides. Its absence in artificial nutrients fed to bees may therefore contribute to CCD.
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 the effects of
electromagnetic field exposure on honeybees. A study on the non-thermal effects of
radio frequency (RF) on honey bees (
Apis mellifera carnica) reported there were no changes in behavior due to RF exposure from
DECT cordless phone base stations operating at 1,880–1,900
MHz. A later study established that close-range
electromagnetic field (EMF) may reduce the ability of bees to return to their hive. In the course of their study, one-half of their colonies broke down, including some control hives that did not have embedded DECT base stations. 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. Although
cellular phones were implicated at the time by other media reports, they were not covered in the quoted study. The researchers involved have since stated that their research did not include findings on cell phones, nor their relationship to CCD, and indicated that the
Independent article had misinterpreted their results and created "a horror story". A review of 919 peer-reviewed scientific studies investigating the effects of EMF on wildlife, humans, and plants included 7 studies involving honey bees; 6 of which reported negative effects from exposure to EMF radiation, but none demonstrated any specific link to CCD. A 2004 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.
Genetically modified crops GM crops are not considered to be a cause of CCD. In 2008 a meta-analysis of 25 independent studies assessing the effects of
Bt Cry proteins on honeybee survival (mortality) showed that Bt proteins used in commercialized
GE crops to control lepidopteran and coleopteran pests did not negatively impact the survival of honeybee larvae or adults. Additionally, larvae consumed only a small percent of their protein from pollen, and there was also a lack of geographic correlation between GM crop locations and regions where CCD occurred. == Management ==