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Colony Collapse Disorder (or CCD) is the name of the phenomenon that describes the massive die-off affecting an entire beehive or bee colony. The BBC has referred to it as VBS (Vanishing Bee Syndrome). It was originally apparently limited to colonies of the Western honey bee in North America,^[1] but European beekeepers have recently claimed to be observing a similar phenomenon in Poland and Spain, with initial reports coming in from Switzerland and Germany, albeit to a smaller degree.^[2] The cause (or causes) of the syndrome is not yet well understood and even the existence of this disorder remains disputed. Theories include environmental change-related stresses^[3], malnutrition, unknown pathogens, mites, pesticides such as neonicotinoids, disease^[4], or genetically modified (GM) crops^[5].

From 1971 to 2006 approximately one half of the U.S. honey bee colonies have vanished, but 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, and has been fairly gradual. Late in the year 2006 and in early 2007, however, 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.^[1]

Limited occurrences resembling CCD have been documented as early as 1896,^[4] 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. In none of the past appearances of this syndrome has anyone been able to determine its cause(s). Upon recognition that the syndrome does not seem to be seasonally-restricted, and that it may not be a "disease" in the standard sense (in that there may not be a specific causative agent), the syndrome was re-named.^[6]

Contents 1 Phenomenology 2 Possible causes and research 2.1 Poor nutrition or malnutrition 2.2 Pesticides 2.3 Pathogens and immunodeficiency 2.4 Poisonous plants 2.5 Genetically modified crops (GMO) 3 Scale of the disorder 4 See also 5 References 6 External links

A colony which has collapsed from CCD is generally characterized by all of these conditions occurring simultaneously:^[7]

• Complete absence of adult bees in colonies, with no or little build-up of dead bees in or in front of the colonies.
• Presence of capped brood in 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 is not immediately robbed by other bees

ii. when attacked by hive pests such as wax moth and small hive beetle, the attack is noticeably delayed.

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
• Queen is uncharacteristically evident outside the hive
• The colony members are reluctant to consume provided feed, such as sugar syrup and protein supplement.

While the exact mechanisms of CCD are unknown, pathogens, pesticides, mites and transgenic crops, or genetically modified (GM) crops have all been proposed as causative agents. 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 this 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,^[4] based primarily at Penn State University. Their preliminary report pointed out some patterns, but drew no strong conclusions.^[6]

One of the patterns reported by the aforementioned group at Penn State was that all producers in a preliminary survey noted a period of "extraordinary stress" affecting the colonies in question prior to the die-off, most commonly involving poor nutrition and/or drought.^[6] To date, this is the only factor that all of the reported cases of CCD have in common; accordingly, there is at least some significant possibility that this phenomenon is correlated to nutritional stress, and may not manifest in healthy, well-nourished colonies.

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.^[8] However, if this were the sole factor involved, 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.

One recently published view is that bees are falling victim to new varieties of nicotine-based pesticides;^[9] beekeepers in Canada are also losing their bees and are blaming neonicotinoid pesticides^{[citation needed]}. CCD is possibly linked to pesticide use though several studies have found no common environmental factors between unrelated outbreaks studied.

One of the more common general hypotheses concerns pesticides (or, more technically, insecticides). For example, the effects of the top Bayer product, labelled Gaucho (based on the agent imidacloprid) on insects would be perfectly in keeping with the symptoms;^[10][11] e.g., the effects of imidacloprid on termites are apparent failure of the immune system and disorientation^{[citation needed]}. However, 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 very 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. 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 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. No detailed studies of toxicity or pesticide residue in remaining honey or pollen in failed colonies are yet published, however.

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^[6] 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 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,^[12] not unlike the analog of HIV in humans, 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 have further 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.^[13] This research group is reported to be focusing on a search for possible viral, bacterial, or fungal pathogens which may be involved.^[6]

Some have suggested that the syndrome may be an inability by beekeepers to correctly identify known diseases such as European foulbrood or 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^[6]. Despite this, in Europe it is supposed that CCD is due to Nosema ceranae^{[citation needed]}.

When a colony is dying, and there are other healthy colonies nearby (as is typical in a bee yard), those healthy colonies may 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) would suggest that of a contagious disease. However, it is often reported in CCD cases that provisions of dying colonies are not being robbed, suggesting that at least this particular factor is not involved in CCD.

Certain plants' nectars (and even some pollens) such as rhododendrons, azaleas, Passiflora, almond^{[citation needed]}, aconites, hellebore, skunk cabbage, golden rain tree, Yellow Jessamine, Aloe littoralis, oleander and Chamaecrista fasciculata (Partridge-pea) are a few of the species known to be mildly toxic and poisonous to bees (and humans). These plants' nectars are known to include toxic or poisonous substances including alkaloids, anthraquinones, and grayanotoxin. Catalpa speciosa (makes bees mildly to very inebriated), honey from Kalmia latifolia, the "mountain laurel" of the northern United States, and allied species such as sheep laurel, Kalmia angustifolia, can produce sickness or even death. The nectar of the Wharangi Bush, Melicope ternata, in New Zealand also produces toxic honey, and this has been fatal. Datura plants, belladonna flowers, henbane (Hyoscamus niger), and Serjania lethalis (a liana used in making fish killing mixtures) from Brazil also produce toxins at dangerous to deadly levels in honey. The changing climate, cultural, and other environmental factors may be enabling more of some of these plants' nectars to affect bees and other nectar gatherers, either through changes in the distribution of the plants (both natural and artificial, the latter due to use of these plants as ornamentals), changes in the likelihood of exposure to these plants due to movement of beehives by beekeepers, or a lack of alternative nectar sources driving bees to use plants they might normally avoid.

Potential effects of gathering pollen and nectar from genetically modified (GM) crops that produce Bacillus thuringiensis (Bt) toxin have not been thoroughly investigated. Corn, the major such crop, is not a preferred plant for honey bees, although beekeepers who keep bees near corn fields state that "corn is an excellent source of pollen when in tassel".^[14] Cotton, the second important Bt crop, is highly subject to bee visitation for nectar (pollen is only consumed if there is no other pollen available^[15]), but there is little evidence of toxicity of GM cotton, other than that from insecticides used during bloom. 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".^[16] It suggested that GMO, besides other factors, might contribute to honey bee 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."^[17]

The Sierra Club Genetic Engineering Committee recently published a letter to Senator Thomas Harkin on the web with the title "GE and bee Colony Collapse Disorder -- science needed!".^[18] They are of the opinion that "highly respected scientists believe that exposure to genetically engineered crops and their plant-produced pesticides merit serious consideration as either the cause or a contributory factor to the development and spread of CCD." Nine literature references which might support this theory are cited.^[19]

On March 28 2007, the "Mid-Atlantic Apiculture Research and Extension Consortium"^[20] 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"^[21].

Most of the short summaries of US risk assessment studies on Bt in relation to honey bees are published on the United States Environmental Protection Agency (EPA) homepage for Biopesticides Registration Action Documents^[22], especially there is a document concerning the environmental effects of Bacillus thuringiensis as plant incorporated protectant.^[23] (Literature references of studies, which are in the public domain, are included.) For Bt cotton there are written some paragraphs in a fact sheet with the title "Bacillus thuringiensis Cry2Ab2 protein and the Genetic Material Necessary for Its Production in Cotton".^[24] These tests were usually made according to "Honey bee testing Tier I".^[25] Such tests seem to have a rather short duration time. ("Control and treated bees should be observed for at least 30 days after dosing.") The Fact Sheets for plant-incorporated protectants^[26] - retrievable and not retrievable - are listed in a special EPA homepage. The original studies on the effects of Bt pollen on honeybees do not seem to be in the public domain.

The primary effects of Bt on insects is in the larval stage. Thus the studies on Bt-toxins and effects on honey bees originally concentrated more on larvae and their development. However, as pollen is an important part of bee bread, which is also food for adult bees, some beekeepers think that adult bees may be more affected by ingredients of pollen, because adult bees are something like a filter for larvae. And as the CCD phenomenon involves the disappearance of the adult bees, some think there could be a direct connection^[27] despite the absence of symptoms in the larvae, and despite any evidence that the bees experiencing CCD have ever been exposed to GM crops.

Research conducted in Germany suggests that exposure to corn pollen containing genes for Bt production may weaken the adult bees' defense against Nosema, though in the absence of such an infection, there were no detectable effects: "When the trial was repeated the colonies were treated prophylactically with antibiotics to prevent re-infection...This indicates that healthy bee colonies are not impaired in any way by the toxin in any of the tested vital functions of colony size, foraging activity, brood care activity or development, even when exposed to extreme levels of Bt maize pollen over a period of six weeks."^[28]. However, if "the bee colonies happened to be infested with parasites (microsporidia), this infestation led to a reduction in the number of bees and subsequently to reduced broods....This effect was significantly more marked in the Bt-fed colonies." It has further been suggsted that "genetically modified corn may have altered the surface of the bee's intestines, sufficiently weakening the bees to allow the parasites to gain entry -- or perhaps it was the other way around" though it was also noted "Of course, the concentration of the toxin was ten times higher in the experiments than in normal Bt corn pollen. In addition, the bee feed was administered over a relatively lengthy six-week period."^[29]. Other more recent studies have similarly failed to show any adverse effects of Bt pollen on healthy bee colonies^[21].

The preliminary report of the Colony Collapse Disorder Working Group^[4] concerning "Fall Dwindle Disease"^[6] indicated that "all PA samples were found to have nosema spores in their rectal contents. The sting gland of many examined bees were obviously scarred with distinct black “marks”; this type of pin-point melanization or darkening is indicative of an immune response to some sort of pathogen." If the bees in Pennsylvania were gathering Bt-toxin-containing corn pollen, it could potentially have interacted with Nosema and thus contributed to CCD in those colonies; however, there is no evidence that these colonies were gathering corn pollen at any point prior to their deaths, nor has it been reported that colonies afflicted by CCD elsewhere had been collecting corn pollen. The vast majority of the colonies reported to be dying from CCD occur in locations where GM corn is not grown (at least in the United States), nor were bees from other areas outside of Pennsylvania reported to be significantly infected by Nosema, meaning that even if GM crops were involved in this fashion, it could only potentially account for a very small number of the reported cases of CCD.

In 2005 Bt maize, which is commercially planted in the US since 1996, accounted for 35% (10.64 million ha) of total US maize plantings. GM insect resistant Bt cotton has also been grown commercially in the US since 1996 and by 2005, was planted on 52% (2.8 million ha) of total cotton plantings.^[30] According to David Hackenberg, former president of the American Beekeeping Federation and leading the public information concerning CCD as a beekeeper, "beekeepers that have been most affected so far have been close to corn, cotton, soybeans, canola, sunflowers, apples, vine crops and pumpkins."^[14] Thus some of the commercially grown Bt plants seem to be included in gaps of pollination management. However, similar massive bee die-offs have been recorded for decades prior to the introduction of these crops^[4], and also occur in areas in Europe and Canada where there are no GM crops grown at all^[21].

In the end, a comprehensive review of the scientific literature published in Bee World^[31] examined the effects of various commercialized and uncommercialized transgenes on honey bees. It concludes that "Evidence available so far shows that none of the GM plants currently commercially available have significant impacts on honey bee health."

In North America, at least 24 different states^[3] as well as portions of Canada are known to have been affected by Colony Collapse Disorder. The disorder has been identified in a geographically diverse group of states including Georgia, Oklahoma, Pennsylvania, Wisconsin and California^[32]. In some states the loss of honey bee colonies is estimated as high as 75 percent of the population. The phenomenon is particularly important for crops such as the almond growing in California, where honey bees are the predominant pollinator and the crop value in 2006 was $US 1.5 billion. In 2000, the total U.S. crop value that was wholly dependent on the honey bee pollination was estimated to exceed $US 15 billion.^[33]

Honey bees are not native to the Americas, therefore their necessity as pollinators in the US is limited to strictly agricultural uses. 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, and strawberries; many but not all of these plants can be (and often are) pollinated by other insects, including other kinds of bees, in the U.S., 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, the native pollinators quickly reclaim the niche, typically being better adapted to serve those plants (assuming that the plants normally occur in that specific area). On the 30% of crop types where honey bees are used -- even though many other creatures are actually more efficient at pollinating, on a per-individual basis -- most native pollinators cannot be mass-utilized as easily or as effectively as honey bees, if they will 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.

In Europe, the same (or similar) phenomenon has been recently reported in Spain and Poland, and to a lesser degree in Switzerland and Germany ^[34]and Turkey.^{[citation needed]}

• Bees and toxic chemicals
• Diseases of the honey bee
• Pollinator decline
• Endangered arthropod
• Pesticide toxicity to bees
• Imidacloprid effects on bee population (This pesticide, while banned in France, has been rapidly increasing in usage in the USA)

• John Finnerty, Agriculture: Disease Killing Bees, February 9, 2007
• February 5, 2007: NHB Funds Research for “Colony Collapse Disorder”
• Beebits and cases of honey poisoning
• BackYardHive Discusses Colony Collapse Disorder
• Comment On Blog about Bee Colony Collapse Disorder
• WikiNews Report about CCD
• Matt Wells, "Vanishing bees threaten US crops", BBC News 11 March 2007, (includes picture of a comb from an affected hive).
• "Honeybees, Gone With the Wind, Leave Crops and Keepers in Peril" New York Times article on CCD, 23 February 2007 (subscription required)
• "Mystery Bee Disappearances Sweeping U.S.", Stefan Lovgren, National Geographic News, February 23, 2007
• "Honey bees in US facing extinction", Michael Leidig in Vienna, telegraph.co.uk, 14/03/2007
• The American Beekeeping Federation