Colony Collapse Disorder

  Colony Collapse Disorder (or CCD) is a little-understood phenomenon in which worker bees from a beehive or Western honey bee colony abruptly disappear. CCD was originally found in Western honey bee colonies in North America in late 2006.^[1]

European beekeepers observed a similar phenomenon in Belgium, France, the Netherlands, Greece, Italy, Portugal, and Spain^[2], and initial reports have also come in from Switzerland and Germany, albeit to a lesser degree.^[3] Possible cases of CCD have also been reported in Taiwan since April 2007.^[4]

The cause (or causes) of the syndrome is not yet well understood. Theories include environmental change-related stresses,^[5] malnutrition, pathogens (i.e., disease^[6] including Israel acute paralysis virus^[7][8]), mites, pesticides such as neonicotinoids or imidacloprid, radiation from cellular phones or other man-made devices,^[9] and genetically modified (GM) crops with pest control characteristics such as transgenic maize.^[10] Some claim that the disappearances have not been reported from organic beekeepers, suggesting to some that beekeeping practices can be a primary factor.^[11]

Additional recommended knowledge

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Background

From 1971 through 2006, there was a dramatic reduction in the number of feral (wild) honeybees in the US (now almost absent);^[12] and a significant, though somewhat gradual decline in the number of colonies maintained by beekeepers. This decline includes the cumulative losses from all factors such as urbanization, pesticide use, tracheal and Varroa mites, and commercial beekeepers retiring and going out of business. However, late in the year 2006 and in early 2007 the rate of attrition was alleged to have reached new proportions, and the term "Colony Collapse Disorder" was proposed to describe this sudden rash of disappearances.^[1]

Limited occurrences resembling CCD have been documented as early as 1896,^[6][13] 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).^[14] Most recently, a similar phenomenon in the winter of 2004/2005 occurred, and was attributed to Varroa mites (the "Vampire Mite" scare), though this was never ultimately confirmed. Nobody has been able to determine the cause of any past appearances of this syndrome. Upon recognition that the syndrome does not seem to be seasonally-restricted, and that it may not be a "disease" in the standard sense — that there may not be a specific causative agent — the syndrome was renamed.^[15]

Symptoms

A colony which has collapsed from CCD is generally characterized by all of these conditions occurring simultaneously^[16]:

• Complete absence of adult bees in colonies, with little or no build-up of dead bees in or around 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 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.

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 Queen is present (i.e. she is not lost)
• The colony members are reluctant to consume provided feed, such as sugar syrup and protein supplement.

Scale of the disorder

In the U.S., at least 24 different states^[5][17] as well as portions of Canada^[18] have reported at least one case of CCD. However, in many cases, beekeepers reporting significant losses of bees did not experience CCD, and a major part of the subsequent analysis of the phenomenon hinges upon distinguishing between true CCD losses and non-CCD losses.^[19] In a survey of 384 responding beekeepers from 13 states, reporting the number of hives containing few or no bees in spring, only 23.8% met the specified criteria 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).^[19] In the US, despite highly variable anecdotal claims appearing in the media, the best documentation indicates that 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; it is further noted that 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%.^[19]

There are also putative cases reported by the media from India, Brazil^[20] and parts of Europe.[3] Since the beginning of the 1990s, France, Belgium, Italy, Germany, Switzerland, Spain, Greece, Slovenia and the Netherlands have been affected by honey bee disappearances, though this is not necessarily associated with CCD;^[2] Austria and England (where it has been dubbed the "Mary Celeste" phenomena, after the name of a ship whose crew disappeared in 1872) have also reportedly been affected.^[4] It is far from certain that all or any of these reported non-US cases are indeed CCD: there has been considerable publicity, but only rarely was the phenomenon described in sufficient detail. In Germany, for example, where some of the first reports of CCD in Europe appeared, and where — according to the German national association of beekeepers — 40% of the honey bee colonies died,^[4] there has been no scientific confirmation; as of early May 2007, the German media were reporting that no confirmed CCD cases seemed to have occurred in Germany.^[21]

Possible causes and research

The exact mechanisms of CCD are still unknown. One report indicates a strong but possibly non-causal association between the syndrome and the presence of the Israel acute paralysis virus.^[8] Other factors may also be involved, however, and several have been proposed as causative agents; malnutrition, pesticides, pathogens, immunodeficiencies, mites, fungus, genetically modified (GM) crops, beekeeping practices (such as the use of antibiotics, or long-distance transportation of beehives) and electromagnetic radiation. Whether any single factor is responsible, or a combination of factors (acting independently in different areas affected by CCD, or acting in tandem), is still unknown. It is likewise still uncertain whether CCD is a genuinely new phenomenon, as opposed to a known phenomenon that previously only had a minor impact.

At present, the primary source of information, and presumed "lead" group investigating the phenomenon, is the Colony Collapse Disorder Working Group, based primarily at Penn State University. Their preliminary report pointed out some patterns, but drew no strong conclusions.^[15] A survey of beekeepers early in 2007 indicates that most hobbyist beekeepers believed that starvation was the leading cause of death in their colonies, while commercial beekeepers overwhelmingly believed that invertebrate pests (Varroa mites, honey bee tracheal mites, and/or small hive beetles) were the leading cause of colony mortality.^[19] A scholarly review in June, 2007, similarly addressed numerous theories and possible contributing factors, but left the issue unresolved.^[14]

In July, 2007, the USDA released its "CCD Action Plan", which indicates "The current strategy for addressing the CCD crisis involves four main components [4]:

1. survey and data collection;
2. analysis of samples;
3. hypothesis-driven research; and,
4. mitigation and preventative action.

As of late 2007, there is still no consensus of opinion, and no definitive causes have emerged; the schedule of presentations for a planned national symposium on CCD, titled "Colony Collapse Disorder in Honey Bees: Insight Into Status, Potential Causes, and Preventive Measures," which is scheduled for December 11, 2007, at the meeting of the Entomological Society of America in San Diego, California, gives no indication of any major breakthroughs.[5]

Poor nutrition or malnutrition

One of the patterns reported by the 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 their die-off, most commonly involving poor nutrition and/or drought.^[15] 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.^[19]

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.^[3] 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.

Pathogens and immunodeficiency theories

Further information: Pathogen, immunodeficiency, and diseases of the honey bee

General

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,^[22] potentially linked to the aforementioned "stress" leading to a weakened immune system. Specifically, according to researchers at Penn State: "The magnitude of detected infectious agents in the adult bees suggests some type of immunosuppression." These researchers initially suggested a connection between Varroa destructor mite infestation and CCD, suggesting that a combination of these bee mites, deformed wing virus (which the mites transmit) and bacteria work together to suppress immunity and may be one cause of CCD.^[23] This research group is reported to be focusing on a search for possible viral, bacterial, or fungal pathogens which may be involved.^[15]

When a colony is dying, for whatever cause, and there are other healthy colonies nearby (as is typical in a bee yard), those healthy colonies often enter the dying colony and rob its provisions for their own use. If the dying colony's provisions were contaminated (by natural or man-made toxins), the resulting pattern (of healthy colonies becoming sick when in proximity to a dying colony) might suggest to an observer that a contagious disease is involved. However, it is typical in CCD cases that provisions of dying colonies are not being robbed, suggesting that at least this particular mechanism (toxins being spread via robbing, thereby mimicking a disease) is not involved in CCD.

Additional evidence that CCD might be an infectious disease came from the following observation: the hives of colonies that had died from CCD could be reused with a healthy colony only if they were first treated with DNA-destroying radiation.^[8]

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.^[23] Affliction with Varroa mites also tends to weaken the immune system of the bees. As such, Varroa have been considered as a possible cause of CCD, though not all dying colonies contain these mites.^[24]

In September 2007, results of a large-scale statistical RNA sequencing study of afflicted and non-afflicted colonies were reported. RNA from all organisms in a colony was sequenced and compared with sequence databases to detect the presence of pathogens. The study used technology from 454 Life Sciences developed for human genome sequencing. All colonies were found to be infected with numerous pathogens, but only the Israel acute paralysis virus (IAPV) showed a significant association with CCD: the virus was found in 25 of the 30 tested CCD colonies, and only in one of the 21 tested non-CCD colonies.^[8] 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 were planned to deliberately infect colonies with the virus.^[7]

The IAPV was discovered in 2004 and belongs to the Dicistroviridae. It causes paralysis in bees which then die outside of the hive. It can be transmitted by the mite Varroa destructor. These mites, however, were found in only half of the CCD colonies.^[8]

The virus was also found in samples of Australian honey bees. Australian honey bees have been imported into the U.S. since 2004^[7] 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.^[25]

Nosema

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.^[15]

Mariano Higes, a scientist heading a team at a government-funded apiculture centre in Guadalajara, Spain, has reported that when hives of European honey bees were infected with Nosema ceranae, a recently described microsporidian fungus, the colonies were wiped out within eight days.^[26] 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.^[27][28] Various areas in Europe have reported this fungus, but no direct link to CCD has yet been established.^[29][30] Highly preliminary evidence of N. ceranae was recently reported in a few hives in the Merced Valley area of California (USA).^[31][32] 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.^[33]" 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."^[34] Likewise, a Washington State beekeeper familiar with N. ceranae in his own hives discounts it as being the cause of CCD.^[35] A study reported in September 2007 found that 100% of afflicted and 80% of non-afflicted colonies contained Nosema ceranae.^[8]

The primary antibiotic used against Nosema is Fumagillin, which has been used in a German research project to reduce the microsporidian's impact, and is mentioned as a possible remedy by the CCDWG.^[36]

Pesticides

Further information: Pesticide toxicity to bees

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.

It is particularly difficult to evaluate pesticide contributions to CCD for several reasons. First, the variety of pesticides in use in the different areas reporting CCD makes it difficult to test for all possible pesticides simultaneously. Second, many commercial beekeeping operations are mobile, transporting hives over large geographic distances over the course of a season, potentially exposing the colonies to different pesticides at each location. Third, the bees themselves place pollen and honey into long-term storage, effectively meaning that there may be a delay of anywhere from days to months before contaminated provisions are fed to the colony, negating any attempts to associate the appearance of symptoms with the actual time at which exposure to pesticides occurred. Pesticides used on bee forage are far more likely to enter the colony via the pollen stores rather than via nectar (because pollen is carried externally on the bees, while nectar is carried internally, and may kill the bee if too toxic), though not all potentially lethal chemicals, either natural or man-made, affect the adult bees — many primarily affect the brood, but brood die-off does not appear to be happening in CCD. Most significantly, brood are not fed honey, and adult bees consume relatively little pollen; accordingly, the pattern in CCD suggests that if contaminants or toxins from the environment are responsible, it is most likely to be via the honey, as it is the adults that are dying (or leaving), not the brood.

One recently published view is that bees are falling victim to new varieties of nicotine-based pesticides;^[37][38] beekeepers in Canada are also losing their bees and are blaming neonicotinoid pesticides. To date, most of the evaluation of possible roles of pesticides in CCD have relied on the use of surveys submitted by beekeepers, but it seems likely that direct testing of samples from affected colonies will be needed, especially given the possible role of systemic insecticides such as the neonicotinoid imidacloprid (which are applied to the soil and taken up into the plant's tissues, including pollen and nectar), which may be applied to a crop when the beekeeper is not present. The known effects of imidacloprid on insects, including honey bees, are consistent with the symptoms of CCD;^[39] for example, the effects of imidacloprid on termites include apparent failure of the immune system, and disorientation.^[40] In Europe the interaction of the phenomenon of "dying bees" with imidacloprid, has been discussed for quite some time now.^[41][42][43] It was a study from the "Comité Scientifique et Technique (CST)" which was in the center of discussion recently, which led to a partial ban of imidacloprid in France (known as Gaucho), primarily due to concern over potential effects on honey bees.^[44][45][46] 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.^[47] In February 2007, about forty French deputies, led by UMP member Jacques Remiller, requested the creation of a Parliamentary Investigation Commission on Overmortality of Bees, underlining that the honey production was decreasing by 1,000 tons a year for a decade. As of August 2007, no investigations were yet opened.^[28] The imidacloprid pesticide Gaucho was banned, however, in 1999 by the French Minister of Agriculture Jean Glavany. Five other insecticides based on fipronil were also accused of killing bees. However, the scientific committees of the European Union are still of the opinion "that the available monitoring studies were mainly performed in France and EU-member-states should consider the relevance of these studies for the circumstances in their country."^[48]

In 2005, a team of scientists led by the National Institute of Beekeeping in Bologna, Italy, found that pollen obtained from seeds dressed with imidacloprid contains significant levels of the insecticide, and suggested that the polluted pollen might cause honey bee colony death.^[49] Analysis of maize and sunflower crops originating from seeds dressed with imidacloprid suggest that large amounts of the insecticide will be carried back to honey bee colonies.^[50] Sub-lethal doses of imidacloprid in sucrose solution have also been documented to affect homing and foraging activity of honeybees.^[51] Imidacloprid in sucrose solution fed to bees in the laboratory impaired their communication for a few hours.^[52] Sub-lethal doses of imidacloprid in laboratory and field experiment decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired.^[53] However, no detailed studies of toxicity or pesticide residue in remaining honey or pollen in CCD-affected colonies have been published so far, so, despite the similarity in symptoms, no connection of neonicotinoids to CCD has yet been confirmed.

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^[15] 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.^[14] Some reports indicate that organic beekeepers (who do not use antibiotics or miticides) are not affected by CCD, despite proximity to non-organic beekeepers that have been affected.^[11]

Genetically modified crops (GMO)

Further information: Genetically modified organism

Potential effects on honey bees of gathering pollen and nectar from genetically modified (GM) crops that produce Bacillus thuringiensis (Bt) toxin have been investigated, and there is scant evidence of deleterious effects on bees visiting such crops. Corn (maize), 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".^[37] 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),^[54] but there is no credible evidence of toxicity of GM cotton, other than that from insecticides used during bloom.

The Sierra Club Genetic Engineering Committee recently published a letter to Senator Thomas Harkin on the web.^[10] 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.^[10]

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^[55] despite the absence of symptoms in the larvae, and despite any evidence that the bees experiencing CCD have ever been exposed to GM crops.

In 2005 Bt maize, which is commercially planted in the US since 1996, accounted for 35% (106,400 km²) 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% (28,000 km²) of total cotton plantings.^[56] 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", though Hackenberg personally attributes CCD to neonicotinoid pesticides applied to these crops.^[37] Thus, some Bt plants may have been visited by honey bees that later exhibited CCD. However, similar massive bee die-offs (or disappearances) have been recorded for decades prior to the introduction of these crops,^[6] and also "have occurred in Europe and areas of Canada where Bt crops were not grown."^[57] According to the European Union's GMO Compass Bt maize is grown in Spain, France, Czech Republic, Portugal, Germany and Slovakia [6][7]. Various documents relating to 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;^[58][59][60] there is no indication that any of these studies found effects of Bt pollen on honey bees.

In 2004 the knowledge of GMO authorisation agencies was mainly based on a comprehensive review of the scientific literature published in Bee World^[61] which examined the effects of various commercialized and uncommercialized transgenes on honey bees. The review concludes that "evidence available so far shows that none of the GM plants currently commercially available have significant impacts on honey bee health." However, in 2005 a new publication in the Journal Apidologie^[62] indicated that foraging activity of bees fed with CRY1Ab may decline continuously through the treatment stages without any recovery between treatments (though in the treatment with CRY1Ab-enriched feed, no significant differences in bee mortality were found at different treatment stages). The European Union GMO Panel of the European Food Safety Authority (EFSA) did not share the view by the authors “that the above results were mainly CRY1Ab dependent.” The Panel was of the opinion that “negative effects on bees are likely not directly associated with exposure to the CRY1Ab protein because of the design of the experiment and lack of simultaneous controls or replication.^[63]

A research study conducted in Germany suggested that rather than having a direct effect, exposure to Bt maize pollen 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."^[64] 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."^[65] Other more recent studies have failed to show any adverse effects of Bt pollen on healthy bee colonies^[57], but the possibility that Bt pollen weakens already unhealthy colonies has not been explored.

The preliminary report of the Colony Collapse Disorder Working Group^[6] concerning "Fall Dwindle Disease"^[15] indicated that "all PA samples were found to have Nosema spores in their rectal contents. The sting gland of many examined bees was 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. Many of the colonies reported to be dying from CCD occur in locations where GM corn is not grown (at least in the United States; also, 5 of the 10 states with the greatest amount of corn production, including GM corn - Illinois, Indiana, Kansas, Missouri, and Nebraska - have had no reported cases of CCD^[17][14]), nor have bees from other areas outside of Pennsylvania been reported to be significantly infected by Nosema (e.g.,^[15]).

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".^[66] It suggested that GMO, besides other factors, might contribute to pollinator decline because, according to one scientific review of "the small literature on this topic,…in some cases, there are negative but sublethal effects attributable to consumption of transgenic pollens." The report goes on to say that, "These effects varied with the identity of the transgene and the amount of its expression, but in no case have any effects of transgenic crops on honey bee populations been documented."^[67]

On March 28 2007, the "Mid-Atlantic Apiculture Research and Extension Consortium"^[68] 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."^[57]

Bee rentals and Migratory Beekeeping

Further information: Beekeeping

  Since US beekeeper Nephi Miller first began moving his hives to different areas of the country for the winter of 1908, migratory beekeeping has become widespread in America.

Bee rental for pollination is a crucial element of US agriculture, which could not produce anywhere near its current levels with native pollinators alone.^[69] US beekeepers collectively earn much more from renting their bees out for pollination than they do from honey production.

Researchers are concerned that trucking colonies around the country to pollinate crops, where they intermingle with other bees from all over, helps spread viruses and mites among colonies. Additionally, such continuous movement and re-settlement is considered by some a strain and disruption for the entire hive, possibly rendering it less resistant to all sorts of systemic disorder.^[70]

US bee rental travel extent

One major US 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 November -- 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 US has resulted in far greater losses from Varroa mite infections in recent years.^[71]

Climate Change

Some beekeepers think the culprit may be climate change, in which the earth as a whole is warming but regional and local temperatures may drop much lower or rise higher than normal. "Erratic weather patterns caused by global warming could play havoc with bees’ sensitive cycles. A lot of northeastern U.S. beekeepers say a late cold snap is what did the damage to them this year" [8]. Indeed an unusually dry and warm winter prevented the flowering of many plants, "If there is not a common thread, such as a pathogen seen in many of the affected colonies, Professor Eric Mussen of UC Davis said he is convinced that a nutritional deficit helps explain how the honeybees were weakened by the smorgasbord of potential causes of death. That is because dry conditions, certainly in California, did not produce flowers in which bees find their required mix of pollens, he said ... 'In many situations the bees were weakened by not being able to get a nice mix of nutrients that they needed from the pollens, and I think that weakened them,' he said. 'Under those circumstances you can take all the other (causes), and there are plenty of them, and combine them together and down go the bees'" [9].

"Dry conditions in many parts of the country last fall reduced good nectar flow, so fewer good fall pollens were taken into colonies. 'Bees rely on fall pollens to rear a brood and take them through the winter. It was a hard fall, followed by a warm winter, and bees were out flying. There weren’t any resources (food) out there, so the bees were burning up flight muscles'" [10]. "Well, you get this blast of hot temperature, which is about the time the flower buds are forming and the pollen grains are beginning to form. What does that do? You get sterile pollen. A beekeeper could look into the hive and say, "I've got all kinds of pollen in there and the bees disappeared." Well, right, you've got pollen grains, but do they have any nutrition in them? ... I think something happened at the end of last year in many places in the temperate climate around the world, not just here, and fouled up the bees' food supply. Unless somebody tells me differently, I'm blaming it on the weather ... for whatever reason, we are beginning to kind of move into a cycle where we are going to find more extremes than we used to have. The droughts may be hotter and longer, the storms and floods may be more severe. Things aren't going to be so nice in the future" [11]. In fact the first half of 2006 was the warmest on record in U.S.[12].

Some say that flowers are blooming earlier than in the past, "Climate change and earlier springs have also taken a toll. Plants like red maples and pussy willows, typically the first pollen sources for honeybees, have been blossoming weeks before the bees can fly in the spring, Conrad [author of Natural Beekeeping] said, so they miss out on that important source of pollen" [13]. Wayne Esaias, a NASA climatologist and beekeeper has been keeping tabs on the possible connection [14][15]. See also Bees, Pollination and Climate Change: A Guide to Selected Resources.

Electromagnetic radiation

Further information: Electromagnetic radiation and Mobile phone radiation and health

In April 2007, news of a University of Landau study appeared in major media, beginning with an article in The Independent that stated that the subject of the study was mobile phones and had related them to CCD.^[9] Cellular phones were implicated by other media reports, but were in fact not covered in the study, and the researchers have since emphatically disavowed any connection between their research, cell phones, and CCD, specifically indicating that the Independent article had misinterpreted their results and created "a horror story".^[72][73][74]

The 2006 University of Landau pilot study was looking for non-thermal effects of radio frequency ("RF") on honey bees (Apis mellifera carnica) and suggested that when bee hives have DECT cordless phone base stations embedded in them, the close-range electromagnetic field ("EMF") may reduce the ability of bees to return to their hive; they also noticed a slight reduction in honeycomb weight in treated colonies.^[75] In the course of their study, one half of their colonies broke down, including some of their controls which did not have DECT base stations embedded in them.

The team's 2004 exploratory study on non-thermal effects on learning did not find any change in behavior due to RF exposure from the DECT base station operating at 1880-1900 MHz.^[76]

At present the link of either cordless or cellular phones to CCD is entirely speculative, and no research has been done to suggest or demonstrate such a link between the two phenomena. Regardless, such an explanation is not compatible with the historical and present patterns of CCD appearance, which have been intermittent and sudden.

Possible effects

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 US$1.5 billion. In 2000, the total U.S. crop value that was wholly dependent on honey bee pollination was estimated to exceed US$15 billion.^[77]

Honey bees are not native to the Americas, therefore their necessity as pollinators in the US is limited to strictly agricultural/ornamental uses, as no native plants require honey bee pollination, except where concentrated in monoculture situations—where the pollination need is so great at bloom time that pollinators must be concentrated beyond the capacity of native bees (with current technology).

They are responsible for pollination of approximately one third of the United States' crop species, including such species as: almonds, peaches, soybeans, apples, pears, cherries, raspberries, blackberries, cranberries, watermelons, cantaloupes, cucumbers and strawberries. Many but not all of these plants can be (and often are) pollinated by other insects in small holdings in the U.S., including other kinds of bees, but typically not on a commercial scale. While some farmers of a few kinds of native crops do bring in honey bees to help pollinate, none specifically need them, and when honey bees are absent from a region, there is a presumption that native pollinators may reclaim the niche, typically being better adapted to serve those plants (assuming that the plants normally occur in that specific area).

However, even though on a per-individual basis, many other species are actually more efficient at pollinating, on the 30% of crop types where honey bees are used, most native pollinators cannot be mass-utilized as easily or as effectively as honey bees—in many instances they will not visit the plants at all. Beehives can be moved from crop to crop as needed, and the bees will visit many plants in large numbers, compensating via sheer numbers for what they lack in efficiency. The commercial viability of these crops is therefore strongly tied to the beekeeping industry.

Remedies

As of March 1, 2007 MAAREC offers the following tentative recommendations for beekeepers noticing the symptoms of CCD:^[36]

1. Do not combine collapsing colonies with strong colonies.
2. 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.
3. If you feed your bees sugar syrup, use Fumagillin.
4. If you are experiencing colony collapse and see a secondary infection, such as European Foulbrood, treat the colonies with Terramycin, not Tylan.

See also

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

References