Colony collapse disorder

Honey bees entering a beehive

Colony Collapse Disorder (CCD) or sometimes honey bee depopulation syndrome (HBDS)[1] 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.[2] Colony collapse is economically 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,[3] and initial reports have also come in from Switzerland and Germany, albeit to a lesser degree[4] while the Northern Ireland Assembly received reports of a decline greater than 50%.[5] Possible cases of CCD have also been reported in Taiwan since April 2007.[6]

The cause or causes of the syndrome are not yet fully understood, although many authorities attribute the problem to biotic factors such as Varroa mites and insect diseases (i.e., pathogens[7] including Nosema apis and Israel acute paralysis virus).[8][9] Other proposed causes include environmental change-related stresses,[10] malnutrition and pesticides (e.g. neonicotinoids such as imidacloprid), and migratory beekeeping. More speculative possibilities have included both cell phone radiation (e.g.[11]) and genetically modified (GM) crops with pest control characteristics,[12][13] 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.[14][15][16]

Contents

Background

From 1972 to 2006, there was a dramatic reduction in the number of feral honeybees in the U.S. (now almost absent);[17] 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.[2]

Limited occurrences resembling CCD have been documented as early as 1869[18][19] 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).[20] 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.[21]

Symptoms

A colony which has collapsed from CCD is generally characterized by all of these conditions occurring simultaneously:[22]

Precursor symptoms that may arise before the final colony collapse are:

Scale of the disorder

In the U.S., at least 24 different states[10][23] as well as portions of Canada[24] had reported at least one case of CCD in 2007. 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.[25] In a 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 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).[25] 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; 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%.[25]

There were also putative cases reported by the media from India, Brazil[26] and parts of Europe.[27] 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;[3] Austria and United Kingdom (where it has been dubbed the "Mary Celeste" phenomenon (after a ship whose crew disappeared in 1872)[28] had also reportedly been affected.[6] It is far from certain that all or any of these reported non-U.S. cases were indeed CCD: there was 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,[6] 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.[29]

As of 2009, the number of reported cases of CCD in the U.S. had dropped considerably; over the 2008/2009 winter, a total loss of 28.6% of managed honey bee colonies was recorded in the U.S., and only 15% of that subset (equal to only 4.3% of the national total) died with symptoms of CCD.[30] The winter of 2009/2010, however, saw an increase to 33.8% overwintering mortality among surveyed beekeepers,[31] though no statistics are available for the proportion attributed to CCD.

Possible causes and research

The exact mechanisms of CCD are still unknown. A primary focus of research is the possible association between the syndrome and the presence of the Israel acute paralysis virus.[9] Identified by Hebrew University of Jerusalem plant virologist Prof. Ilan Sela in 2004, the virus causes honeybees to suffer from shivering wings, followed by paralysis and death outside the hive. In 2007, the journal Science published research by a team of U.S. scientists and researchers that found a significant connection between IAPV and CCD in honeybees.[32] Other factors may also be involved, however, and several have been proposed as causative agents; malnutrition, pesticides, pathogens, immunodeficiencies, mites, fungus, 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.[21] 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.[25] A scholarly review in June 2007 similarly addressed numerous theories and possible contributing factors, but left the issue unresolved.[20]

In July 2007, the USDA released its "CCD Action Plan", which outlined a strategy for addressing CCD consisting of four main components:[33]

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

In July 2009, the first annual report of the US Colony Collapse Disorder Steering Committee was published.[34] It suggested that colony collapse may be caused by the interaction of many agents in combination.[16]

Similarly, in 2009, the CCD Working Group published a comprehensive descriptive study which 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."[35] At present, therefore, research has not identified any one definitive causative factor, despite having examined nearly all of those listed below.

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.[21] 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.[25]

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.[4] 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; where 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).[36]

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.[37]

Similarly, other researchers in 2009 put forth the untested hypothesis "that a honey bee dietary deficiency of pyrethrums and other micronutrients from pyrethrum producing plants allows parasitic mites to either kill the honey bees directly or reduce honey bee resistance to other pathogens. Intermittent feeding of honey bees on pyrethrum producing plants might reverse or prevent colony collapse disorder";[38] however, this does not address cases of CCD occurring in the absence of mite infestations.

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,[39] 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.[40] This research group is reported to be focusing on a search for possible viral, bacterial, or fungal pathogens which may be involved.[21]

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 comes 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,[9] and the CCD Working Group report in 2010 indicated that CCD-exhibiting hives tended to occur in proximity to one another within apiaries.[35]

Varroa and Israel acute paralysis virus

Varroa destructor on a honey bee host

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.[40] 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.[41] As such, Varroa mites have been considered as a possible cause of CCD, though not all dying colonies contain these mites.[42]

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.[9] 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.[8]

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.[9]

The virus was also found in samples of Australian honey bees. Australian honey bees have been imported into the U.S. since 2004,[8] 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.[43][44]

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.[45][46]

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.[21]

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.[47] 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.[48][49]

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.[50] Higes also claims to have successfully cured colonies with fumagillin.[51][52] 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".[53] Various areas in Europe have reported this fungus, but no direct link to CCD has yet been established.[54][55] Highly preliminary evidence of N. ceranae was recently reported in a few hives in the Merced Valley area of California (USA).[56][57] 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".[58] 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".[59] Likewise, a Washington State beekeeper familiar with N. ceranae in his own hives, discounts it as being the cause of CCD.[60] 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.[61][62] 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.[63]

Pesticides

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;[64][65] 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;[66] for example, the effects of imidacloprid on termites include apparent failure of the immune system, and disorientation.[67] In Europe, the interaction of the phenomenon of "dying bees" with imidacloprid has been discussed for quite some time now.[68][69][70] 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.[71][72][73] 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.[74] 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.[75] 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".[76]

Around the same time French beekeepers succeeded in banning neonicotinoids, the Clinton administration permitted pesticides which were previously banned,[77] including imidacloprid. In 2004, the Bush Administration reduced regulations further and pesticide applications increased.[78][79] Some have claimed use of neonicotinoids on crops may be linked to the increase in cases of CCD in the United States since 2004, but there is no research yet to support such a connection; while such pesticides might have a negative impact upon bees, this appears to be entirely independent of CCD[80]

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.[81] 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.[82] Sublethal doses of imidacloprid in sucrose solution have also been documented to affect homing and foraging activity of honeybees.[83] Imidacloprid in sucrose solution fed to bees in the laboratory impaired their communication for a few hours.[84] Sublethal doses of imidacloprid in laboratory and field experiment decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired.[85]

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;[86] other studies, however, have shown no acute effect on honey bees.[87]

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.[88]

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[21] 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.[20]

Genetically modified crops (GMO)

Some genetically modified (GM) crops produce the natural insecticide Bt toxin, which was hypothesised to affect bees. In the scant literature on the topic, there exists no evidence of any negative effects on honey bee populations,[89] and while research on GM crops is still ongoing, new results continue to suggest GM crops have no negative effect on bee populations.[7][90] Further, CCD cases are known in areas of Europe and Canada where Bt crops are not grown.[91]

Bee rentals and migratory beekeeping

Further information: Beekeeping
Moving spring bees from South Carolina to Maine for blueberry pollination

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.[92] 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.[93]

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 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 U.S. has resulted in far greater losses from Varroa mite infections in recent years.[94]

Climate change

A few scientists have suggested that climate change can make bee hives more vulnerable to CCD, although it is not implicated as a direct cause of the disorder. "We see plants blooming at different times of the year", says amateur beekeeper Wayne Esaias, a researcher at the NASA Goddard Space Flight Center, "and that's why the nectar flows are so much earlier now. I need to underscore that I have no evidence that global warming is a key player in colony collapse disorder. But it might be a contributor, and changes like this might be upping the stress level of our bee populations".[95]

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 honeybees. One of the few peer-reviewed studies was published in 1981 by Gary and Westerdahl. This study was conducted as part of a research program to assess possible environmental impacts of solar power satellite systems, which would beam immense amounts of microwave energy from satellites to receiving stations on the ground to be converted into electrical power. The investigators measured flight, orientation, and memory functions in honeybees after thirty minutes' exposure to 2.45-GHz continuous-wave microwaves at power densities from 30 to 500 watts per square meter - similar in frequency to that used by mobile phone networks but at far higher power densities than produced at nearly all locations from base station antennas except very close to the antennas. 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".[96] This issue (of effect of microwave energy on honeybees) has reappeared in context of the present controversy about possible health risks of wireless communications systems. However, no studies have appeared that have an adequate experimental design and exposure assessment to allow reliable conclusions to be drawn.

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.[97]

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.[98] 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 a study conducted by investigators at University of Landau 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.[99] Though Cellular phones were implicated by other media reports at the time, they were not covered in the 2007 study. Researchers involved with the 2007 study 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". It should be noted however that the frequency range involved in the study, near 1900 MHz, is the more recent band employed by GSM mobile phones (the older band being much lower at 850 MHz) so the test results at the DECT handset's frequency could be correlated to the spread of GSM cellular and wireless handset use.[100][101][102]

In May 2010, two researchers from Chandigarh's Panjab University published a study alleging to find significant changes in honeybee behavior as a result of the placement of two functional cellphones of GSM 900 MHz frequency inside the hive.[103] The study was immediately criticized for systemic errors, primarily based on the low sample size (four colonies). Criticisms also noted that the researchers mischaracterized the electromagnetic environment of areas where CCD has been reported and drew a false comparison to the electromagnetic environment of India.[104]

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 honeybees can detect weak static or low-frequency magnetic fields, which they use as one of several cues in navigation.[105]

UK bee database

In the United Kingdom, a national bee database is to be set up to monitor colony collapse as a result of a 15% reduction in the bee population over the last two years.[106] 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.

Possible commercial 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 $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.[107]

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 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 (e.g., squash bees on cucurbits[108]), 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 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.[109]

Remedies

As of March 1, 2007 MAAREC offered the following tentative recommendations for beekeepers noticing the symptoms of CCD:[50]

  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.

Another proposed remedy for farmers of pollinated crops is simply to switch from using beekeepers to the use of native 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).[110][111]

In April 2009, it was reported that Russian bees that were resistant to the varroa mite had been introduced into the U.S., and that this was helping to solve the problem.[112] Similarly, a British beekeeper successfully developed another strain of bees that are resistant to varroa mites.[113][114][115][116]

In 2009, a group of scientists that originally discovered the CCD-causing IAPV virus [117] showed that the virus infection can be successfully eradicated by using the RNAi silencing technology.[118] This approach is used by Beeologics, a USA-Israeli biotechnology company that develops CCD-combating products.

Media portrayal

A number of documentaries have been produced in which possible causes of CCD have been explored. The 2009 documentary Vanishing of the Bees points to the neonicotinoid category of pesticides as being the most likely culprit, though the experts interviewed concede that no firm data yet exists.[119]

"Silence of the Bees" (Oct, 2007) is a part of the Nature (TV series) and covers several recent investigative discoveries.[120]

The 2008 film "The Happening" has a theme which relates CCD and the events of the film as "an act of nature which we will never fully understand".

See also

References

  1. ↑ Alan Cane (April 17, 2009). "Scientists isolate bee pathogen". Financial Times. http://www.ft.com/cms/s/0/ae4b031c-2ae6-11de-8415-00144feabdc0.html. 
  2. ↑ 2.0 2.1 "Honey Bee Die-Off Alarms Beekeepers, Crop Growers and Researchers". Penn State University College of Agricultural Sciences. 2007-01-29. http://www.aginfo.psu.edu/News/07Jan/HoneyBees.htm. 
  3. ↑ 3.0 3.1 Gaëlle Dupont, Les abeilles malades de l'homme, Le Monde, 29 August 2007 (French).
  4. ↑ 4.0 4.1 "Das spurlose Sterben" (in German). sueddeutsche.de. 2007-03-12. http://www.sueddeutsche.de/,ra13l5/wissen/artikel/352/105247/. 
  5. ↑ "Minutes of Northern Ireland Assembly". Theyworkforyou.com. 2009-06-08. http://www.theyworkforyou.com/ni/?id=2009-06-08.9.1. Retrieved 2010-06-22. 
  6. ↑ 6.0 6.1 6.2 Paul Molga, La mort des abeilles met la planète en danger, Les Echos, 20 August 2007 (French).
  7. ↑ 7.0 7.1 "Colony Collapse Disorder Working Group". Archived from the original on 2007-02-14. http://web.archive.org/web/20070214133122/http://www.ento.psu.edu/MAAREC/pressReleases/ColonyCollapseDisorderWG.html. 
  8. ↑ 8.0 8.1 8.2 "Virus Is Seen as Suspect in Death of Honeybees". The New York Times. 2007-09-07. http://www.nytimes.com/2007/09/07/science/07bees.html?hp. Retrieved 2007-09-07. 
  9. ↑ 9.0 9.1 9.2 9.3 9.4 "Mysterious Honeybee Disappearance Linked to Rare Virus". Science News (Scientific American). 2007-09-07. http://www.sciam.com/article.cfm?chanID=sa003&articleID=E0E0362F-E7F2-99DF-3F4F781839D6C879&pageNumber=1&catID=1. Retrieved 2007-09-07. 
  10. ↑ 10.0 10.1 "The mysterious deaths of the honeybees". CNN Money. 2007-03-29. http://money.cnn.com/2007/03/29/news/honeybees/. Retrieved 2007-04-04. 
  11. ↑ "Study links bee decline to cell phones". 2010-06-30. http://www.cnn.com/2010/WORLD/europe/06/30/bee.decline.mobile.phones/index.html?hpt=C2. Retrieved 2010-06-30. 
  12. ↑ "GE and bee Colony Collapse Disorder -- science needed!". 2005-03-21. http://www.sierraclub.org/biotech/whatsnew/whatsnew_2007-03-21.asp. Retrieved 2007-03-23. 
  13. ↑ "Collapsing Colonies: Are GM Crops Killing Bees? - International - SPIEGEL ONLINE - News". www.spiegel.de. 2007-03-22. http://www.spiegel.de/international/world/0,1518,473166,00.html. Retrieved 2008-02-24. 
  14. ↑ Honeybees under attack on all fronts.
  15. ↑ 'No proof' of bee killer theory.
  16. ↑ 16.0 16.1 Francis L. W. Ratnieks and Norman L. Carreck, "Clarity on Honey Bee Collaps", Science, 8 January 2010, Vol. 327, p. 152
  17. ↑ "Pollination worries rise as honey bees decline.". Science, vol. 265. 1994-08-26. p. 1170. 
  18. ↑ "Colony Collapse Disorder: Have We Seen This Before?". The Pennsylvania State University, Department of Entomology. http://www.beeculture.com/content/ColonyCollapseDisorderPDFs/7%20Colony%20Collapse%20Disorder%20Have%20We%20Seen%20This%20Before%20-%20Robyn%20M.%20Underwood%20and%20Dennis%20vanEngelsdorp.pdf. Retrieved 2010-05-02. 
  19. ↑ Benjamin Lester (2007-03-07). "Mystery of the dying bees". Cosmos Online. http://www.cosmosmagazine.com/node/1087?page=1. 
  20. ↑ 20.0 20.1 20.2 [1] Oldroyd BP (2007) What's Killing American Honey Bees? PLoS Biology 5(6): e168 doi:10.1371/journal.pbio.0050168) Retrieved on 2007-05-17.
  21. ↑ 21.0 21.1 21.2 21.3 21.4 21.5 "Colony Collapse Disorder Preliminary Report". Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC) - CCD Working Group. 2006-01-05. p. 22. http://maarec.cas.psu.edu/pressReleases/FallDwindleUpdate0107.pdf. Retrieved 2007-04-24. 
  22. ↑ "Discussion of phenomenon of Colony disorder collapse". Canadian Honey Council. 2007-01-27. Archived from the original on 2007-07-29. http://web.archive.org/web/20070729004717/http://honeycouncil.ca/users/news_view.asp?FolderID=3219&NewsID=1146. 
  23. ↑ [2] Map of affected states within the U.S.
  24. ↑ Strange times for bees, The Vancouver Courier.com.
  25. ↑ 25.0 25.1 25.2 25.3 25.4 Van Engelsdorp, D., Underwood, R., Caron, D. Hayes, Jr., J. (2007) An Estimate of Managed Colony Losses in the Winter of 2006–2007: A Report Commissioned by the Apiary Inspectors of America. American Bee Journal.
  26. ↑ "Mysterious Honeybee Killer Could Make Meals Bland". CBS 11/AP. 2007-05-08. http://cbs11tv.com/consumer/bees.honeybees.dying.2.502236.html. Retrieved 2007-12-31. 
  27. ↑ Are mobile phones wiping out our bees?.
  28. ↑ BBC Wild bee decline 'catastrophic' 23 April 2008.
  29. ↑ n-tv: Immer weniger Imker - Deutschen Bienen geht es gut. Version of May 11, 2007.
  30. ↑ "Preliminary Results concerning the loss of Honey Bee colonies" (PDF). http://maarec.cas.psu.edu/pdfs/PrelimLosses2009.pdf. Retrieved 2010-06-22. 
  31. ↑ Alison Benjamin (2010-05-02). "Fears for crops as shock figures from America show scale of bee catastrophe | Environment | The Observer". Guardian. http://www.guardian.co.uk/environment/2010/may/02/food-fear-mystery-beehives-collapse. Retrieved 2010-06-22. 
  32. ↑ "Israelis discover cure for bee colony collapse-associated virus | environment". Israel21c.org. 2008-09-22. http://www.israel21c.org/bin/en.jsp?enDispWho=Articles^l2290&enPage=BlankPage&enDisplay=view&enDispWhat=object&enVersion=0&enZone=Health. Retrieved 2010-06-22. 
  33. ↑ ""Colony Collapse Disorder Action Plan"" (PDF). USDA. 2007-06-20. http://www.ars.usda.gov/is/br/ccd/ccd_actionplan.pdf. 
  34. ↑ "CCD Steering Committee, ''Colony Collapse Disorder Progress Report'' (US Department of Agriculture, Washington, DC, 2009)" (PDF). http://www.extension.org/mediawiki/files/c/c7/CCDReport2009.pdf. Retrieved 2010-06-22. 
  35. ↑ 35.0 35.1 doi:10.1371/journal.pone.0006481
    This citation will be automatically completed in the next few minutes. You can jump the queue or expand by hand
  36. ↑ Pickert, Kate (March 12, 2009). "Postcard from Hughson". Time Magazine. http://www.time.com/time/magazine/article/0,9171,1884835,00.html. Retrieved 12 December 2009. 
  37. ↑ Bee decline linked to falling biodiversity Richard Black, BBC News, 20 January 2010
  38. ↑ Sharpe, Richard J. and Heyden, Lisa C. (2009). "Honey bee colony collapse disorder is possibly caused by a dietary pyrethrum deficiency". Bioscience Hypotheses, Volume 2, Issue 6, pp. 439-440. doi:10.1016/j.bihy.2009.01.004.
  39. ↑ "Colony Collapse Disorder". Penn State University 26 (1). 2007-01-23. http://fruittimes.cas.psu.edu/FT2601.html#Colony. 
  40. ↑ 40.0 40.1 "Bee Mites Suppress Bee Immunity, Open Door For Viruses And Bacteria". http://www.sciencedaily.com/releases/2005/05/050517110843.htm. 
  41. ↑ Guzmán-Novoa, E., Eccles, L., Calvete, Y., Mcgowan, J., Kelly, P. G., and Correa-Benítez, A. (2009). Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apodologie. Published online 8 January 2010 at [3]
  42. ↑ Dr. Jamie Ellis (2007-04-16). "Colony Collapse Disorder (CCD) in Honey Bees". University of Florida. http://pestalert.ifas.ufl.edu/Colony_Collapse_Disorder.htm. 
  43. ↑ Kim Kaplan (2007-11-19). "Imported Bees Not Source of Virus Associated with Colony Collapse Disorder)". USDA. http://www.ars.usda.gov/is/pr/2007/071119.htm. Retrieved 2007-11-29. 
  44. ↑ Science Express (Science 12 October 2007) 318 (no. 5848): 283–287. 6 September 2007. doi:10.1126/science.1146498. http://www.sciencemag.org/cgi/content/full/318/5848/283. 
  45. ↑ Genomic Study Yields Plausible Cause Of Colony Collapse Disorder at Science Daily on 2009-8-25
  46. ↑ Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera) Reed M. Johnson, Jay D. Evans, Gene E. Robinson and May R. Berenbaum PNAS August 24, 2009
  47. ↑ Higes, M., R. Martin, A. Meana (2006). "Nosema ceranae, a new microsporidian parasite in honeybees in Europe". Journal of Invertebrate Pathology 92 (2): 93–95. doi:10.1016/j.jip.2006.02.005. PMID 16574143. 
  48. ↑ Asian Parasite Killing Western Bees - Scientist, Planet Ark, SPAIN: July 19, 2007
  49. ↑ Maria Mancilla, Les abeilles sont-elles en train de disparaître?, Rue 89, 29 August 2007 (French)
  50. ↑ 50.0 50.1 Dennis vanEngelsdorp, M.Frazier, and D. Caron (2007-03-01). "Tentative Recommendations for Hives Experiencing CCD" (PDF). Mid-Atlantic Apiculture Research and Extension Consortium. http://maarec.cas.psu.edu/pdfs/CCDRecommendations.pdf. 
  51. ↑ "Higes", M.; "Martín-Hernández", R.; "Garrido-Bailón", E.; "González-Porto", A.V.; "García-Palencia", P.; "Meana", A.; Del Nozal, M.J.; "Mayo", R. et al. (2009). "Honeybee colony collapse due to Nosema ceranae in professional apiaries". Environmental Microbiology Reports 1 (2): 110–113. doi:10.1111/j.1758-2229.2009.00014.x. http://www3.interscience.wiley.com/journal/122204880/abstract. Retrieved 2009-04-22. 
  52. ↑ Cure For Honey Bee Colony Collapse? Science Daily article
  53. ↑ Microbiology: Colony collapse cured? Nature 458, 949 (23 April 2009) doi 10.1038/458949d.
  54. ↑ Dr Wolfgang Ritter. "Nosema ceranae - Asiatischer Nosema-Erreger festgestellt – neu verbreitet oder erst jetzt entdeckt?" (in German). Albert-Ludwigs-Universität Freiburg. http://www.imkerschule-sh.de/index.php?jahr%5B%5D=2006&imk_themen=j&n=28. 
  55. ↑ Dr Wolfgang Ritter. "Nosema ceranae - Asian Nosema Disease Vector Confirmed – is this a new infestation or only now discovered?" (in translated into English). Albert Ludwigs University of Freiburg. Archived from the original on 2007-02-14. http://web.archive.org/web/20070214004709/http://www.moraybeekeepers.co.uk/nosema.htm. 
  56. ↑ Sabin Russell (2007-04-26). "UCSF scientist tracks down suspect in honeybee deaths". San Francisco Chronicle. http://www.sfgate.com/cgi-bin/article.cgi?file=/c/a/2007/04/26/MNGK7PFOMS1.DTL. 
  57. ↑ Edgewood Chemical and Biological Center (2007-04-25). "Scientists Identify Pathogens That May Be Causing Global Honeybee Deaths" (PDF). Press release. http://www.ecbc.army.mil/pr/download/042507_honey_bee_pathogens.pdf. 
  58. ↑ Jia-Rui Chong and Thomas H. Maugh II (2007-04-26). "Experts may have found what's bugging the bees". Los Angeles Times. http://www.latimes.com/news/science/la-sci-bees26apr26,0,896792.story?coll=la-home-headlines. 
  59. ↑ Seth Borenstein (2007-05-02). "Honeybee Die-Off Threatens Food Supply, The Associated Press (5/2/2007)". Associated Press. Archived from the original on 2007-05-05. http://web.archive.org/web/20070505110220/http://news.yahoo.com/s/ap/20070502/ap_on_sc/honeybee_die_off. Retrieved 2007-05-07. 
  60. ↑ Paul Boring (2007-04-25). "Whidbey hives collapse". Whidbey News-Times. http://www.whidbeynewstimes.com/portals-code/list.cgi?paper=84&cat=23&id=970700&more. 
  61. ↑ Chapon, L., M.D. Ellis, and A.L. Szalanski. 2009. Nosema and tracheal mites in the north central region – 2008 survey. Proceedings of the American Bee Research Conference. American Bee Journal 149: 585-586.
  62. ↑ "Population genetics and distribution of ''N. ceranae'' in the United States, University of Arkansas Insect Genetics Lab". Comp.uark.edu. http://comp.uark.edu/~aszalan/Apis/Nosema_ceranae_&_N_apis.html. Retrieved 2010-06-22. 
  63. ↑ Szalanski, A.L., J. Whitaker, and P. Cappy. 2010. Molecular diagnostics of Nosema ceranae and N. apis from honey bees in New York. Proceedings of the American Bee Research Conference. American Bee Journal 150: 508
  64. ↑ David Hackenberg (former president of the American Beekeeping Federation)) (2007-03-14). ""Letter from David Hackenberg to American growers from March 14, 2007"" (DOC). Plattform Imkerinnen — Austria. Archived from the original on 2007-06-04. http://web.archive.org/web/20070604214622/http://www.imkerinnen.at/Hauptseite/Menues/News/Brief+David+Hackenberg+307+engl.doc. Retrieved 2007-03-27. 
  65. ↑ Matt Wells (2007-03-11). "Vanishing bees threaten US crops". www.bbc.co.uk (BBC News). http://news.bbc.co.uk/2/hi/americas/6438373.stm. Retrieved 2007-03-12. 
  66. ↑ Philipp Mimkes (2003-02). "Französische Regierung verlängert Teilverbot von Gaucho - Bienensterben jetzt auch in Deutschland" (in German). CGB Network. http://www.cbgnetwork.org/Ubersicht/Zeitschrift_SWB/SWB_2003/SWB_02_2003/Gaucho_02_03/gaucho_02_03.html. 
  67. ↑ Sven Preger (2003-11-23). "Verstummtes Summen - Französische Forscher: Insektizid ist Grund für Bienensterben" (in German). CGB Network. http://www.cbgnetwork.org/536.html. 
  68. ↑ "Betrayed and sold out–German bee monitoring- Walter Haefeker, Deutscher Berufs- und Erwerbsimkerbund". 2000-08-12. http://www.beekeeping.com/articles/us/german_bee_monitoring.htm. Retrieved 2007-04-26. 
  69. ↑ "Schadet Imidacloprid den Bienen - von Eric Zeissloff" (in German). 2001. http://www.beekeeping.com/artikel/imidacloprid_1.htm. Retrieved 2007-04-26. 
  70. ↑ "Gaucho – ein Risiko, Studie: Mitschuld des Bayer-Pestizids für Bienensterben (Neues Deutschland)" (in German). 2003-11-23. http://www.beekeeping.com/artikel/gaucho_ein_risiko.htm. Retrieved 2007-04-26. 
  71. ↑ "Imidaclopride utilisé en enrobage de semences (Gaucho) et troubles des abeilles - Rapport final - 18 septembre 2003" (in French) (PDF). 2003-09-18. http://www.agriculture.gouv.fr/spip/IMG/pdf/rapportfin.pdf. Retrieved 2007-04-26. 
  72. ↑ "France: Governmental report claims BAYER's pesticide GAUCHO responsible for bee-deaths Coalition against Bayer-Dangers is calling for a ban". 2003-12. http://www.cbgnetwork.org/355.html. Retrieved 2007-04-26. 
  73. ↑ "Millions of bees dead - Bayer's Gaucho blamed". 2003-11-26. http://www.newmediaexplorer.org/sepp/2003/11/26/millions_of_bees_dead_bayers_gaucho_blamed.htm. Retrieved 2007-04-26. 
  74. ↑ "Alarm Sounds on Bee-Killing Pesticides (by Julio Godoy)". 2004. http://www.tierramerica.net/2004/0313/iacentos.shtml. Retrieved 2007-05-06. 
  75. ↑ Maria Mancilla, Les abeilles sont-elles en train de disparaître?, Rue 89, 29 August 2007 (French).
  76. ↑ "EFSA Scientific Report (2006) 65, 1-110, Conclusion regarding the peer review of the pesticide risk assessment of the active substance fipronil" (PDF). 2006-03-03. http://www.efsa.europa.eu/etc/medialib/efsa/science/praper/conclusions/1470.Par.0002.File.dat/praper_concl_sr65_fipronil_summary_en_rev12.pdf. Retrieved 2007-04-26. 
  77. ↑ RE-REGULATION OF PESTICIDES PBS
  78. ↑ State notes small increase in pesticide use Western Farm Press
  79. ↑ Pesticide Use Reporting California Department of Pesticide Regulation
  80. ↑ Schacker, Michael. A Spring Without Bees. Guilford, CT: The Lyons, 2008. Print.
  81. ↑ Bonmatin JM, Marchand PA, Charvet R, Moineau I, Bengsch ER and Colin ME (2005-06-29). "Quantification of imidacloprid uptake in maize crops". J Agric Food Chem. 53 (13): 5336–41. doi:10.1021/jf0479362. 
  82. ↑ Rortaisa A, Arnolda G, Halmbm M and Touffet-Briensb F. (2005). "Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees". Apidologie 36: 71–83. doi:10.1051/apido:2004071. 
  83. ↑ Bortolotti L, Monanari R, Marcelino J and Porrini P. (2003). "Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees". Bulletin of Insectology 56 (1): 63–67. 
  84. ↑ Medrzycki P, Monntanari L, Bortolotti L, Sabatinin S and Maini S.. "Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests". Bulletin of Insectology 56 (1): 59–62. 
  85. ↑ Thompson H. (2003). "Behavior effects of pesticides in bees-their potential for use in risk assessment". Ecotoxicology 12: 317–30. doi:10.1023/A:1022575315413. 
  86. ↑ "Colony Collapse Disorder linked to Fipronil". http://revistagloborural.globo.com/GloboRural/0,6993,EEC1707683-5809,00.html. Retrieved 2010-06-17. 
  87. ↑ "No acute mortalities in honey bee colonies (Apis mellifera) after the exposure to sunflower cultures". http://popups.ulg.ac.be/NFG/document.php?id=1258. Retrieved 2010-06-27. 
  88. ↑ Paula Sackmann, Mauricio Rabinovich, Juan Carlos Corley (25 September 2000). "Successful Removal of German Yellowjackets (Hymenoptera: Vespidae) by Toxic Baiting". J. Econ. Entomol. 94(4): 811Ð816 (2001) (Laboratorio de Ecologõ´a de Insectos, Grupo Forestal, EEA INTA Bariloche CC 277, Bariloche, Rõ´o Negro, Argentina). http://www.inta.gov.ar/bariloche/ssd/nqn/ecologiadeinsectos/pdfs/Sackmann%20et%20al%202001.pdf. Retrieved 2010-06-22. 
  89. ↑ ""Status of Pollinators in North America — Committee on the Status of Pollinators in North America — The National Academies Press Washington, D.C. www.nap.edu; page 81". 2006. http://books.nap.edu/openbook.php?record_id=11761&page=81. Retrieved 2007-04-27. "the small literature on this topic, ... in some cases, there are negative but sublethal effects attributable to consumption of transgenic pollens. .... 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." 
  90. ↑ ""Mid-Atlantic Apiculture Research and Extension Consortium"". 2007-03-28. http://maarec.cas.psu.edu/. Retrieved 2007-03-29. "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"" 
  91. ↑ ""Summary Of Research on the Non-Target Effects of Bt Corn Pollen on Honeybees" — Department of Entomology, University of Maryland" (PDF). 2007-03-28. http://maarec.cas.psu.edu/CCDPpt/NontargeteffectsofBt.pdf. Retrieved 2007-03-29. 
  92. ↑ Berenbaum, Prof. May R. (2007-03-29). "Colony Collapse Disorder and Pollinator Decline". Presentation to Subcommittee on Horticulture and Organic Agriculture, U.S. House of Representatives. The National Academies. http://www7.nationalacademies.org/ocga/testimony/Colony_Collapse_Disorder_and_Pollinator_Decline.asp. Retrieved 2007-10-22. , specifically, "Close to 100 crop species in the U.S. rely to some degree on pollination services provided by this one species—collectively, these crops make up approximately 1/3 of the U.S. diet [...] Although economists differ in calculating the exact dollar value of honey bee pollination to American agriculture, virtually all estimates are in the range of billions of dollars".
  93. ↑ Alexi Barrionuevo (2007-02-27). "Honeybees, Gone With the Wind, Leave Crops and Keepers in Peril". New York Times. http://select.nytimes.com/gst/abstract.html?res=F10B1FF8355A0C748EDDAB0894DF404482. 
  94. ↑ Hannah Nordhaus (2007-03-19). "The Silence of the Bees". High Country News. Archived from the original on 2007-09-28. http://web.archive.org/web/20070928040457/http://www.hcn.org/servlets/hcn.Article?article_id=16891&gclid=CIG7z7e2oIwCFSG9SgodQ3MG2w. 
  95. ↑ Kevin Berger (2007-04-06). "Where have all the bees gone? Blame people, not cell phones". Seattlepi.com. http://seattlepi.nwsource.com/opinion/322781_focusbees08.html. 
  96. ↑ Flight, orientation, and homing abilities of honeybees following exposure to 2.45-GHz CW microwaves Bioelectromagnetics Volume 2 Issue 1, Pages 71 - 75
  97. ↑ Stever, H. J., Kuhn, (2004) (PDF). How Electromagnetic Exposure can influence Learning Process - Modelling Effects of Electromagnetic Exposure on Learning Processes. http://www.bienenarchiv.de/forschung/2004_lernprozesse/Electromagnetic%20Exposure_Learning%20Processes.doc.pdf. 
  98. ↑ Harst, W., Kuhn, J., Stever, H. (2006). "Can Electromagnetic Exposure Cause a Change in Behaviour? Studying Possible Non-Thermal Influences on Honey Bees – An Approach within the Framework of Educational Informatics". Acta Systemica 6 (1): 1–6. http://agbi.uni-landau.de/material_download/IAAS_2006.pdf. 
  99. ↑ Are mobile phones wiping out our bees? The Independent.
  100. ↑ Eric Sylvers (2007-04-22). "Wireless: Case of the disappearing bees creates a buzz about cellphones". International Herald Tribune. http://www.iht.com/articles/2007/04/22/news/wireless23.php. 
  101. ↑ Chloe Johnson (2007-04-22). "Researchers: Often-cited study doesn't relate to bee colony collapse". Foster's Online. http://www.fosters.com/apps/pbcs.dll/article?AID=/20070422/FOSTERS01/104220119/0/CITIZEN. 
  102. ↑ "Cellphone researchers claim data misinterpreted". ColonyCollapse.org. http://colonycollapse.org/content/view/23/33/. 
  103. ↑ Ved Parkash Sharma, Neelima R. Kumar (25 May 2010). "Changes in honeybee behaviour and biology under the influence of cellphone radiations". Current Science 98 (no. 10). http://www.ias.ac.in/currsci/25may2010/1376.pdf. Retrieved 2010-06-22. 
  104. ↑ Douglas, Ian (2010-06-01). "Mobile phones and bees: shoddy research helps no one – Telegraph Blogs". Blogs.telegraph.co.uk. http://blogs.telegraph.co.uk/technology/iandouglas/100005223/mobile-phones-and-bees-shoddy-research-helps-no-one/. Retrieved 2010-06-22. 
  105. ↑ Measurement of the threshold sensitivity of honeybees to weak, extremely low-frequency magnetic fields J Kirschvink, S Padmanabha, C Boyce and J Oglesby Journal of Experimental Biology, Vol 200, Issue 9 1363-1368 1997
  106. ↑ National Bee Database to be set up to monitor colony collapse from Telegraph.com. Retrieved 10 March 2009.
  107. ↑ Morse, R.A.; Calderone, N.W., The Value of Honey Bees as Pollinators of US Crops in 2000. Cornell University (2000)
  108. ↑ Tepedino, V. J. (1981) The pollination efficiency of the squash bee (Peponapis pruinosa) and the honey bee (Apis mellifera) on summer squash (Cucurbita pepo). Journal of the Kansas Entomological Society, 54:359–377
  109. ↑ Partap, Uma Partap and Tej. Pollination of apples in China. 2 September 2005
  110. ↑ "Establishing a healthy population of native bees on your land". Conservationinformation.org. http://www.conservationinformation.org/partners/090107/rnt2.asp. Retrieved 2010-06-22. 
  111. ↑ Previous post Next post. "Use of native bees to counter colony collapse disorder". Wired.com. http://www.wired.com/wiredscience/2009/06/beecounting/. Retrieved 2010-06-22. 
  112. ↑ Russians Saving U.S. from Colony Collapse Disorder, The Daily Green, April 14, 2009.
  113. ↑ http://www.dailyexpress.co.uk/posts/view/195322/Briton-sends-bee-world-abuzz-with-cure-for-killer-bug/
  114. ↑ http://www.metro.co.uk/news/838981-british-beekeepers-parasite-resistant-bee-could-save-the-world
  115. ↑ http://www.fastcompany.com/1684629/a-for-british-beekeeper-as-he-develops-mite-resistant-strain-of-honeybee
  116. ↑ http://www.treehugger.com/files/2010/08/new-honeybee-breed-key-to-combating-colony-collapse-disorder.php
  117. ↑ USA (2010-06-01). "Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra- and inter-species recombination". Ncbi.nlm.nih.gov. http://www.ncbi.nlm.nih.gov/pubmed/18024913/. Retrieved 2010-06-22. 
  118. ↑ USA (2010-06-01). "IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion". Ncbi.nlm.nih.gov. http://www.ncbi.nlm.nih.gov/pubmed/19196347/. Retrieved 2010-06-22. 
  119. ↑ "2009 documentary ''Vanishing of the Bees''". Vanishingbees.co.uk. http://vanishingbees.co.uk/. Retrieved 2010-06-22. 
  120. ↑ The Silence of Bees (2008)

Further reading

External links