Colony collapse disorder

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Colony collapse disorder (or CCD) is a phenomenon in which worker bees from a beehive or Western 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.[1] Aside from fundamental concerns about the survival of bee species, colony collapse is significant because many agricultural crops worldwide are pollinated by bees.

Honey bees entering a beehive.

European beekeepers observed similar phenomena 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 are not yet fully understood, although many authorities attribute the problem to biotic factors such as Varroa mites and insect diseases (i.e., pathogens[5] including Nosema apis and Israel acute paralysis virus[6][7]). Other proposed causes include environmental change-related stresses,[8] malnutrition and pesticides (e.g. neonicotinoids such as imidacloprid), and migratory beekeeping. More speculative possibilities have included both cell phone radiation and genetically modified (GM) crops with pest control characteristics,[9][10] though experts point out 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. [11] [12]


[edit] Background

From 1971 to 2006, there was a dramatic reduction in the number of feral honeybees in the US (now almost absent);[13] 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,[5][14] 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).[15] 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.[16]

[edit] Symptoms

A colony which has collapsed from CCD is generally characterized by all of these conditions occurring simultaneously[17]:

  • 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:
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
  • The colony members are reluctant to consume provided feed, such as sugar syrup and protein supplement.

[edit] Scale of the disorder

In the U.S., at least 24 different states[8][18] as well as portions of Canada[19] 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.[20] 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).[20] In the US, 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%.[20]In the winter of 2008 a survey by the US Department of Agriculture/Agricultural Research Services (USDA-ARS) and Apiary inspectors showed that 36% of America's 2.4 million hives were lost to CCD. The survey covered almost 20% of America's 1,500 commercial beekeepers, and suggested an increase of 11% over the losses of 2007, and 40% over the losses of 2006. [21]

There are also putative cases reported by the media from India, Brazil[22] and parts of Europe.[23] 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 United Kingdom (where it has been dubbed the "Mary Celeste" phenomenon, after a ship whose crew disappeared in 1872[24]) 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.[25]

[edit] 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.[7] 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 prestigious team of US scientists and researchers that found a significant connection between IAPV and CCD in honeybees. [26] 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.[16]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.[20] A scholarly review in June 2007, similarly addressed numerous theories and possible contributing factors, but left the issue unresolved.[15]

In July 2007, the USDA released its "CCD Action Plan", which outlines a strategy for addressing CCD consisting of four main components:[27]

  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]

[edit] 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.[16] 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.[20]

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.

[edit] Pathogens and immunodeficiency theories

[edit] 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,[28] 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.[29] This research group is reported to be focusing on a search for possible viral, bacterial, or fungal pathogens which may be involved.[16]

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.[7]

[edit] 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.[29] 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.[30]

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.[7] 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.[6]

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.[7]

The virus was also found in samples of Australian honey bees. Australian honey bees have been imported into the U.S. since 2004[6] 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.[31][32]

[edit] 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.[16]

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.[33] 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.[34][35] Various areas in Europe have reported this fungus, but no direct link to CCD has yet been established.[36][37] Highly preliminary evidence of N. ceranae was recently reported in a few hives in the Merced Valley area of California (USA).[38][39] 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."[40] 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."[41] Likewise, a Washington State beekeeper familiar with N. ceranae in his own hives discounts it as being the cause of CCD.[42] A study reported in September 2007 found that 100% of afflicted and 80% of non-afflicted colonies contained Nosema ceranae.[7]

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.[43]

[edit] 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;[44][45] 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;[46] for example, the effects of imidacloprid on termites include apparent failure of the immune system, and disorientation.[47] In Europe the interaction of the phenomenon of "dying bees" with imidacloprid, has been discussed for quite some time now.[48][49][50] 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.[51][52][53] 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.[54] 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.[35] 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."[55]

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.[56] 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.[57] Sub-lethal doses of imidacloprid in sucrose solution have also been documented to affect homing and foraging activity of honeybees.[58] Imidacloprid in sucrose solution fed to bees in the laboratory impaired their communication for a few hours.[59] Sub-lethal doses of imidacloprid in laboratory and field experiment decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired.[60] 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.

[edit] 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[16] 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.[15] 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.[61]

[edit] Genetically modified crops (GMO)

Some genetically modified (GM) crops produce the natural insecticide Bacillus thuringiensis (Bt), which was hypothesised to affect bees. No experiments have found evidence of any negative effect whatsoever on honey bee populations,[62] and while research on GM crops is still ongoing, new results continue to suggest that GM crops have no negative effect on bee populations.[5][63] Further, CCD cases are known in areas of Europe and Canada where Bt crops are not grown.[64]

[edit] Bee rentals and migratory beekeeping

Moving spring bees from South Carolina to Maine for blueberry pollination

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.[65] 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.[66]

[edit] 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.[67]

[edit] 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."[68]

[edit] Electromagnetic radiation

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.[69] 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".[70][71][72]

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.[73] 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.[74]

Like the links to CCD from variants (herbicides, genetically modified crops, etc), the link of either cordless or cellular phones, cell towers, wifi, interference by the High Frequency Active Auroral Research Program (HAARP) or Ground Wave Emergency Network (GWEN) to CCD is speculative.

[edit] 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.[75] In particular, the register, funded by the Department for the Environment, 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.

[edit] 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 $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.[76]

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 saturation pollination for what they lack in efficiency. The commercial viability of these crops is therefore strongly tied to the beekeeping industry.

[edit] Remedies

As of March 1, 2007 MAAREC offers the following tentative recommendations for beekeepers noticing the symptoms of CCD:[43]

  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.

[edit] See also

[edit] References

  1. ^ a b "Honey Bee Die-Off Alarms Beekeepers, Crop Growers and Researchers". Penn State University College of Agricultural Sciences. 2007-01-29. 
  2. ^ a b Gaëlle Dupont, Les abeilles malades de l'homme, Le Monde, 29 August 2007 (French)
  3. ^ a b "Das spurlose Sterben" (in German). 2007-03-12.,ra13l5/wissen/artikel/352/105247/. 
  4. ^ a b c Paul Molga, La mort des abeilles met la planète en danger, Les Echos, 20 August 2007 (French)
  5. ^ a b c "Colony Collapse Disorder Working Group". 
  6. ^ a b c "Virus Is Seen as Suspect in Death of Honeybees". The New York Times. 2007-09-07. Retrieved on 2007-09-07. 
  7. ^ a b c d e f "Mysterious Honeybee Disappearance Linked to Rare Virus". Science News (Scientific American). 2007-09-07. Retrieved on 2007-09-07. 
  8. ^ a b "The mysterious deaths of the honeybees". CNN Money. 2007-03-29. Retrieved on 2007-04-04. 
  9. ^ ""GE and bee Colony Collapse Disorder -- science needed!"". 2005-03-21. Retrieved on 2007-03-23. 
  10. ^ "Collapsing Colonies: Are GM Crops Killing Bees? - International - SPIEGEL ONLINE - News". 2007-03-22.,1518,473166,00.html. Retrieved on 2008-02-24. 
  11. ^ Honeybees under attack on all fronts
  12. ^ 'No proof' of bee killer theory
  13. ^ "Pollination worries rise as honey bees decline.". Science, vol. 265. 1994-08-26. p. 1170. 
  14. ^ Benjamin Lester (2007-03-07). "Mystery of the dying bees". Cosmos Online. 
  15. ^ a b c [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.
  16. ^ a b c d e f "Colony Collapse Disorder Preliminary Report". Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC) - CCD Working Group. 2006-01-05. pp. pp. 22. Retrieved on 2007-04-24. 
  17. ^ "Discussion of phenomenon of Colony disorder collapse". Canadian Honey Council. 2007-01-27. 
  18. ^ [2] Map of affected states within the US
  19. ^ Strange times for bees, The Vancouver,
  20. ^ a b c d e 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
  21. ^ [3]
  22. ^ "Mysterious Honeybee Killer Could Make Meals Bland". CBS 11/AP. 2007-05-08. Retrieved on 2007-12-31. 
  23. ^ Are mobile phones wiping out our bees?
  24. ^ BBC Wild bee decline 'catastrophic' 23 April 2008
  25. ^ n-tv: Immer weniger Imker - Deutschen Bienen geht es gut. Version of May 11, 2007.
  26. ^ [4]
  27. ^ ""Colony Collapse Disorder Action Plan"" (PDF). USDA. 2007-06-20. 
  28. ^ "Fruit Times Colony Collapse Disorder". Penn State University 26 (1). 2007-01-23. Fruit Times. 
  29. ^ a b "Bee Mites Suppress Bee Immunity, Open Door For Viruses And Bacteria". 
  30. ^ Dr. Jamie Ellis (2007-04-16). "Colony Collapse Disorder (CCD) in Honey Bees". University of Florida. 
  31. ^ Kim Kaplan (2007-11-19). "Imported Bees Not Source of Virus Associated with Colony Collapse Disorder)". USDA. Retrieved on 2007-11-29. 
  32. ^ [Originally published in Science Express on 6 September 2007 Science 12 October 2007: Vol. 318. no. 5848, pp. 283 - 287 DOI: 10.1126/science.1146498]
  33. ^ Higes, M., R. Martin, A. Meana (2006). "Nosema ceranae, a new microsporidian parasite in honeybees in Europe". Journal of Invertebrate Pathology 92: pp. 93–95. doi:10.1016/j.jip.2006.02.005. 
  34. ^ Asian Parasite Killing Western Bees - Scientist, Planet Ark, SPAIN: July 19, 2007
  35. ^ a b Maria Mancilla, Les abeilles sont-elles en train de disparaître?, Rue 89, 29 August 2007 (French)
  36. ^ Dr Wolfgang Ritter. "Nosema ceranae - Asiatischer Nosema-Erreger festgestellt – neu verbreitet oder erst jetzt entdeckt?" (in German). Albert-Ludwigs-Universität Freiburg. 
  37. ^ 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. 
  38. ^ Sabin Russell (2007-04-26). "UCSF scientist tracks down suspect in honeybee deaths". San Francisco Chronicle. 
  39. ^ "Scientists Identify Pathogens That May Be Causing Global Honeybee Deaths". PR Newswire. 2007-04-25. 
  40. ^ Jia-Rui Chong and Thomas H. Maugh II (2007-04-26). "Experts may have found what's bugging the bees". Los Angeles Times.,0,896792.story?coll=la-home-headlines. 
  41. ^ Seth Borenstein (2007-05-02). "Honeybee Die-Off Threatens Food Supply, The Associated Press (5/2/2007)". The Associated Press. Retrieved on 2007-05-07. 
  42. ^ Paul Boring (2007-04-25). "Whidbey hives collapse". Whidbey News-Times. 
  43. ^ a b Dennis vanEngelsdorp, M.Frazier, and D. Caron (2007-03-01). "Tentative Recommendations for Hives Experiencing CCD" (PDF). Mid-Atlantic Apiculture Research and Extension Consortium. 
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  45. ^ Matt Wells (2007-03-11). "Vanishing bees threaten US crops". (BBC News). Retrieved on 2007-03-12. 
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