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Honey bees at a hive entrance: One is about to land and the other is fanning.
Colony collapse disorder (
CCD) is a phenomenon in which worker bees from a
European honey bee colony abruptly disappear. While such disappearances have occurred throughout the history of
apiculture,
and were known by various names (disappearing disease, spring dwindle,
May disease, autumn collapse, and fall dwindle disease),
[1] the syndrome was renamed colony collapse disorder in late 2006
[2] in conjunction with a drastic rise in the number of disappearances of western
honeybee colonies in North America.
[3] European beekeepers observed similar phenomena in Belgium, France, the Netherlands, Greece, Italy, Portugal, and Spain,
[4] and initial reports have also come in from Switzerland and Germany, albeit to a lesser degree
[5] while the
Northern Ireland Assembly received reports of a decline greater than 50%.
[6]
Colony collapse disorder is significant economically because
many agricultural crops worldwide are
pollinated
by European honey bees. According to the Agriculture and Consumer
Protection Department of the Food and Agriculture Organization of the
United Nations, the worth of global crops with honeybee’s pollination
was estimated to be close to $200 billion in 2005.
[7] Shortages of bees in the US have increased the cost to farmers renting them for pollination services by up to 20%.
[8]
The mechanisms of CCD and the reasons for its increasing prevalence
remain unclear, but many possible causes have been proposed:
pesticides, primarily
neonicotinoids; infections with
Varroa and
Acarapis mites;
malnutrition; various
pathogens;
genetic factors;
immunodeficiencies;
loss of habitat; changing
beekeeping practices; or a combination of factors.
[9]
History
Limited occurrences resembling CCD have been documented as early as 1869
[10][11]
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).
[1] 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. The cause of the appearance of this
syndrome
has never been determined. 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.
[12]
A well-documented outbreak of colony losses spread from the Isle of
Wight to the rest of the UK in 1906. These losses later were attributed
to a combination of factors, including adverse weather, intensive
apiculture leading to inadequate forage, and a new infection, the
chronic bee paralysis virus,
[13] but at the time, the cause of this agricultural beekeeping problem was similarly mysterious and unknown.
Reports show this behavior in hives in the US in 1918
[14] and 1919.
[15] Coined "mystery disease" by some,
[16] it eventually became more widely known as "disappearing disease".
[17] Oertel, in 1965,
[18]
reported that hives afflicted with disappearing disease in Louisiana
had plenty of honey in the combs, although few or no bees were present,
discrediting reports that attributed the disappearances to lack of food.
From 1972 to 2006, dramatic reductions continued in the number of
feral honey bees in the U.S.
[19]
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, in late 2006 and early
2007, the rate of attrition was alleged to have reached new proportions,
and the term "colony collapse disorder" began to be used to describe
this sudden rash of disappearances (sometimes referred to as
"spontaneous hive collapse" or the "
Mary Celeste syndrome" in the United Kingdom).
[3][20]
Losses had remained stable since the 1990s at 17%–20% per year
attributable to a variety of factors, such as mites, diseases, and
management stress.
[21]
The first report of CCD was in mid-November 2006 by a Pennsylvania
beekeeper overwintering in Florida. By February 2007, large commercial
migratory beekeepers in several states had reported heavy losses
associated with CCD. Their reports of losses varied widely, ranging from
30% to 90% of their bee colonies; in some cases, beekeepers reported
losses of nearly all of their colonies with surviving colonies so
weakened that they might no longer be viable to pollinate or produce
honey.
[22]
Losses were reported in migratory operations wintering in California,
Florida, Oklahoma, and Texas. In late February, some larger
nonmigratory beekeepers in the mid-Atlantic and Pacific Northwest
regions also reported significant losses of more than 50%.
[citation needed]
Colony losses also were reported in five Canadian provinces, several
European countries, and countries in South and Central America and Asia.
In 2010, the
USDA
reported that data on overall honey bee losses for 2010 indicated an
estimated 34% loss, which is statistically similar to losses reported in
2007, 2008, and 2009.
[22]
After bee populations dropped 23% in the winter of 2013, the
Environmental Protection Agency and Department of Agriculture formed a
task force to address the issue.
[23]
Signs and symptoms
In collapsed colonies, CCD is suspected when a complete absence of
adult bees is found in colonies, with no or little buildup of dead bees
in the hive or in front of the hive. A colony which has collapsed from
CCD is generally characterized by all of these conditions occurring
simultaneously:
[24]
- Presence of capped brood in abandoned colonies: Bees normally will not abandon a hive until the capped brood have all hatched.
- Presence of food stores, both honey and bee pollen:
- Presence of the queen bee: If the queen is not present, the hive died because it was queenless, which is not considered CCD.
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 colony members are reluctant to consume provided feed, such as sugar syrup and protein supplement.
Scope and distribution
North America
The National Agriculture Statistics Service reported 2.44 million
honey-producing hives were in the United States in February 2008, down
from 4.5 million in 1980, and 5.9 million in 1947, though these numbers
underestimate the total number of managed hives, as they exclude several
thousand hives managed for pollination contracts only, and also do not
include hives managed by beekeepers owning fewer than five hives. This
under-representation may be offset by the practice of counting some
hives more than once; hives that are moved to different states to
produce honey are counted in each state's total and summed in total
counts.
[25]
Non-CCD winter losses as high as 50% have occurred in some years and regions (e.g., 2000–2001 in
Pennsylvania).
Normal winter losses are typically considered to be in the range of
15–25%. In many cases, beekeepers reporting significant losses of bees
did not experience true CCD, but losses due to other causes.
In 2007 in the US, at least 24 different states,
[26] as well as portions of Canada, had reported at least one case of CCD.
[27]
In a 2007 survey of 384 responding beekeepers from 13 states, 23.8% met
the specified criterion 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).
[27]
In the US in 2006–2007, 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.
[25][27]
A 2007–2008 survey of over 19% of all colonies revealed a total loss
of 35.8%. Operations that pollinated almonds lost, on average, the same
number of colonies as those that did not. The 37.9% of operations that
reported having at least some of their colonies die with a complete lack
of bees had a total loss of 40.8% of colonies compared to the 17.1%
loss reported by beekeepers without this symptom. Large operations were
more likely to have this symptom, suggesting a contagious condition may
be a causal factor. About 60% of all colonies that were reported dead in
this survey died without the presence of dead bees in the hive, thus
possibly suffered from CCD.
[25]
In 2010, the USDA reported that data on overall honey bee losses for
the year indicate an estimated 34% loss, which is statistically similar
to losses reported in 2007, 2008, and 2009.
[22] In 2011, the loss was 30%.
[28]
In 2012–2013, CCD was blamed for the loss of about half of the US
honeybee hives, far more than the 33% losses observed on average over
previous years.
Europe
According to the European Food Safety Authority (EFSA), in 2007, the
United Kingdom had 274,000 hives, Italy had 1,091,630, and France
1,283,810. In 2008, the
British Beekeepers Association
reported the bee population in the United Kingdom dropped by around 30%
between 2007 and 2008, and an EFSA study revealed that in Italy the
mortality rate was 40–50%. However, EFSA officials point out the figures
are not very reliable because before the bees started dying, no
harmonisation was used in the way different countries collected
statistics on their bee populations. At that time (2008), the reports
blamed the high death rate on the varroa mite, two seasons of unusually
wet European summers, and some pesticides.
[29]
In 2010, David Aston of the British Beekeepers’ Association stated,
"We still do not believe CCD (which is now better defined) is a cause of
colony losses in the UK, however we are continuing to experience colony
losses, many if not most of which can be explained". He feels recent
studies suggest "further evidence to the evolving picture that there are
complex interactions taking place between a number of factors,
pathogens, environmental, beekeeping practices and other stressors,
which are causing honey bee losses described as CCD in the US".
[30]
In 2009, Tim Lovett, president of the British Beekeepers'
Association, said: "Anecdotally, it is hugely variable. There are
reports of some beekeepers losing almost a third of their hives and
others losing none. John Chapple, chairman of the London Beekeepers'
Association, put losses among his 150 members at between a fifth and a
quarter. "There are still a lot of mysterious disappearances; we are no
nearer to knowing what is causing them." The government's National Bee
Unit continued to deny the existence of CCD in Britain; it attributes
the heavy losses to the varroa mite and rainy summers that stop bees
foraging for food.
[31]
Beekeepers in Scotland also reported losses for the past three years.
Andrew Scarlett, a Perthshire-based bee farmer and honey packer, lost
80% of his 1,200 hives during the 2009 winter. He attributed the losses
to a virulent bacterial infection that quickly spread because of a lack
of bee inspectors, coupled with sustained poor weather that prevented
honeybees from building up sufficient pollen and nectar stores.
[31]
In Germany, 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,
[32]
there was no scientific confirmation; in early May 2007, the German
media reported no confirmed CCD cases seemed to have occurred in
Germany.
[33][34]
At the end of May 2012, the Swiss government reported about half of
the bee population had not survived the winter. The main cause of the
decline was thought to be the parasite
Varroa destructor.
[35]
Possible causes
The mechanisms of CCD are still unknown, but many causes are currently being considered, such as
pesticides,
mites, fungus, beekeeping practices (such as the use of
antibiotics or long-distance transportation of beehives), malnutrition, other
pathogens, and
immunodeficiencies.
The current scientific consensus is that no single factor is causing
CCD, but that some of these factors in combination may lead to CCD
either additively or synergistically.
[36][37][38][39][40][41][42]
In 2006, the
Colony Collapse Disorder Working Group, based primarily at
Pennsylvania State University, was established. Their preliminary report pointed out some patterns, but drew no strong conclusions.
[2]
A survey of beekeepers early in 2007 indicated most hobbyist beekeepers
believed that starvation was the leading cause of death in their
colonies, while commercial beekeepers overwhelmingly believed
invertebrate pests (
Varroa mites, honey bee tracheal mites, and/or small hive beetles) were the leading cause of colony mortality.
[27]
A scholarly review in June 2007 similarly addressed numerous theories
and possible contributing factor, but left the issue unresolved.
[1]
In July 2007, the
United States Department of Agriculture (USDA) released its "CCD Action Plan", which outlined a strategy for addressing CCD consisting of four main components:
[43]
- survey and data collection
- analysis of samples
- hypothesis-driven research
- mitigation and preventive action
In July 2009, the first annual report of the U.S. Colony Collapse Disorder Steering Committee was published.
[44] It suggested CCD may be caused by the interaction of many agents in combination.
[45]
Similarly, in 2009, the CCD Working Group published a comprehensive
descriptive study that concluded: "Of the 61 variables quantified
(including adult bee physiology, pathogen loads, and pesticide levels),
no single factor was found with enough consistency to suggest one causal
agent. Bees in CCD colonies had higher pathogen loads and were
co-infected with more pathogens than control populations, suggesting
either greater pathogen exposure or reduced defenses in CCD bees."
[46]
The second annual Steering Committee report was released in November
2010. The group reported, although many associations, including
pesticides, parasites, and pathogens have been identified throughout the
course of research, "it is becoming increasingly clear that no single
factor alone is responsible for [CCD]". Their findings indicated an
absence of damaging levels of the parasite
Nosema or parasitic
Varroa mites at the time of collapse.
[22]
They did find an association of sublethal effects of some pesticides
with CCD, including two common miticides in particular, coumaphos and
fluvalinate, which are pesticides registered for use by beekeepers to
control varroa mites. Studies also identified sublethal effects of
neonicotinoids and fungicides, pesticides that may impair the bees'
immune systems and may leave them more susceptible to bee viruses.
[22][47][48]
Pesticides
According to the USDA, pesticides may be contributing to CCD.
[49]
A 2013 peer-reviewed literature review concluded neonicotinoids in the
amounts typically used harm bees and safer alternatives are urgently
needed.
[50]
At the same time, other sources suggest the evidence is not conclusive,
and that clarity regarding the facts is hampered by the role played by
various issue advocates and lobby groups.
[51]
Scientists have long been concerned that pesticides and possibly some
fungicides
may have sublethal effects on bees, not killing them outright, but
instead impairing their development and behavior. Of special interest is
the class of insecticides called
neonicotinoids, which contain the active ingredient
imidacloprid, and similar other chemicals, such as
clothianidin and
thiamethoxam.
Honey bees may be affected by such chemicals when they are used as a
seed treatment because they are known to work their way through the
plant up into the flowers and leave residues in the nectar. The doses
taken up by bees are not lethal, but possible chronic problems could be
caused by long-term exposure.
[21] Most corn grown in the US is treated with neonicoticoids, and a 2012 study found high levels of clothianidin in
pneumatic
planter exhaust. In the study, the insecticide was present in the soil
of unplanted fields near those planted with corn and on dandelions
growing near those fields.
[52] Another 2012 study also found clothianidin and imidacloprid in the exhaust of pneumatic seeding equipment.
A 2010 survey reported 98 pesticides and metabolites detected in
aggregate concentrations up to 214 ppm in bee pollen; this figure
represents over half of the individual pesticide incidences ever
reported for apiaries. It was suggested that "while exposure to many of
these neurotoxicants elicits acute and sublethal reductions in honey bee
fitness, the effects of these materials in combinations and their
direct association with CCD or declining bee health remains to be
determined."
[53]
Evaluating pesticide contributions to CCD is particularly difficult
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 a delay may occur
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
by the pollen stores rather than 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, if
contaminants or toxins from the environment 'are' responsible, it is
most likely to be via the honey, as the adults are dying (or leaving),
not the brood (though possibly effects of contaminated pollen consumed
by juveniles may only show after they have developed into adults).
To date, most of the evaluation of possible roles of pesticides in
CCD have relied on the use of surveys submitted by beekeepers, but
direct testing of samples from affected colonies seems likely to be
needed, 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;
[54] for example, the effects of imidacloprid on
termites include apparent failure of the immune system, and disorientation.
[55]
In Europe, the interaction of the phenomenon of "dying bees" with imidacloprid has been discussed for quite some time.
[56][57][58]
A study from the "Comité Scientifique et Technique (CST)" was at the
center of discussion, and led to a partial ban of imidacloprid in
France. The imidacloprid pesticide Gaucho was banned in 1999 by the
French Minister of Agriculture Jean Glavany, primarily due to concern over potential effects on honey bees.
[59][60][61] Subsequently, 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.
[62]
In February 2007, about 40 French deputies, led by
Jacques Remiller of the
UMP,
requested the creation of a parliamentary investigation commission on
overmortality of bees, underlining that honey production had decreased
by 1,000 tons a year for a decade. By August 2007, no investigation had
opened.
[63]
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".
[64]
Around the same time French beekeepers succeeded in banning neonicotinoids, the
Clinton administration permitted pesticides which were previously banned,
[65] including imidacloprid. In 2004, the
Bush administration reduced regulations further and pesticide applications increased.
[66][67]
In 2005, a team of scientists led by the National Institute of
Beekeeping in Bologna, Italy, found pollen obtained from seeds dressed
with imidacloprid contain significant levels of the insecticide, and
suggested the polluted pollen might cause honey bee colony death.
[68]
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.
[69]
Sublethal doses of imidacloprid in sucrose solution have also been
documented to affect homing and foraging activity of honey bees.
[70]
Imidacloprid in sucrose solution fed to bees in the laboratory impaired their communication for a few hours.
[71] Sublethal doses of imidacloprid in laboratory and
field experiment decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired.
[72]
Research, in 2008, by scientists from Pennsylvania State University found high levels of the pesticides
fluvalinate and
coumaphos in samples of wax from hives, as well as lower levels of 70 other pesticides.
[46]
These chemicals have been used to try to eradicate varroa mites, a bee
pest that itself has been thought to be a cause of CCD. Researchers from
Washington State University,
under entomology professor Steve Sheppard in 2009, confirmed high
levels of pesticide residue in hive wax and found an association between
it and significantly reduced bee longevity.
[73]
The WSU work also focused on the impact of the
microsporidian pathogen
Nosema ceranae, the build-up of which was high in the majority of the bees tested, even after large doses of the antibiotic
fumagillin.
Penn State's Dr. Maryann Frazier said, "Pesticides alone have not shown
they are the cause of CCD. We believe that it is a combination of a
variety of factors, possibly including mites, viruses and pesticides."
[73]
In 2010,
fipronil
was blamed for the spread of CCD among bees, in a study by the
Minutes-Association for Technical Coordination Fund in France, which
found that even at very low nonlethal doses, this pesticide still
impairs the ability to locate the hive, resulting in large numbers of
foragers lost with every pollen-finding expedition, though no mention
was made regarding any of the other symptoms of CCD;
[74] other studies, however, have shown no acute effect of fipronil on honey bees.
[75] Fipronil is designed to eliminate insects similar to bees, such as yellowjackets (
Vespula germanica)
and many other colonial pests by a process of 'toxic baiting', whereby
one insect returning to the hive spreads the pesticide among the brood.
[76]
A large 2010 survey of healthy and CCD-affected colonies also
revealed elevated levels of pesticides in wax and pollen, but the
amounts of pesticides were similar in both failing and healthy hives.
They also confirmed suspected links between CCD and poor colony health,
inadequate diet, and long-distance transportation. Studies continue to
show very high levels of pathogens in CCD-affected samples and lower
pathogen levels in unaffected samples, consistent with the empirical
observation that healthy honey bee colonies normally fend off pathogens.
These observations have led to the hypothesis that bee declines are
resulting from immune suppression.
[22]
In 2012, researchers announced findings that sublethal exposure to
imidacloprid rendered honey bees significantly more susceptible to
infection by the fungus
Nosema, thereby suggesting a potential link to CCD, given that
Nosema is increasingly considered to contribute to CCD.
[77]
Neonicotinoids may interfere with bees' natural homing abilities,
causing them to become disoriented and preventing them from finding
their way back to the hive.
[78][79][80]
Also, in 2012, researchers in Italy published findings that the
pneumatic drilling machines that plant corn seeds coated with
clothianidin and imidacloprid release large amounts of the pesticide
into the air, causing significant mortality in foraging honey bees.
According to the study, "Experimental results show that the
environmental release of particles containing neonicotinoids can produce
high exposure levels for bees, with lethal effects compatible with
colony losses phenomena observed by beekeepers."
[81]
Commonly used pesticides, such as the imidacloprid, reduce colony
growth and new queen production in experimental exposure matched to
field levels.
[82] Lu
et al. (2012) reported they were able to replicate CCD with imidacloprid.
[83] Another neonicotinoid,
thiamethoxam, causes navigational homing failure of foraging bees, with high mortality.
[84]
A 2012
in situ study provided strong evidence that exposure to sublethal levels of imidacloprid in
high fructose corn syrup
(HFCS) used to feed honey bees when forage is not available causes bees
to exhibit symptoms consistent to CCD 23 weeks after imidacloprid
dosing. The researchers suggested, "the observed delayed mortality in
honey bees caused by imidacloprid in HFCS is a novel and plausible
mechanism for CCD, and should be validated in future studies".
[85][86]
In March 2013, two studies were published showing that neonicotinoids
affect bee long-term and short-term memory, suggesting a cause of
action resulting in failure to return to the hive.
[87][88]
In another study done in 2013, scientists reported that experiments
suggested that exposure to the neonicotinoid pesticides clothianidin and
imidicloprid results in increased levels of a particular protein in
bees that inhibits a key molecule involved in the immune response,
making the insects more susceptible to attack by harmful viruses.
[89] Growth in the use of neonicotinoid pesticides has roughly tracked rising bee deaths.
[8][90]
A 2013 peer reviewed literature review concluded that neonicotinoids in
the amounts that they are typically used harm bees and that safer
alternatives are urgently needed.
[50]
European Food Safety Authority statement
In 2012, several peer-reviewed independent studies were published
showing that neonicotinoids had previously undetected routes of exposure
affecting bees including through dust, pollen, and nectar
[81] and that subnanogram toxicity resulted in failure to return to the hive without immediate lethality,
[91] one primary symptom of CCD.
[77] Research also showed environmental persistence in agricultural irrigation channels and soil.
[92] These reports prompted a formal peer review by the
European Food Safety Authority,
which stated in January 2013 that some neonicotinoids pose an
unacceptably high risk to bees, and identified several data gaps not
previously considered. Their review concluded, "A high acute risk to
honey bees was identified from exposure via dust drift for the seed
treatment uses in maize, oilseed rape and cereals. A high acute risk was
also identified from exposure via residues in nectar and/or pollen."
[93][94] Dave Goulson,
an author of one of the studies which prompted the EFSA review, has
suggested that industry science pertaining to neonicotinoids may have
been deliberately deceptive, and the UK Parliament has asked
manufacturer
Bayer Cropscience to explain discrepancies in evidence they have submitted to an investigation.
[95]
Neonicotinoids banned by European Union
Early in 2013, the European Food Safety Authority issued a
declaration that three specific neonicotinoid pesticides pose an acute
risk to honeybees, and the
European Commission (EC) proposed a two-year ban on them.
[96] David Goulson, who led one of the key 2012 studies at the
University of Stirling,
said the decision "begs the question of what was going on when these
chemicals were first approved." The chemical manufacturer Bayer said it
was "ready to work with" the EC and member states.
[97] In April 2013, the
European Union
voted for a two-year restriction on neonicotinoid insecticides. The ban
will restrict the use of imidacloprid, clothianidin, and thiamethoxam
for use on crops that are attractive to bees. Eight nations voted
against the motion, including the British government, which argued that
the science was incomplete.
[98]
The ban can be seen as an application of the "precautionary principle",
established at the 1992 Rio Conference on the Environment and
Development, which advocates that "lack of full scientific certainty
shall not be used as a reason for postponing cost-effective measures to
prevent environmental degradation".
[99][100]
Initiatives to ban neonicotinoids in the United States
In March 2013, professional beekeepers and environmentalists jointly filed a lawsuit against the United States
Environmental Protection Agency
(EPA) for continuing to allow the use of neonicotinoids in the United
States. The suit specifically asks for suspension of clothianidin and
thiamethoxam. The lawsuit follows a dramatic die off of bees in the
United States, with some beekeepers losing 50% of their hives.
[101] The EPA responded to the suit by issuing a report blaming the
Varroa mite for the decline in bees and claiming the role of neonicotinoids in bee extinction has been overstated.
[102]
Also in 2013, the Save America's Pollinators Act of 2013 (H.R. 2692) was introduced in Congress by
Earl Blumenauer of Oregon.
[103][104] The proposed act, spearheaded by Representatives
John Conyers (D, MI) and
Earl Blumenauer (D, OR), and cosponsored by Rep.
Lucille Roybal-Allard (D, CA) and Rep.
Carol Shea-Porter (D, NH), asks that neonicotinoids be suspended until a full review of their impacts has occurred.
In 2010 a French study found that even at very low nonlethal doses,
it still impairs the ability to locate the hive, resulting in large
numbers of foragers lost with every pollen-finding expedition.
[74] Other studies, however, showed no acute effect of Fipronil on honey bees.
[75]
Pathogens and immunodeficiency theories
Early researchers commented that the pathway of propagation functions in the manner of a
contagious disease; however, some sentiment existed that the disorder may involve an
immunosuppressive mechanism,
[105]
potentially linked to "stress" leading to a weakened immune system.
Specifically, according to research done in 2007 at the Pennsylvania
State University: "The magnitude of detected infectious agents in the
adult bees suggests some type of immunosuppression". These researchers
initially suggested a connection between
Varroa destructor mite infestation and CCD, suggesting that a combination of these bee mites,
deformed wing virus (which the mites transmit) and bacteria work together to suppress immunity and may be one cause of CCD.
[2][106]
When a colony is dying, for whatever cause, and other healthy colonies are 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 is an infectious disease
came 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,
[107]
and the CCD Working Group report in 2010 indicated that CCD-exhibiting
hives tended to occur in proximity to one another within apiaries.
[46]
Varroa mites
Varroa destructor on a honey bee host
According to a 2007 article, the
mite Varroa destructor
remains the world's most destructive honey bee killer, due in part to
the viruses it carries, including deformed wing virus and
acute bee paralysis virus, which have both been implicated in CCD.
[106][108] 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.
[109] As such,
Varroa mites have been considered as a possible cause of CCD, though not all dying colonies contain these mites.
[110]
Israeli acute paralysis virus
In 2004,
Israeli acute paralysis virus (IAPV), was discovered in
Israel
and at one time it was considered the cause of CCD. It was named after
the place it was first identified; its place of origin is unknown. In
September 2007, results of a large-scale statistical
RNA sequencing
study of afflicted and unafflicted colonies were reported. RNA from all
organisms in a colony was sequenced and compared with sequence
databases to detect the presence of pathogens. All colonies were found
to be infected with numerous pathogens, but only the IAPV virus showed a
significant association with CCD: the virus was found in 25 of the 30
tested CCD colonies, and only in one of the 21 tested non-CCD colonies.
[107][111]
Research in 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.
[112][113]
Nosema
Some have suggested the syndrome may be an inability by beekeepers to correctly identify known diseases such as
European foulbrood or the
microsporidian fungus
Nosema apis.
The testing and diagnosis of samples from affected colonies (already
performed) makes this highly unlikely, as the symptoms are fairly well
known and differ from what is classified as CCD. A high rate of
Nosema infection was reported in samples of bees from Pennsylvania, but this pattern was not reported from samples elsewhere.
[2]
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.
[114] 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.
[115][116]
However, a 2009 comprehensive survey of CCD-affected bee populations in
the United States suggested CCD likely involves an interaction between
pathogens and other stress factors. They reported their survey found
only about half of the colonies sampled, both in CCD and control
populations, were infected with
N. ceranae.
[46]
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.
[117] Higes also claims to have successfully cured colonies with fumagillin.
[118][119] A review of these results described these results as promising, but cautioned "
N. ceranae may not be to blame for all cases of colony collapse".
[120] Various areas in Europe have reported this fungus, but no direct link to CCD has yet been established.
[121][122]
Highly preliminary evidence of
N. ceranae was recently reported in a few hives in the Merced Valley area of California.
[123][124]
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".
[125] 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".
[126] Likewise, a Washington beekeeper familiar with
N. ceranae in his own hives, discounts it as being the cause of CCD.
[127]
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.
[128][129] In New York,
N. ceranae was detected in 49 counties, and of the 1,200 honey bee samples collected, 528 (44%) were positive for
Nosema, from which,
PCR analysis of 371 spore positive samples revealed 96% were
N. ceranae, 3% had both
N. ceranae and
N. apis, and 1% had
N. apis only.
[130]
Viral and fungal combination
A University of Montana and Montana State University team of
scientists headed by Jerry Bromenshenk and working with the US Army's
Edgewood Chemical Biological Center published a paper in October 2010 saying that a new
DNA virus, invertebrate iridescent virus or IIV6, and the fungus
Nosema ceranae
were found in every killed colony the group studied. In their study,
they found neither agent alone seemed deadly, but a combination of the
virus and
N. ceranae was always 100% fatal.
[131][132][133] Information about the study was released to the public in a front page article in
The New York Times.
[134] A few days later, an article was published in
Fortune Magazine
with the title, "What a scientist didn't tell the New York Times about
his study on bee deaths". Professor of entomology at Penn State
University James Frazier, who is currently researching the sublethal
impact of pesticides on bees, said that while Bromenshenk's study
generated some useful data, Bromenshenk has a conflict of interest as
CEO of a company developing scanners to diagnose bee diseases.
[135]
A few months later, the methods used to interpret the mass spectrometry
data in the Bromenshenk study were called into question, raising doubts
as to whether IIV6 was ever correctly identified in any of the samples
examined.
[136][137]
Fungicides
In 2013, researchers collected pollen from hives and fed it to
healthy bees. The pollen had an average of nine different pesticides and
fungicides. Further, the researchers discovered that bees that ate
pollen with fungicides were three times more likely to be infected by
parasites. Their study shows that fungicides, thought harmless to bees,
may actually play a significant role in CCD. Their research also showed
that spraying practices may need to be reviewed because the bees sampled
by the authors foraged not from crops, but almost exclusively from
weeds and wildflowers, suggesting that bees are more widely exposed to
pesticides than thought.
[138]
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
[2]
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.
[1][139]
Fluvalinate/coumaphos
Research, in 2008, by scientists from
Pennsylvania State University found high levels of the pesticides
fluvalinate and
coumaphos in samples of wax from hives, as well as lower levels of 70 other pesticides.
[46] These chemicals have been used to try to eradicate
varroa mites,
a bee pest that itself has been thought to be a cause of CCD. A 2009
study confirmed high levels of pesticide residue in hive wax and found
an association between it and significantly reduced bee longevity.
[73] The
microsporidian pathogen
Nosema ceranae, was found in high concentrations in the majority of the bees tested, even after administering large doses of the antibiotic
fumagillin.
Maryann Frazier commented, "Pesticides alone have not shown they are
the cause of CCD. We believe that it is a combination of a variety of
factors, possibly including mites, viruses and pesticides."
[73]
Bee rentals and migratory 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.
[140] 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.
[141]
Selective commercial breeding and lost genetic diversity in industrial apiculture
Most of the focus on CCD has been toward environmental factors. CCD
is a condition recognised for greatest impact in regions of 'industrial'
or agricultural use of commercially bred bee colonies.
Natural breeding
and colony reproduction of wild bees is a complex and highly selective
process, leading to a
diverse genetic makeup in large populations of bees, both within
[142] and between colonies.
[citation needed] Genetic diversity through sexual reproduction is a significant evolutionary factor in resistance to parasites and infectious diseases.
[citation needed] Many artificially bred species, especially domestic and agricultural species, suffer from lack of genetic variation.
[citation needed] resulting in increased risk of hereditable diseases, loss of vitality or
vigour, and heightened uniform susceptibility to infectious diseases.
[citation needed] There may be an analogy in artificially introduced invasive ants, which displace native species by their
ecological release
and supercolonies (a manifestation of genetic homogeneity), only to
suffer collapse of colonies attributed to lack of genetic diversity.
[143][144] Displaced indigenous species rebounded from residual populations.
Industrial apiculture has adopted simple breeding programs
[145]
for uniform desired traits, and seasonal transportation of colonies
over vast distances causes increased infectious exposures from mixing of
these domestic and residual displaced wild populations..
[citation needed] Brood incubation conditions may be stressful with respect to deficient nutrition, temperature
[146] and other basics. This combination of ecological factors, especially the host factor of loss of genetic variation and
hybrid vigor, may account for the apparent multifactorial environmental 'causes' of CCD including concurrent infections.
[citation needed]
Malnutrition
In 2007, one of the patterns reported by the CCD Study Group at
Pennsylvania State was that all producers in a preliminary survey noted a
period of "extraordinary stress" affecting the colonies in question
prior to their die-off, most commonly involving poor nutrition and/or
drought.
[2] This was the only factor that
all
of the cases of CCD had in common in the report; accordingly, there
appeared to be at least some significant possibility that the phenomenon
was correlated to nutritional stress that may not manifest in healthy,
well-nourished colonies. This was similar to the findings of another
independent survey done in 2007 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.
[27]
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. One European writer
has suggested a possible connection with HFCS produced from genetically
modified corn.
[5]
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 when 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).
[147]
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.
[148]
A 2013 study found that
p-coumaric acid,
which is normally present in honey, assists bees in detoxifying certain
pesticides. Its absence in artificial nutrients fed to bees may
therefore contribute to CCD.
[149]
Electromagnetic radiation
Despite considerable discussion on the Internet and in the lay media,
there have been few studies published in peer reviewed scientific
literature on effects of
electromagnetic radiation on honey bees. In 2004, an exploratory study was conducted by investigators at the
University of Landau on the non-thermal effects of
radio frequency ("RF") on honey bees (
Apis mellifera carnica). The investigators did not find any change in behavior due to RF exposure from
DECT cordless phone base stations embedded in them, operating at 1880–1900 MHz.
[150] In 2006, these same investigators extended this study and this time suggested that 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.
[151]
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 this study appeared in various
media outlets, beginning with an article in
The Independent, which stated that the subject of the study included mobile phones and had related them to CCD.
[152] Though
cellular phones
were implicated by other media reports at the time, they were not
covered in the study. Researchers involved 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".
[153][154]
In October 2011, a review study was published by the Indian government's
Ministry of Environment and Forests
that looked at 919 peer-reviewed scientific studies investigating
impacts of EMF on birds, bees, humans, animals/wildlife, and plants.
[155]
Only 7 of the 919 studies involved honey bees, and 6 of these claimed
negative effects from exposure to EMF radiation, but none specifically
demonstrated any link to CCD. The review noted that according to one
study,
[156]
when active mobile phones were kept inside beehives, worker bees
stopped coming to the hives after ten days. The same study also found
drastic decrease in the egg production of queen bees in these colonies
and goes on to claim that "electromagnetic radiation exposure provides a
better explanation for Colony Collapse Disorder (CCD) than other
theories". In view of evidence from this and several other studies, the
review authors concluded: "existing literature shows that the EMRs are
interfering with the biological systems in more ways than one" and
recommended recognising EMF as a pollutant. However, they also noted
that "these studies are not representative of the real life situations
or natural levels of EMF exposure. More studies need to be taken up to
scientifically establish the link, if any, between the observed
abnormalities and disorders in bee hives such as Colony Collapse
Disorder (CCD)".
Parasitic phorid fly
While there are many possible causes of this CCD, research has not
shown why the workers abandon the hive, one of the key markers of CCD.
In January 2012, a researcher discovered
Apocephalus borealis
larvae, a parasitic fly known to prey on bumble bees and wasps, in the
test tube of a dead honey bee believed to have been affected by CCD.
[157]
Since that time, it has been suggested that the phorid fly may be one
of the causes of CCD. The fly lays eggs in the bees' abdomen and after
they hatch the larva feed on the bee. Infected bees act oddly, foraging
at night and gathering around lights like moths. Eventually the bee
leaves the colony to die. The mature phorid fly larvae then emerge from
the neck of the bee.
[158][159]
Genetically modified crops
In 2008 a meta-analysis
[160] of 25 independent studies assessing effects of
Bt Cry proteins on honeybee survival (mortality) showed that Bt proteins used in commercialized
GE crops
to control lepidopteran and coleopteran pests do not negatively impact
the survival of honeybee larvae or adults. Additionally, larvae consume
only a small percent of their protein from pollen, and there is also a
lack of geographic correlation between GM crop locations and regions
where CCD occurs.
[161]
Management
As of 1 March 2007, the
Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC) offered the following tentative recommendations for beekeepers noticing the symptoms of CCD:
[117]
- Do not combine collapsing colonies with strong colonies.
- 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.
- If you feed your bees sugar syrup, use Fumagillin.
- If you are experiencing colony collapse and see a secondary infection, such as European Foulbrood, treat the colonies with oxytetracycline, not tylosin.
Another proposed remedy for farmers of pollinated crops is simply to switch from using beekeepers to the use of
native bees, such as
bumble bees and
mason bees.
[162][163]
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).
[164][165]
A British beekeeper successfully developed a strain of bees that are resistant to varroa mites.
[166][167][168][169] Russian honey bees also resist infestations of
varroa mites
but are still susceptible to other factors associated with colony
collapse disorder, and have detrimental traits that limit their
relevance in commercial apiculture.
In the United Kingdom, a national bee database was set up in March
2009 to monitor colony collapse as a result of a 15% reduction in the
bee population that had taken place over the previous two years.
[170] In particular, the register, funded by the
Department for Environment, Food and Rural Affairs 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. In October
2010, David Aston of the British Beekeepers’ Association stated, ‘We
still do not believe CCD is a cause of colony losses in the UK, however
we are continuing to experience colony losses, many if not most of which
can be explained. The approach being taken in UK beekeeping is to raise
the profile of integrated bee health management, in other words
identifying and trying to eliminate factors which reduce the health
status of a colony. This incorporates increasing the skill level of
beekeepers through training and education, raising the profile of
habitat destruction and its effect of forage (nectar and pollen)
availability, and of course research on the incidence and distribution
of diseases and conditions in the UK together with more applied research
and development on providing solutions."
[29][30]
Consequences
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.
[171]
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, 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
[172]),
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.
[173][174]
Media
A number of documentaries have been produced in which possible causes of CCD have been explored.
- Silence of the Bees (October 2007) is a part of the Nature television series and covers several recent investigative discoveries.[175]
- The 2009 documentary Vanishing of the Bees
pointed to neonicotinoid pesticides as being the most likely culprit,
though the experts interviewed concede that no firm data yet exists.[176]
- Colony is a 2009 feature length documentary focusing on several beekeepers in the United States coping with colony collapse disorder.
- The 2010 feature length documentary Queen of the Sun: What are the bees telling us? features interviews with beekeepers, scientists, farmers, and philosophers.[177]
- The 2012 documentary, Nicotine Bees, appears to offer
substantial anecdotal and scientific proof that the class of neo
nicotinoid pesticides are principally responsible for Colony Collapse
Disorder.[178]
- More than Honey, a 2012 documentary, examines the relationship between humans and bees and explores the possible causes of CCD.[179]
