Colony collapse disorder (CCD) is the phenomenon that occurs when the majority of worker bees in a colony disappear and leave behind a queen, plenty of food and a few nurse bees to care for the remaining immature bees. While such disappearances have occurred sporadically throughout the history of apiculture, and were known by various names (disappearing disease, spring dwindle, May disease, autumn collapse, and fall dwindle disease), the syndrome was renamed colony collapse disorder in late 2006 in conjunction with a drastic rise in the number of disappearances of western honey bee (Apis mellifera) colonies in North America.
Most European countries observed a similar phenomenon since 1998, especially marked in Belgium, France, the Netherlands, the UK, Greece, Italy, Portugal, and Spain, Switzerland and Germany; the Northern Ireland Assembly received reports of a decline greater than 50%. The phenomenon became more global when it touched some Asian and African countries too.
Colony collapse disorder causes significant economic losses because many agricultural crops worldwide are pollinated by western 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 honey bee pollination was estimated at close to $200 billion in 2005. Shortages of bees in the US have increased the cost to farmers renting them for pollination services by up to 20%.
In the six years leading up to 2013, more than 10 million colonies were lost, often to CCD,nearly twice the normal rate of loss. In comparison, according to U.N. FAO data, the world’s beehive stock rose from around 50 million in 1961 to around 83 million in 2014, which is about 1.3% average annual growth. Average annual growth has accelerated to 1.9% since 2009.
Before the symptomatic manifestation of Colony Collapse Disorder, there are physio-pathological traits which serve as biomarkers for colony health as well as predict CCD status. Bees of collapsing colonies tend to have a soft fecal matter, half filled rectums, rectal enteroliths (rectal stone), and Malpighian tubuleiridescence. The defective rectum indicates nutritional disruption or water imbalance whereas rectal enteroliths suggest a malfunction of excretory physiology which might further lead to constipation and poor osmoregulation in CCD bees.
These traits express at various degrees across four bee age groups (newly-emerged bee, nurse, non-pollen foragers, and pollen foragers) and were confirmed to not be associated with age. In addition, there are genetic indications in the gut that suggest the susceptibility of honey bees to CCD. 65 transcripts have been determined as potential signs for CCD status. These transcript expressions were either upregulated or downregulated depending on genes when comparing them to healthy bees’. The abundance of unusual ribosomal RNA (rRNA) fragments that contained poly(A)-rich 3’ tail was detected via microarray analysis and qPCR in CCD bees’ gut. This evidence suggests that these poly(A)-rRNA sequences play the role of degradation intermediates to help in protein folding and enzymatic activity of rRNA. Furthermore, the presence of deformed wing virus and Israeli acute paralysis virus as well as the expression of poly(A)-rRNA are genetic indications for the appearance of CCD .
The mechanisms of CCD are still unknown, but many causes are currently being considered, such as pesticides, mites, fungi, beekeeping practices (such as the use of antibiotics or long-distance transportation of beehives), malnutrition, poor quality queens, starvation, 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.
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. 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. A scholarly review in June 2007 similarly addressed numerous theories and possible contributing factor, but left the issue unresolved.
In July 2007, the United States Department of Agriculture (USDA) released a CCD Action Plan, which outlined a strategy for addressing CCD consisting of four main components: survey and data collection; analysis of samples; hypothesis-driven research; mitigation and preventive action. The first annual report of the U.S. Colony Collapse Disorder Steering Committee was published in 2009. It suggested CCD may be caused by the interaction of many agents in combination. The same year, 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.”
The second annual Steering Committee report was released in November 2010. The group reported that although many associations—including pesticides, parasites, and pathogens—had 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. 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.
A 2015 review examined 170 studies on colony collapse disorder and stressors for bees, including pathogens, agrochemicals, declining biodiversity, climate change and more. The review concluded that “a strong argument can be made that it is the interaction among parasites, pesticides, and diet that lies at the heart of current bee health problems.” Furthermore:
“Bees of all species are likely to encounter multiple stressors during their lives, and each is likely to reduce the ability of bees to cope with the others. A bee or bee colony that appears to have succumbed to a pathogen may not have died if it had not also been exposed to a sublethal dose of a pesticide and/or been subject to food stress (which might in turn be due to drought or heavy rain induced by climate change, or competition from a high density of honey bee hives placed nearby). Unfortunately, conducting well-replicated studies of the effects of multiple interacting stressors on bee colonies is exceedingly difficult. The number of stressor combinations rapidly becomes large, and exposure to stressors is hard or impossible to control with free-flying bees. Nonetheless, a strong argument can be made that it is the interaction among parasites, pesticides, and diet that lies at the heart of current bee health problems.”
New Holland TL 90 with a field sprayer on a Narcissus field in Europe.
According to the USDA, pesticides may be contributing to CCD. A 2013 peer-reviewed literature review concluded neonicotinoids in the amounts typically used harm bees and safer alternatives are urgently needed. 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.
Scientists have long been concerned that pesticides, including 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 other similar 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 containment of neonicotinoids to crops and fields designated for treatment is difficult, and many times inefficient. Run-off from treated fields and farm machinery that is not properly cleaned after field treatments can lead to exposure and uptake of pesticides by untreated plants. Therefore, honey bees are not only exposed to neonicotinoids by foraging on treated plants, but also by foraging on plants unintentionally exposed to these chemicals. The doses taken up by bees are not lethal, but possible chronic problems could be caused by long-term exposure. In a laboratory setting, both lethal and sub-lethal effects on foraging behavior, memory, and learning ability have been observed in honey bees exposed to neonicotinoids. However, these effects were not seen in field studies with field-realistic dosages. Most corn grown in the US is treated with neonicotinoids, 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. 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.”
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 when exposure to pesticides occurred.
Imidacloprid map of use, US, 2012 (estimated)
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; for example, the effects of imidacloprid on termites include apparent failure of the immune system, and disorientation.
In Europe, the interaction of the phenomenon of “dying bees” with imidacloprid has been discussed for quite some time. 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. 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.
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. 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.”
Around the time when French beekeepers succeeded in banning neonicotinoids, the Clinton administration permitted pesticides that were previously banned, including imidacloprid. In 2004, the Bush administration reduced regulations further and pesticide applications increased.
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. 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. Sublethal doses of imidacloprid in sucrose solution have also been documented to affect homing and foraging activity of honey bees. Imidacloprid in sucrose solution fed to bees in the laboratory impaired their communication for a few hours. Sublethal doses of imidacloprid in laboratory and field experiment decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired.
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. 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.
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.”
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; other studies, however, have shown no acute effect of fipronil on honey bees. 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.
Honeycomb of honey bees with eggs and larvae. The walls of the cells have been removed. The larvae (drones) are about 3 or 4 days old.
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.
In 2010, a sequencing of the honey bee genome provided a possible explanation for the sensitivity of bees to pesticides. Its genome is deficient in the number of genes encoding detoxification enzymes, including cytochrome P450 monooxygenases (P450s), glutathione-S-transferases, and carboxylesterases.
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.
Neonicotinoids may interfere with bees’ natural homing abilities, causing them to become disoriented and preventing them from finding their way back to the hive
Bees are having a really hard time right now. For about a decade, they’ve been dying off at an unprecedented rate—up to 30 percent per year, with a total loss of domesticated honeybee hives in the United States worth an estimated $2 billion.
At first, no one knew why. But as my colleague Tom Philpott has reported extensively, in the last few years scientists have accumulated a compelling pile of evidence pointing to a class of insecticides called neonicotinoids. These chemicals are widely used in commercial agriculture but can have lethal effects on bees. Other pesticides are also adding to the toll. So are invasive parasites and a general decline in the quality of bees’ diets.
(This article was written 4 years ago…so now things are worse)
Clearly, that combination of factors poses a pretty serious problem for anyone who likes to eat, since bees—both the domesticated kind and their wild bumblebee cousins, both of which are in decline—are the main pollinators of many major fruit and nut crops. The problem is so severe that this spring President Barack Obama unveiled the first-ever national strategy for improving the health of bees and other key pollinators.
Now, it appears that lurking in the background behind the ag-industry-related problems is an even more insidious threat: climate change. According to new research published in the journal Science, dozens of bumblebee species began losing habitat as early as the 1970s—well before neonicotinoids were as widespread as they are today. Since then, largely as a result of global warming, bees have lost nearly 200 miles off the southern end of their historic wild range in both the US and in Europe, a trend that is continuing at a rate of about five miles every year.
As temperatures increase (the US is about 1.5 degrees Fahrenheit warmer today, on average, than in 1900), many plant and animal species in the Northern Hemisphere are shifting their range north. But by analyzing a vast archive of bee distribution records reaching back more than a century, ecologists at the University of Ottawa showed that bees are not joining that trend. Instead of shifting north like many other species, the bees’ range is only compressing in from the south, leaving less and less available habitat. That finding is illustrated in the chart below (and explained in more detail in the video at the bottom of this post, produced by Science).
Kerr et al, Science 2015
In a call with reporters, lead scientist Jeremy Kerr stressed that although pesticide use is a critical cause of bee mortality at local levels, it doesn’t explain the continent-wide habitat shrinkage that stands out in the bee data. But temperature trends do.
“They are in serious and immediate risk from human-caused climate change,” Kerr said. “The impacts are large and they are underway.”
The question of why bees aren’t pushing northward is a bit trickier, and it isn’t resolved in this paper. But Kerr said he suspects the answer could be the relatively long time it takes for bees to reach a critical mass of population that can be sustained in new places.