Colony collapse disorder (CCD) is a strange event that happens when most worker bees in a honey bee colony suddenly disappear, leaving the queen, plenty of food, and a few nurse bees to care for the young bees. This has happened from time to time in the history of beekeeping and has been called by other names, such as disappearing disease or autumn collapse. In early 2007, the condition was named colony collapse disorder after a big increase in reports of missing western honey bee (Apis mellifera) colonies in North America. Beekeepers in many European countries had seen similar events since 1998, especially in Southern and Western Europe, where Northern Ireland reported a drop of more than 50%. The problem later spread to parts of Asia and Africa. Despite this, from 1990 to 2021, the United Nations' FAO reported that the total number of honeybee colonies worldwide grew by 47%, reaching 102 million.

Colony collapse disorder could lead to major economic losses because many crops around the world rely on pollination by western honey bees. According to FAO, the value of global crops pollinated by honey bees was nearly US$200 billion in 2005. In the United States, a shortage of bees has raised the cost for farmers renting bees for pollination by up to 20%. However, bee numbers had already been decreasing for many years before CCD: the number of managed hives in the U.S. has been slowly shrinking since 1961.

In contrast, the global population of managed bees has grown steadily since 1975 to support honey production, with China contributing most of the increase. The slowest growth in worldwide honey production happened between 1991 and 1999 due to economic problems after the end of communism in the former Soviet countries. By 2020, honey production had risen 50% compared to 2000, growing twice as fast as in earlier decades, even with CCD. Experts believe there are now more honey bees alive worldwide than at any other time in human history.

Scientists have suggested several possible causes for CCD, but no single explanation is widely accepted. These include pesticides, infections from diseases spread by mites, poor nutrition, genetic issues, weak immune systems, loss of natural habitats, or changes in beekeeping methods. Some combinations of these factors have also been considered. Many people have discussed the role of a type of pesticide called neonicotinoids in CCD, but many affected bee colonies show no signs of these chemicals.

History

Colony collapse disorder is a condition defined by a specific set of symptoms. It was previously called by many names, such as "disappearing disease," "spring dwindle," "May disease," "autumn collapse," and "fall dwindle disease." The cause of these historic bee colony losses has never been clearly determined. However, scientists have described colony collapse disorder as "death by a thousand cuts," with the most obvious cause being Varroa mites. After it was recognized that the condition is not limited to certain seasons and may not be a traditional "disease" with one clear cause, the condition was renamed "colony collapse disorder" in 2007.

Similar colony losses were reported as early as 1869. In 1891 and 1896, beekeepers in Colorado called these losses "May Disease." A well-documented outbreak of colony losses spread from the Isle of Wight to the rest of the United Kingdom in 1906. These losses were later linked to multiple factors, such as bad weather, overuse of beekeeping practices that reduced food sources, Acarine mites, and a new virus called chronic bee paralysis virus. However, during the outbreak, the cause of the problem was unknown.

Similar hive losses were reported in the United States in 1918 and 1919. These were sometimes called "mystery disease" and later became known as "disappearing disease." In 1965, a scientist named Oertel found that hives affected by disappearing disease in Louisiana had plenty of honey in their combs but few or no bees, which showed that the loss of bees was not due to a lack of food.

In the United States, the number of bee colonies kept by beekeepers has been decreasing since the 1960s because of reasons like urbanization, pesticide use, mites, and beekeepers retiring. However, in late 2006 and early 2007, beekeepers reported unusually high colony losses, leading to the use of the term "colony collapse disorder." Before 2007, colony losses had been about 17–20% per year, caused by mites, diseases, and stress from beekeeping practices. In the winter of 2004–2005, a sudden collapse was linked to Varroa mites, but this was never confirmed.

The first report of colony collapse disorder was made in mid-November 2006 by a beekeeper in Pennsylvania. By February 2007, large beekeepers in California, Florida, Oklahoma, and Texas reported heavy losses from colony collapse disorder, with losses ranging from 30% to 90% of their colonies. Some beekeepers lost nearly all their colonies, and the remaining colonies were too weak to pollinate or make honey. In late February 2007, beekeepers in the mid-Atlantic and Pacific Northwest regions also reported losses of more than 50%. Colony losses were also reported in five Canadian provinces, several European countries, and countries in South and Central America and Asia.

In 2010, the United States Department of Agriculture reported that honey bee losses were about 34%, similar to losses in 2007, 2008, and 2009. Fewer colony losses occurred in the winter of 2013–2014 compared to recent years, with 23.2% of colonies lost nationwide. This was an improvement from the 30.5% loss in 2012–2013 and the eight-year average of 29.6%.

After bee populations dropped by 23% in the winter of 2013, the Environmental Protection Agency and the Department of Agriculture formed a task force to address the issue. Since 2014, Congress has provided financial support for the pollinator industry through the 2014 Farm Bill. This law allowed up to $20 million in subsidies each year for honeybee conservation and other efforts. In 2017, Congress added funding to protect bees from pesticide exposure during pollination work. The 2018 Farm Bill increased the financial aid cap for emergency assistance from $20 million to $34 million.

A 2023 survey by the University of Maryland and Auburn University found that the number of honey bee colonies in the United States remained relatively stable, but 48% of colonies were lost in the year ending April 1, 2023. The average annual loss over 12 years was 39.6%. In the previous year (2021–2022), the loss was 39%, and in 2020–2021, it was 50.8%. Beekeepers said that a 21% loss over winter is acceptable, but more than three-fifths of those surveyed reported losses higher than in 2022–2023.

In 2024, the United States Census of Agriculture reported a record high in commercial honey bee hives, mostly in Texas. These hives are now the fastest-growing livestock segment in the country.

Signs and symptoms

CCD is different from colony decline, which can be caused by problems like queen health, varroa mite infestation, nutrition, and diseases. When a colony collapses, CCD is suspected if there are very few adult bees left in the hive. Unlike other sudden causes, like pesticide exposure, there are usually no dead bees found near the hive, as if the hive had been abandoned. A hive that collapses from CCD usually has all these signs at the same time: Early signs that may appear before the collapse include:

Genetic and physio-pathological predictions

Before bees show symptoms of colony collapse disorder (CCD), certain physical and health traits can indicate colony health and predict whether a colony is at risk for CCD. Bees in collapsing colonies often have soft fecal matter, partially filled rectums, rectal stones (hard deposits in the rectum), and a shimmering appearance in their Malpighian tubules (organs involved in waste removal). A weakened rectum suggests problems with nutrition or water balance, while rectal stones point to issues with the body's ability to remove waste, which may lead to constipation and difficulty regulating body fluids in CCD-affected bees. These traits appear in varying degrees across four bee age groups (newly emerged bees, nurse bees, non-pollen foragers, and pollen foragers) and are not linked to the bees' age.

Additionally, genetic changes in the gut of honey bees can signal their susceptibility to CCD. Scientists have identified 65 different RNA fragments that may indicate CCD status. The activity of these RNA fragments is either higher or lower in CCD bees compared to healthy bees, depending on the specific genes involved. Microarray analysis and qPCR testing revealed an increased presence of unusual ribosomal RNA (rRNA) fragments with poly(A)-rich 3′ tails in the guts of CCD bees. This suggests these poly(A)-rRNA sequences may help in processes like protein folding and enzyme function. The presence of deformed wing virus and Israeli acute paralysis virus, along with the expression of poly(A)-rRNA, are genetic signs that may contribute to the development of CCD.

Scope and distribution

The National Agricultural Statistics Service (NASS) reported that in February 2008, there were 2.44 million honey-producing hives in the United States. This number was lower than 4.5 million in 1980 and 5.9 million in 1947. However, these numbers do not count all managed hives, as they exclude hives used only for pollination contracts and those managed by beekeepers with fewer than 5 hives. Some hives are counted more than once if they are moved to different states to produce honey, which may affect the accuracy of the totals.

In 2007, at least 24 U.S. states reported at least one case of Colony Collapse Disorder (CCD). A 2007 survey of 384 beekeepers from 13 states found that 23.8% of them met the criteria for CCD, meaning at least half of their dead colonies were found without bees or with very few dead bees. During 2006–2007, beekeepers affected by CCD lost 45% of their colonies, compared to 25% lost by beekeepers not affected by CCD.

A 2007–2008 survey of over 19% of U.S. bee colonies showed a total loss of 35.8%. Beekeepers who pollinated almonds lost about the same number of colonies as those who did not. Beekeepers who reported colonies dying completely without bees had a 40.8% loss, compared to 17.1% loss for those without this symptom. Larger operations were more likely to have this symptom, suggesting a possible contagious cause. About 60% of all dead colonies reported in this survey had no dead bees in the hive, which may indicate CCD.

Between 2007 and 2013, annual winter colony losses in the U.S. doubled from 15% before CCD to 30% after its discovery. Loss rates dropped to 24% from 2014 to 2017, and CCD symptoms were less commonly linked to hive losses. Despite increased hive losses from CCD, honey bee numbers in the U.S. remained stable or grew since CCD was identified.

In 2017, NASS reported that U.S. operations with more than 5 hives had between 2.63 and 2.99 million hives, while those with fewer than 5 hives had between 35,000 and 43,000 hives. Operations with more than 5 hives lost 77,800 hives (2.6–3.0%) with CCD symptoms, and those with fewer than 5 hives lost 6,000 hives (14–17%) with CCD symptoms.

By 2022, the number of U.S. colonies reached 3.8 million, a 31% increase since 2007, mainly due to growth in small beekeepers in Texas.

In 2007, the European Food Safety Authority (EFSA) reported that the United Kingdom had 274,000 hives, Italy had 1,091,630, and France had 1,283,810. In 2008, the UK reported a 30% drop in its bee population from 2007, and Italy had a mortality rate of 40–50%. However, EFSA noted these numbers were unreliable because countries used different methods to collect data before CCD was widely recognized. Reports in 2008 linked high bee deaths in Europe to the varroa mite, wet summers, and pesticides.

In 2009, Tim Lovett, president of the British Beekeepers' Association, said beekeepers reported losses ranging from nearly a third of hives to none. John Chapple, chairman of the London Beekeepers' Association, noted losses among his 150 members ranged from a fifth to a quarter. Officials in the UK denied CCD existed there, blaming losses on the varroa mite and rainy summers.

In 2010, David Aston of the British Beekeepers' Association stated that CCD was not a confirmed cause of colony losses in the UK but that many losses could be explained by factors like pathogens, environmental conditions, and beekeeping practices.

In Scotland, beekeeper Andrew Scarlett lost 80% of his 1,200 hives during the 2009–2010 winter. He attributed the loss to a bacterial infection that spread due to a lack of bee inspectors and poor weather.

In Germany, where some of the first European reports of CCD appeared, 40% of honey bee colonies died, but no scientific confirmation of CCD was found. In 2007, German media reported no confirmed CCD cases.

A 2012 study identified a colony loss incident in Switzerland as the first confirmed case of CCD outside the U.S. The incident matched U.S. criteria for CCD, but laboratory tests found no significant differences in pathogen levels between CCD and non-CCD hives. The study noted that Varroa destructor and Nosema spp were not at harmful levels during the collapse but could not rule out pathogens as a cause.

In May 2012, the Swiss government reported that about half of the bee population had died over the winter. The main cause was the Varroa destructor parasite.

In China, a 2010–2013 survey using COLOSS questionnaires found an average colony loss of 10.1%. Comb renewal and queen problems were identified as major risk

Possible causes

Scientists do not yet know the exact causes of Colony Collapse Disorder (CCD), but they are studying many possible reasons, such as pesticides, mites, fungi, beekeeping practices (like using antibiotics or moving hives long distances), poor nutrition, weak queen bees, starvation, other diseases, and weak immune systems. Scientists agree that no single factor causes CCD, but several factors together might be responsible, either by adding up or working together to cause harm.

In 2006, a group called the Colony Collapse Disorder Working Group (CCDWG) was created, mostly at Pennsylvania State University. Their first report found some patterns but did not give clear answers. A 2007 survey showed that hobbyist beekeepers thought starvation was the main cause of colony deaths, while commercial beekeepers believed pests like Varroa mites, tracheal mites, or small hive beetles were the main cause. A review of research in June 2007 also discussed many theories but did not solve the problem.

In July 2007, the U.S. Department of Agriculture (USDA) created a plan to study CCD. The plan had four parts: collecting data, analyzing samples, doing research based on ideas, and taking steps to prevent CCD. In 2009, the U.S. Colony Collapse Disorder Steering Committee published its first report, suggesting that CCD might be caused by the combination of many factors. That same year, the CCD Working Group released a study showing that no one factor was consistently linked to CCD. However, bees in CCD colonies had more infections and were sick from more diseases than healthy bees, suggesting they might have weaker defenses.

In 2010, the Steering Committee reported that no single cause alone explains CCD. They found that some pesticides, like coumaphos and fluvalinate, might harm bees in ways that are not immediately deadly. Studies also showed that neonicotinoids and fungicides might weaken bees’ immune systems, making them more likely to get sick from viruses.

A 2015 review of 170 studies on CCD and bee stressors, such as diseases, chemicals, and climate change, concluded that the interaction of parasites, pesticides, and poor nutrition is likely a major cause of bee health problems. Bees often face many stressors at once, and each one can make it harder for them to survive the others. For example, a colony that dies from a disease might have also been exposed to pesticides or had trouble finding food. However, studying how these stressors work together is very difficult because there are so many combinations, and it is hard to control how bees are exposed to them.

Early researchers thought CCD might spread like a disease, but others believed it could be linked to stress that weakens bees’ immune systems. A 2007 study at Pennsylvania State University found that bees in CCD colonies had high levels of infections, suggesting their immune systems were not working properly. Researchers linked this to Varroa mites, which carry viruses and may weaken bees’ defenses.

Parasites like Varroa mites, tracheal mites, and small hive beetles, along with diseases and fungi, have caused problems for bees in the U.S. in the last 20 years. When a colony dies, nearby healthy colonies may take food from it. If the food is poisoned, it might look like a disease is spreading. However, in most CCD cases, this does not happen, suggesting that toxins are not spreading through this behavior.

Some evidence suggests CCD might act like an infectious disease. For example, healthy bees placed in hives that had CCD needed to be treated with radiation to destroy DNA before they could survive. Also, CCD hives often appear near each other in bee yards.

A 2007 study found that Varroa mites are the most dangerous threat to bees worldwide. They carry viruses like deformed wing virus and acute bee paralysis virus, which are linked to CCD. Varroa mites also weaken bees’ immune systems. A 2007–2008 study in Canada found that 85% of winter colony deaths were linked to Varroa mites. These mites also harm queen bees, making it harder for hives to survive.

Varroa destructor is a mite that lives in beehives and harms bees by feeding on their body fluids. It attaches to nurse bees and then moves to larvae, where it reproduces. This makes the mites more likely to have more offspring. Because Varroa mites harm all types of bees, they are a major threat to colonies, especially in winter.

In 2020, a group of scientists announced…

Management

As of 1 March 2007, the Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC) provided the following suggestions for beekeepers who noticed signs of colony collapse disorder (CCD):

One idea for farmers who rely on bees to pollinate crops is to use native bees, such as bumble bees and mason bees, instead of hired beekeepers. Farmers can support these native bees by creating nesting areas and planting extra crops that provide food for the bees after the main pollination season ends.

A British beekeeper successfully bred a type of bee that is less affected by varroa mites. Russian honey bees also resist varroa mites but are still vulnerable to other causes of colony collapse. These bees have traits that make them less useful for commercial beekeeping.

In the United Kingdom, a national bee database was created in March 2009 to track colony collapse after a 15% drop in the bee population over two years. The database, supported by the Department for Environment, Food and Rural Affairs and managed by the National Bee Unit, will monitor bee health and determine if colony collapse disorder is threatening the honey industry. All 20,000 beekeepers in the UK were invited to join the program. In October 2010, David Aston of the British Beekeepers' Association said, "We do not believe colony collapse disorder is causing colony losses in the UK. However, we are still seeing colony losses, many of which have clear explanations. Beekeepers in the UK are focusing on improving overall bee health by identifying and reducing factors that harm colonies. This includes training beekeepers, addressing habitat loss that affects food sources for bees, and researching diseases and conditions in the UK to find solutions."

Economic and ecological impact

Honey bees are not originally from the Americas. Because of this, their role as pollinators in the United States and other areas of the Western Hemisphere is limited to helping grow crops and ornamental plants. Native plants in these regions do not need honey bees for pollination, except in large fields of a single crop type, where the need for pollination is so high that native bees cannot meet the demand with current technology.

This is especially important for crops like almonds in California, where honey bees are the main pollinator. In 2011, the value of California’s almond crop was $3.6 billion. In 2000, the total value of U.S. crops that depended completely on honey bee pollination was more than $15 billion. California’s almond production grew from 370 million pounds in 1995 to 2.5 billion pounds in 2019, with a 30% increase in the last 10 years alone. Because of the high demand for pollinators, the cost of renting honey bees has risen. During the spring, California’s almond industry rents about 1.6 million honey bee colonies to pollinate its crops. Worldwide, honeybees provide pollination services worth about $200 billion.

Honey bees help pollinate about one-third of the United States’ crops, including almonds, peaches, apples, pears, cherries, raspberries, blackberries, cranberries, watermelons, cantaloupes, cucumbers, and strawberries. Many of these plants can be pollinated by other insects, such as other types of bees, but not always on a large scale. Some farmers use honey bees to help pollinate native crops, but no native plants require them. If honey bees are not present in an area, native pollinators may take their place, as they are often better suited to pollinate local plants.

Although many other pollinators are more efficient at pollinating individual plants, honey bees are the best choice for about 30% of crop types because native pollinators cannot be used in large numbers as easily. Honeybees can be moved between crops, and they visit many plants at once, which helps compensate for their lower efficiency. The success of these crops depends heavily on the beekeeping industry. In China, pollinating apple orchards by hand is very hard, time-consuming, and expensive.

In areas where honeybees are native, such as parts of the Old World, they are among the most important pollinators. They help maintain natural habitats and support food production for humans. When honeybee populations decline, plant populations also decline. Some crops depend completely on honeybees to produce fruit, while others rely on them to improve fruit quality. Honeybees also help plants produce fruit faster, reducing risks from pests, diseases, weather, and other problems. Plants that need honeybees to pollinate are more likely to suffer if honeybee numbers drop, while plants that use other pollinators, wind, or self-pollination are less affected.

Honeybees help pollinate nearly 75% of all plant species used for human food worldwide. A major loss of honeybees could have serious effects. It is estimated that seven of the 60 major crops in North America would be lost, and this is only for one region. Farms with large, dense crop areas will be most affected because they depend heavily on honeybees. In the United States alone, the cost of honeybee pollination services is $1.25 billion each year. However, globally, honeybees as pollinators generate between 22.8 and 57 billion Euros annually.