Colony collapse disorder (CCD) is a strange event that happens when most worker bees in a honey bee colony suddenly disappear. When this occurs, the queen bee, plenty of food, and a few nurse bees remain to care for the young bees. While similar events have been reported in beekeeping history and have had other names, such as disappearing disease or autumn collapse, the term "colony collapse disorder" was first used in early 2007. This was after a sharp increase in reports about missing honey bee colonies in North America. Beekeepers in many European countries had also noticed similar problems since 1998, especially in Southern and Western Europe. In Northern Ireland, reports showed a drop in bee populations of more than 50%. The issue later spread to some countries in Asia and Africa. Despite these challenges, the United Nations' FAO reported that the number of honeybee colonies worldwide increased by 47% from 1990 to 2021, reaching 102 million colonies.
Colony collapse disorder can cause major economic problems because many crops around the world rely on honey bees for pollination. According to the FAO, the value of crops pollinated by honey bees was nearly $200 billion globally in 2005. In the United States, a shortage of bees has raised the cost of renting bees for pollination by up to 20%. However, bee numbers have been decreasing for many years before CCD began. The number of managed hives in the United States has been shrinking since 1961.
In contrast, the number of managed bees worldwide has grown steadily since 1975 to support honey production, with China contributing most of the increase. Honey production growth slowed between 1991 and 1999 due to economic problems after the fall of communism in the former Soviet region. By 2020, honey production had risen by 50% compared to 2000, growing at twice the rate of previous decades, even with CCD. Experts believe that today, more honey bees are alive worldwide than at any time in human history.
Scientists have suggested many possible causes for CCD, but no single explanation has been widely accepted. These include pesticides, infections from diseases spread by mites, poor nutrition, genetic issues, weakened immune systems, habitat loss, and changes in beekeeping practices. Some combinations of these factors have also been considered. Many people have questioned the role of a group of pesticides called neonicotinoids in CCD, but many affected bee colonies show no signs of these chemicals.
History
Colony collapse disorder is a condition described by a group of specific symptoms that were once called by many different names, such as "disappearing disease," "spring dwindle," "May disease," "autumn collapse," and "fall dwindle disease." The cause of these past bee colony losses has never been clearly identified, but scientists have described colony collapse disorder as "death by a thousand cuts," with the most obvious factor being the Varroa mite. After researchers realized that the condition does not happen only in certain seasons and may not be a "disease" in the traditional sense—because there may not be one single cause—the condition was renamed colony collapse disorder in 2007.
Similar events to colony collapse disorder were recorded as early as 1869. In 1891 and 1896, beekeepers in Colorado called these losses "May Disease."
A major event involving bee colony losses spread from the Isle of Wight to the rest of the United Kingdom in 1906. At that time, the cause of the losses was unknown. Later, scientists linked the losses to several factors, including bad weather, overuse of beekeeping practices that reduced food sources for bees, tracheal mites, and a new virus called chronic bee paralysis virus.
Reports of similar hive losses in the United States occurred in 1918 and 1919. These events were sometimes called "mystery disease" but later became known as "disappearing disease." In 1965, a scientist named Oertel studied hives in Louisiana and found that hives with disappearing disease had plenty of honey but very few or no bees, proving that food shortages were not the cause.
Since the 1960s, the number of bee colonies managed by beekeepers in the United States has decreased for many reasons, such as urban development, pesticide use, mites, and beekeepers retiring. However, in late 2006 and early 2007, beekeepers reported unusually high losses, and the term "colony collapse disorder" was used to describe these sudden disappearances.
From the 1990s until 2004–2005, bee colony losses averaged about 17–20% each year, caused by mites, diseases, and stress from beekeeping. In 2004–2005, a sudden loss of colonies was linked to Varroa mites, though this was never confirmed. The first confirmed case of colony collapse disorder was reported in mid-November 2006 by a beekeeper in Pennsylvania. By February 2007, large beekeeping operations in California, Florida, Oklahoma, and Texas reported heavy losses, with some losing up to 90% of their colonies. Similar losses were also reported in Canada, Europe, South America, Central America, and Asia.
In 2010, the United States Department of Agriculture reported that about 34% of bee colonies were lost, a rate similar to losses in 2007, 2008, and 2009. Fewer losses occurred in the winter of 2013–2014, with 23.2% of colonies lost nationwide, an improvement compared to previous years.
After bee populations dropped 23% in the winter of 2013, the Environmental Protection Agency and Department of Agriculture created a task force to study the issue. Since 2014, Congress has provided financial support for pollinators through the Farm Bill. This law allows up to $20 million each year to help protect honeybees, livestock, and fish affected by disease, weather, or other challenges. In 2017, Congress added more funding to protect bees from pesticide exposure during pollination work. In 2018, the Farm Bill increased the financial aid cap for emergency assistance to $34 million annually.
A 2023 survey by the University of Maryland and Auburn University found that the number of honeybee colonies in the United States remained relatively stable. However, 48% of colonies were lost during the year ending April 1, 2023, with an average annual loss of 39.6% over 12 years. In the previous year (2021–2022), the loss was 39%, and in 2020–2021, it was 50.8%. Beekeepers said a 21% loss over winter is normal, but more than three-fifths of those surveyed reported higher losses than in 2022–2023.
In 2024, the United States Census of Agriculture reported a record high in commercial honeybee hives, mostly in Texas, making them the fastest-growing livestock group in the country.
Signs and symptoms
Colony Collapse Disorder (CCD) is different from colony decline, which can happen because of problems like poor queen health, varroa mite infection, poor nutrition, and diseases. When a hive collapses from CCD, there are usually very few adult bees left in the colony. Unlike sudden causes of bee deaths, such as pesticide exposure, there are rarely any dead bees found near the hive, as if the hive was suddenly abandoned. A hive that has collapsed from CCD is usually marked by these conditions happening at the same time:
Early signs that may appear before the hive collapses include:
Genetic and physio-pathological predictions
Before any visible signs of colony collapse disorder (CCD) appear, certain physical and health-related traits in bees can act as early indicators of colony health and help predict whether a colony is at risk for CCD. Bees in collapsing colonies often show signs such as soft stool, partially filled rectums, rectal stones (hard deposits in the rectum), and a shimmering appearance of the Malpighian tubules (organs involved in waste removal). A weak or damaged rectum suggests problems with nutrition or water balance, while rectal stones indicate issues with the excretory system, which may lead to constipation and difficulty maintaining proper water balance in affected bees. These signs 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 age of the bees.
In addition, genetic changes in the gut of bees provide clues about their susceptibility to CCD. Scientists have identified 65 different RNA transcripts (gene-related molecules) that may signal whether a colony is at risk for CCD. The activity of these transcripts changes in bees with CCD compared to healthy bees, either increasing or decreasing depending on the specific gene. Studies using microarray analysis and qPCR (laboratory techniques) found unusual ribosomal RNA (rRNA) fragments with poly(A)-rich 3′ tails in the guts of CCD bees. These fragments may help in the folding of proteins and the function of rRNA. Furthermore, the presence of deformed wing virus and Israeli acute paralysis virus, along with the appearance of poly(A)-rRNA, are genetic signs that may indicate 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 the 4.5 million hives in 1980 and the 5.9 million hives in 1947. However, these numbers do not include all hives because they exclude some hives used only for pollination contracts and hives managed by beekeepers with fewer than 5 hives. Some hives may also be counted more than once if they are moved between states to produce honey.
In 2007, at least 24 U.S. states reported at least one case of Colony Collapse Disorder (CCD). A survey of 384 beekeepers from 13 states found that 23.8% met the criteria for CCD, which includes colonies that had 50% or more dead bees missing from hives. 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 all U.S. honey bee colonies found a total loss of 35.8%. Beekeepers who pollinated almonds did not lose more colonies than those who did not. Beekeepers who reported colonies missing all their bees had a total loss of 40.8% of their colonies, compared to 17.1% for beekeepers without this symptom. Larger beekeeping operations were more likely to experience this symptom, which may suggest a contagious condition. About 60% of all dead colonies reported in this survey had no dead bees in the hive, which could indicate CCD.
Between 2007 and 2013, winter colony losses in the U.S. doubled from 15% before CCD to 30%. From 2014 to 2017, losses dropped to 24%, and CCD was less often linked to hive deaths. Even though CCD increased hive losses, the total number of honey bee colonies in the U.S. stayed the same or increased since CCD was first identified.
In 2017, NASS reported that the number of U.S. hives ranged between 2.63 and 2.99 million for operations with more than 5 colonies, and between 35,000 and 43,000 hives for operations with fewer than 5 colonies. Operations with more than 5 colonies lost 77,800 hives (2.6–3.0%) with CCD symptoms, while operations with fewer than 5 colonies lost 6,000 hives (14–17%) with CCD symptoms.
By 2022, the number of U.S. colonies reached a record high of 3.8 million, a 31% increase since 2007. This growth is largely due to small beekeepers in Texas.
According to the European Food Safety Authority (EFSA), in 2007, the United Kingdom had 274,000 hives, Italy had 1,091,630 hives, and France had 1,283,810 hives. In 2008, the British Beekeepers Association reported a 30% drop in the UK bee population between 2007 and 2008. EFSA noted that Italy had a mortality rate of 40–50%, but these numbers are not reliable because countries used different methods to collect bee population data. Reports from 2008 blamed high bee deaths on the varroa mite, wet summers, and some pesticides.
In 2009, Tim Lovett, president of the British Beekeepers’ Association, said that beekeeper losses varied widely, with some losing nearly a third of their hives and others losing none. John Chapple, chairman of the London Beekeepers’ Association, reported that members lost between a fifth and a quarter of their colonies. He noted that many hive disappearances remained unexplained. The UK government’s National Bee Unit denied that CCD existed in Britain, blaming losses instead on the varroa mite and rainy summers.
In 2010, David Aston of the British Beekeepers’ Association said that while CCD is now better defined, it is not believed to cause colony losses in the UK. He noted that recent studies suggest colony losses are caused by complex interactions between factors like pathogens, environmental conditions, beekeeping practices, and other stressors.
In Scotland, beekeepers reported losses from 2007 to 2009. Andrew Scarlett, a beekeeper in Perthshire, lost 80% of his 1,200 hives during the 2009–2010 winter. He blamed the losses on a bacterial infection that spread due to a lack of bee inspectors and poor weather that prevented bees from collecting enough food.
In Germany, where some of the first European reports of CCD appeared, the German national association of beekeepers reported that 40% of colonies died. However, no scientific confirmation of CCD was found. In early 2007, German media reported no confirmed CCD cases in Germany.
A 2012 study in Switzerland identified a colony loss incident as the first 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 colonies did not have high levels of Varroa destructor or Nosema spp. at the time, but it could not rule out pathogens as a possible cause.
In May 2012, the Swiss government reported that about half of the bee population did not survive the winter. The main cause was the varroa mite.
In China, a three-year survey from 2010 to 2013 found an average colony loss of 10.1%. Comb renewal and queen problems were identified as major risk factors for colony losses.
Possible causes
The causes of Colony Collapse Disorder (CCD) are not fully understood. Scientists are studying many possible factors, such as pesticides, mites, fungi, beekeeping practices (like using antibiotics or moving hives long distances), poor nutrition, weak queen bees, starvation, other diseases, and weakened immune systems. Scientists agree that no single cause leads to CCD, but a combination of these factors may contribute to the problem in different ways.
In 2006, a group called the Colony Collapse Disorder Working Group (CCDWG) was formed at Pennsylvania State University. Their first report found some patterns but did not reach clear conclusions. A survey in early 2007 showed that hobbyist beekeepers mostly thought starvation was the main cause of colony deaths, while commercial beekeepers believed invertebrate pests, such as Varroa mites, tracheal mites, and small hive beetles, were the main cause. A review of research in June 2007 also discussed many theories but did not solve the mystery.
In July 2007, the U.S. Department of Agriculture (USDA) created a CCD Action Plan with four goals: collecting data, analyzing samples, conducting research based on hypotheses, and taking steps to prevent CCD. In 2009, the first report from the U.S. Colony Collapse Disorder Steering Committee said CCD might result from the combined effects of many factors. That same year, the CCD Working Group published a study that found no single cause of CCD. Bees in affected colonies had higher levels of disease and were infected with more pathogens than healthy bees, suggesting they had weaker defenses or were exposed to more germs.
The second report from the Steering Committee in 2010 said no one factor alone causes CCD. Researchers found that colonies collapsing from CCD often had no signs of the Nosema parasite or Varroa mites. However, they did find that some pesticides, including coumaphos and fluvalinate, might harm bees in ways that do not kill them but weaken their health. Other studies also found that neonicotinoids and fungicides might harm 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, loss of plant diversity, and climate change, concluded that the interaction of parasites, pesticides, and poor nutrition is likely the main cause of current bee health problems. Bees often face multiple stressors, and each can make it harder for them to survive other challenges. For example, a colony that dies from a virus might not have survived if it was also exposed to low levels of pesticides or had a lack of food due to drought or competition from other hives. 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 spread like a disease, but others believed it might be linked to stress that weakens bees' immune systems. A 2007 study from Pennsylvania State University found that the high number of germs in bees suggested their immune systems were not working properly. Researchers connected Varroa mites, which carry viruses like deformed wing virus, to CCD. These mites, along with bacteria, might weaken bees' defenses and contribute to colony deaths. Parasites, mites, fungi, bacteria, and viruses are all recent problems for beekeepers in the U.S.
When a colony dies, nearby healthy colonies often take food from it. If the food is contaminated, it might look like a disease is spreading. However, in CCD cases, the food is not usually taken, so toxins do not spread this way. Other signs that CCD might be infectious include the need to use radiation to clean hives before reusing them and the fact that CCD colonies often appear near each other in bee yards.
A 2007 article said Varroa destructor 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. These mites also weaken bees' immune systems. A study of 413 bee colonies in Ontario found that 27% did not survive the winter, and Varroa mites were the cause in 85% of those cases. The mites also harm queens' ability to reproduce, which is bad for hive survival. While Varroa mites are a possible cause of CCD, not all dying colonies have them.
Varroa destructor mites live in beehives and feed on bees' blood-like fluid called hemolymph. They attach to nurse bees during their life cycle, then feed on larvae. This helps the mites reproduce more. Because they affect all types of bees, Varroa mites are a major threat, especially in winter. In 2020, scientists announced new findings about Varroa mites and their impact on bee health.
Management
As of 1 March 2007, the Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC) suggested the following possible steps for beekeepers who notice signs of colony collapse disorder (CCD):
Another idea for farmers who grow crops that need bees for pollination is to use native bees, such as bumble bees and mason bees, instead of hired beekeepers. Native bees can be supported by creating spaces for them to nest and by planting extra crops that provide food for them 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. However, 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. Funded by the Department for Environment, Food and Rural Affairs and managed by the National Bee Unit, the database 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. In October 2010, David Aston of the British Beekeepers' Association said, "We still believe colony collapse disorder is not the main cause of bee losses in the UK, but we are still seeing colony losses. Many of these losses can be explained. The focus in UK beekeeping is to improve 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 affecting bees in the UK, as well as finding practical 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 in the Western Hemisphere is limited to agriculture and ornamental plants. Native plants in these regions do not require honey bees for pollination, except in large fields with only one type of plant, where the need for pollination is so great that native bees cannot meet the demand with current methods.
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 relied completely on honey bees for pollination was more than $15 billion. California’s almond production grew from 370 million pounds in 1995 to 2,500 million pounds in 2019, with a more than 30% increase in the last 10 years alone. Because of the high demand for pollinators, the cost to rent honey bees has risen. During the spring, California’s almond industry rents about 1.6 million honey bee colonies to pollinate its crops. Worldwide, honey bees provide pollination services worth about $200 billion.
Honey bees pollinate about one-third of the United States’ crop species, 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 usually 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, native pollinators may take their place, as they are often better adapted to local plants.
Although some other pollinators are more efficient individually, honey bees are better suited for pollinating 30% of crop types because they can be moved easily between crops and visit many plants at once. This 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 time-consuming and expensive.
In regions where honey bees are native, such as parts of the Old World, they are vital for pollinating plants and supporting natural habitats. When honey bee populations decline, plant populations also decline. Some plants depend completely on honey bees to produce fruit, while others rely on them to improve fruit quality. Honey bees also help plants produce fruit faster, reducing risks from pests, diseases, and weather. Plants that depend only on honey bees are more vulnerable if their numbers drop, while plants that use other pollinators or wind/self-pollination are less affected.
Honey bees pollinate nearly 75% of all plant species used for human food worldwide. A major loss of honey bees could cause serious problems, with estimates suggesting that seven of the 60 major crops in North America might be lost. Farms with large-scale crop systems depend heavily on honey bees and spend about $1.25 billion annually on pollination services in the U.S. alone. However, honey bees as pollinators generate between 22.8 and 57 billion Euros globally each year.