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 only a few nurse bees to care for the young. Although similar disappearances have been reported in beekeeping history under different names, such as "disappearing disease" or "autumn collapse," the term "colony collapse disorder" was first used in early 2007 after a sharp increase in reports of missing honey bee colonies in North America. Beekeepers in many European countries had noticed similar events since 1998, especially in Southern and Western Europe, where Northern Ireland reported a decline of more than 50%. The problem later spread to parts of Asia and Africa. Despite this, from 1990 to 2021, the United Nations' Food and Agriculture Organization (FAO) reported that the total number of honeybee colonies worldwide grew by 47%, reaching 102 million.
Colony collapse disorder can lead to large financial losses because many crops around the world rely on honey bees for pollination. FAO estimated that in 2005, the value of crops pollinated by honey bees was nearly $200 billion globally. 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 declining for many years before CCD: the number of managed beehives in the U.S. has steadily decreased since 1961.
At the same time, the number of managed bees worldwide has grown since 1975, mainly to produce honey, with China contributing most of the increase. Honey production grew the least between 1991 and 1999 due to economic challenges after the fall of communism in parts of Eastern Europe. By 2020, honey production had increased by 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 many possible causes for CCD, but no single explanation is widely accepted. Possible reasons include pesticides, infections from diseases spread by mites, poor nutrition, genetic issues, weakened immune systems, habitat loss, or changes in beekeeping practices. Some combinations of these factors have also been considered. While some people suspect that a type of pesticide called neonicotinoids plays a role, many affected bee colonies show no signs of these chemicals.
History
Colony collapse disorder is a condition that has certain symptoms. It was 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 fully understood. However, scientists have described colony collapse disorder as "death by a thousand cuts," with the most noticeable factor being Varroa mites. After it was realized that this condition does not happen only in certain seasons and may not be a disease in the traditional sense—because there may not be one specific cause—the condition was renamed 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 event involving large numbers of bee colony losses spread from the Isle of Wight to the rest of the UK in 1906. At that time, the cause of these losses was unknown. Later, scientists linked the event to several factors, including bad weather, overuse of beekeeping practices that reduced food sources for bees, Acarine (tracheal) mites, and a new infection called the chronic bee paralysis virus.
Similar patterns of colony losses were reported in the US in 1918 and 1919. These were sometimes called "mystery disease" but 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 stored, but very few or no bees remained. This discovery showed that the loss of bees was not caused by a lack of food.
Since the 1960s, the number of bee colonies kept by beekeepers in the US has been decreasing because of reasons like urban development, pesticide use, mites, and beekeepers retiring. However, in late 2006 and early 2007, beekeepers reported colony losses at an unusually high rate. This led people to use the term "colony collapse disorder" to describe the sudden and widespread disappearance of bees.
Before 2006, bee colony losses had been steady at about 17–20% each year, caused by factors like mites, diseases, and stress from beekeeping practices. In the winter of 2004–2005, a sudden collapse was linked to Varroa mites, though this was never confirmed. The first report of colony collapse disorder was in mid-November 2006 by a beekeeper in Pennsylvania. By February 2007, large beekeeping operations in California, Florida, Oklahoma, and Texas reported heavy losses from colony collapse disorder, with some losing up to 90% of their colonies. Similar losses were also reported in Canada, several European countries, and parts of South and Central America and Asia. In 2010, the US Department of Agriculture reported that about 34% of bee colonies were lost, a number similar to those reported in 2007, 2008, and 2009. Fewer colony losses were reported in the winter of 2013–2014 compared to recent years, with 23.2% of colonies lost nationwide.
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 to the pollinator industry through the 2014 Farm Bill. This law allowed up to $20 million each year to be used for protecting honeybees, livestock, and farmed fish that suffer losses from disease, weather, or other problems. In 2017, Congress added more funding to help 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 US "remained relatively stable," but 48% of colonies were lost during the year ending April 1, 2023. The average annual loss over 12 years was 39.6%. The previous year (2021–2022) saw a 39% loss, and the year before that (2020–2021) had a 50.8% loss. Beekeepers told researchers that a 21% loss during winter is considered normal, and more than three-fifths of beekeepers surveyed said their losses were higher than in 2022–2023.
In 2024, the US Census of Agriculture reported a record high in commercial honey bee hives, mostly in Texas. These hives are now 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 infestation, poor nutrition, and diseases. CCD is suspected when there are very few adult bees left in a hive. Unlike other sudden causes of bee deaths, such as pesticide exposure, there are usually no dead bees found near the hive, as if the hive was abandoned. A hive that has collapsed from CCD usually shows these signs at the same time:
- Capped brood cells are present in the abandoned hive. Bees typically do not leave a hive until all the capped brood has hatched.
- Food stores, such as honey and bee pollen, remain in the hive. Other bees do not quickly take the food, and pests like wax moths and small hive beetles attack the hive much later than usual.
- The queen bee is still present. If the queen is missing, the hive likely died because it had no queen, which is not considered CCD.
- No dead honey bee bodies are found near the hive.
Symptoms that may appear before a hive collapses include:
- The hive cannot care for its brood because there are not enough worker bees.
- The hive has mostly young adult bees.
- Bees do not want to eat food given to them, such as sugar syrup or protein supplements.
Genetic and physio-pathological predictions
Before any visible signs of colony collapse disorder (CCD) appear, certain physical and health-related signs can indicate colony health and predict whether a colony is likely to experience CCD. Bees in collapsing colonies often have soft feces, half-filled rectums, rectal stones (also called rectal enteroliths), and a shiny or colorful appearance in their Malpighian tubules. A weak or damaged rectum may signal problems with nutrition or water balance, while rectal stones suggest issues with the excretory system that could lead to constipation and poor regulation of body fluids in CCD bees. These signs occur in varying degrees among four different age groups of bees: newly emerged bees, nurse bees, non-pollen foragers, and pollen foragers. These signs were found not to be related to the age of the bees.
In addition, genetic changes in the gut of honey bees can indicate susceptibility to CCD. Scientists have identified 65 specific RNA molecules that may be linked to CCD. The activity of these RNA molecules changes compared to healthy bees, either increasing or decreasing depending on the gene involved. Tests using microarray analysis and qPCR found an unusual amount of ribosomal RNA (rRNA) fragments with poly(A)-rich 3′ tails in the guts of CCD bees. These findings suggest that these special RNA fragments may help in the breakdown of proteins and the function of rRNA. Also, 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 there were 2.44 million honey-producing hives in the United States in February 2008. 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 managed hives, as they exclude hives used only for pollination contracts and hives managed by beekeepers with fewer than 5 hives. Some hives may be counted more than once if they are moved to different states to produce honey.
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% met the criteria for CCD, which is defined as 50% or more of dead colonies being found without bees or with very few dead bees. In 2006–2007, beekeepers experiencing CCD had a total loss of 45% of their colonies, compared to 25% for beekeepers not affected by CCD.
A 2007–2008 survey of over 19% of all U.S. colonies found a total loss of 35.8%. Operations that pollinated almonds had the same average colony loss as those that did not. Beekeepers who reported colonies dying without bees had a total loss of 40.8%, compared to 17.1% for those who did not experience this symptom. Large operations were more likely to report this symptom, which may suggest a contagious condition is involved. About 60% of dead colonies reported in this survey were found without dead bees in the hive, possibly indicating CCD.
Between 2007 and 2013, annual winter colony losses in the U.S. doubled from 15% before CCD was identified to 30%. Loss rates dropped to 24% from 2014 to 2017, and CCD symptoms were less commonly linked to hive losses. While CCD increased hive losses, honey bee numbers in the U.S. remained stable or grew after CCD was identified.
In 2017, NASS reported that U.S. hives ranged between 2.63 and 2.99 million for operations with more than five colonies, and 35–43 thousand hives for those with fewer than five colonies. Operations with more than five colonies lost 77.8 thousand hives (2.6–3.0%) with CCD symptoms, while those with fewer than five colonies lost 6 thousand hives (14–17%) with CCD symptoms.
By 2022, the number of U.S. colonies reached 3.8 million, a 31% increase since 2007, according to NASS. This growth was largely due to the rise of small producers in Texas.
In 2007, the United Kingdom had 274,000 hives, Italy had 1,091,630, and France had 1,283,810. In 2008, the British Beekeepers Association reported a 30% drop in the UK’s bee population between 2007 and 2008. An EFSA study found Italy had a mortality rate of 40–50%, but these figures are not reliable because countries used different methods to collect bee population data. Reports from 2008 linked high bee deaths to the varroa mite, wet summers, and pesticides.
In 2009, Tim Lovett of the British Beekeepers’ Association said beekeeper losses varied greatly, with some losing nearly a third of their hives and others losing none. John Chapple of the London Beekeepers’ Association reported losses among his 150 members ranged from a fifth to a quarter. He noted many hive disappearances remained unexplained. The UK’s National Bee Unit denied the existence of CCD, attributing losses to the varroa mite and rainy summers.
In 2010, David Aston of the British Beekeepers’ Association stated that while CCD was better defined, it was not believed to cause colony losses in the UK. He noted that recent studies suggested complex interactions between factors like pathogens, environmental conditions, beekeeping practices, and other stressors caused honey bee losses similar to CCD in the U.S.
In Scotland, beekeeper Andrew Scarlett lost 80% of his 1,200 hives during the 2009–2010 winter. He blamed the loss on a bacterial infection that spread due to a lack of bee inspectors and poor weather that prevented bees from gathering food.
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 in the country.
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 factor.
In May 2012, the Swiss government reported that about half of the bee population did not survive the winter, with the main cause being the Varroa destructor parasite.
In China, a three-year survey from 2010 to 2013 found an average colony loss of 10.1%. Comb renewal and queen-related problems were identified as significant risk factors.
Possible causes
The causes of Colony Collapse Disorder (CCD) are not fully understood, but scientists are studying many possible factors. These include 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 alone, but a combination of these factors may contribute to the disorder.
In 2006, a group called the Colony Collapse Disorder Working Group (CCDWG) was formed, mostly at Pennsylvania State University. Their early report found some patterns but did not draw clear conclusions. A 2007 survey of beekeepers showed that hobbyist beekeepers often thought starvation was the main cause of colony deaths, while commercial beekeepers believed invertebrate pests, such as 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 mystery.
In July 2007, the U.S. Department of Agriculture (USDA) created a CCD Action Plan. This plan included four steps: collecting data, analyzing samples, doing research based on hypotheses, and taking actions to prevent or reduce CCD. In 2009, the first report from the U.S. Colony Collapse Disorder Steering Committee said that CCD might result from the combined effects of many factors. That same year, the CCD Working Group published a study showing that no single factor was consistently linked to CCD. However, bees in CCD colonies had higher levels of disease-causing agents and were infected with more pathogens than healthy bees, suggesting they might be more exposed to diseases or have weaker defenses.
In 2010, the Steering Committee reported that no single cause was responsible for CCD. They found that colonies collapsing from CCD often had low levels of Nosema parasites or Varroa mites at the time of collapse. However, they did find that some pesticides, like coumaphos and fluvalinate (used to control mites), and others like neonicotinoids and fungicides, could harm bees’ immune systems, making them more likely to get sick from viruses.
A 2015 review of 170 studies on CCD and bee stressors concluded that the interaction of parasites, pesticides, and poor nutrition is likely a major cause of bee health problems. 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 the high levels of disease-causing agents in adult bees suggested their immune systems might be suppressed. Researchers linked this to Varroa mites, which carry viruses like deformed wing virus and may work with bacteria to weaken bees’ defenses.
Parasites, such as Varroa mites, tracheal mites, fungi, bacteria, and viruses, have appeared in bee colonies in the U.S. in the last 20 years. When a colony dies, nearby healthy colonies may enter the dying hive to steal food. If the food is contaminated, it could make the healthy colonies sick, mimicking a disease. However, in typical CCD cases, the food is not stolen, suggesting that toxins are not spread this way.
Other evidence that CCD might act like a disease came from observations that healthy bees could only be placed in hives that had previously had CCD if the hives were first treated with radiation to destroy DNA. Also, CCD-affected hives often appeared near each other in bee yards.
In 2007, scientists noted that Varroa destructor mites are the most dangerous threat to bees worldwide. These mites carry viruses, like deformed wing virus and acute bee paralysis virus, which are linked to CCD. They also weaken bees’ immune systems. A 2007–2008 study of 413 bee colonies in Ontario, Canada, found that 85% of winter colony deaths were linked to Varroa mites. The mites also harm queens’ ability to reproduce, which can destroy hives. While Varroa mites are a likely cause of CCD, not all dying colonies have them.
Varroa destructor mites live in beehives and feed on bees’ hemolymph (a fluid similar to blood). They attach to nurse bees during their life cycle and later feed on larvae. This feeding helps the mites reproduce. Because Varroa mites can harm all types of bees, they are a major threat, especially during winter.
In 2020, scientists began testing a genetically modified bacterium that could reduce Varroa mite survival and suppress infection by deformed wing virus.
In 2004, a virus called Israeli acute paralysis virus (IAPV) was discovered in Israel. At one point, it was thought to cause CCD. A 2007 study found that IAPV was present in 25 of 30 CCD colonies but only in one of 21 non-CCD colonies, linking it more strongly to CCD.
Management
As of 1 March 2007, the Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC) provided the following suggested advice for beekeepers observing signs of colony collapse disorder (CCD):
- Do not merge colonies that are dying with healthy colonies.
- If a colony has collapsed, store its equipment in a place where bees cannot reach it, and take steps to prevent further problems.
- When feeding bees sugar syrup, add Fumagillin to the mixture.
- If a colony has collapsed and shows signs of a secondary infection, such as European Foulbrood, treat the colony with oxytetracycline instead of tylosin.
Another 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. Native bees can be encouraged to live and grow by offering them safe places to nest and planting extra crops that provide food 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 they remain vulnerable to other causes of colony collapse. However, these bees have traits that make them less useful for large-scale beekeeping.
In the United Kingdom, a national bee database was created in March 2009 to track colony losses after a 15% drop in bee numbers 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 harming the honey industry. All 20,000 beekeepers in Britain were invited to join the program. In October 2010, David Aston of the British Beekeepers' Association said, "We still believe colony collapse disorder is not the main reason for bee losses in the UK. However, we are still seeing colony losses, many of which have clear causes. UK beekeepers are focusing on improving bee health by identifying and reducing factors that harm colonies. This includes training beekeepers, addressing habitat loss that limits food sources for bees, and researching diseases and conditions affecting bees in the UK."
Economic and ecological impact
Honey bees are not originally from the Americas. In the United States and other parts of the Western Hemisphere, they are only used to pollinate crops and ornamental plants because native plants do not depend on honey bees for pollination, except in large fields with only one type of plant. In these fields, 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 almonds was $3.6 billion. In 2000, the total value of U.S. crops that relied entirely on honey bee pollination was over $15 billion. California almond production grew from 370 million pounds in 1995 to 2.5 billion pounds in 2019, with a 30% increase in the last decade alone. Because of the high demand for pollination, the cost of renting honey bees has risen. During the spring, California’s almond industry rents about 1.6 million honey bee colonies. Worldwide, honeybees contribute about $200 billion in pollination services each year.
Honey bees 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 specifically require them. If honey bees are not present, native pollinators may take their place, as they are often better suited to local plants.
Although other species of bees may be more efficient at pollinating individual plants, honey bees are more useful for the 30% of crops that depend on them. Native pollinators are harder to use on a large scale because they may not visit the plants at all. Beehives can be moved between crops, and honey bees visit many plants in large numbers, making up for lower efficiency through high numbers. The success of these crops depends heavily on the beekeeping industry. In China, hand pollination of apple orchards is very hard, time-consuming, and expensive.
In regions where honey bees are native, such as parts of the Old World, they are important for pollinating plants and helping sustain natural habitats. 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, and weather. Plants that need honeybees will suffer more if their numbers drop, while plants that use other pollinators, wind, or self-pollination will be less affected.
Honeybees pollinate about 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 could be lost, and this is only for one region. Farms with large, dense crop areas depend most on honeybees, as they rely heavily on their pollination services. In the U.S. alone, this costs $1.25 billion annually. However, honeybees as pollinators generate between 22.8 and 57 billion Euros globally each year.
In popular culture
- A 2007 episode of Nature titled "Silence of the Bees" presented several possible reasons for the phenomenon.
- The 2009 documentary Vanishing of the Bees suggested that neonicotinoid pesticides were the most likely cause, though experts interviewed in the film admitted no strong evidence had been found.
- The 2010 documentary Queen of the Sun: What Are the Bees Telling Us? included interviews with beekeepers, scientists, farmers, and philosophers.
- In the "Kwanzaa" segment of the Futurama episode "The Futurama Holiday Spectacular" (season 6, episode 15, first aired 11/21/2010), the show depicted CCD—called "Colony Collapse Syndrome"—in a hive of giant space bees when the Planet Express crew visited the hive to collect beeswax for Kwanzaa candles.
- The 2012 documentary Nicotine Bees claimed that neonicotinoid pesticides were mainly responsible for colony collapse disorder.
- The 2012 film More Than Honey explored the relationship between humans and bees and examined possible causes of CCD.
- In season 3 of the TV series Elementary, CCD was a recurring topic. In episode 10, Holmes blamed pesticides, and in episode 14, he proposed possible solutions. In episode 23, titled "Absconded," Holmes and Watson investigated the death of a USDA researcher who was studying a CCD outbreak in the Northeast United States.
- The 2016 short film Colony Collapse Disorder: A Life Without Bees showed a dramatic, futuristic world where life without bees had severe consequences.
- The Black Mirror episode "Hated in the Nation" depicted a future in which mechanical bees were created to address CCD.
- In the Cloak & Dagger episode "Funhouse Mirrors," characters Tandy Bowen and Mina Hess discussed the decline of American bumblebees over time. The season 1 finale was titled "Colony Collapse."
- In the 2025 movie Bugonia, a character named Teddy believes the phenomenon is caused by the CEO of a biomedicine company, whom he thinks is an alien. In his view, CCD reflects the idea of humans being gradually erased from Earth by an alien race.