Honey Bee Colony Collapse Disorder: A Literature Review

colony collapse disorder
Photo by Yvan leduc via Wikipedia.

Editor’s Note: There is so much information out there on Colony Collapse Disorder. Wouldn’t it be nice if someone summarized it in one place? Kyle Bailey, undergraduate in biology at Iowa State, has done just that. The following, posted with permission, is an up-to-date review of CCD research. It includes information from a variety of sources, from fact sheets to peer-reviewed journal articles.


Honeybees (apis mellifera) are the primary pollinator available to agriculturalists in the United States. This makes them a critical part of US agriculture.  Crops such as “almonds (82% of the world’s supply and 100% dependent on interstate pollinators); apples; cherries; blueberries; broccoli; carrots; cranberries; cucurbits like cucumber, melons, squash, pumpkins, and gourds” (Stankus 2008) are heavily reliant on honey bees for pollination.  Traveling hives provided by commercial apiary services pollinates many of these crops.

A current epidemic, called Colony Collapse Disorder (CCD), affecting honeybee hives throughout the US threatens the apiarist industry.  In the US during 2006-2007 29% of beekeepers reported some loss to CCD with some losing up to 75% of their stock (Winfree, Williams, Dushoff, et al).  CCD is characterized as a mysterious loss of worker bees in the hive.  There are no corpses to be found as the bees apparently wander far from the hive to die.  The hive generally has sufficient food stores to maintain the population.  The hives also generally still have undeveloped brood stock.  The new brood (as well as the queen) is of course doomed without any adult workers present to care for them and they soon die.  Because the bees travel far from the hive there are no bodies to necropsy and attempt to determine a cause (Stankus 2008).

This paper will explore the US economic and agricultural impacts of pollinator loss, and recent research into the causes of and potential solutions to CCD.

US Economic and Agricultural Impacts

The monoculture nature of agriculture tends to produce large numbers of flowers that all need pollinating simultaneously. A lack of honeybee colonies available to ship and set up for pollinating the variety of crops throughout the US will have a major impact on production.  Dr. Caird Rexroad, an associate administrator of agricultural research for the United States Department of Agriculture, in testimony before the United States House of Representatives Agriculture Committee states:

“CCD poses a problem for many segments of the agricultural community, particularly the pollination industry and many growers that depend on pollinating services.  In total, bee pollination is responsible for $15 billion in added crop value, particularly for specialty crops such as almonds and other tree nuts, berries, fruits, and vegetables.  The California almond crop alone requires 1.3 million colonies of bees, a need that is projected to grow significantly by 2010.  Due to CCD, the bee industry is facing great difficulty meeting the demand of almond producers.  If researchers are unable to solve the problem and beekeepers are unable to meet demands for this and other crops, agriculture will be significantly impacted.” (2007).

Recent Research on CCD

CCD is far from explained.  There is apparently no single explanatory factor.  There is strong evidence, however, that it is biologically transmitted (Cox-Foster, Conlan, Holmes, et.al.). It would appear to be a combination of factors.  Most of them well known and others new, emerging, or as yet unknown.  CCD is however strongly associated with hives that have been under stress from any of a number of known stressors (Stankus 2008).  These include mites, bacteria, fungi, viruses, protozoa, and insecticides.  The various fungi, and bacteria are not thought to be major contributors to CCD directly.  A major indicator for CCD is, however, hive stress and any infection or infestation could contribute.

There are two mites that are of significant impact to A. mellifera.  They are Varroa destructor and Acarapis woodi. A. woodi is a very small mite that lives in the tracheal tubes of the adult worker honeybee (http://www.sel.barc.usda.gov/acari/frames/beemites.html).  It is also associated with additional bacterial infections (Stankus 2008).  V. destructor is by far the more important mite and is more strongly associated with CCD.  V. destructor is a mite that primarily infects the brood while it is still capped off in the comb.  When out of the comb such as when the colony is over wintering and there is no brood left the mite infests the adult worker bee piercing the exoskeleton on the back and sucking hemolymph (Bowen-Walker, Martin, and Gunn 1996). V. destructor is also associated with additional infections, this time viral. Infestation by V. destructor affects bee size, weight, population, timeliness of emergence, lifespan and even the ability of bees to learn (Stankus 2008).

Viruses affecting honeybees are more diverse.  There are at least 15 serious strains.  Strongly associated with Varroa mite infestation is deformed wing virus (DWV).  DWV is usually spread by the mites to developing larvae who develop small non-functional wings.  The resulting adult can crawl but not fly.  It has also been shown that the learning ability of bees may be affected (Stankus 2008).

A 2007 study looked at samples from 51 separate colonies, all of them mobile. In all 25 hives suffering from CCD they found Israeli acute paralysis virus (IAPV) and they found the virus in only one healthy hive.  This strongly correlates IAPV with CCD (Cox-Foster, Conlan, Holmes, et al.).  The causal relationship of IAPV to CCD is currently under study (Cox-Foster 2008).  Vertical transmission from Queen to offspring has also been shown for a variety of viruses (Chen, Pettis, Collins et al. 2005).

The most common protozoans found in honeybees are cryptosporidian called Nosema apis and a close cousin Nosema ceranae. N. ceranae is a more serious disease and is jumping the species barrier from Asian bees (Apis ceranae) to European bees (Apis mellifera). N. ceranae reduces hive survivability to one in six (Martin-Hernandez, Meana, Prieto, et al. 2007).  Given the recent emergence of N. ceranae and the uncanny similarity in hive survival rates, the prospect of finding a link to CCD seems promising (Stankus 2008).

Certain pesticides in wide use in the US have also been suggested to be players.  Specifically a class of pesticides called neonicotinoids.  The most widely used of these in the US is imidacloprid.  It is used as a seed coat and can show up in plant tissues such as pollen and nectar in low doses.  It is known to be toxic to bees, but when used in this way the bees receive a sub-lethal dose. One of the principal effects of imidacloprid on honeybees is a loss of learning ability (Decourtye, Lacassie, and Pham-Delegue 2003).  Learning ability in bees is considered critical for the hive to continue thriving (Stankus 2008).  The use of neonicotinoid pesticides varies widely by region, but the occurrence of CCD is fairly uniform. The manufacturer of imidacloprid has released a press release strongly denying its product plays any part in CCD and suggesting studies that show this to be true (Bayer CropScience, 2008).

Dr. Cox-Foster, one of the leading researchers in CCD also suggests the unnatural diet bees are subjected to may be a factor.  One day bees can be in a field with nothing but almonds, another day nothing but watermelon, and in between fed an artificial sugar syrup.  This is not the diet bees evolved with and as such may be a stressor.  She also mentioned the practice of frequent hive splitting.  This produces new hives more often than bees would choose to do so on their own.  The last possible factor mentioned is the decrease in genetic diversity.  Beekeepers who have some Africanized bees have not suffered from CCD (Bodnar 2008).

Possible Solutions

There is a study looking at how Africanized bees seem to be resistant to many of the diseases currently stressing European bees (Frazier Tumlinson, Tomasko 2008).  One possibility is to breed resistance into our bees.

There is also the possibility of moving away from our dependence on a single species to do all of our pollinating.  Unfortunately not many other bees are social so keeping them in very large numbers is difficult.  The solitary bees tend to wander away when they perceive their population is too high. One study currently under way has as one of its main goals to “Improve management of bumble bee pollinators through research aimed at identifying factors believed to affect worker pollen foraging and pollination efficiency.” (Delaplane Visscher,Eitzer 2008).  In some areas native pollinators may be able to pick up the slack and provide sufficient pollination (Winfree, Williams, Dushoff, et al. 2007).

Depending on the findings of some current studies, we may simply find that a few changes in our managements of bees could make all the difference.  The careful use of novel miticides, maintaining more diverse food sources such as wild flowers in proximity to the crops we want pollinated, and maintaining a larger portion of the bee population as stationary hives instead of mobile operations that move state to state would all seem to be prudent, easy, and inexpensive first steps to staving off CCD.


CCD is obviously an important disease.  It is currently a major area of study and our government through the USDA is pouring millions of dollars into research projects all over the country.  At this point we are just beginning to understand the possible mitigating factors to CCD and how they may interplay with each other.  The coming few years will likely be hard ones on the apiary and agricultural industries.  Hopefully, solutions will be swift in coming and cheap in implementing.

Works Cited

Bee safety and Colony Collapse Disorder. (2008) Retrieved November 15, 2008

Bodnar, A. Colony Collapse Disorder (2008) Retrieved November 18, 2008

Chen, Y. P., Pettis, J. S., Collins, A., Feldlaufer, M. F. (2006). Prevalence and Transmission of Honeybee Viruses. [Electronic version] Applied And Environmental Microbiology,72, 606-611.

Cooperative State Research Education and Extension Service (2008) Colony Collapse Disorder – Determination Of Role Of Pathogens In Unique-Colony Losses Of Honey Bees And Funding Of Workshop On Ccd Retrieved November 15, 2008

Cooperative State Research Education and Extension Service (2008) A New Collaboration To Understand African Bee Biology, Ecology, And Management As A Key To Sustaining Honey Bee Health In The U.S. Retrieved November 15, 2008

Cooperative State Research Education and Extension Service (2008) SUSTAINABLE SOLUTIONS TO PROBLEMS AFFECTING HEALTH OF MANAGED BEES Retrieved November 15, 2008

Cox-Foster, D.L.,Conlan, S., Holmes, E.C., Palacios, G., Evans, J.D., Moran N.A. (2007). A Metagenomic Survey of Microbes in Honey Bee Colony Collapse Disorder. Science 318, 283-287

Decourtye, A., Lacassie, E., Pham-Dele`gue M. (2003) Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Management Science 59, 269-278

Martı´n-Herna´ndez, R., Meana, A., Prieto, L.,  Salvador, A. M., Garrido-Bailo´n, E., Higes M. (2007). Outcome of Colonization of Apis mellifera by Nosema ceranae. 73(20), 6331-6338.

P. L. BOWEN-WALKER, S. J. MARTIN, A. GUNN (1996). Preferential distribution of the parasitic mite, Varroa jacobsoni Oud. on overwintering honeybee (Apis mellifera L.) workers and changes in the level of parasitism. Parasitology, 114, 151-157

Stankus, T. (2008).  A Review and Bibliography of the Literature of Honey Bee Colony Collapse Disorder: A Poorly Understood Epidemic that Clearly Threatens the Successful Pollination of Billions of Dollars of Crops in America. Journal of Agricultural & Food Information. 9(2), 115-143.

Subcommittee On Horticulture And Organic Agriculture Of The Committee On Agriculture House Of Representatives (1997) Review Colony Collapse Disorder In Honey Bee Colonies Across The United States (36-465 PDF) Washington, DC: U.S. Government Printing Office

“Tracheal Mites” Tarsonemidae. (n.d.) Retrieved November 16, 2008

Winfree, R., Williams, N., Dushoff, J., Kremen, C. (2007) Native bees provide insurance against ongoing honey bee losses. Ecology, 10, 1105-1113



  1. Thank you for the summation! This is more important than the Pay Raise in Penna. and the book Fruitless Fall claims that the international losses last year were at least forty percent of the surveyed hive owners responding. The food increases have been about 37% which unfortunately, many are attributing to the cost of fuel only.

  2. Just curious, the increase in disappearances seems to track the increased lull in solar activity. You mention that they wander off. If I remember correctly they navigate via magnetic fields and sun position. Has anyone looked to see if there is a correlation here?

  3. Colony collapse is caused by artificial hives.
    Unhygienic hives create a breeding ground for bee illnesses and explain the many illnesses attributed to “colony collapse disorder”.

    The design of domestic (artificial) bee hives make bees vulnerable to pests (for an illustration see http://vandermerwe.co.nz/?p=8 )

    Organic and in-organic dirt land at the bottom of the beehive (the hive entrance). Bees walk in and out over accumulated dirt, providing an ideal opportunity for Varroa, pests and disease to spread.

    The hive is an ecosystem that include bees and bee pests. The introduction of the artificial hive has changed this ecosystem, allowing pests to evolve their behavior to gain a competitive advantage. This explains the delay since the introduction of artificial hives and the onset of colony collapse disorder.

    Kris van der Merwe

  4. Adelaide, I don’t know what you mean by “Pay Raise in Penna”, please elaborate. Fruitless Fall was an excellent book.

    W, I don’t know if any solar activity / bee interaction has been discovered. If you find anything interesting, please let me know.

    Kris, I agree. Environmental stress is certainly a factor in CCD. I hope your hive design allows your bees to be healthier. Perhaps you could do an experiment with some hives having the empty floor and others having a normal floor, then share your findings with other bee keepers.

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