colony collapse disorder (CCD)
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Colony loss and economic impact
The unexplained loss of honeybee colonies that came to be known as CCD was first reported in the fall of 2006 by a commercial beekeeper from Pennsylvania, U.S., who was overwintering his colonies in Florida. (Subsequent investigations suggested that beekeepers had experienced unexplained colony losses for at least the previous three years; similar losses had been reported previously as well, including in the late 19th century and in various decades of the 20th century.) By February 2007 several large commercial migratory beekeeping operations in the United States had reported cases of CCD, with some operators suffering the loss of 50–90 percent of their colonies. Many of these larger operations were overwintering their colonies in California, Florida, Oklahoma, and Texas. By late February 2007 some nonmigratory operations located in the mid-Atlantic region and the Pacific Northwest of the United States also had reported the loss of more than 50 percent of their colonies. The absence of dead bees in the affected hives made initial investigations difficult and inconclusive. That same year, other countries, including Canada, Portugal, Italy, Spain, Greece, Germany, Poland, France, and Switzerland, also reported substantial losses of honeybees. From 2006 to 2011 total annual colony losses in the United States averaged around 33 percent; beekeepers cited CCD as the cause of roughly one-third of those losses.
Beekeeping is a critical component of modern agriculture. CCD not only threatens the beekeeping operations that provide pollination service and honey production but also has the potential for crippling the production of the many crops that are dependent on honeybees for pollination. In the United States, beekeepers provide pollination service for more than 90 commercially grown crops, including many fruits and vegetables. The economic value of U.S. crops that benefit from honeybee pollination has been estimated at $15 billion annually. In 2006 the California almond export crop alone was valued at $1.9 billion and required more than one million bee colonies for pollination (out of a total of about 2.6 million colonies in the United States). With the number of available colonies for crop pollination in the country in decline, the beekeeping industry faced a tremendous challenge in meeting the demand for pollination services.
Suspected causes
The Agricultural Research Service of the U.S. Department of Agriculture organized efforts to address the CCD crisis through surveys and data collection, samples analysis, and mitigation and preventive measures. A variety of possible causes of CCD were suggested. They included chemical contamination of colony food stores or beeswax; poisoning from pesticides, including insecticides based on nicotine derivatives (neonicotinoids, the use of which has been restricted in some countries); the introduction of genetically modified crops (see genetically modified organism); possible lack of genetic diversity in colonies; and infection of colonies by pathogens or parasites, including known honeybee parasites such as the single-celled microsporidian (parasitic fungus) Nosema ceranae and the invasive varroa mite (Varroa jacobsoni).
While some of these suggestions were discounted, a 2007 study stated that Israeli acute paralysis virus (IAPV) appeared to be strongly associated with the disorder. The virus—which was first identified in Israel—had not been previously reported in the United States, but a subsequent genetic screening of preserved honeybee specimens showed that IAPV had been present in honeybees in the United States since at least 2002. A study in 2008 determined that there were three types of the virus and that two of them had infected honeybees in the United States. Although the virus was a consistent marker of CCD, a cause-and-effect relationship had yet to be established.
Many scientists suspect that CCD might be the result of a combination of two or more pathogens or stressors. Bee colonies are commonly found to be infested with pathogens and parasites, and the investigation of the interactions of all the possible causative agents has proved to be a challenge for bee scientists. In 2010 researchers reported that colonies affected by CCD in different regions of the United States were coinfected with an agent known as invertebrate iridescent virus (IIV; an iridovirus) and the fungus Nosema. The researchers used a technique known as mass spectrometry-based proteomics (MSP) to identify proteins isolated from healthy and CCD-affected colonies. This approach led to the discovery of two RNA viruses (varroa destructor-1 virus and Kakugo virus) that were previously unknown pathogens of honeybees in North America, as well as to the identification of IIV in bees from hives that were in the process of succumbing to CCD. These bees were also found to be coinfected with Nosema. In contrast, healthy bee colonies did not show evidence of coinfection with IIV and Nosema. However, while the two pathogens were consistently found together, whether their coinfection caused CCD or whether colonies with the disorder were rendered more susceptible to coinfection remained unclear.
In 2012 scientists reported that the phorid fly Apocephalus borealis was capable of parasitizing honeybees, causing them to abandon their hives and then die shortly thereafter. Honeybees from parasitized hives commonly were infected with N. ceranae and deformed wing virus. Many of the phorid larvae that emerged from dead bees were also found to be infected with these pathogens, suggesting that phorid flies may serve as a reservoir for the agents, transmitting them to bees upon parasitization. The hive abandonment behaviour observed in association with phorid flies indicated a possible link between the flies and CCD.
The full sequence of the honeybee genome, which was published in late 2006, was a technological advance that could conceivably help in discovering the underlying cause of CCD in honeybees. Knowledge of the sequence made available new molecular approaches and introduced honeybee genomics to the investigation of CCD. It also enabled scientists to study the impact of the possible causal agents on specific genes and honeybee colony health. Likewise, the advance might help identify new pathogens in honeybees and unravel the complex effects of multiple combinations of pathogens and environmental toxins.
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