Colony collapse disorder
Colony collapse disorder (CCD) is an abnormal phenomenon that occurs when the majority of worker bees in a honey bee colony disappear, leaving behind a queen, plenty of food, and a few nurse bees to care for the remaining immature bees.[1] While such disappearances have occurred sporadically throughout the history of apiculture, and have been known by various names (including disappearing disease, spring dwindle, May disease, autumn collapse, and fall dwindle disease),[2] the syndrome was renamed colony collapse disorder in early 2007[3] in conjunction with a drastic rise in reports of disappearances of western honey bee (Apis mellifera) colonies in North America.[4] Beekeepers in most European countries had observed a similar phenomenon since 1998, especially in Southern and Western Europe;[5][6] the Northern Ireland Assembly received reports of a decline greater than 50%.[7] The phenomenon became more global when it affected some Asian and African countries as well.[8][9] From 1990 to 2021, the United Nation’s FAO calculated that the worldwide number of honeybee colonies increased 47%, reaching 102 million.[10]
Colony collapse disorder could cause significant economic losses because many agricultural crops worldwide depend on pollination by western honey bees. According to FAO, the total value of global crops pollinated by honey bees was estimated at nearly US$200 billion in 2005.[11] In the United States, shortages of bees have increased the cost to farmers renting them for pollination services by up to 20%.[12] Declining numbers of bees predate CCD by several decades, however: the US managed hive industry has been shrinking at a steady pace since 1961.[13]
In contrast, the bee population worldwide has been increasing steadily since 1975, based on honey production, with China responsible for most of the growth.[14] The period of time with the lowest growth in worldwide honey production was between 1991 and 1999, due to the economic collapse after the dissolution of communism in the former Soviet sphere of influence.[13] As of 2020, the production has increased further by 50% compared to 2000, double the rate of growth in previous decades, notwithstanding CCD.[15] Experts estimate that there are currently more honey bees alive worldwide than at any other point in human history.[16]
Several possible causes for CCD have been proposed, but no single proposal has gained widespread acceptance among the scientific community. Suggested causes include pesticides;[17] infections with various pathogens, especially those transmitted by Varroa and Acarapis mites; malnutrition; genetic factors; immunodeficiencies; loss of habitat; changing beekeeping practices; or a combination of factors.[18][19] A large amount of speculation has surrounded the contributions of the neonicotinoid family of pesticides to CCD, but many collapsing apiaries show no trace of neonicotinoids.[19]
History[edit]
Colony collapse disorder is a syndrome defined by a specific set of symptoms which, in the past several decades, has been given many different names (among them "disappearing disease", "spring dwindle", "May disease", "autumn collapse", and "fall dwindle disease").[2] The cause of these symptoms has never been determined. Only very recently, upon recognition that the syndrome does not seem to be seasonally restricted, and that it may not be a "disease" in the standard sense—that there may not be one specific causative agent or pathogenesis—was the syndrome renamed.[3]
Limited occurrences resembling CCD were documented as early as 1869.[20][21] A well-documented outbreak of colony losses spread from the Isle of Wight to the rest of the UK in 1906. These losses were later attributed to a combination of factors, including adverse weather, intensive apiculture leading to inadequate forage, Acarine (tracheal) mites, and a new infection, the chronic bee paralysis virus,[22] but during the outbreak, the cause of this agricultural beekeeping problem was unknown.[23]
Reports show similar behavior in hives in the US in 1918[24] and 1919.[25] Coined "mystery disease" by some,[26] it eventually became more widely known as "disappearing disease".[27] Oertel, in 1965,[28] reported that hives afflicted with disappearing disease in Louisiana had plenty of honey in the combs, although few or no bees were present, discrediting reports that attributed the disappearances to lack of food.
In the US, the number of colonies maintained by beekeepers had been in decline since the 1960s, for various reasons including urbanization, pesticide use, tracheal and Varroa mites, and commercial beekeepers retiring and going out of business.[13] However, in late 2006 and early 2007, the rate of attrition was alleged to have reached new proportions, and people began to use the term colony collapse disorder to describe the sudden rash of disappearances (or sometimes spontaneous hive collapse or the Mary Celeste syndrome in the United Kingdom).[29]
Losses had remained stable since the 1990s at 17–20% per year, attributable to a variety of factors, such as mites, diseases, and management stress.[30] In the winter of 2004–2005, a spontaneous collapse occurred and was attributed to varroa mites (the "vampire mite" scare), though this was ultimately never confirmed. The first report classified as CCD was in mid-November 2006 by a Pennsylvania beekeeper overwintering in Florida.[3] By February 2007, large commercial migratory beekeepers wintering in California, Florida, Oklahoma, and Texas had reported heavy losses associated with CCD.[30] Their reports of losses varied widely, ranging from 30% to 90% of their bee colonies; in some cases, beekeepers reported losses of nearly all of their colonies, with surviving colonies so weakened that they might no longer be able to pollinate or produce honey.[17] In late February 2007, some larger non-migratory beekeepers in the mid-Atlantic and Pacific Northwest regions also reported significant losses of more than 50%.[30] 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 data on overall honey bee losses for 2010 indicated an estimated 34% loss, which is statistically similar to losses reported in 2007, 2008, and 2009.[17] Fewer colony losses occurred in the US over the winter of 2013–2014 than in recent years. Total losses of managed honey bee colonies from all causes were 23.2% nationwide, a marked improvement over the 30.5% loss reported for the winter of 2012–2013 and the eight-year average loss of 29.6%.[31]
After bee populations dropped 23% in the winter of 2013, the Environmental Protection Agency and Department of Agriculture formed a task force to address the issue.[32] Since 2014, Congress has substantially subsidized the pollinator industry through the 2014 Farm Bill.[33] The 2014 Farm Bill has allowed for up to $20 million worth of subsidies every fiscal year to be put toward conservation of honeybees, livestock, and farm-raised fish that suffer losses due to disease, weather events, or adverse conditions.[34] In 2017, Congress implemented additional funding to protect bees from agricultural pesticide spray and dust applications while they are under contract to provide pollination services.[35] The Agriculture Improvement Act of 2018, also known as the 2018 Farm Bill, increased the monetary cap for the annual financial aid for emergency assistance from $20 million to $34 million.[33]
CCD is not the same as colony decline that can be caused by various issues such as queen health, varroa mite infestation, nutrition, and various diseases.[36] In collapsed colonies, CCD is suspected when it is observed that few adult bees are physically present in the colony. Unlike with other acute causes of die-off such as pesticide exposure, few if any dead bees are found in or near the hive, as if the hive had simply been abandoned.[37] A colony that has collapsed from CCD is generally characterized by all of these conditions occurring simultaneously:[38][39]
Precursor symptoms that may arise before the final colony collapse include:
Genetic and physio-pathological predictions[edit]
Before any symptomatic manifestation of colony collapse disorder, various physio-pathological traits may serve as biomarkers for colony health as well as predict CCD status. Bees of collapsing colonies tend to have a soft fecal matter, half-filled rectums, rectal enteroliths (rectal stones), and Malpighian tubule iridescence. The defective rectum indicates nutritional disruption or water imbalance, whereas rectal enteroliths suggest a malfunction of excretory physiology which might further lead to constipation and poor osmoregulation in CCD bees. These traits express at various degrees across four bee age groups (newly emerged bees, nurse bees, non-pollen foragers, and pollen foragers) and were confirmed not to be associated with age.[44]
In addition, there are genetic indications in the gut that suggest the susceptibility of honey bees to CCD. Sixty-five different RNA transcripts have been determined as potential signs for CCD status. Genetic expression of these transcripts were either upregulated or downregulated depending on genes when comparing them to healthy bees. The abundance of unusual ribosomal RNA (rRNA) fragments containing poly(A)-rich 3′ tails was detected via microarray analysis and qPCR in the guts of CCD bees.[45] This evidence suggests that these poly(A)-rRNA sequences play the role of degradation intermediates to help in protein folding and enzymatic activity of rRNA.[46] Furthermore, the presence of deformed wing virus and Israeli acute paralysis virus as well as the expression of poly(A)-rRNA are genetic indications for the appearance of CCD.[45]