View source for Colony collapse disorder

{{Short description|Aspect of apiculture}}
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{{Use dmy dates|date=September 2020}}
[[File:Honeybee-cooling cropped.jpg|thumb|Honey bees at a hive entrance: one is about to land and another is fanning]]

'''Colony collapse disorder''' ('''CCD''') is an abnormal phenomenon that occurs when the majority of [[worker bee]]s in a [[honey bee]] [[bee colony|colony]] disappear, leaving behind a [[queen bee|queen]], plenty of food, and a few nurse bees to care for the remaining immature bees.<ref>{{Cite web |url=https://www.epa.gov/pollinator-protection/colony-collapse-disorder |title=Colony Collapse Disorder |date=2013-08-29 |website=US EPA |access-date=2019-09-18}}</ref> While such disappearances have occurred sporadically throughout the history of [[Beekeeping|apiculture]], and have been known by various names (including '''disappearing disease''', '''spring dwindle''', '''May disease''', '''autumn collapse''', and '''fall dwindle disease'''),<ref name = "Oldroyd">{{cite journal |last1=Oldroyd |first1=Benjamin P. |title=What's Killing American Honey Bees? |journal=PLOS Biology |volume=5 |issue=6 |at=e168 |year=2007 |pmid=17564497 |pmc=1892840 |doi=10.1371/journal.pbio.0050168 |doi-access=free }}</ref> the syndrome was renamed colony collapse disorder in early 2007<ref name=Prelim>{{cite news |author1=Dennis vanEngelsdorp |author2=Diana Cox-Foster |author3=Maryann Frazier |author4=Nancy Ostiguy |author5=Jerry Hayes |title=Colony Collapse Disorder Preliminary Report |url=http://www.beekeeping.com/articles/us/ccd.pdf |publisher = Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC) – CCD Working Group |page = 22 |date = 5 January 2007 |access-date = 2007-04-24 |archive-url=https://web.archive.org/web/20150925065318/http://www.beekeeping.com/articles/us/ccd.pdf |archive-date=2015-09-25 |url-status=dead}}</ref> in conjunction with a drastic rise in reports of disappearances of [[western honey bee]] (''Apis mellifera'') colonies in North America.<ref>{{Cite journal |title=Colony Collapse Disorder: A Descriptive Study |last1=van Engelsdorp |first1=Dennis |journal=PLOS ONE |date=2009-08-03 |volume=4 |issue=8 |at=e6481 |doi=10.1371/journal.pone.0006481 |doi-access=free |pmid=19649264 |pmc=2715894 |bibcode=2009PLoSO...4.6481V }}</ref> Beekeepers in most European countries had observed a similar phenomenon since 1998, especially in Southern and Western Europe;<ref name=Monde>{{cite news |last1=Dupont |first1=Gaëlle |title=Les abeilles malades de l'homme |url=http://www.lemonde.fr/planete/article/2007/08/29/les-abeilles-malades-de-l-homme_948835_3244.html |access-date=2018-03-23 |work=[[Le Monde]] |date=29 August 2007 |language=fr}}</ref><ref>[https://www.anses.fr/fr/system/files/SANT-Ra-MortaliteAbeilles.pdf Weakening, collapse and mortality of bee colonies; November 2008 – Updated April 2009] anses.fr</ref> the [[Northern Ireland Assembly]] received reports of a decline greater than 50%.<ref>{{cite web |url=https://www.theyworkforyou.com/ni/?id=2009-06-08.9.1 |title=Minutes of Northern Ireland Assembly |via=Theyworkforyou.com |date=8 June 2009 |access-date=2010-06-22}}</ref> The phenomenon became more global when it affected some Asian and African countries as well.<ref>{{Cite web |url=https://www.independent.co.uk/environment/nature/decline-of-honey-bees-now-a-global-phenomenon-says-united-nations-2237541.html |title=Decline of honey bees now a global phenomenon, says United Nations |website=[[Independent.co.uk]] |date=2011-03-10}}</ref><ref>{{Cite web |url=http://www.unep.org/dewa/Portals/67/pdf/Global_bee_colony_disorder_and_threats_insect_pollinators.pdf |archive-url=http://archive.wikiwix.com/cache/20140926182023/http://www.unep.org/dewa/Portals/67/pdf/Global_bee_colony_disorder_and_threats_insect_pollinators.pdf |url-status=dead |archive-date=2014-09-26 |title=Global Honey Bee Colony Disorders and Other Threats to Insect Pollinators}}</ref>  From 1990 to 2021, the United Nation’s [[FAO]] calculated that the worldwide number of honeybee colonies increased 47%, reaching 102 million.<ref>{{cite web |access-date=2 April 2024 |date=2 March 2023 |language=en |publisher=[[Federal Statistical Office of Germany]] |quote=The FAO estimated the number of bee colonies worldwide to be around 101.6 million in 2021. Compared to 1990, this corresponded to an increase of 47% |title=Bee colonies: Worldwide population on the rise |url=https://www.destatis.de/EN/Themes/Countries-Regions/International-Statistics/Data-Topic/AgricultureForestryFisheries/Bees.html |work=International Statistics}}<!-- auto-translated from Spanish by Module:CS1 translator --></ref>

Colony collapse disorder could cause significant economic losses because [[List of crop plants pollinated by bees|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&nbsp;billion in 2005.<ref>[http://www.fao.org/ag/magazine/0512sp1.htm Spotlight: Protecting the pollinators] {{webarchive |url=https://web.archive.org/web/20130708064328/http://www.fao.org/ag/magazine/0512sp1.htm |date=8 July 2013 }}. Fao.org. Retrieved on 2014-04-12.</ref> In the United States, shortages of bees have increased the cost to farmers renting them for pollination services by up to 20%.<ref name=TimesWines>{{cite news |last=Wines |first=Michael |title=Mystery Malady Kills More Bees, Heightening Worry on Farms |url=https://www.nytimes.com/2013/03/29/science/earth/soaring-bee-deaths-in-2012-sound-alarm-on-malady.html |access-date=31 March 2013 |newspaper=[[The New York Times]] |date=28 March 2013}}</ref> Declining numbers of bees predate CCD by several decades, however: the US managed hive industry has been shrinking at a steady pace since 1961.<ref name=Aizen2009/>

In contrast, the bee population worldwide has been increasing steadily since 1975, based on honey production, with China responsible for most of the growth.<ref>{{cite book |last=Ciesla |first=William M. |date=2002 |title=Non-Wood Forest Products from Temperate Broad-Leaved Trees |url=http://www.fao.org/3/y4351e/y4351e08.htm |location=Rome |publisher=[[Food and Agriculture Organization]] |isbn=92-5-104855-X}}</ref> 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.<ref name=Aizen2009>{{cite journal |last1=Aizen |first1=Marcelo A. |last2=Harder |first2=Lawrence D. |date=9 June 2009 |title=The Global Stock of Domesticated Honey Bees Is Growing Slower Than Agricultural Demand for Pollination |url=http://www.fao.org/tempref/AG/Reserved/DAD-Net/Aizen2009CurrentBiolHoneybees.pdf |journal=Current Biology |volume=19 |issue=11 |pages=915–918 |doi=10.1016/j.cub.2009.03.071 |pmid=19427214 |s2cid=12353259 |access-date=10 September 2020|doi-access=free |bibcode=2009CBio...19..915A }}</ref> {{As of|2020}}, the production has increased further by 50% compared to 2000, double the rate of growth in previous decades, notwithstanding CCD.<ref>{{cite web |url=https://www.statista.com/statistics/755215/natural-honey-production-volume-worldwide/ |title=Production volume of natural honey worldwide from 2010 to 2018 (in 1,000 metric tons) |author=<!--Not stated--> |date=24 April 2020 |website=Statista |access-date=10 September 2020}}</ref> Experts estimate that there are currently more honey bees alive worldwide than at any other point in human history.<ref name="Segal2023">{{cite news |last1=Segal |first1=David |last2=Jazbec |first2=Ciril |title=The Beekeepers Who Don't Want You to Buy More Bees |url=https://www.nytimes.com/2023/08/19/business/beekeeping-companies-colony-collapse.html |access-date=3 November 2023 |work=The New York Times |date=19 August 2023}}</ref>

Several possible causes for CCD have been proposed, but no single proposal has gained widespread acceptance among the scientific community. Suggested causes include [[pesticides]],<ref name="CCDPR2010" /> infections with various [[pathogen]]s, especially those transmitted by ''[[Varroa]]'' and ''[[Acarapis woodi|Acarapis]]'' [[mite]]s, [[malnutrition]], [[genetics|genetic factors]], [[immunodeficiency|immunodeficiencies]], [[habitat destruction|loss of habitat]], or changing [[beekeeping]] practices, including a combination of these factors.<ref>{{cite news |url= http://www.3news.co.nz/Multiple-causes-for-colony-collapse---report/tabid/1160/articleID/296401/Default.aspx |work= 3 News NZ |title= Multiple causes for colony collapse – report |date= 3 May 2013 |access-date= 3 May 2013 |archive-url= https://web.archive.org/web/20131029191137/http://www.3news.co.nz/Multiple-causes-for-colony-collapse---report/tabid/1160/articleID/296401/Default.aspx |archive-date= 29 October 2013 |url-status= dead}}</ref><ref name=Cepero2014>{{cite journal |last1=Cepero |first1=Almudena |last2=Ravoet |first2=Jorgen |last3=Gómez-Moracho |first3=Tamara |last4=Bernal |first4=José Luis |last5=Del Nozal |first5=Maria J. |last6=Bartolomé |first6=Carolina |last7=Maside |first7=Xulio |last8=Meana |first8=Aránzazu |last9=González-Porto |first9=Amelia V. |last10=de Graaf |first10=Dirk C. |last11=Martín-Hernández |first11=Raquel |last12=Higes |first12=Mariano |title=Holistic screening of collapsing honey bee colonies in Spain: a case study |journal=BMC Research Notes |date=15 September 2014 |volume=7 |pages=649 |doi=10.1186/1756-0500-7-649 |pmid=25223634 |pmc=4180541 |issn=1756-0500 |doi-access=free }}</ref> 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.<ref name=Cepero2014/>

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== History ==
Colony collapse disorder is a [[syndrome]] defined by a specific set of symptoms that was previously given many different names (among them "disappearing disease", "spring dwindle", "May disease", "autumn collapse", and "fall dwindle disease").<ref name="Oldroyd" /> The cause of these historic collapses has never been determined, but CCD has been described as "[[death by a thousand cuts]] with the most obvious one being ''[[Varroa]]''".<ref>{{cite web | url=https://www.pbs.org/newshour/economy/struggling-beekeepers-stabilize-u-s-honeybee-population-after-nearly-half-of-colonies-died-last-year | title=Struggling beekeepers stabilize U.S. Honeybee population after nearly half of colonies died last year | website=[[PBS]] | date=22 June 2023 }}</ref> After it was recognized that the syndrome does not seem to be seasonally restricted and that it may not be a "disease" in the standard sense—there may not be one specific [[Disease causative agent|causative agent]] or [[pathogenesis]]—the syndrome was renamed in 2007.<ref name=Prelim />

Limited occurrences resembling CCD were documented as early as 1869.<ref>{{cite news|author1=Robyn M. Underwood |author2=Dennis van Engelsdorp |title = Colony Collapse Disorder: Have We Seen This Before?|url=http://ento.psu.edu/pollinators/publications/underwood | publisher = The Pennsylvania State University, Department of Entomology|access-date = 2010-05-02}}</ref><ref>{{cite news|url=http://www.cosmosmagazine.com/node/1087?page=1|title=Mystery of the dying bees|author=Benjamin Lester|work=[[Cosmos (Australian magazine)|Cosmos]] |date=7 March 2007|url-status=dead|archive-url=https://web.archive.org/web/20080324131409/http://www.cosmosmagazine.com/node/1087?page=1|archive-date=24 March 2008}}</ref> Colony collapses were called "May Disease" in Colorado in 1891 and 1896.<ref>https://nature.berkeley.edu/garbelottoat/wp-content/uploads/vanengelsdorp2009.pdf {{Bare URL PDF|date=August 2024}}</ref>

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, [[List of diseases of the honey bee#Acarine (tracheal) mites|Acarine (tracheal) mites]], and a new infection, the chronic bee paralysis virus,<ref>{{cite journal|last1=Neumann|first1= Peter |last2=Carreck|first2= Norman L.|year=2010|title=Honey bee colony losses|journal=Journal of Apicultural Research|volume=49|issue=1|pages=1–6|doi=10.3896/IBRA.1.49.1.01|bibcode= 2010JApiR..49....1N |s2cid= 84512885 |url=http://sro.sussex.ac.uk/43682/1/Neumann_%26_Carreck%2C_2010.pdf}}{{open access}}</ref> but during the outbreak, the cause of this agricultural beekeeping problem was unknown.<ref>{{Cite news|date=1920|title=BEE DISEASE MYSTERY SOLVED?: DISCOVERY AT ABERDEEN UNIVERSITY|page=8|work=The Manchester Guardian (1901–1959)|url=https://www.proquest.com/docview/476426126|access-date=February 1, 2022|id={{ProQuest|476426126}}}}</ref>

Reports show similar behavior in hives in the US in 1918<ref name='H.R. "Rob" Stevenson'>{{cite journal|last=Anonymous|title=Strange Behavior |journal=American Bee Journal|year=1918|volume=58|page=353|url=http://www.americanbeejournal.com/|access-date=23 July 2012}}</ref> and 1919.<ref name=autogenerated2>{{cite journal|last=Anonymous|title=Bees leave hive|journal=American Bee Journal|year=1919|volume=59 |page=385 |url=http://www.americanbeejournal.com/}}</ref> Coined "mystery disease" by some,<ref name=autogenerated1>{{cite journal|last=Mraz |first=Charles|title=The Mystery Disease|journal=Gleanings in Bee Culture|year=1965|volume=93|pages=422–24}}</ref> it eventually became more widely known as "disappearing disease".<ref name=autogenerated4>{{cite journal|last=Mraz|first=Charles|title=Disappearing Disease in Mexico|journal=Gleanings in Bee Culture|year=1977|volume=105|page=198}}</ref> Oertel, in 1965,<ref name='Oertel'>{{cite journal|last=Oertel |first=E.|title=Many bee colonies dead of an unknown cause|journal=American Bee Journal|year=1965|volume=105|pages=48–49}}</ref> 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.{{Citation needed|date=January 2021}}

In the US, the number of colonies maintained by beekeepers had been in decline since the 1960s, for various reasons including urbanization, [[pesticide]] use, [[Acarapis woodi|tracheal]] and ''[[Varroa]]'' mites, and commercial beekeepers retiring and going out of business.<ref name=Aizen2009/> However, in late 2006 and early 2007, the rate of attrition was alleged to have reached new proportions,<ref>{{cite web | url=https://www.pbs.org/newshour/economy/struggling-beekeepers-stabilize-u-s-honeybee-population-after-nearly-half-of-colonies-died-last-year | title=Struggling beekeepers stabilize U.S. Honeybee population after nearly half of colonies died last year | website=[[PBS]] | date=22 June 2023 }}</ref> 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).<ref>{{cite news| url=http://news.bbc.co.uk/2/hi/uk_news/scotland/highlands_and_islands/7360832.stm | work=BBC News | title=Wild bee decline 'catastrophic' | date=23 April 2008}}</ref>

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.<ref name="fas.org">{{cite web|url=http://www.fas.org/sgp/crs/misc/RL33938.pdf |title=Honey Bee Colony Collapse Disorder |publisher=Congressional Research Service |first=Renée |last=Johnson |date=7 January 2010 |access-date=2012-05-24}}</ref> In the winter of 2004–2005, a spontaneous collapse occurred and was attributed to [[Diseases of the honey bee#Varroa mites|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.<ref name=Prelim /> By February 2007, large commercial migratory beekeepers wintering in California, Florida, Oklahoma, and Texas had reported heavy losses associated with CCD.<ref name="fas.org"/> 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.<ref name="CCDPR2010" /> 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%.<ref name="fas.org"/> 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.<ref name="CCDPR2010" /> 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%.<ref name="USDA2014">{{cite web|title= Yearly survey shows better results for pollinators, but losses remain significant Release No. 0088.14 |author=USDA|publisher=USDA |year=2014|url=http://www.usda.gov/wps/portal/usda/usdahome?contentid=2014/05/0088.xml|access-date=21 August 2015}}</ref>

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.<ref>{{cite news |date=20 June 2014|title=US sets up honey bee loss task force|url=https://www.bbc.com/news/world-us-canada-27951040|newspaper=[[BBC News]]|access-date=21 June 2014}}</ref> Since 2014, Congress has substantially subsidized the pollinator industry through the [[Agricultural Act of 2014|2014 Farm Bill]].<ref name="auto">{{Cite news|url=https://www.washingtonpost.com/business/2019/07/05/last-winter-saw-highest-honeybee-colony-losses-record/|title=This past winter saw the highest honeybee colony losses on record |first=Laura |last=Reiley|newspaper=The Washington Post|language=en|access-date=2019-12-01}}</ref> 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.<ref>{{Cite web|url=https://www.fsa.usda.gov/programs-and-services/disaster-assistance-program/emergency-assist-for-livestock-honey-bees-fish/index|title=Emergency Assistance for Livestock, Honey Bees, and Farm-raised Fish (ELAP)|website=temp_FSA_02_Landing_InteriorPages|language=en|access-date=2019-12-01}}</ref> 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.<ref>{{Cite web|url=https://www.epa.gov/pollinator-protection/epa-actions-protect-pollinators|title=EPA Actions to Protect Pollinators|last=US EPA|first=OCSPP|date=2013-09-03|website=US EPA|language=en|access-date=2019-12-01}}</ref> [[2018 United States farm bill|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.<ref name="auto"/>

A survey by the [[University of Maryland]] and [[Auburn University]] published in 2023 found the number of United States honey bee colonies "remained relatively stable" although 48% of colonies were lost in the year that ended April 1, 2023, with a 12-year average annual mortality rate of 39.6%. The previous year (2021–2022) the loss was 39% and the 2020–2021 loss was 50.8%. Beekeepers told the surveying scientists that 21% loss over the winter is acceptable and more than three-fifths of beekeepers surveyed said their losses were higher than in 2022–2023.<ref>{{cite web | url=https://www.pbs.org/newshour/economy/struggling-beekeepers-stabilize-u-s-honeybee-population-after-nearly-half-of-colonies-died-last-year | title=Struggling beekeepers stabilize U.S. Honeybee population after nearly half of colonies died last year | website=[[PBS]] | date=22 June 2023 }}</ref>

In 2024, the [[United States Census of Agriculture]] reported an all-time high in commercial honey bee hives (mostly in Texas), making them the fastest-growing livestock segment in the country.<ref>{{cite news |url=https://www.washingtonpost.com/business/2024/03/29/bees-boom-colony-collapse/ |title=Wait, does America suddenly have a record number of bees? |last1=Van Dam |first1=Andrew |date=29 March 2024 |accessdate=4 May 2024}}</ref>

==Signs and symptoms==
[[File:Inspecting the bees' work.JPG|thumb|Visit to a bee colony in West Virginia]]
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.<ref name="CornellPollinator"/> 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.<ref>{{cite web |last1=US EPA |title=Colony Collapse Disorder |url=https://www.epa.gov/pollinator-protection/colony-collapse-disorder#dead%20bees%20don%27t%20equal%20ccd |website=US EPA |access-date=10 December 2018 |date=29 August 2013}}</ref> A colony that has collapsed from CCD is generally characterized by all of these conditions occurring simultaneously:<ref>{{cite web |title=Colony Collapse Disorder |url=http://sfyl.ifas.ufl.edu/agriculture/colony-collapse-disorder/ |website=sfyl.ifas.ufl.edu |publisher=UF/IFAS Extension |access-date=10 December 2018}}</ref><ref>{{cite web|url=http://honeycouncil.ca/users/news_view.asp?FolderID=3219&NewsID=1146|archive-url=https://web.archive.org/web/20070729004717/http://honeycouncil.ca/users/news_view.asp?FolderID=3219&NewsID=1146|archive-date=29 July 2007|title=Discussion of phenomenon of Colony disorder collapse|publisher=Canadian Honey Council|date=27 January 2007}}</ref>
* Presence of [[Brood (honey bee)|capped brood]] in abandoned colonies. Bees normally do not abandon a hive until the capped brood have all hatched.
* Presence of food stores, both [[honey]] and [[bee pollen]]:
** that other bees do not rob immediately
** with significantly delayed attacks by hive [[Pest (organism)|pests]] such as [[Lesser wax moth|wax moths]] and [[small hive beetle]]s<ref name="CornellPollinator">{{cite web |title=Colony Collapse Disorder |url=https://pollinator.cals.cornell.edu/pollinator-conservation/colony-collapse-disorder/ |website=pollinator.cals.cornell.edu |publisher=Pollinator Network @ Cornell |access-date=10 December 2018}}</ref>
* Presence of the [[queen bee]]. If the queen is not present, the hive likely died because it was queenless, which is not considered CCD.<ref name="Vanengeletal2010">{{cite journal |last1=vanEngelsdorp |first1=Dennis |last2=Evans |first2=Jay D. |last3=Saegerman |first3=Claude |last4=Mullin |first4=Chris |last5=Haubruge |first5=Eric |last6=Nguyen |first6=Bach Kim |last7=Frazier |first7=Maryann |last8=Frazier |first8=Jim |last9=Cox-Foster |first9=Diana |last10=Chen |first10=Yanping |last11=Underwood |first11=Robyn |last12=Tarpy |first12=David R. |last13=Pettis |first13=Jeffery S. |title=Colony Collapse Disorder: A Descriptive Study |journal=PLOS ONE |date=3 August 2009 |volume=4 |issue=8 |pages=e6481 |doi=10.1371/journal.pone.0006481 |pmid=19649264 |pmc=2715894 |bibcode=2009PLoSO...4.6481V |doi-access=free }}</ref><ref name="VanEngelsdorpetal2010b">{{cite journal |last1=vanEngelsdorp |first1=Dennis |last2=Meixner |first2=Marina Doris |title=A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them |journal=Journal of Invertebrate Pathology |date=January 2010 |volume=103 |pages=S80–S95 |doi=10.1016/j.jip.2009.06.011 |pmid=19909973 |bibcode=2010JInvP.103S..80V }}</ref><ref name="vanEngelsdorpetal2010a">{{cite journal |last1=vanEngelsdorp |first1=Dennis |last2=Hayes |first2=Jerry |last3=Underwood |first3=Robyn M |last4=Pettis |first4=Jeffery S |title=A survey of honey bee colony losses in the United States, fall 2008 to spring 2009 |journal=Journal of Apicultural Research |date=January 2010 |volume=49 |issue=1 |pages=7–14 |doi=10.3896/IBRA.1.49.1.03 |s2cid=86029370 |doi-access=free |bibcode=2010JApiR..49....7V }}</ref><ref name="Dainatetal2012">{{cite journal |last1=Dainat |first1=Benjamin |last2=vanEngelsdorp |first2=Dennis |last3=Neumann |first3=Peter |title=Colony collapse disorder in Europe |journal=Environmental Microbiology Reports |date=February 2012 |volume=4 |issue=1 |pages=123–25 |doi=10.1111/j.1758-2229.2011.00312.x |pmid=23757238 |bibcode=2012EnvMR...4..123D }}</ref> 
* No dead honey bee bodies present<ref name="vanEngelsdorpetal2010a" />

Precursor symptoms that may arise before the final colony collapse include:
* Inability to maintain current brood due to low [[Worker bee|workforce]]{{Citation needed|date=January 2021}}
* Colony includes mostly young adult bees  {{Citation needed|date=January 2021}}
* Bees are reluctant to consume provided feed, such as sugar syrup and [[Dietary supplement|protein supplement]].{{Citation needed|date=January 2021}}

==Genetic and physio-pathological predictions==
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 [[rectum]]s, rectal enteroliths (rectal stones), and [[Malpighian tubule system|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.<ref>{{Cite web|url=https://www.researchgate.net/publication/318990996|title=Colony Collapse Disorder (CCD) and bee age impact honey bee pathophysiology|website=ResearchGate|access-date=2019-05-06}}</ref>

In addition, there are genetic indications in the gut that suggest the susceptibility of honey bees to CCD. Sixty-five different [[primary transcript|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 [[Polyadenylation|poly(A)]]-rich 3′ tails was detected via [[Microarray analysis techniques|microarray analysis]] and [[Real-time polymerase chain reaction|qPCR]] in the guts of CCD bees.<ref name=":7">{{cite journal |last1=Johnson |first1=R. M. |last2=Evans |first2=J. D. |last3=Robinson |first3=G. E. |last4=Berenbaum |first4=M. R. |title=Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera) |journal=Proceedings of the National Academy of Sciences |date=24 August 2009 |volume=106 |issue=35 |pages=14790–95 |doi=10.1073/pnas.0906970106 |pmid=19706391 |pmc=2736458 |bibcode=2009PNAS..10614790J |doi-access=free }}</ref> 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.<ref>{{cite journal |last1=Kong |first1=Qiongman |last2=Stockinger |first2=Michael P. |last3=Chang |first3=Yueming |last4=Tashiro |first4=Hirofumi |last5=Lin |first5=Chien-liang Glenn |title=The presence of rRNA sequences in polyadenylated RNA and its potential functions |journal=Biotechnology Journal |date=August 2008 |volume=3 |issue=8 |pages=1041–46 |doi=10.1002/biot.200800122 |pmid=18683164 |s2cid=27571129 }}</ref> 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.<ref name=":7" />

==Scope and distribution==
===United States===
[[File:US honey bee hives 1982-2015.png|US honey bee hives 1982–2015|thumb|350px]]
The [[National Agricultural Statistics Service]] (NASS) reported 2.44&nbsp;million honey-producing hives were in the United States in February 2008, down from 4.5&nbsp;million in 1980, and 5.9&nbsp;million in 1947, though these numbers underestimate the total number of managed hives, as they exclude several thousand hives managed for pollination contracts only, and also do not include hives managed by beekeepers owning fewer than 5&nbsp;hives. This under-representation may be offset by the practice of counting some hives more than once; hives that are moved to different states to produce honey are counted in each state's total and summed in total counts.<ref name="plosone.org">{{Cite journal|doi=10.1371/journal.pone.0004071 |pmid=19115015 |title=A survey of honey bee colony losses in the U.S., Fall&nbsp;2007 to Spring&nbsp;2008 |journal=PLOS ONE |volume=3 |issue=12 |page=e4071 |year=2008 |last1=Vanengelsdorp |first1=Dennis |last2=Hayes |first2=Jerry |last3=Underwood |first3=Robyn M. |last4=Pettis |first4=Jeffery |pmc=2606032|bibcode = 2008PLoSO...3.4071V |doi-access=free }}</ref>

In 2007 in the US, at least 24&nbsp;different states<ref name=cnn>{{cite web |author=Sahba, Amy |title=The mysterious deaths of the honeybees |url=https://money.cnn.com/2007/03/29/news/honeybees/ |website=[[CNN Money]] |date=29 March 2007 |access-date=2007-04-04}}</ref> had reported at least one case of CCD.<ref name=ABJ707>{{cite journal |author1=van Engelsdorp, D. |author2=Underwood, R. |author3=Caron, D. |author4=Hayes, J. Jr. |year=2007 |title=An estimate of managed colony losses in the winter of 2006–2007: A report commissioned by the Apiary Inspectors of America |journal=American Bee Journal}}{{full citation needed|date=June 2020}}</ref> In a 2007 survey of 384 responding beekeepers from 13&nbsp;states, 23.8% met the specified criterion for CCD (that 50% or more of their dead colonies were found without bees and / or with very few dead bees in the hive or apiary).<ref name=ABJ707/> In 2006–2007, CCD-suffering operations had a total loss of 45% compared to the total loss of 25% of all colonies experienced by non-CCD suffering beekeepers.<ref name="plosone.org"/><ref name=ABJ707/>

A 2007–2008 survey of over 19% of all US colonies revealed a total loss of 35.8%. Operations that [[Pollination#Economics of pollination|pollinated almonds]] lost, on average, the same number of colonies as those that did not. The 37.9% of operations that reported having at least some of their colonies die with a complete lack of bees had a total loss of 40.8% of colonies compared to the 17.1% loss reported by beekeepers without this symptom. Large operations were more likely to have this symptom, suggesting a contagious condition may be a causal factor. About 60% of all colonies that were reported dead in this survey died without the presence of dead bees in the hive, thus possibly suffered from CCD.<ref name="plosone.org"/>

Between 2007 and 2013 after CCD was described in the US, annual winter colony losses doubled from 15% pre-CCD to 30%. Such loss rates fell to 24% from 2014 to 2017 and CCD symptoms were not as commonly associated with hive losses.<ref name="USDA-ERS">{{cite web |title=Despite elevated loss rate since 2006, U.S. honey bee colony numbers are stable |url=https://www.ers.usda.gov/amber-waves/2018/october/despite-elevated-loss-rate-since-2006-us-honey-bee-colony-numbers-are-stable/ |website=www.ers.usda.gov |publisher=United States Department of Agriculture |department=Economic Research Service |access-date=29 January 2019 |archive-date=4 August 2019 |archive-url=https://web.archive.org/web/20190804051418/https://www.ers.usda.gov/amber-waves/2018/october/despite-elevated-loss-rate-since-2006-us-honey-bee-colony-numbers-are-stable/ |url-status=dead }}</ref> While CCD has increased hive losses, honey bee colony numbers in the US have remained stable or grown since the identification of CCD.<ref name="USDA-ERS2">{{cite web |title=Economic effects and responses to changes in honey bee health |url=https://www.ers.usda.gov/webdocs/publications/88117/err-246.pdf?v=0 |publisher=United States Department of Agriculture |department=Economic Research Service |access-date=29 January 2019}}</ref>

Throughout the year in 2017, NASS reported total US hives ranged between 2.63 and 2.99&nbsp;million throughout the year for operations with more than five colonies, and 35–43&nbsp;thousand hives for those with fewer than 5&nbsp;colonies. In the same year, operations with more than 5&nbsp;colonies lost 77.8&nbsp;thousand hives (2.6–3.0%) with CCD symptoms and those with fewer than 5&nbsp;colonies lost 6&nbsp;thousand hives (14–17%) with CCD symptoms.<ref name="NASS">{{cite web |title=Honey bee colonies |url=https://downloads.usda.library.cornell.edu/usda-esmis/files/rn301137d/jq085n95f/mc87pt22m/BeeColonies-08-01-2018.pdf |publisher=USDA |access-date=29 January 2019}}</ref>

As of 2022, the number of colonies had reached an all-time high of 3.8 million, rising by 31% since 2007, according to the [[National Agricultural Statistics Service]], largely due to the growth of small producers in Texas.<ref>{{Cite news |last=Van Dam |first=Andrew |date=2024-03-29 |title=Analysis {{!}} Wait, does America suddenly have a record number of bees? |url=https://www.washingtonpost.com/business/2024/03/29/bees-boom-colony-collapse/ |access-date=2024-04-01 |newspaper=Washington Post |language=en}}</ref>

=== Europe ===
According to the [[European Food Safety Authority]] (EFSA), in 2007, the United Kingdom had 274,000&nbsp;hives, Italy had 1,091,630, and France 1,283,810. In 2008, the [[British Beekeepers Association]] reported the bee population in the United Kingdom dropped by around 30% between 2007 and 2008, and an EFSA study revealed that in Italy the mortality rate was 40–50%. However, EFSA officials point out the figures are not very reliable because before the bees started dying, no harmonisation was used in the way different countries collected statistics on their bee populations. At that time (2008), the reports blamed the high death rate on the varroa mite, two seasons of unusually wet European summers, and some pesticides.<ref name="BBC NEWS"/>

In 2009, Tim Lovett, president of the British Beekeepers' Association, said: "Anecdotally, it is hugely variable. There are reports of some beekeepers losing almost a third of their hives and others losing none." John Chapple, chairman of the London Beekeepers' Association, put losses among his 150&nbsp;members at between a fifth and a quarter. "There are still a lot of mysterious disappearances; we are no nearer to knowing what is causing them." The government's [[National Bee Unit]] continued to deny the existence of CCD in Britain; it attributes the heavy losses to the varroa mite and rainy summers that stop bees foraging for food.<ref name="Benjamin">{{cite news| url=https://www.theguardian.com/environment/2010/may/02/food-fear-mystery-beehives-collapse | location=London | work=The Guardian | first=Alison | last=Benjamin | title=Fears for crops as shock figures from America show scale of bee catastrophe | date=2 May 2010}}</ref>

In 2010, David Aston of the British Beekeepers' Association stated, "We still do not believe CCD (which is now better defined) is a cause of colony losses in the UK, however we are continuing to experience colony losses, many if not most of which can be explained." He feels recent studies suggest "further evidence to the evolving picture that there are complex interactions taking place between a number of factors, pathogens, environmental, beekeeping practices and other stressors, which are causing honey bee losses described as CCD in the US".<ref name="Telegraph"/>

Beekeepers in Scotland also reported losses from 2007 to 2009.<ref name="Benjamin" /> Andrew Scarlett, a Perthshire-based bee farmer and honey packer, lost 80% of his 1,200&nbsp;hives during the 2009–2010 winter. He attributed the losses to a virulent bacterial infection that quickly spread because of a lack of bee inspectors, coupled with sustained poor weather that prevented honey bees from building up sufficient pollen and nectar stores.<ref name="Benjamin"/>

In Germany, where some of the first reports of CCD in Europe appeared, and where, according to the German national association of beekeepers, 40% of the honey bee colonies died,<ref name=Echos>{{cite web |author=Paul Mga |url=http://www.lesechos.fr/20/08/2007/LesEchos/19985-063-ECH_la-mort-des-abeilles-met-la-planete-en-danger.htm |title=La mort des abeilles met la planète en danger |work=[[Les Échos (France)|Les Échos]] |date=20 August 2007 |language=fr}}</ref> there was no scientific confirmation. In early May 2007, the German media reported no confirmed CCD cases seemed to have occurred in Germany.<ref>{{cite web |publisher=N-TV |url=http://www.n-tv.de/wissen/Deutschen-Bienen-geht-es-gut-article341072.html |title=Immer weniger Imker – Deutschen Bienen geht es gut |date=11 May 2007 |language=de}}</ref><ref name="Benjamin" />

A case study published in 2012 examined and identified a colony loss incident in Switzerland, surveyed by the Swiss Bee Research Centre in October 2009, as the first case of CCD outside of the United States.<ref name="Dainatetal2012" />  While the incident matched the criteria suggested by prior US hive surveys,<ref name="vanEngelsdorpetal2010a" /> analysis of laboratory tests for pathogens found a lack of differentiation in pathogen loads or co-infection levels between CCD and non-CCD hives.<ref name="Dainatetal2012" />  The case study further notes that the colonies did not have damaging levels of ''Varroa destructor'' or ''Nosema'' spp at the time of collapse but emphasized that pathogens could not be ruled out as playing a role.

At the end of May 2012, the Swiss government reported about half of the bee population had not survived the winter. The main cause of the decline was thought to be the parasite ''[[Varroa destructor]]''.<ref>{{cite news | url = http://www.rts.ch/info/sciences-tech/4011954-hiver-fatal-pour-la-moitie-des-colonies-d-abeilles-en-suisse.html | publisher = Radio Télévision Suissse | date = 22 May 2012 | access-date = 22 May 2012 |title=Hiver fatal pour la moitié des colonies d'abeilles en Suisse|language=fr}}</ref>

=== Asia ===
In China, a three-year survey from 2010 to 2013 (using COLOSS questionnaires) showed colony losses of 10.1% on average. Comb renewal and queen problems were identified as significant risk factors.<ref>{{cite journal |last1=Liu |first1=Zhiguang |last2=Chen |first2=Chao |last3=Niu |first3=Qingsheng |last4=Qi |first4=Wenzhong |last5=Yuan |first5=Chunying |last6=Su |first6=Songkun |last7=Liu |first7=Shidong |last8=Zhang |first8=Yingsheng |last9=Zhang |first9=Xuewen |last10=Ji |first10=Ting |last11=Dai |first11=Rongguo |last12=Zhang |first12=Zhongyin |last13=Wang |first13=Shunhai |last14=Gao |first14=Fuchao |last15=Guo |first15=Haikun |last16=Lv |first16=Liping |last17=Ding |first17=Guiling |last18=Shi |first18=Wei |title=Survey results of honey bee (''Apis mellifera'') colony losses in China (2010–2013) |journal=Journal of Apicultural Research |date=5 August 2016 |volume=55 |issue=1 |pages=29–37 |doi=10.1080/00218839.2016.1193375 |bibcode=2016JApiR..55...29L |s2cid=89081470 }}</ref>

== Possible causes ==
The mechanisms of CCD are still unknown, but many causes are currently being considered, such as [[Pesticide toxicity to bees|pesticides]], [[mite]]s, fungi, beekeeping practices (such as the use of [[antibiotics]] or long-distance transportation of beehives), malnutrition, poor quality queens, starvation, other [[pathogen]]s, and [[immunodeficiency|immunodeficiencies]]. The current scientific consensus is that no single factor is causing CCD, but that some of these factors in combination may lead to CCD either additively or synergistically.<ref name="plosone.org" /><ref name="motherjones.com">{{cite web |last1=McDonnell|first1=Tim|title=Here's why all the bees are dying|url=https://www.motherjones.com/environment/2015/07/climate-change-killing-bumblebees|website=Mother Jones|access-date= 2017-02-08 |date=9 July 2015}}</ref><ref>{{cite journal | title =Colony Collapse Disorder in context | journal = BioEssays | volume =32 | issue = 10 |  pages =845–46 | year =2010 | doi= 10.1002/bies.201000075 | pmid = 20730842 | last1 = Williams | first1 = Geoffrey R. | last2 = Tarpy | first2 = David R. | last3 = Vanengelsdorp | first3 = Dennis | last4 = Chauzat | first4 = Marie-Pierre | last5 = Cox-Foster | first5 = Diana L. | last6 = Delaplane | first6 = Keith S. | last7 = Neumann | first7 = Peter | last8 = Pettis | first8 = Jeffery S. | last9 = Rogers | first9 = Richard E. L. | last10 = Shutler | first10 = Dave | pmc=3034041}}</ref><ref>{{cite journal|last1=Le Conte|first1=Yves|last2=Ellis|first2=Marion|last3=Ritter|first3=Wolfgang|title=''Varroa'' mites and honey bee health: can ''Varroa'' explain part of the colony losses?| journal=Apidologie|date=12 April 2010|volume=41|issue=3|pages=353–63|doi=10.1051/apido/2010017|s2cid=7708607|url=https://hal.archives-ouvertes.fr/hal-00892103/file/hal-00892103.pdf|doi-access=free}}{{open access}}</ref><ref>{{cite journal | title =Towards a systems approach for understanding honeybee decline: a stocktaking and synthesis of existing models | journal = Journal of Applied Ecology | volume =50 | issue = 4 |  pages =868–80 | year =2013 | doi=10.1111/1365-2664.12112| pmid = 24223431 | last1 = Becher | first1 = Matthias A. | last2 = Osborne | first2 = Juliet L. | last3 = Thorbek | first3 = Pernille | last4 = Kennedy | first4 = Peter J. | last5 = Grimm | first5 = Volker | pmc=3810709}}</ref><ref name="vanderSluijs"/><ref>{{Cite report |author= USDA |date= 17 October 2012 |title= Report on the National Stakeholders Conference on Honey Bee Health National Honey Bee Health Stakeholder Conference Steering Committee |url= http://www.usda.gov/documents/ReportHoneyBeeHealth.pdf |access-date= 4 June 2014 |archive-url= https://web.archive.org/web/20140520063250/http://www.usda.gov/documents/ReportHoneyBeeHealth.pdf |archive-date= 20 May 2014 |url-status= dead}}</ref><ref>{{cite journal | title = Honey bee pathology: current threats to honey bees and beekeeping | journal = Appl Microbiol Biotechnol | volume = 87 | issue = 1 | pages = 87–97 | year = 2010 | url = http://site.xavier.edu/Blairb/sustainable-agriculture-2/honey-bees/honey-bee-pathology-current.pdf | access-date = 28 May 2014 | doi = 10.1007/s00253-010-2573-8 | pmid = 20401479 | last1 = Genersch | first1 = Elke | s2cid = 859133 | url-status = dead | archive-url = https://web.archive.org/web/20140607001818/http://site.xavier.edu/Blairb/sustainable-agriculture-2/honey-bees/honey-bee-pathology-current.pdf | archive-date = 7 June 2014}}</ref><ref>{{cite journal | title =Pathogens, Pests, and Economics: Drivers of Honey Bee Colony Declines and Losses | journal = EcoHealth | volume =10 | issue = 4 |  pages = 434–45 | year =2013 | doi= 10.1007/s10393-013-0870-2 | pmid = 24496582 | last1 = Smith | first1 = Kristine M. | last2 = Loh | first2 = Elizabeth H. | last3 = Rostal | first3 = Melinda K. | last4 = Zambrana-Torrelio | first4 = Carlos M. | last5 = Mendiola | first5 = Luciana | last6 = Daszak | first6 = Peter | s2cid = 1297723 }}</ref><ref name="Woddy 2013" />

In 2006, the [[Colony Collapse Disorder Working Group]] (CCDWG), based primarily at [[Pennsylvania State University]], was established. Their preliminary report pointed out some patterns, but drew no strong conclusions.<ref name=Prelim/> A survey of beekeepers early in 2007 indicated most hobbyist beekeepers believed that starvation was the leading cause of death in their colonies, while commercial beekeepers overwhelmingly believed invertebrate pests (''Varroa'' mites, honey bee tracheal mites, and/or small hive beetles) were the leading cause of colony mortality.<ref name = ABJ707/> A scholarly review in June 2007 similarly addressed numerous theories and possible contributing factor, but left the issue unresolved.<ref name="Oldroyd"/>

In July 2007, the [[United States Department of Agriculture]] (USDA) released a ''CCD Action Plan'', which outlined a strategy for addressing CCD consisting of four main components:<ref>{{cite web |title=Colony Collapse Disorder Action Plan |url=http://www.ars.usda.gov/is/br/ccd/ccd_actionplan.pdf |publisher=[[USDA]] |date=20 June 2007}}</ref> survey and data collection; analysis of samples; hypothesis-driven research; mitigation and preventive action. The first annual report of the U.S. Colony Collapse Disorder Steering Committee was published in 2009.<ref>{{cite web |url=http://www.extension.org/mediawiki/files/c/c7/CCDReport2009.pdf |title=CCD Steering Committee, ''Colony Collapse Disorder Progress Report'' (US Department of Agriculture, Washington, DC, 2009) |access-date=2010-06-22 |url-status=dead |archive-url=https://web.archive.org/web/20110718044124/http://www.extension.org/mediawiki/files/c/c7/CCDReport2009.pdf |archive-date=18 July 2011}}</ref> It suggested CCD may be caused by the interaction of many agents in combination.<ref name="science-08-01-2010">{{cite journal |last1=Ratnieks |first1=F.L.W. |last2=Carreck |first2=N.L. |title=Clarity on Honey Bee Collapse? |journal=Science |volume=327 |issue=5962 |pages=152–53 |year=2010 |pmid=20056879 |doi=10.1126/science.1185563|bibcode = 2010Sci...327..152R |s2cid=206524895 }}</ref> The same year, the CCD Working Group published a comprehensive descriptive study that concluded: "Of the 61 variables quantified (including adult bee physiology, pathogen loads, and pesticide levels), no single factor was found with enough consistency to suggest one causal agent. Bees in CCD colonies had higher pathogen loads and were co-infected with more pathogens than control populations, suggesting either greater pathogen exposure or reduced defenses in CCD bees."<ref name = "Vanengeletal2010" />

The second annual Steering Committee report was released in November 2010. The group reported that although many associations—including pesticides, parasites, and pathogens—had been identified throughout the course of research, "it is becoming increasingly clear that no single factor alone is responsible for [CCD]". Their findings indicated an absence of damaging levels of the parasite ''Nosema'' or parasitic ''Varroa'' mites at the time of collapse.<ref name="CCDPR2010"/> They did find an association of sublethal effects of some pesticides with CCD, including two common miticides in particular, coumaphos and fluvalinate, which are pesticides registered for use by beekeepers to control varroa mites. Studies also identified sublethal effects of neonicotinoids and fungicides, pesticides that may impair the bees' immune systems and may leave them more susceptible to bee viruses.<ref name="CCDPR2010"/><ref>Dennis vanEngelsdorp, [http://therealnews.com/t2/index.php?option=com_content&task=view&id=31&Itemid=74&jumival=10521 Why are the bees dying?] {{Webarchive|url=https://web.archive.org/web/20140222235329/http://therealnews.com/t2/index.php?option=com_content&task=view&id=31&Itemid=74&jumival=10521 |date=22 February 2014 }}, [[The Real News Network]], 2013.08.04</ref><ref>Dennis vanEngelsdorp, [http://therealnews.com/t2/index.php?option=com_content&task=view&id=31&Itemid=74&jumival=11484 Stop Selling Bee-Harming Plants] {{Webarchive|url=https://web.archive.org/web/20140216162014/http://therealnews.com/t2/index.php?option=com_content&task=view&id=31&Itemid=74&jumival=11484 |date=16 February 2014 }}, [[The Real News Network]], 2014.02.14</ref>

A 2015 review examined 170 studies on colony collapse disorder and stressors for bees, including [[pathogen]]s, [[agrochemical]]s, declining [[biodiversity]], [[climate change]] and more. The review concluded that "a strong argument can be made that it is the interaction among parasites, pesticides, and diet that lies at the heart of current bee health problems."<ref name = "sciencebees">{{Cite journal
| last1 = Goulson | first1 = Dave | last2 = Nicholls | first2 = Elizabeth | last3 = Botías | first3 = Cristina | last4 = Rotheray | first4 = Ellen L. | title = Bee Declines Driven by Combined Stress from Parasites, Pesticides and Lack of Flowers | journal = Science
| date =  26 February 2015 | volume = 347 | issue = 6229 | pages = 1255957 | doi = 10.1126/science.1255957| pmid = 25721506 | s2cid = 206558985 | url = http://sro.sussex.ac.uk/54228/1/Science_1255957_Goulson_RV_revised_CA_edited.pdf }}</ref><ref name="jrbees">{{cite news
| url= http://journalistsresource.org/studies/environment/sustainability/bee-declines-combined-stress-parasites-pesticides-lack-of-flowers
| title= What's behind bee declines and colony collapse? Latest science on stress from parasites, pesticides, habitat loss}}</ref> Furthermore:

<blockquote>
Bees of all species are likely to encounter multiple stressors during their lives, and each is likely to reduce the ability of bees to cope with the others. A bee or bee colony that appears to have succumbed to a pathogen may not have died if it had not also been exposed to a sublethal dose of a pesticide and/or been subject to food stress (which might in turn be due to drought or heavy rain induced by climate change, or competition from a high density of honey bee hives placed nearby). Unfortunately, conducting well-replicated studies of the effects of multiple interacting stressors on bee colonies is exceedingly difficult. The number of stressor combinations rapidly becomes large, and exposure to stressors is hard or impossible to control with free-flying bees. Nonetheless, a strong argument can be made that it is the interaction among parasites, pesticides, and diet that lies at the heart of current bee health problems.<ref name = "sciencebees"/><ref name="jrbees"/></blockquote>

=== Pathogens and immunodeficiency theories ===
{{Further|Pathogen|immunodeficiency|diseases of the honey bee}}
Early researchers commented that the pathway of propagation functions in the manner of a [[contagious disease]]; however, some sentiment existed that the disorder may involve an [[Immunosuppression|immunosuppressive]] mechanism,<ref>{{cite journal|date = 23 January 2007|title =Colony Collapse Disorder|volume = 26|issue = 1|url = http://fruittimes.cas.psu.edu/FT2601.html#Colony|journal = Fruit Times}}</ref> potentially linked to "stress" leading to a weakened immune system. Specifically, according to research done in 2007 at the Pennsylvania State University: "The magnitude of detected infectious agents in the adult bees suggests some type of immunosuppression". These researchers initially suggested a connection between ''[[Varroa destructor]]'' mite infestation and CCD, suggesting that a combination of these bee mites, [[Deformed Wing Virus|deformed wing virus]] (which the mites transmit) and bacteria work together to suppress immunity and may be one cause of CCD.<ref name=Prelim/><ref name="Beemites">{{Cite web|url=https://www.sciencedaily.com/releases/2005/05/050517110843.htm|title=Bee Mites Suppress Bee Immunity, Open Door For Viruses And Bacteria|website=ScienceDaily}}</ref> Parasites, such as varroa mites ''(Varroa destructor''), honey bee tracheal mites ''(Acarapis woodi)'', fungal, bacterial and viral diseases, and kleptoparasites such as small hive beetles (''Aethina tumida''), are all problems that have been introduced within the last 20 years in the continental U.S., and are faced by beekeepers.<ref name="plosone.org" />

When a colony is dying, for whatever cause, and other healthy colonies are nearby (as is typical in a [[bee yard]]), those healthy colonies often enter the dying colony and rob its provisions for their own use. If the dying colony's provisions were contaminated (by natural or man-made toxins), the resulting pattern (of healthy colonies becoming sick when in proximity to a dying colony) might suggest to an observer that a contagious disease is involved. However, in typical CCD cases, provisions of dying colonies are not robbed, suggesting that toxins do not spread via robbing, thereby mimicking a disease.{{citation needed|date=September 2018}}

Additional evidence that CCD is an infectious disease came from the following observations: the hives of colonies that had died from CCD could be reused with a healthy colony only if they were first treated with DNA-destroying radiation,<ref name=sciam>{{cite news|author = JR Minkel|title = Mysterious Honeybee Disappearance Linked to Rare Virus|url = http://www.scientificamerican.com/article.cfm?id=bees-ccd-virus&page=1|department = Science News|work= [[Scientific American]]|date = 7 September 2007|access-date = 2007-09-07}}</ref> and the CCD Working Group report in 2010 indicated that CCD-exhibiting hives tended to occur in proximity to one another within apiaries.<ref name = "Vanengeletal2010"/>

[[File:Varroa destructor on honeybee host.jpg|thumb|''Varroa destructor'' on a honey bee host]]

==== ''Varroa'' mites ====
According to a 2007 article, the [[mite]] ''[[Varroa destructor]]'' remains the world's most destructive honey bee killer, due in part to the viruses it carries, including [[deformed wing virus]] and [[acute bee paralysis virus]], which have both been implicated in CCD.<ref name=Beemites/><ref>{{Cite web|author=Jennifer Welsh|date=2012-06-07|title=Mites and Virus Team Up to Wipe Out Beehives|url=https://www.livescience.com/20815-honeybee-collapse-mite-virus.html|access-date=2023-01-24|website=livescience.com|language=en}}</ref> Affliction with ''Varroa'' mites also tends to weaken the [[immune system]] of the bees. Dr. Ernesto Guzman, an entomological researcher at the [[University of Guelph]] in Canada, studied 413 [[Ontario]] bee colonies in 2007–08. The presence of ''Varroa'' mites within colonies before winter was observed to weaken the immune systems of bees and introduce viruses that led to colony death during the winter. About 27% of hives did not survive the winter, and the ''Varroa'' mite was identified as the cause in 85% of the cases.<ref>{{cite journal|last1=Guzmán-Novoa|first1=Ernesto|last2=Eccles|first2=Leslie|last3=Calvete|first3=Yireli|last4=Mcgowan|first4=Janine|last5=Kelly|first5=Paul G.|last6=Correa-Benítez|first6=Adriana|title=''Varroa destructor'' is the main culprit for the death and reduced populations of overwintered honey bee (''Apis mellifera'') colonies in Ontario, Canada|journal=Apidologie|date=8 January 2010|volume=41|issue=4|pages=443–50|doi=10.1051/apido/2009076|s2cid=10898654|url=https://hal.archives-ouvertes.fr/hal-00892055/file/hal-00892055.pdf}}</ref> ''Varroa'' mites also affect the queen's ability to reproduce, which is detrimental to the survival of the hive.<ref name="Vanengeletal2010" /> As such, ''Varroa'' mites have been considered as a possible cause of CCD, though not all dying colonies contain these mites.<ref>{{cite news|url=http://pestalert.ifas.ufl.edu/Colony_Collapse_Disorder.htm|author= Jamie Ellis|title=Colony Collapse Disorder (CCD) in Honey Bees|publisher=University of Florida|date=16 April 2007|archive-url=https://web.archive.org/web/20090118144423/http://pestalert.ifas.ufl.edu/Colony_Collapse_Disorder.htm|archive-date=18 January 2009|url-status=dead}}</ref>

''Varroa destructor'' is a parasitic mite that colonizes beehives and preys on honey bees by consuming their hemolymph. ''Varroa'' mites parasitize all types of honey bees (workers, nurse bees, larvae) depending on their life cycle stage. During the phoretic stage, ''Varroa'' prefer to attach to nurse bees as this results in higher fitness leading into the reproductive stage. The mites then feed on larvae during their reproductive stage and increased fitness leads to an increase in mite fecundity (number of female offspring).<ref>{{cite journal |last1=Xie |first1=Xianbing |last2=Huang |first2=Zachary Y. |last3=Zeng |first3=Zhijiang |title=Why do Varroa mites prefer nurse bees? |journal=Scientific Reports |date=15 June 2016 |volume=6 |issue=1 |pages=28228 |doi=10.1038/srep28228 |pmid=27302644 |pmc=4908398 |bibcode=2016NatSR...628228X }}</ref> Due to ''Varroa''{{'}}s ability to feed on all types of honey bees, they are one of the biggest threats to colonies, especially over winter.{{Citation needed|date=January 2021}}

In 2020 a group of scientists announced that they were in the early stages of field testing a bacterium with specifically genetically modified [[plasmids]] that both suppressed infection with deformed wing virus but also effectively reduced ''Varroa'' mite survival.<ref>{{cite news|url=https://www.abc.net.au/news/science/2020-01-31/honey-bees-insect-colony-collapse-varroa-mite-deformed-wing/11905980|author= Nick Kilvert|title=Scientists modify honey bee gut bacterium to fight colony collapse-causing Varroa mite and deformed-wing virus|publisher=ABC Science|date=30 January 2020}}</ref>

==== Israeli acute paralysis virus ====
In 2004, [[Israeli acute paralysis virus]] (IAPV) was discovered in [[Israel]] and at one time it was considered the cause of CCD. It was named after the place it was first identified; its place of origin is unknown. In September 2007, results of a large-scale statistical [[RNA]] [[sequencing]] study of afflicted and unafflicted colonies were reported. RNA from all organisms in a colony was sequenced and compared with sequence databases to detect the presence of pathogens. All colonies were found to be infected with numerous pathogens, but only the IAPV virus showed a significant association with CCD: the virus was found in 25 of the 30 tested CCD colonies, and only in one of the 21 tested non-CCD colonies.<ref name=sciam/><ref name=nytvirus>{{cite news|author = Andrew C. Refkin|title = Virus Is Seen as Suspect in Death of Honeybees|url = https://www.nytimes.com/2007/09/07/science/07bees.html|work =The New York Times |date = 7 September 2007|access-date = 2007-09-07}}</ref>

Research in 2009 has found that an indicator for an impaired protein production is common among all bees affected by CCD, a pattern consistent with IAPV infection. It is conjectured that [[Dicistroviridae]], like the IAPV, cause degradation of the [[ribosome]]s, which are responsible for [[protein synthesis|protein production]] of [[cell (biology)|cells]], and that this reduced ribosomal function weakens the bees, making them more vulnerable to factors that might not otherwise be lethal.<ref name=":7" /><ref>{{Cite web |date=2009-08-25 |title=Genomic Study Yields Plausible Cause Of Colony Collapse Disorder |url=https://www.sciencedaily.com/releases/2009/08/090824151256.htm |access-date=2023-01-24 |website=ScienceDaily |language=en}}</ref>

==== ''Nosema'' ====
Some have suggested the syndrome may be an inability by beekeepers to correctly identify known diseases such as [[European foulbrood]] or the [[microsporidia]]n fungus ''[[Nosema apis]]''. The testing and diagnosis of samples from affected colonies (already performed) makes this highly unlikely, as the symptoms are fairly well known and differ from what is classified as CCD. A high rate of ''Nosema'' infection was reported in samples of bees from Pennsylvania, but this pattern was not reported from samples elsewhere.<ref name=Prelim/>

Hives of western honey bees infected with ''Nosema ceranae'' are wiped out within eight days<ref>{{cite journal |last1=Higes |first1=M |last2=Martin |first2=R |last3=Meana |first3=A |title=''Nosema ceranae'', a new microsporidian parasite in honeybees in Europe |journal=Journal of Invertebrate Pathology |volume=92 |issue=2 |pages=93–95 |year=2006 |pmid=16574143 |doi=10.1016/j.jip.2006.02.005|bibcode=2006JInvP..92...93H }}</ref> indicating that CCD may be caused by ''N.&nbsp;ceranae''. A research team claim to have ruled out many other potential causes,<ref>{{usurped|1=[https://web.archive.org/web/20070720131716/http://www.planetark.com/dailynewsstory.cfm/newsid/43163/story.htm ''Asian Parasite Killing Western Bees&nbsp;– Scientist'']}}, Planet Ark, SPAIN: 19 July 2007</ref><ref name=autogenerated5>Maria Mancilla, [http://rue89.com/2007/08/29/les-abeilles-sont-elles-en-train-de-disparaitre Les abeilles sont-elles en train de disparaître?], ''[[Rue 89]]'', 29 August 2007 {{in lang|fr}}.</ref> however, a 2009 survey of US CCD-affected bee populations found only about half of the colonies sampled, both in CCD and control populations, were infected with ''N.&nbsp;ceranae''.<ref name= "Vanengeletal2010"/>

[[File:Parasite140019-fig4 Nosema podocotyloidis - Hyperparasitic Microsporidia.tif|left|thumb|A [[Hyperparasite|hyperparasitic]] [[microsporidia]]n, ''Nosema podocotyloidis'', a parasite of a [[digenea]]n, ''Podocotyloides magnatestis'', which is itself a parasite of the fish ''Parapristipoma octolineatum'' ([[Teleost]]ei)]]

The primary [[Antifungal drug|antifungal agent]] used against ''Nosema'' is [[fumagillin]], which has been used in a German research project to reduce the microsporidian's impact, and is mentioned as a possible remedy by the CCDWG.<ref name = "MAAREC">{{cite web|url=http://maarec.cas.psu.edu/pdfs/CCDRecommendations.pdf|title=Tentative Recommendations for Hives Experiencing CCD|author1=Dennis vanEngelsdorp, M.Frazier |author2=D. Caron|date=1 March 2007|publisher=[[Mid-Atlantic Apiculture Research and Extension Consortium]]}}</ref> Higes also claims to have successfully cured colonies with fumagillin.<ref>{{cite journal |last1=Higes |first1=Mariano |last2=Martín-Hernández |first2=Raquel |last3=Garrido-Bailón |first3=Encarna |last4=González-Porto |first4=Amelia V. |last5=García-Palencia |first5=Pilar |last6=Meana |first6=Aranzazu |last7=Del Nozal |first7=María J. |last8=Mayo |first8=R. |last9=Bernal |first9=José L. |title=Honeybee colony collapse due to ''Nosema ceranae'' in professional apiaries |journal=Environmental Microbiology Reports |volume=1 |issue=2 |pages=110–13 |year=2009 |doi=10.1111/j.1758-2229.2009.00014.x |pmid=23765741 |bibcode=2009EnvMR...1..110H }}</ref><ref>{{Cite web|title=Cure For Honey Bee Colony Collapse?|url=https://www.sciencedaily.com/releases/2009/04/090414084627.htm|access-date=2023-01-24|website=ScienceDaily|language=en}}</ref> A review of these results described these results as promising, but cautioned "''N.&nbsp;ceranae'' may not be to blame for all cases of colony collapse".<ref>{{cite journal |title=Microbiology: Colony collapse cured? |journal=Nature |volume=458 |issue=7241 |page=949 |year=2009 |pmid=<!--none--> |doi=10.1038/458949d|bibcode = 2009Natur.458T.949. |doi-access=free }}</ref> Various areas in Europe have reported this fungus, but no direct link to CCD has yet been established.<ref>{{cite web|url=http://www.imkerschule-sh.de/index.php?jahr%5B%5D=2006&imk_themen=j&n=28|title=''Nosema ceranae''&nbsp;– Asiatischer Nosema-Erreger festgestellt – neu verbreitet oder erst jetzt entdeckt?|author= Wolfgang Ritter|language=de|publisher=[[Albert-Ludwigs-Universität Freiburg]] }}</ref><ref>{{cite web|url=http://www.moraybeekeepers.co.uk/nosema.htm|archive-url=https://web.archive.org/web/20070214004709/http://www.moraybeekeepers.co.uk/nosema.htm|archive-date=14 February 2007|title=''Nosema ceranae'' – Asian Nosema Disease Vector Confirmed – is this a new infestation or only now discovered?|first=Wolfgang |last=Ritter|translator-last=McArthur |translator-first=Eric |website=MorayBeeKeepers}}</ref>

In 2007, ''N.&nbsp;ceranae'' was reported in a few hives in California.<ref>{{cite news|url=http://www.sfgate.com/cgi-bin/article.cgi?file=/c/a/2007/04/26/MNGK7PFOMS1.DTL|title=UCSF scientist tracks down suspect in honeybee deaths|author=Sabin Russell|date=26 April 2007|newspaper=San Francisco Chronicle}}</ref> The researcher did not, however, believe this was conclusive evidence of a link to CCD; "We don't want to give anybody the impression that this thing has been solved".<ref>{{cite news|url=https://www.latimes.com/archives/la-xpm-2007-apr-26-sci-bees26-story.html|title=Experts may have found what's bugging the bees|author1=Jia-Rui Chong |author2=Thomas H. Maugh II |date=26 April 2007|newspaper=[[Los Angeles Times]]|access-date=2010-12-31}}</ref> A [[USDA]] bee scientist has similarly stated, "while the parasite ''Nosema ceranae'' may be a factor, it cannot be the sole cause. The fungus has been seen before, sometimes in colonies that were healthy".<ref>{{cite news|url=https://news.yahoo.com/s/ap/20070502/ap_on_sc/honeybee_die_off|archive-url=https://web.archive.org/web/20070505110220/http://news.yahoo.com/s/ap/20070502/ap_on_sc/honeybee_die_off|archive-date=5 May 2007|title= Honeybee Die-Off Threatens Food Supply, The Associated Press (5/2/2007)|author=Seth Borenstein|access-date=2007-05-07|date=2 May 2007|agency=Associated Press}}</ref>

''N. ceranae'' has been detected in honey bees from several states using [[Polymerase chain reaction|PCR]] of the [[16S ribosomal RNA|16S]] gene.<ref>Chapon, L., M.D. Ellis, and A.L. Szalanski. 2009. "''Nosema'' and tracheal mites in the north central region – 2008 survey". ''Proceedings of the American Bee Research Conference. American Bee Journal'' 149: 585–86.</ref><ref>{{cite web |url=http://comp.uark.edu/~aszalan/Apis/Nosema_ceranae_&_N_apis.html |title=Population genetics and distribution of ''N. ceranae'' in the United States, University of Arkansas Insect Genetics Lab |publisher=Comp.uark.edu |access-date=2010-06-22 |archive-url=https://web.archive.org/web/20180118120217/http://comp.uark.edu/~aszalan/Apis/Nosema_ceranae_%26_N_apis.html |archive-date=18 January 2018 |url-status=dead }}</ref> In New York, ''N.&nbsp;ceranae'' was detected in 49 counties, and of the 1,200 honey bee samples collected, 528 (44%) were positive for ''Nosema'', from which, PCR analysis of 371 spore positive samples revealed 96% were ''N.&nbsp;ceranae'', 3% had both ''N.&nbsp;ceranae'' and ''N.&nbsp;apis'', and 1% had ''N.&nbsp;apis'' only.<ref>Szalanski, A.L., J. Whitaker, and P. Cappy. 2010. "Molecular diagnostics of ''Nosema ceranae'' and ''N. apis'' from honey bees in New York". ''Proceedings of the American Bee Research Conference. American Bee Journal'' 150: 508</ref>

When healthy bees are fed pollen filled with fungicides, insecticides, and other agrochemicals—including imidacloprid<ref name=Pettis>{{cite journal|last1=Pettis|first1=Jeffery S.|title=Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema|journal=[[Naturwissenschaften]]|date=February 2012|volume=99|issue=2|pages=153–58|doi=10.1007/s00114-011-0881-1|pmid=22246149|url=http://www.boerenlandvogels.nl/sites/default/files/Pettisetal2012Naturwissen_5.pdf|access-date=27 March 2013|pmc=3264871|bibcode = 2012NW.....99..153P |last2=Johnson |first2=Josephine |last3=Dively |first3=Galen }}</ref>—they are more likely to be infected by ''N.&nbsp;ceranae'', thereby suggesting a potential link to CCD.<ref name="Benjamin2013">{{cite news|author1=Benjamin, A.|author2=Holpuch, A.|author3= Spencer, R.|newspaper=The Guardian|year=2013|access-date=21 August 2015|title=Buzzfeeds: The effects of colony collapse disorder and other bee news|url=https://www.theguardian.com/environment/2013/jul/30/buzzfeeds-bees-colony-collapse-disorder}}</ref><ref name="Woddy 2013">{{cite news|url=http://qz.com/107970/scientists-discover-whats-killing-the-bees-and-its-worse-than-you-thought/|title=Scientists discover what's killing the bees and it's worse than you thought|first=Todd|last=Woody|date=24 July 2013|work=Quartz}}</ref>

=== Viral and fungal combination ===
A University of Montana and Montana State University team of scientists headed by Jerry Bromenshenk and working with the US Army's [[Edgewood Chemical Biological Center]] published a paper in October 2010 saying that a new [[DNA virus]], [[List of diseases of the honey bee#Invertebrate iridescent virus type 6 (IIV-6)|invertebrate iridescent virus type 6]] (IIV-6), and the fungus ''Nosema ceranae'' were found in every killed colony the group studied. In their study, they found neither agent alone seemed deadly, but a combination of the virus and ''N.&nbsp;ceranae'' was always 100% fatal.<ref name=leal>{{cite journal |last1=Leal |first1=Walter S. |last2=Bromenshenk |first2=Jerry J. |last3=Henderson |first3=Colin B. |last4=Wick |first4=Charles H. |last5=Stanford |first5=Michael F. |last6=Zulich |first6=Alan W. |last7=Jabbour |first7=Rabih E. |last8=Deshpande |first8=Samir V. |last9=McCubbin |first9=Patrick E. |last10=Welch |first10=P.M. |last11=Williams |first11=T |last12=Firth |first12=D.R. |last13=Skowronski |first13=E |last14=Lehmann |first14=M.M. |last15=Bilimoria |first15=S.L. |last16=Gress |first16=J |last17=Wanner |first17=K.W. |last18=Cramer Jr |first18=R.A. |editor1-last=Leal |editor1-first=Walter S. |title=Iridovirus and Microsporidian Linked to Honey Bee Colony Decline |journal=PLOS ONE |volume=5 |issue=10 |page=e13181 |year=2010 |pmid=20949138 |pmc=2950847 |doi=10.1371/journal.pone.0013181|bibcode = 2010PLoSO...513181B |doi-access=free }}</ref><ref>{{cite news| url=https://www.nytimes.com/2010/10/07/science/07bees.html | work=The New York Times | first=Kirk | last=Johnson | title=Honeybee Killer Found by Army and Entomologists | date=6 October 2010}}</ref><ref name="Drew Armstrong">{{cite magazine|author=Drew Armstrong|url=http://www.businessweek.com/news/2010-10-07/bee-killing-disease-may-be-combination-attack-researchers-say.html |archive-url=https://web.archive.org/web/20101009213659/http://www.businessweek.com/news/2010-10-07/bee-killing-disease-may-be-combination-attack-researchers-say.html |url-status=dead |archive-date=9 October 2010 |title=Bee-Killing Disease May Be Combination Attack, Researchers Say |magazine=[[BusinessWeek]] |date=7 October 2010 |access-date=2010-11-21}}</ref> Information about the study was released to the public in a front-page article in ''The New York Times''.<ref name=nyt0610>{{cite news| url=https://www.nytimes.com/2010/10/07/science/07bees.html|title=Scientists and Soldiers Solve a Bee Mystery|author=Kirk Johnson|work=The New York Times|date=6 October 2010 |access-date=2010-11-21}}</ref> A few days later, an article was published in ''[[Fortune (magazine)|Fortune]]'' magazine with the title, "What a scientist didn't tell the ''New York Times'' about his study on bee deaths". Professor of entomology at Penn State University James Frazier, who was researching the sublethal impact of pesticides on bees, said that while Bromenshenk's study generated some useful data, Bromenshenk has a conflict of interest as CEO of a company developing scanners to diagnose bee diseases.<ref>{{cite news|last=Eban |first=Katherine |url=https://money.cnn.com/2010/10/08/news/honey_bees_ny_times.fortune/index.htm |title=What a scientist didn't tell the New York Times about his study on bee deaths |publisher=CNN Money |date=8 October 2010 |access-date=2010-11-21}}</ref> A few months later, the methods used to interpret the mass spectrometry data in the Bromenshenk study were called into question, raising doubts as to whether IIV-6 was ever correctly identified in any of the samples examined.<ref name=foster>{{cite journal|last1=Foster|first1=LJ|title=Interpretation of data underlying the link between colony collapse disorder (CCD) and an invertebrate iridescent virus|journal=Molecular & Cellular Proteomics|date=March 2011|volume=10|issue=3|pages=M110.006387|doi=10.1074/mcp.M110.006387 |doi-access=free |pmid=21364086|pmc=3047166}}</ref><ref name=knudsen>{{Cite journal|last1=Knudsen |first1=Giselle |last2=Chalkley | first2=Robert |title=The Effect of Using an Inappropriate Protein Database for Proteomic Data Analysis |journal=PLOS ONE |volume=6 |issue=6 |pages=e20873 |date=14 June 2011 |doi=10.1371/journal.pone.0020873 |pmid=21695130 |bibcode = 2011PLoSO...620873K |pmc=3114852|doi-access=free }}</ref>

=== Pesticides ===
{{Further|Pesticide toxicity to bees|Bees and toxic chemicals}}
[[File:New Holland TL 90 and field sprayer 1.jpg|thumb|New Holland TL 90 with a field sprayer on a Narcissus field in Europe]]
According to the USDA pesticides may be contributing to CCD.<ref name="CCDPR2010">{{cite web|url=http://www.ars.usda.gov/is/br/ccd/ccdprogressreport2010.pdf |title=Colony Collapse Disorder Progress Report|date=June 2010 |author=CCD Steering Committee |publisher=United States Department of Agriculture  |access-date=2014-06-09}}</ref> Scientists have long{{When|date=July 2021}} been concerned that pesticides, including possibly some [[fungicide]]s, may have sublethal effects on bees, not killing them outright, but instead impairing their development and behavior.<ref>{{cite journal |last1=Desneux |first1=Nicolas |last2=Decourtye |first2=Axel |last3=Delpuech |first3=Jean-Marie |title=The Sublethal Effects of Pesticides on Beneficial Arthropods |journal=Annual Review of Entomology |date=January 2007 |volume=52 |issue=1 |pages=81–106 |doi=10.1146/annurev.ento.52.110405.091440 |pmid=16842032 }}</ref><ref>{{cite journal |last1=Chmiel |first1=JA |last2=Daisley |first2=BA |last3=Pitek |first3=AP |last4=Thompson |first4=GJ |last5=Reid |first5=G |title=Understanding the effects of sublethal pesticide exposure on honey bees: a role for probiotics as mediators of environmental stress |journal=Frontiers in Ecology and Evolution |date=2020 |volume=8 |pages=22 |doi=10.3389/fevo.2020.00022|doi-access=free }}</ref> Maryann Frazier{{Who|date=July 2021}} said "pesticides alone have not shown they are the cause of CCD. We believe that it is a combination of a variety of factors, possibly including mites, viruses and pesticides."<ref name="Environment News Service"/>

Evaluating pesticide contributions to CCD is particularly difficult for several reasons. First, the variety of pesticides in use in the different areas reporting CCD makes it difficult to test for all possible pesticides simultaneously. Second, many commercial beekeeping operations are mobile, transporting hives over large geographic distances over the course of a season, potentially exposing the colonies to different pesticides at each location. Third, the bees themselves place [[pollen]] and honey into long-term storage, effectively meaning a delay may occur from days to months before contaminated provisions are fed to the colony, negating any attempts to associate the appearance of symptoms with the actual time when exposure to pesticides occurred.{{Citation needed|date=January 2021}}

In 2010 a sequencing of the honey bee genome provided a possible explanation for the sensitivity of bees to pesticides. Its genome is deficient in the number of genes encoding detoxification enzymes, including cytochrome P450 monooxygenases (P450s), glutathione-S-transferases, and carboxylesterases.<ref>{{Cite journal|title = Pesticides and honey bee toxicity – USA|last = Johnson|first = Reed|date = 2010|journal = Apidologie|doi = 10.1051/apido/2010018|volume=41|issue = 3|pages=312–31|s2cid = 12927448|url = https://hal.archives-ouvertes.fr/hal-00892096/file/hal-00892096.pdf}}</ref>

{{Update|section|date=July 2021}}

====Neonicotinoids====
A class of insecticides called [[neonicotinoids]] has come under particular scrutiny. Neonicotinoids are [[systemic pesticide]]s, typically used as seed treatments in order to reduce the application of foliar pesticides as the plants grow.<ref name="Budge 2015"/> The three main compounds in agricultural use are [[imidacloprid]], [[clothianidin]], and [[thiamethoxam]]. Potentially toxic effects studied in the laboratory have often been followed by field studies that fail to show effects on actual bee populations.<ref>{{cite journal | doi = 10.3896/IBRA.1.53.5.08 | title = The dose makes the poison: have "field realistic" rates of exposure of bees to neonicotinoid insecticides been overestimated in laboratory studies? | volume=53 | issue = 5 | journal=Journal of Apicultural Research | pages=607–614 | year=2014 | author=Carreck Norman L| bibcode = 2014JApiR..53..607C | s2cid = 15038464 | url = http://sro.sussex.ac.uk/53342/1/Carreck_%26_Ratnieks_%282014%29.pdf }}</ref> Despite gaps in the scientific evidence, regulators have restricted the use of neonicotinoids in Europe<ref name="Reuters2018">{{cite news|title=EU to fully ban neonicotinoid insecticides to protect bees|url=https://www.reuters.com/article/eu-environment-bees/eu-to-fully-ban-neonicotinoid-insecticides-to-protect-bees-idUSS8N1QI00F|access-date=29 April 2018|work=Reuters|date=27 April 2018}}</ref> and elsewhere<ref>{{Cite web|url=https://fijisun.com.fj/2019/10/11/paraquat-imidacloprid-pesticide-to-be-banned-from-january-2020/|title=Paraquat, Imidacloprid Pesticide To Be Banned From January, 2020|language=en-US|access-date=23 July 2021|first=Jennis|last=Naidu|work=[[Fiji Sun]]|date=11 October 2019}}</ref> largely on the basis of concerns for bee health.

=====Evidence of risk to bees=====
Use of neonicotinoid pesticides in the US increased after 2005, coincident with rising bee deaths.<ref name="The New York Times 2013">{{cite web | title=Soaring Bee Deaths in 2012 Sound Alarm on Malady | website=The New York Times | date=29 March 2013 | url=https://www.nytimes.com/2013/03/29/science/earth/soaring-bee-deaths-in-2012-sound-alarm-on-malady.html | access-date=22 July 2021}}</ref>

Most corn (maize) grown in the US is grown from seeds treated with neonicotinoids. Although maize is wind-pollinated, honey bees that happen to be foraging on the plants may be exposed to pesticide residues in the nectar and pollen. Honey bees may also be exposed by foraging on wild plants unintentionally exposed to nicotinoids.<ref>{{cite journal |last1=Krupke |first1=Christian H. |last2=Hunt |first2=Greg J. |last3=Eitzer |first3=Brian D. |last4=Andino |first4=Gladys |last5=Given |first5=Krispn |last6=Smagghe |first6=Guy |title=Multiple Routes of Pesticide Exposure for Honey Bees Living Near Agricultural Fields |journal=PLOS ONE |date=3 January 2012 |volume=7 |issue=1 |pages=e29268 |doi=10.1371/journal.pone.0029268 |pmid=22235278 |pmc=3250423 |bibcode=2012PLoSO...729268K |doi-access=free }}</ref>

[[File:Imidacloprid USA 2012.png|thumb|left|Imidacloprid map of use, US, 2012 (estimated)]]

To date,{{When|date=July 2021}} most of the evaluation of possible roles of pesticides in CCD have relied on the use of surveys submitted by beekeepers, but direct testing of samples from affected colonies seems likely to be needed.

======Laboratory studies======
Neonicotinoids may interfere with bees' natural homing abilities, causing them to become disoriented and preventing them from finding their way back to the hive.<ref name = whitehorn/><ref>{{cite news |last=Kelland |first=Kate |url=https://www.reuters.com/article/science-pesticides-bees-idUSL6E8ET2JM20120329 |title=Studies show how pesticides make bees lose their way |work=[[Reuters]]|date= 29 March 2012|access-date=2012-05-24}}</ref><ref name = 2012henry>{{cite journal|title=A Common Pesticide Decreases Foraging Success and Survival in Honey Bees |journal=Science |volume=336 |issue=6079 |pages=348–50 |doi= 10.1126/science.1215039 |pmid=22461498 |year=2012 |last1=Henry |first1=M. |last2=Beguin |first2=M. |last3=Requier |first3=F. |last4=Rollin |first4=O. |last5=Odoux |first5=J.-F. |last6=Aupinel |first6=P. |last7=Aptel |first7=J. |last8=Tchamitchian |first8=S. |last9=Decourtye |first9=A. |s2cid=41186355 |bibcode=2012Sci...336..348H |url=https://hal.archives-ouvertes.fr/hal-00731655/file/51503_20120420060922456_1.pdf }}</ref><ref>{{cite journal|last1=Bortolotti|first1=L.|last2=Monanari|first2= R.|last3= Marcelino|first3= J.|last4= Porrini|first4= P. |year = 2003|title = Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees|journal=[[Bulletin of Insectology]] |volume = 56|issue = 1|pages = 63–67|url=http://www.bulletinofinsectology.org/pdfarticles/vol56-2003-063-067bortolotti.pdf}}</ref><ref name=Schneider>{{cite journal|last1=Schneider|first1=Christof W.|title=RFID Tracking of Sublethal Effects of Two Neonicotinoid Insecticides on the Foraging Behavior of Apis mellifera|journal=PLOS ONE|date=11 January 2012|volume=7|issue=1|page=e30023|doi=10.1371/journal.pone.0030023|pmid=22253863|pmc=3256199|editor1-last=Chaline|editor1-first=Nicolas|bibcode = 2012PLoSO...730023S |last2=Grünewald |first2=B. |last3=Fuchs |first3=S.|doi-access=free}}</ref> These impairments may result from effects of neonicotinoids on the long-term and short-term memory of bees.<ref>{{cite journal|last1=Palmer|first1=Mary J.|title=Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees|journal=Nature Communications|date=27 March 2013|volume=4|page=1634|doi=10.1038/ncomms2648|bibcode = 2013NatCo...4.1634P |issue=3  |last2=Moffat |first2=Christopher |last3=Saranzewa |first3=Nastja |last4=Harvey |first4=Jenni |last5=Wright |first5=Geraldine A. |last6=Connolly |first6=Christopher N. |pmid=23535655 |pmc=3621900}}</ref><ref>{{cite journal|last=Williamson|first=Sally M.|author2=Geraldine A. Wright |author-link2=Geraldine Wright|title=Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees|journal=[[Journal of Experimental Biology]]|date=7 February 2013|doi=10.1242/jeb.083931|pmid=23393272|volume=216|issue=10|pages=1799–1807|pmc=3641805}}</ref> Sublethal doses of imidacloprid in laboratory and [[field experiment]]s decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired.<ref>{{cite journal|author = Thompson H.|year = 2003|title = Behavior effects of pesticides in bees-their potential for use in risk assessment|journal = [[Ecotoxicology]]|volume = 12|issue = 1/4|pages = 317–30|doi = 10.1023/A:1022575315413|pmid = 12739878| bibcode=2003Ecotx..12..317T |s2cid = 11446612}}</ref>

Exposure to Imidacloprid matched to field levels has been shown to reduce colony growth and new queen production.<ref name=whitehorn>{{cite journal|title=Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth and Queen Production |first1=Penelope R. |last1=Whitehorn |first2=Stephanie |last2=O'Connor |first3=Felix L. |last3=Wackers |first4=Dave |last4=Goulson |date=29 March 2012 |doi=10.1126/science.1215025  |pmid=22461500 |journal=Sciencexpress |volume= 336 |issue=6079 |pages=351–52 |url=https://www.science.org/toc/science/0/0|bibcode=2012Sci...336..351W |s2cid=2738787 |doi-access=free }}</ref> 
A 2012 ''in situ'' study suggested that exposure to sublethal levels of imidacloprid in [[high-fructose corn syrup]] (HFCS), which is used to feed honey bees when forage is not available, caused bees to exhibit symptoms consistent with CCD. The control group fed HFCS without insecticide does not show such symptoms.<ref name="Lu2012">{{Cite journal|first1=Chensheng| last1=Lu |first2=Kenneth M. |last2=Warchol |first3=Richard A. |last3=Callahan |year=2012|title=''In situ'' replication of honey bee colony collapse disorder|journal=[[Bulletin of Insectology]]|volume=65|issue=1|pages=99–106|url=http://www.bulletinofinsectology.org/pdfarticles/vol65-2012-099-106lu.pdf}}</ref><ref>{{cite web|url=http://news.harvard.edu/gazette/story/2012/04/pesticide-tied-to-bee-colony-collapse/ |title=Pesticide tied to bee colony collapse |work=[[Harvard Gazette]] |access-date=2012-05-24|date=2012-04-05 }}</ref>

[[File:Bee Collecting Pollen 2004-08-14.jpg|left|thumb|Bee collecting pollen]]

A 2013 literature review concluded that neonicotinoids in the amounts typically used were harmful to bees and that alternatives were urgently needed.<ref name=vanderSluijs>{{cite journal|last1=van der Sluijs|first1=Jeroen P|last2=Simon-Delso|first2=Noa|last3=Goulson|first3=Dave|last4=Maxim|first4=Laura|last5=Bonmatin|first5=Jean-Marc|last6=Belzunces|first6=Luc P|title=Neonicotinoids, bee disorders and the sustainability of pollinator services|journal=Current Opinion in Environmental Sustainability|date=September 2013|volume=5|issue=3–4|pages=293–305|doi=10.1016/j.cosust.2013.05.007|bibcode=2013COES....5..293V |doi-access=free}}</ref> The doses taken up by bees were not lethal, but possible chronic problems could be caused by long-term exposure.<ref name="fas.org"/>

======Field studies======
In 2005 a team of scientists found pollen obtained from seeds dressed with imidacloprid contain significant levels of the insecticide, and suggested that polluted pollen might cause honey bee colony death.<ref>{{cite journal|vauthors=Bonmatin JM, Marchand PA, Charvet R, Moineau I, Bengsch ER, Colin ME |s2cid = 37987577|date = 29 June 2005|title = Quantification of imidacloprid uptake in maize crops|journal = [[J Agric Food Chem]]|volume = 53|issue = 13|pages = 5336–41|doi = 10.1021/jf0479362|pmid=15969515}}</ref>

A meta-analysis study published in February 2010 found evidence from laboratory studies showing sublethal effects of imidacloprid on honey bees, but a lack of evidence on the environmental relevance of these findings.<ref>{{cite journal |title=A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees |author=James E. Cresswell |date=January 2011 |journal=Ecotoxicology |doi=10.1007/s10646-010-0566-0 |pmid=21080222 |volume=20 |issue=1 |pages=149–57|bibcode=2011Ecotx..20..149C |s2cid=12510461 }}</ref> Similarly, a 2012 review concluded that in a laboratory setting, both lethal and sub-lethal effects on foraging behavior, memory, and learning ability were observed in honey bees exposed to neonicotinoids, but that these effects were not seen in field studies with field-realistic dosages.<ref>{{cite journal |last1=Blacquière |first1=Tjeerd |last2=Smagghe |first2=Guy |last3=van Gestel |first3=Cornelis A. M. |last4=Mommaerts |first4=Veerle |title=Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment |journal=Ecotoxicology |date=18 February 2012 |volume=21 |issue=4 |pages=973–92 |doi=10.1007/s10646-012-0863-x |pmid=22350105 |pmc=3338325 |bibcode=2012Ecotx..21..973B }}</ref>

In 2012 several studies were published showing that neonicotinoids had previously undetected routes of exposure affecting bees including through dust, pollen, and nectar.<ref name=Tapparo>{{cite journal|last1=Tapparo|first1=Andrea|title=Assessment of the Environmental Exposure of Honeybees to Particulate Matter Containing Neonicotinoid Insecticides Coming from Corn Coated Seeds|journal=[[Environmental Science and Technology]]|date=31 January 2012|volume=46|issue=5|pages=2592–99|doi=10.1021/es2035152|pmid=22292570|url=http://www.entomology.umn.edu/cues/pollinators/pdf-pesticides/2012Tapparoseedtreatedcorn.pdf|access-date=27 March 2013|bibcode=2012EnST...46.2592T|last2=Marton |first2=Daniele|last3=Giorio|first3=Chiara|last4=Zanella|first4=Alessandro|last5=Soldà|first5=Lidia|last6=Marzaro|first6=Matteo|last7=Vivan|first7=Linda|last8=Girolami|first8=Vincenzo|url-status=dead|archive-url=https://web.archive.org/web/20141006122159/http://www.entomology.umn.edu/cues/pollinators/pdf-pesticides/2012Tapparoseedtreatedcorn.pdf|archive-date=6 October 2014|citeseerx=10.1.1.454.6772}}</ref> Research also showed environmental persistence in agricultural irrigation channels and soil.<ref name=Krupke>{{cite journal|last1=Krupke|first1=Christian H.|title=Multiple Routes of Pesticide Exposure for Honey Bees Living Near Agricultural Fields|journal=PLOS ONE|date=3 January 2012|volume=7|issue=1|page=e29268|doi=10.1371/journal.pone.0029268|pmid=22235278|pmc=3250423|editor1-last=Smagghe|editor1-first=Guy|bibcode = 2012PLoSO...729268K |last2=Hunt |first2=Greg J. |last3=Eitzer |first3=Brian D. |last4=Andino |first4=Gladys |last5=Given |first5=Krispn |doi-access=free}}</ref> The machines that plant corn seeds coated with clothianidin and imidacloprid release certain amounts of the pesticide into the air, another possible route of exposure.<ref name=Tapparo/>

In 2015, an 11-year British study showed a correlation between increasing agricultural use of neonicotinoid seed treatments and escalating honey bee colony losses at a landscape level.<ref name="Budge 2015">{{cite journal |title=Evidence for pollinator cost and farming benefits of neonicotinoid seed coatings on oilseed rape |author1=G.E. Budge |author2= D. Garthwaite |author3= A. Crowe|author4=N.D. Boatman|author5=K.S. Delaplane|author6=M.A. Brown|author7=H.H. Thygesen|author8=S. Pietravalle |journal=Scientific Reports |volume=5 |pages=12574 |date=20 August 2015 |bibcode=2015NatSR...512574B |doi=10.1038/srep12574 |pmid=26270806 |pmc=4535276 }}</ref> This was the first field study to establish a link between neonicotinoids and CCD.<ref name=McPherson>{{cite news |title=Pesticides Killing Bees: Study Shows What 'Everybody's Suspected' |author=Coco McPherson |magazine=[[Rolling Stone]] |date=26 August 2015 |url=https://www.rollingstone.com/politics/news/pesticides-killing-bees-study-shows-what-everybodys-suspected-20150826 |access-date=21 February 2016 }}</ref>

=====Regulatory policy=====
In Europe, the interaction of the phenomenon of "dying bees" with imidacloprid has been discussed for quite some time{{When|date=July 2021}}.<ref>{{cite web|url=http://www.beekeeping.com/articles/us/german_bee_monitoring.htm|title=Betrayed and sold out – German bee monitoring – Walter Haefeker, Deutscher Berufs- und Erwerbsimkerbund|access-date=26 April 2007|date=12 August 2000}}</ref><ref>{{cite web|url=http://www.beekeeping.com/artikel/imidacloprid_1.htm|title=Schadet Imidacloprid den Bienen&nbsp;– von Eric Zeissloff|access-date=26 April 2007|year=2001|language=de }}</ref><ref>{{cite web|url=http://www.beekeeping.com/artikel/gaucho_ein_risiko.htm|title=Gaucho – ein Risiko, Studie: Mitschuld des Bayer-Pestizids für Bienensterben (Neues Deutschland)|access-date=2007-04-26|date=23 November 2003|language=de }}</ref> A study from the {{Lang|fr|Comité Scientifique et Technique|italic=no}} (CST) was at the center of discussion, and led to a partial ban of imidacloprid in France. The imidacloprid pesticide Gaucho was banned in 1999 by the [[French Minister of Agriculture]] [[Jean Glavany]], primarily due to concern over potential effects on honey bees.<ref>{{cite web|url=http://www.agriculture.gouv.fr/spip/IMG/pdf/rapportfin.pdf|title=Imidaclopride utilisé en enrobage de semences (Gaucho®) et troubles des abeilles&nbsp;– Rapport final&nbsp;– 18 septembre 2003|access-date=26 April 2007|date=18 September 2003|language=fr|archive-url = https://web.archive.org/web/20061130003627/http://agriculture.gouv.fr/spip/IMG/pdf/rapportfin.pdf |archive-date = 30 November 2006}}</ref><ref>{{cite web|url=http://www.cbgnetwork.org/355.html|title=France: Governmental report claims BAYER's pesticide GAUCHO responsible for bee-deaths Coalition against Bayer-Dangers is calling for a ban|access-date=26 April 2007|date=December 2003}}</ref><ref>{{cite web|url=http://www.newmediaexplorer.org/sepp/2003/11/26/millions_of_bees_dead_bayers_gaucho_blamed.htm|title=Millions of bees dead&nbsp;– Bayer's Gaucho blamed|access-date=26 April 2007|date=26 November 2003}}</ref>

While French beekeepers succeeded in banning neonicotinoids, the [[Clinton administration]] permitted pesticides that were previously banned,<ref>[https://www.pbs.org/newshour/backgrounders/pesticides.html Re-Regulation of Pesticides]. [[Public Broadcasting Service|PBS]]. {{webarchive |url=https://web.archive.org/web/20121212070302/http://www.pbs.org/newshour/backgrounders/pesticides.html |date=12 December 2012 }}.</ref> including imidacloprid. In 2004, the [[Presidency of George W. Bush|Bush administration]] reduced regulations further and pesticide applications increased.<ref>{{cite web|url=http://westernfarmpress.com/news/1-31-06-State-pesticide-use-increases/|title=State notes small increase in pesticide use|work=westernfarmpress.com|url-status=dead|archive-url=https://web.archive.org/web/20081120013039/http://westernfarmpress.com/news/1-31-06-State-pesticide-use-increases/|archive-date=20 November 2008}}</ref><ref>{{cite web|url=http://www.cdpr.ca.gov/docs/pur/purmain.htm|title=Pesticide Use Reporting|work=ca.gov}}</ref>

In 2013, a formal review by the [[European Food Safety Authority]] (EFSA), reported that some neonicotinoids posed an unacceptably high risk to bees, and identified several data gaps not previously considered. Their review concluded, "A high acute risk to honey bees was identified from exposure via dust drift for the seed treatment uses in maize, [[Rapeseed|oilseed rape]] and cereals. A high acute risk was also identified from exposure via residues in nectar and/or pollen."<ref name=EFSA>{{cite journal | author = European Food Safety Authority | year = 2013 | title = Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin | url = http://www.efsa.europa.eu/en/efsajournal/pub/3066 | journal = [[EFSA Journal]] | volume = 11 | issue = 1| page = 3066 | doi = 10.2903/j.efsa.2013.3066 | doi-access =  }}</ref>

Subsequent to the 2013 EFSA review, the [[European Commission]] (EC) proposed a two-year ban on neonicotinoids.<ref>{{cite news |first=Bernhard |last=Warner|url=http://www.businessweek.com/articles/2013-02-19/to-revive-honey-bees-europe-proposes-a-pesticide-ban |archive-url=https://web.archive.org/web/20130222024809/http://www.businessweek.com/articles/2013-02-19/to-revive-honey-bees-europe-proposes-a-pesticide-ban |url-status=dead |archive-date=22 February 2013 |title=To Revive Honey Bees, Europe Proposes a Pesticide Ban |date=19 February 2013 |publisher=Bloomberg |newspaper=[[BusinessWeek]] |access-date=6 March 2013}}</ref> In April 2013, the [[European Union]] voted for a two-year restriction on neonicotinoid insecticides. The ban restricted the use of imidacloprid, clothianidin, and thiamethoxam for use on crops that are attractive to bees. Eight nations voted against the motion, including the British government, which argued that the science was incomplete.<ref name=victory>{{cite news|title='Victory for bees' as European Union bans neonicotinoid pesticides blamed for destroying bee population|work=[[The Independent]]|date=29 April 2013|author=Charlotte McDonald-Gibson|url=https://www.independent.co.uk/environment/nature/victory-for-bees-as-european-union-bans-neonicotinoid-pesticides-blamed-for-destroying-bee-population-8595408.html|access-date=1 May 2013}}</ref> The ban can be seen as an application of the "[[precautionary principle]]", established at the 1992 Rio Conference on the Environment and Development, which advocated that "lack of full scientific certainty shall not be used as a reason for postponing cost-effective measures to prevent [[environmental degradation]]."<ref name="sapiens.revues.org">{{cite journal|last1=McGrath|first1=Peter F.|date=30 March 2014|title=Politics meets Science: The case of neonicotinoid insecticides in Europe|url=https://journals.openedition.org/sapiens/1648|journal=Surveys and Perspectives Integrating Environment and Society|volume=7|issue=1}}</ref><ref>{{cite web|url=https://www.un.org/documents/ga/conf151/aconf15126-1annex1.htm|title=A/CONF.151/26 (Vol. I) Report of the United Nations Conference on Environment and Development|work=un.org}}</ref>

[[File:Pollinationn.jpg|thumb|Pollination]]

In 2013 beekeepers and environmentalists jointly filed a lawsuit blaming the United States [[Environmental Protection Agency]] (EPA) for continuing to allow the use of neonicotinoids in the United States. The suit specifically asked for suspension of clothianidin and thiamethoxam.<ref name=AP>{{cite news|last=Wozniacka|first=Gosia|title=Beekeepers sue EPA to ban pesticide, protect bees|url=https://news.yahoo.com/beekeepers-sue-epa-ban-pesticide-194327726.html|access-date=22 August 2013|agency=[[Associated Press]]|date=21 March 2013}}</ref> The EPA responded to the suit by pointing to research which found the ''Varroa'' mite responsible for the decline in bees and showed that the role of neonicotinoids in CCD had been overstated.<ref>{{cite news|last=Boyle|first=Alan|title=Pesticides aren't the biggest factor in honeybee die-off, EPA and USDA say|url=http://www.nbcnews.com/science/pesticides-arent-biggest-factor-honeybee-die-epa-usda-say-6C9745740|access-date=22 August 2013|newspaper=[[NBC News]]|date=2 May 2013|archive-url=https://web.archive.org/web/20140123222126/http://www.nbcnews.com/science/pesticides-arent-biggest-factor-honeybee-die-epa-usda-say-6C9745740|archive-date=23 January 2014|url-status=dead}}</ref> The Save America's Pollinators Act (H.R. 2692) was introduced in Congress in 2013,<ref name="Save America's Pollinators">{{cite web | url=https://www.govtrack.us/congress/bills/113/hr2692/text | title=Text of the Saving America's Pollinators Act of 2013 | work=[[GovTrack]] | date=16 July 2013 | access-date=6 October 2014}}</ref><ref>{{cite web|title=Blumenauer Announces Legislation to Protect Pollinators, Prevent Mass Bee Die-Offs|url=http://blumenauer.house.gov/images/stories/2013/Save_Americas_Pollinators_One_Pager.pdf|work=Blumenauer.house.gov|publisher=[[United States House of Representatives]]|access-date=6 October 2014|url-status=dead|archive-url=https://web.archive.org/web/20140918210922/http://blumenauer.house.gov/images/stories/2013/Save_Americas_Pollinators_One_Pager.pdf|archive-date=18 September 2014}}</ref> and reintroduced in 2015. The proposed act asked that neonicotinoids be suspended until a full review of their impacts had occurred.<ref>https://www.congress.gov/bill/114th-congress/house-bill/1284 Saving America's Pollinators Act (H.R. 1284)</ref>

====Fipronil====
[[Fipronil]] is a [[Phenylpyrazole insecticides|phenylpyrazole insecticide]], with a broad-spectrum [[systemic pesticide|systemic]] mode of action. Fipronil is designed to eliminate insects similar to bees, such as yellowjackets (''[[Vespula germanica]]'') and many other colonial pests by a process of 'toxic baiting', whereby one insect returning to the hive spreads the pesticide among the brood.<ref name="autogenerated811">{{cite journal |doi=10.1603/0022-0493-94.4.811 |last1=Sackmann |first1=P |last2=Rabinovich |first2=M |last3=Corley |first3=JC |title=Successful removal of German yellowjackets (Hymenoptera: Vespidae) by toxic baiting |journal=[[Journal of Economic Entomology]] |volume=94 |issue=4 |pages=811–16 |year=2001 |pmid=11561837|s2cid=44836981 }}</ref>

In May 2003, the French Directorate-General of Food at the Ministry of Agriculture determined that a case of mass bee mortality observed in southern France was related to acute fipronil toxicity. Toxicity was linked to defective seed treatment, which generated dust. In February 2003, the ministry decided to temporarily suspend the sale of BASF crop protection products containing fipronil in France, including the "Regent" brand.<ref>{{cite web | url = http://www.agro.basf.com/agr/AP-Internet/en/content/news_room/news/basf-fipronil-temporary-suspension-in-france-statement | title = BASF statement regarding temporary suspension of sales of crop protection products containing fipronil in France |author1=Elise Kissling |author2=BASF SE | year = 2003 }}</ref>

In 2010 fipronil was blamed for the spread of CCD among bees, in a study by the Minutes-Association for Technical Coordination Fund in France, which found that even at very low nonlethal doses, this pesticide impaired the ability to locate the hive, resulting in large numbers of foragers lost with every pollen-finding expedition, though no mention was made regarding any of the other symptoms of CCD;<ref name="globo1">{{cite web|last1=Lima|first1=P|title=Abelhas com microchip|url=http://revistagloborural.globo.com/GloboRural/0,6993,EEC1707683-5809,00.html|publisher=GloboRural|access-date=2017-08-20|language=pt|date=June 2010|archive-url=https://web.archive.org/web/20100112092243/http://revistagloborural.globo.com/GloboRural/0,6993,EEC1707683-5809,00.html|archive-date=12 January 2010|url-status=dead}}</ref> other studies, however, have shown no acute effect of fipronil on honey bees.<ref name="autogenerated6">{{cite journal|url=http://popups.ulg.ac.be/NFG/document.php?id=1258|title=No acute mortalities in honey bee colonies (''Apis mellifera'') after the exposure to sunflower cultures|journal=Entomologie Faunistique – Faunistic Entomology|access-date=2010-06-27|date=January 2009|last1=Carpentier|first1=Patrice|last2=Faucon|first2=Jean-Paul|last3=Clément|first3=Marie-Claude|last4=Cougoule|first4=Nicolas|last5=Chauzat|first5=Marie-Pierre|archive-date=3 October 2011|archive-url=https://web.archive.org/web/20111003130010/http://popups.ulg.ac.be/NFG/document.php?id=1258|url-status=dead}}</ref>

[[File:Bienenwabe mit Eiern und Brut 5.jpg|thumb|Honeycomb of honey bees with eggs and larvae. The walls of the cells have been removed. The larvae (drones) are about 3 or 4 days old.]]

=== Fungicides ===
In 2013, researchers collected pollen from hives and fed it to healthy bees. The pollen had an average of nine different pesticides and fungicides. Further, the researchers discovered that bees that ate pollen with fungicides were three times more likely to be infected by parasites. Their study shows that fungicides, thought harmless to bees, may actually play a significant role in CCD. Their research also showed that spraying practices may need to be reviewed because the bees sampled by the authors foraged not from crops, but almost exclusively from weeds and wildflowers, suggesting that bees are more widely exposed to pesticides than thought.<ref>{{cite journal| title= Crop Pollination Exposes Honey Bees to Pesticides Which Alters Their Susceptibility to the Gut Pathogen Nosema ceranae | journal=PLOS ONE | volume= 8 | issue= 7 | pages= e70182 |author= Jeffery S. Pettis |author2=Elinor M. Lichtenberg |author3=Michael Andree |author4=Jennie Stitzinger |author5=Robyn Rose |author6=Dennis van Engelsdorp | year = 2013 | doi= 10.1371/journal.pone.0070182 | pmid= 23894612 |bibcode = 2013PLoSO...870182P | pmc=3722151| doi-access=free }}</ref>

[[Dennis vanEngelsdorp]], an entomologist at the University of Maryland, has been quoted as saying "Fungicides, which we didn't expect to harm insects, seem to have a sub-lethal effect on bee health". He went on further to state this is important because fungicides are not heavily regulated.<ref name="Benjamin2013" />

=== Antibiotics and miticides ===
Most beekeepers affected by CCD report that they use [[antibiotic]]s and [[Acaricide|miticides]] in their colonies, though the lack of uniformity as to which particular chemicals they use<ref name=Prelim/> makes it unlikely that any single such chemical is involved. However, it is possible that not all such chemicals in use have been tested for possible effects on honey bees, and could therefore potentially be contributing to the CCD phenomenon.<ref name="Oldroyd"/><ref>{{cite journal |last1=Hawthorne |first1=David J. |last2=Dively |first2=Galen P. |last3=Smagghe |first3=Guy |title=Killing Them with Kindness? In-Hive Medications May Inhibit Xenobiotic Efflux Transporters and Endanger Honey Bees |journal=PLOS ONE |date=2 November 2011 |volume=6 |issue=11 |pages=e26796 |doi=10.1371/journal.pone.0026796 |editor1-last=Smagghe |editor1-first=Guy |pmid=22073195 |pmc=3206626 |doi-access=free |bibcode=2011PLoSO...626796H }}</ref>

====Antibiotics====
A study at the University of Texas in Austin found that commonly used antibiotics found in beekeeping to prevent disease lower the gut microbial levels in honeybees,<ref name=":3" /> making them more susceptible to disease.<ref>{{Cite journal|last1=Daisley|first1=Brendan A.|last2=Chmiel|first2=John A.|last3=Pitek|first3=Andrew P.|last4=Thompson|first4=Graham J.|last5=Reid|first5=Gregor|date=December 2020|title=Missing Microbes in Bees: How Systematic Depletion of Key Symbionts Erodes Immunity|url=https://linkinghub.elsevier.com/retrieve/pii/S0966842X20301852|journal=Trends in Microbiology|language=en|volume=28|issue=12|pages=1010–1021|doi=10.1016/j.tim.2020.06.006|pmid=32680791|s2cid=220630113}}</ref> A widespread occurrence of viral infections within a beehive can lead to colony collapse. Researchers state that although the antibiotics are necessary, beekeepers should exercise caution when determining amount and length of use.<ref name=":3">{{cite journal |last1=Raymann |first1=Kasie |last2=Shaffer |first2=Zack |last3=Moran |first3=Nancy A. |title=Antibiotic Exposure Perturbs the Gut Microbiota and Elevates Mortality in Honeybees |journal=PLOS Biology |date=2017 |volume=15 |issue=3 |pages=e2001861 |doi=10.1371/journal.pbio.2001861 |pmid=28291793 |pmc=5349420 |doi-access=free }}</ref> A widespread occurrence of viral infections within a beehive can lead to colony collapse.

====Miticides====
Beekeepers use miticides to rid colonies of ''Varroa'' infestations; however, treatment can lead to higher levels of viral infections in colonies. High doses of treatment or the use of miticides for an extended period of time can lead to immune-suppression in honey bees, making them more susceptible to viruses.<ref>{{cite journal |last1=Francis |first1=Roy M. |last2=Nielsen |first2=Steen L. |last3=Kryger |first3=Per |last4=Martin |first4=Stephen J. |title=Varroa-Virus Interaction in Collapsing Honey Bee Colonies |journal=PLOS ONE |date=19 March 2013 |volume=8 |issue=3 |pages=e57540 |doi=10.1371/journal.pone.0057540 |pmc=3602523 |pmid=23526946 |bibcode=2013PLoSO...857540F |doi-access=free }}</ref>

2008 research by scientists from Pennsylvania State University found high levels of the miticides [[fluvalinate]] and [[coumaphos]] in samples of wax from hives, as well as lower levels of 70 other pesticides.<ref name = "Vanengeletal2010"/> Increased levels of the organophosphate Coumaphos in wax have been associated with decreased survivorship of developing queens.<ref name="Vanengeletal2010"/> Researchers from [[Washington State University]], under entomologist Steve Sheppard in 2009, confirmed high levels of pesticide residue in hive wax and found an association between it and significantly reduced bee longevity.<ref name="Environment News Service">{{cite web|title=Scientists Untangle Multiple Causes of Bee Colony Disorder|url=http://www.ens-newswire.com/ens/jul2009/2009-07-29-094.asp|archive-url=https://web.archive.org/web/20090802120305/http://www.ens-newswire.com/ens/jul2009/2009-07-29-094.asp|url-status=dead|archive-date=2 August 2009|publisher=[[Environment News Service]]|access-date=20 January 2011|year=2009}}</ref> A large 2010 survey of healthy and CCD-affected colonies also revealed elevated levels of pesticides in wax and pollen, but the amounts of pesticides were similar in both failing and healthy hives.<ref name="CCDPR2010"/>

===Climate change===
Environmental changes are known to have an effect on honeybee development. The increase in temperature and precipitation levels induced by [[climate change]] has been proven to decrease the likelihood of a bee colony surviving by 30% in a single generation, as well as decreasing the amount of new bee colonies being established.<ref>{{Cite web |title=Climate change is killing the bumblebees, study says |url=https://www.cbsnews.com/news/climate-change-is-killing-the-bumble-bees-study-says/ |access-date=2023-01-20 |website=www.cbsnews.com |date=6 February 2020 |language=en-US}}</ref> Extreme rainfall and lack thereof can both limit the extent to which bees are able to forage, thereby reducing their numbers and health.<ref>{{Cite web |last=Kerlin |first=Katherine E. |date=2022-10-14 |title=Climate Change Is Ratcheting Up the Pressure on Bees |url=https://www.ucdavis.edu/climate/blog/bees-face-many-challenges-and-climate-change-ratcheting-pressure |access-date=2023-01-20 |website=UC Davis |language=en}}</ref> 
[[File:Bee migration 9045.JPG|thumb|Moving spring bees from South Carolina to Maine for blueberry pollination]]

=== Bee rentals and migratory beekeeping ===
{{Further|Beekeeping}}
Since U.S. beekeeper [[Nephi Miller]] first began moving his hives to different areas of the country for the winter of 1908, migratory beekeeping has become widespread in America. Bee rental for pollination is a crucial element of U.S. agriculture, which could not produce anywhere near its current levels with native pollinators alone.<ref>{{cite web|last = Berenbaum|first = Prof. May R.|title = Colony Collapse Disorder and Pollinator Decline|work = Presentation to Subcommittee on Horticulture and Organic Agriculture, U.S. House of Representatives|publisher = The National Academies|date = 29 March 2007|url = http://www7.nationalacademies.org/ocga/testimony/Colony_Collapse_Disorder_and_Pollinator_Decline.asp|access-date = 2007-10-22|archive-date = 3 December 2013|archive-url = https://web.archive.org/web/20131203045756/http://www7.nationalacademies.org/ocga/testimony/Colony_Collapse_Disorder_and_Pollinator_Decline.asp|url-status = dead}}, specifically, "Close to 100 crop species in the U.S. rely to some degree on pollination services provided by this one species—collectively, these crops make up approximately 1/3 of the U.S. diet&nbsp;... Although economists differ in calculating the exact dollar value of honey bee pollination to American agriculture, virtually all estimates are in the range of billions of dollars".</ref> U.S. beekeepers collectively earn much more from renting their bees out for pollination than they do from honey production.{{Citation needed|date=January 2021}}

Researchers are concerned that trucking colonies around the country to pollinate crops, where they intermingle with other bees from all over, helps spread viruses and mites among colonies. Additionally, such continuous movement and re-settlement is considered by some a strain and disruption for the entire hive, possibly rendering it less resistant to all sorts of systemic disorder.<ref>{{cite news|url=https://select.nytimes.com/gst/abstract.html?res=F10B1FF8355A0C748EDDAB0894DF404482|author=Alexi Barrionuevo|title=Honeybees, Gone With the Wind, Leave Crops and Keepers in Peril|work=The New York Times|date=27 February 2007 }}</ref> In addition to the concern surrounding viruses and mites in transporting bees across the country, the stress bees experience in transport is a potential mechanism involved in colony collapse disorder.<ref>{{Cite web|url=https://www.epa.gov/pollinator-protection/colony-collapse-disorder|title=Colony Collapse Disorder|date=29 August 2013}}</ref>

=== Selective commercial breeding and lost genetic diversity in industrial apiculture ===
Most of the focus on CCD has been toward environmental factors. CCD is a condition recognised for greatest impact in regions of 'industrial' or agricultural use of commercially bred bee colonies. Natural breeding and colony reproduction of wild bees is a complex and highly selective process, leading to a [[genetic diversity|diverse genetic makeup]] in large within-colony populations of bees,<ref>{{cite web |url=http://www.ibra.org.uk/articles/20100421_1 |title=Levels of polyandry and intracolonial genetic relationships in Apis koschevnikovi |publisher=International Bee Research Association |date=21 April 2010 |access-date=2012-05-24 |url-status=dead |archive-url=https://web.archive.org/web/20120401094244/http://www.ibra.org.uk/articles/20100421_1 |archive-date=1 April 2012}}</ref> which might not be reproduced in commercially bred colonies.{{citation needed|date=February 2019}}{{explain|reason=this section needs some evidence of lost genetic diversity in industrial apiculture|date=February 2019}}

=== Malnutrition ===
In 2007, one of the patterns reported by the CCD Study Group at Pennsylvania State was that all producers in a preliminary survey noted a period of "extraordinary stress" affecting the colonies in question prior to their die-off, most commonly involving poor nutrition and/or drought.<ref name="Prelim" /> This was the only factor that ''all'' of the cases of CCD had in common in the report; accordingly, there appeared to be at least some significant possibility that the phenomenon was correlated to nutritional stress that may not manifest in healthy, well-nourished colonies. This was similar to the findings of another independent survey done in 2007 in which small-scale beekeeping operations (up to 500 colonies) in several states reported their belief that malnutrition and/or weak colonies was the factor responsible for their bees dying in over 50% of the cases, whether the losses were believed to be due to CCD or not.<ref name="ABJ707" />

Some researchers have attributed the syndrome to the practice of feeding [[high-fructose corn syrup]] (HFCS) to supplement winter stores. The variability of HFCS may be relevant to the apparent inconsistencies of results. One European writer has suggested a possible connection with HFCS produced from [[genetically modified maize|genetically modified corn]].<ref name=sueddeutsche>{{cite news|author = Petra Steinberger|title = Das spurlose Sterben|url = http://www.sueddeutsche.de/wissen/raetselhafter-exitus-der-bienen-das-spurlose-sterben-1.911906|work=[[Süddeutsche Zeitung]]|date = 12 March 2007|language = de|access-date=31 December 2010}}</ref> At least one researcher has stated, however, that if this were the sole factor involved, this should have led to the exclusive appearance of CCD in wintering colonies being fed HFCS, but many reports of CCD had occurred in other contexts with beekeepers who had not used HFCS.<ref>{{cite web |last1=Bromenshenk |first1=Jerry |title=HFCS and CCD |url=https://community.lsoft.com/scripts/wa-LSOFTDONATIONS.exe?A2=ind0702B&L=BEE-L&P=R5433 |website=BEE-L Archives (LSoft archive) |access-date=18 March 2019 |archive-url=https://archive.today/20190318042753/https://community.lsoft.com/scripts/wa-LSOFTDONATIONS.exe?A2=ind0702B&L=BEE-L&P=R5433 |archive-date=18 March 2019 |date=14 February 2007 |quote=Our surveys,&nbsp;... indicate that HFCS is NOT, in many cases, a factor. It may contribute (as another stressor), but we've got beekeepers who have never fed HFCS with the CCD problem.  We have bees that had great stores of honey and natural pollen, STRONG bee populations, and the bees crashed with CCD.  And feeding with sucrose does not necessarily protect the bees from CCD.}}</ref><!--This sentence is sourced to J. Bromenshenk, Professor of Research Division of Biological Sciences at the University of Montana, one of the primary researchers into the CCD phenomenon. I'm sure there is a better source somewhere, but in the meantime his comments on this topic can be found in the BEE-L archives (http://listserv.albany.edu:8080/archives/bee-l.html). -->

Other researchers have speculated that colony collapse disorder is mainly a problem of feeding the bees a [[monoculture]] diet when they should receive food from a variety of sources/plants. In winter, these bees are given a single food source such as [[corn syrup]] (high-fructose or other), sugar and pollen substitute. In summer, they may only pollinate a single crop (e.g., almonds, cherries, or apples).<ref>{{cite magazine|url=http://www.time.com/time/magazine/article/0,9171,1884835,00.html|archive-url=https://web.archive.org/web/20090315035531/http://www.time.com/time/magazine/article/0,9171,1884835,00.html|url-status=dead|archive-date=15 March 2009|title=Postcard from Hughson|last=Pickert|first=Kate |date=12 March 2009|magazine=[[Time (magazine)|Time]] |access-date=12 December 2009}}</ref> The monoculture diet is thus attributed to bee rentals and migratory bee keeping. While it is claimed that single pollen diets are greatly inferior to mixed pollen diets, there are a few pollens, however, that are acceptable for honey bees to be introduced to exclusively, including [[Melilotus|sweet clover]] and [[Mustard plant|mustard]].<ref name="Brodschneider 278–294">{{cite journal|last1=Brodschneider|first1=Robert|last2=Crailsheim|first2=Karl|title=Nutrition and health in honey bees|journal=Apidologie|date=21 April 2010|volume=41|issue=3|pages=278–94|doi=10.1051/apido/2010012|s2cid=40046635|url=https://hal.archives-ouvertes.fr/hal-00892087/file/hal-00892087.pdf}}{{open access}}</ref>

[[File:Drohnenpuppen 79d.jpg|thumb|left|Pupae of honeybee drones in opened cells at both sides of a honeycomb. The drones at the right side are some days older and more developed.]]

A study published in 2010 found that bees that were fed pollen from a variety of different plant species showed signs of having a healthier immune system than those eating pollen from a single species. Bees fed pollen from five species had higher levels of [[glucose oxidase]] than bees fed pollen from one species, even if the pollen had a higher protein content. The authors hypothesised that CCD may be linked to a loss of plant diversity.<ref>[http://news.bbc.co.uk/1/hi/sci/tech/8467746.stm Bee decline linked to falling biodiversity] Richard Black, BBC News, 20 January 2010</ref> Researchers found a proper diet that does lead to a healthy honey bee population. "The authors recommended a diet containing 1000 ppm potassium, 500 ppm calcium, 300 ppm magnesium and 50 ppm each of sodium, zinc, manganese, iron and copper."<ref name="Brodschneider 278–294"/> A 2014 studies found that bees fed high-fructose corn syrup or sugar shows downregulation in several genes related to protein metabolism and oxidation reduction as compared to those fed the similarly low-protein honey.<ref>{{cite journal |last1=Wheeler |first1=MM |last2=Robinson |first2=GE |title=Diet-dependent gene expression in honey bees: honey vs. sucrose or high fructose corn syrup. |journal=Scientific Reports |date=17 July 2014 |volume=4 |pages=5726 |doi=10.1038/srep05726 |pmid=25034029 |pmc=4103092|bibcode=2014NatSR...4E5726W }}</ref>

A 2013 study found that [[p-Coumaric acid|''p''-coumaric acid]], which is normally present in honey, assists bees in detoxifying certain pesticides. Its absence in artificial nutrients fed to bees may therefore contribute to CCD.<ref name=Berenbaum>{{cite journal | doi = 10.1073/pnas.1303884110  | title = Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera | year = 2013 | vauthors = Mao W, Schuler MA, Berenbaum MR | journal = Proceedings of the National Academy of Sciences of the United States of America | issue = 29 April 2013 | volume = 110 | pages = 8842–46|bibcode = 2013PNAS..110.8842M | pmid=23630255 | pmc=3670375| doi-access = free }}</ref>

=== Electromagnetic radiation ===
Despite considerable discussion on the Internet and in the lay media, there have been almost no careful studies, published in peer reviewed scientific literature, on effects of [[electromagnetic field]] exposure on honeybees.<ref name=":4"/><ref name=":6"/> One of the few peer-reviewed studies was published in 1981 and found that even at microwave radiation powers far higher than used in communication, that bees were not significantly affected.<ref>{{cite journal |last1=Gary |first1=Norman E. |last2=Westerdahl |first2=Becky Brown |title=Flight, orientation, and homing abilities of honeybees following exposure to 2.45-GHz CW microwaves |journal=Bioelectromagnetics |date=1981 |volume=2 |issue=1 |pages=71–75 |doi=10.1002/bem.2250020108|pmid=7284043 }}</ref>

A study on the non-thermal effects of [[radio frequency]] (RF) on honey bees (''[[Carniolan honey bee|Apis mellifera carnica]]'') reported there were no changes in behavior due to RF exposure from [[DECT]] [[Cordless telephone|cordless phone]] base stations operating at 1,880–1,900&nbsp;[[MHz]].<ref name="Stever Kuhn 2004">{{cite web |author=Stever, H. |author2=Kuhn, J. |year=2004 |title=How electromagnetic exposure can influence learning process |series=Modelling Effects of Electromagnetic Exposure on Learning Processes |url=http://www.bienenarchiv.de/forschung/2004_lernprozesse/Electromagnetic%20Exposure_Learning%20Processes.doc.pdf |via=www.bienenarchiv.de}}</ref> A later study established that close-range [[electromagnetic field]] (EMF) may reduce the ability of bees to return to their hive.<ref name="Harts Kuhn Stever 2006">{{cite journal |author1=Harst, W. |author2=Kuhn, J. |author3=Stever, H. |year=2006 |title=Can electromagnetic exposure cause a change in behaviour? Studying possible non-thermal influences on honey bees – an approach within the framework of educational informatics |journal=Acta Systemica |volume=6 |issue=1 |pages=1–6 |url=http://agbi.uni-landau.de/material_download/IAAS_2006.pdf |archive-url=https://web.archive.org/web/20120218185250/http://agbi.uni-landau.de/material_download/IAAS_2006.pdf |archive-date=2012-02-18|url-status=dead}}</ref> In the course of their study, one half of their colonies broke down, including some control hives that did not have embedded DECT base stations. In April 2007, news of this study appeared in various media outlets, beginning with an article in ''[[The Independent]]'', which stated that the subject of the study included mobile phones and had related them to CCD.<ref>{{cite news |last1=Lean |first1=Geoffrey |last2=Shawcross |first2=Harriet |title=Are mobile phones wiping out our bees? |url=https://www.independent.co.uk/environment/nature/are-mobile-phones-wiping-out-our-bees-5332810.html |access-date=9 November 2019 |newspaper=[[The Independent]] |place=UK |date=15 April 2007}}</ref> Although [[Mobile phone|cellular phones]] were implicated at the time by other media reports, they were not covered in the quoted study. The researchers involved have since stated that their research did not include findings on cell phones, nor their relationship to CCD, and indicated that the ''Independent'' article had misinterpreted their results and created "a horror story".<ref name=":4">{{cite news |url=http://www.iht.com/articles/2007/04/22/news/wireless23.php |title=Wireless: Case of the disappearing bees creates a buzz about cellphones |first=Eric |last=Sylvers |date=22 April 2007 |newspaper=International Herald Tribune |archive-url=https://web.archive.org/web/20090203191231/http://www.iht.com/articles/2007/04/22/news/wireless23.php |archive-date=2009-02-03|url-status=dead}}</ref><ref name=":6">{{cite news |title=Researchers: Often-cited study doesn't relate to bee colony collapse |url=http://www.fosters.com/apps/pbcs.dll/article?AID=/20070422/GJNEWS_01/104220119 |date=22 April 2007 |first=Chloe |last=Johnson |work=[[Foster's Daily Democrat]] |access-date=23 February 2022 |archive-date=12 August 2020 |archive-url=https://web.archive.org/web/20200812184114/https://www.fosters.com/apps/pbcs.dll/article?AID=%2F20070422%2FGJNEWS_01%2F104220119 |url-status=dead }}</ref>

A review of 919&nbsp;peer-reviewed scientific studies investigating the effects of EMF on wildlife, humans, and plants included 7&nbsp;studies involving honey bees; 6&nbsp;of which reported negative effects from exposure to EMF radiation, but none demonstrated any specific link to CCD.<ref>{{cite report |url=http://moef.nic.in/downloads/public-information/final_mobile_towers_report.pdf |title=Report on possible impact of communication tower on wildlife birds and bees |department=Ministry of Environment and Forests |publisher=Government of India |year=2011 |archive-url=https://web.archive.org/web/20121102091739/http://moef.nic.in/downloads/public-information/final_mobile_towers_report.pdf |archive-date=2 November 2012}}</ref> A 2004 exploratory study was conducted on the non-thermal effects of electromagnetic exposure and learning. The investigators did not find any change in behavior due to RF exposure from the DECT base station operating at 1880–1900&nbsp;MHz.<ref name="Stever Kuhn 2004" />

Honeybees can detect weak static, or low-frequency magnetic fields, which they use as one of several cues in navigation. However, no mechanism has been established by which weak radio frequency energy can affect the behavior of insects, apart from minor heating effects.<ref>{{cite journal |last1=Kirschvink |first1=Joseph L. |last2=Padmanabha |first2=S. |last3=Boyce |first3=C.K. |last4=Oglesby |first4=J. |title=Measurement of the threshold sensitivity of honeybees to weak, extremely low-frequency magnetic fields |journal=The Journal of Experimental Biology |year=1997 |volume=200 |issue=9 |pages=1363–68 |doi=10.1242/jeb.200.9.1363 |pmid=9319256 |url=https://jeb.biologists.org/content/jexbio/200/9/1363.full.pdf}}</ref>

=== Genetically modified crops ===
GM crops are not considered to be a cause of CCD. In 2008 a meta-analysis<ref>{{cite journal | last1 = Duan | first1 = JJ | last2 = Marvier | first2 = M | last3 = Huesing | first3 = J | last4 = Dively | first4 = G | last5 = Huang | first5 = ZY. | year = 2008 | title = A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae) | journal = PLOS ONE | volume = 3 | issue = 1| page = e1415 | doi=10.1371/journal.pone.0001415 | pmid=18183296 | pmc=2169303|bibcode = 2008PLoSO...3.1415D | doi-access = free }}</ref> of 25 independent studies assessing the effects of [[Bacillus thuringiensis|Bt]] Cry proteins on honeybee survival (mortality) showed that Bt proteins used in commercialized [[genetically modified crops|GE crops]] to control lepidopteran and coleopteran pests did not negatively impact the survival of honeybee larvae or adults. Additionally, larvae consumed only a small percent of their protein from pollen, and there was also a lack of geographic correlation between GM crop locations and regions where CCD occurred.<ref name=lemaux>{{cite journal | last1 = Lemaux | first1 = Peggy G. | s2cid = 52866120 | year =  2009| title = Genetically Engineered Plants and Foods: A Scientist's Analysis of the Issues (Part II) | journal = Annual Review of Plant Biology | volume = 60 | pages = 511–59 | doi = 10.1146/annurev.arplant.043008.092013 | pmid = 19400729 }}</ref>

== Management ==
[[File:Beekeeper keeping bees.jpg|thumb|Beekeeper managing bees]]{{As of|2007|3|alt=As of 1 March 2007}}, the [[Mid-Atlantic Apiculture Research and Extension Consortium]] (MAAREC) offered the following tentative recommendations for beekeepers noticing the symptoms of CCD:<ref name="MAAREC"/>{{Failed verification|date=February 2019}}

# Do not combine collapsing colonies with strong colonies.
# When a collapsed colony is found, store the equipment where you can use preventive measures to ensure that bees will not have access to it.
# If you feed your bees sugar syrup, use [[Fumagillin]].
# If you are experiencing colony collapse and see a secondary infection, such as [[European foulbrood|European Foulbrood]], treat the colonies with [[oxytetracycline]], not [[tylosin]].

Another proposed remedy for farmers of pollinated crops is simply to switch from using beekeepers to the use of [[native bee]]s, such as [[bumble bee]]s and [[mason bee]]s.<ref>{{cite web |url=http://attra.ncat.org/attra-pub/nativebee.html |title=Alternative Pollinators: Native Bees (Summary) |publisher=[[ATTRA]] |date=12 October 2011 |access-date=2012-05-24 |archive-url=https://web.archive.org/web/20110709203745/https://attra.ncat.org/attra-pub/nativebee.html |archive-date=9 July 2011 |url-status=dead }}</ref><ref>{{cite web |url=https://www.scribd.com/doc/40824563/Alternative-Pollinators-Native-Bees |title=Alternative Pollinators: Native Bees |publisher=Scribd.com |access-date=2012-05-24 |archive-date=7 November 2012 |archive-url=https://web.archive.org/web/20121107132909/http://www.scribd.com/doc/40824563/Alternative-Pollinators-Native-Bees |url-status=dead }}</ref> Native bees can be helped to establish themselves by providing suitable nesting locations and some additional crops the bees could use to feed from (e.g. when the pollination season of the commercial crops on the farm has ended).<ref>{{cite web |url=http://www.conservationinformation.org/partners/090107/rnt2.asp |title=Establishing a healthy population of native bees on your land |publisher=Conservationinformation.org |access-date=2010-06-22 |archive-url=https://web.archive.org/web/20110725075333/http://www.conservationinformation.org/partners/090107/rnt2.asp |archive-date=25 July 2011 |url-status=dead }}</ref><ref>{{cite magazine|url=https://www.wired.com/wiredscience/2009/06/beecounting/ |title=Use of native bees to counter colony collapse disorder |magazine=[[Wired (magazine)|Wired]] |access-date=2010-06-22 |first=Alexis |last=Madrigal |date=5 June 2009}}</ref>

A British beekeeper successfully developed a strain of bees that are resistant to varroa mites.<ref>[http://www.metro.co.uk/news/838981-british-beekeepers-parasite-resistant-bee-could-save-the-world Beekeeper Ron Hoskins breeds 'indestructible bees' in Swindon]. Metro.co.uk (24 August 2010). Retrieved on 2010-10-19.</ref><ref>[http://www.fastcompany.com/1684629/a-for-british-beekeeper-as-he-develops-mite-resistant-strain-of-honeybee A+ for British Beekeeper as He Develops Mite-Resistant Strain of Honeybee]. Fast Company (24 August 2010). Retrieved on 2010-10-19.</ref><ref>[http://www.treehugger.com/files/2010/08/new-honeybee-breed-key-to-combating-colony-collapse-disorder.php New Honeybee Breed Key to Combating Colony Collapse Disorder] {{Webarchive|url=https://web.archive.org/web/20100828055446/http://www.treehugger.com/files/2010/08/new-honeybee-breed-key-to-combating-colony-collapse-disorder.php |date=28 August 2010 }}. TreeHugger. Retrieved on 2010-10-19.</ref> [[Russian honey bee]]s also resist infestations of [[varroa mites]] but are still susceptible to other factors associated with colony collapse disorder, and have detrimental traits that limit their relevance in commercial apiculture.{{Citation needed|date=January 2021}}

In the United Kingdom, a national bee database was set up in March 2009 to monitor colony collapse as a result of a 15% reduction in the bee population that had taken place over the previous two years.<ref>{{cite news|last1=Prince|first1=Rosa|title=National Bee Database to be set up to monitor colony collapse|url=https://www.telegraph.co.uk/news/earth/wildlife/4963510/National-Bee-Database-to-be-set-up-to-monitor-colony-collapse.html|access-date=2017-08-20|work=Telegraph.co.uk|date=9 March 2009}}</ref> In particular, the register, funded by the [[Department for Environment, Food and Rural Affairs]] and administered by the [[National Bee Unit]], will be used to monitor health trends and help establish whether the honey industry is under threat from supposed colony collapse disorder. Britain's 20,000 beekeepers have been invited to participate. In October 2010, David Aston of the British Beekeepers' Association stated, "We still do not believe CCD is a cause of colony losses in the UK, however we are continuing to experience colony losses, many if not most of which can be explained. The approach being taken in UK beekeeping is to raise the profile of integrated bee health management, in other words identifying and trying to eliminate factors that reduce the health status of a colony. This incorporates increasing the skill level of beekeepers through training and education, raising the profile of habitat destruction and its effect of forage (nectar and pollen) availability, and of course research on the incidence and distribution of diseases and conditions in the UK together with more applied research and development on providing solutions."<ref name="BBC NEWS">{{cite news| url=http://news.bbc.co.uk/2/hi/europe/7739798.stm | work=BBC News | title=Why are Europe's bees dying? | date=20 November 2008}}</ref><ref name="Telegraph">{{cite news| url=https://www.telegraph.co.uk/gardening/beekeeping/8050583/Study-finds-causes-of-Colony-Collapse-Disorder-in-bees.html | location=London | work=The Daily Telegraph | first=Ian | last=Douglas | title=Study finds causes of Colony Collapse Disorder in bees | date=8 October 2010}}</ref>

== Economic and ecological impact ==
{{See also|List of crop plants pollinated by bees}}
Honey bees are not native to [[the Americas]], therefore their necessity as pollinators in the U.S. and other regions in the Western Hemisphere is limited to strictly agricultural and ornamental uses, as no native plants require honey bee pollination, except where concentrated in [[monoculture]] situations—where the pollination need is so great at bloom time that pollinators must be concentrated beyond the capacity of native bees (with current technology).{{Citation needed|date=January 2021}}

The phenomenon is particularly important for crops such as [[almond]] growing in California, where honey bees are the predominant pollinator and the crop value in 2011 was $3.6&nbsp;billion.<ref>{{Cite journal|title = Nesting site density and distribution affect Osmia lignaria (Hymenoptera: Megachilidae) reproductive success and almond yield in a commercial orchard|last = Artz|first = DR|date = November 2013|journal = Insect Conservation and Diversity|doi = 10.1111/icad.12026|volume=6|issue = 6|pages=715–24|s2cid = 84798030}}</ref> In 2000, the total U.S. crop value that was wholly dependent on honey bee pollination was estimated to exceed $15&nbsp;billion.<ref>{{cite web |author1=Morse, R.A. |author2=Calderone, N.W. |title=The value of honey bees as pollinators of US crops in 2000 |publisher=[[Cornell University]] |year=2000 |url=http://www.beeculture.com/content/PollinationReprint07.pdf |url-status=dead |archive-url=https://web.archive.org/web/20120815060751/http://www.beeculture.com/content/PollinationReprint07.pdf |archive-date=15 August 2012}}</ref> California almond production increased from 370&nbsp;million pounds in 1995 to a record 2,500&nbsp;million pounds in 2019, with an increase of over 30% in the last decade alone.<ref>{{cite web |title=2019 California almond forecast |url=https://www.nass.usda.gov/Statistics_by_State/California/Publications/Specialty_and_Other_Releases/Almond/Forecast/201905almpd.pdf |website=USDA National Agricultural Statistics Service |access-date=9 November 2019 |date=10 May 2019}}</ref> Because of such high demand in pollinators, the cost of renting honey bees has increased significantly, and California's almond industry rents approximately 1.6''&nbsp;''million honey bee colonies during the spring to pollinate their crop.<ref>{{cite web|url=http://www.almonds.com/pollination|title=Honey Bees Are Essential for a Successful Almond Crop|publisher=California Almonds}}</ref> Worldwide, honeybees yield roughly $200&nbsp;billion in pollination services.<ref name="Oldroyd" />

They are responsible for [[pollination]] of approximately one third of the United States' crop species, including such species as almonds, [[peach]]es, apples, pears, [[cherry|cherries]], [[raspberry|raspberries]], [[blackberry|blackberries]], [[Cranberry|cranberries]], [[watermelon]]s, [[cantaloupe]]s, [[cucumber]]s, and [[strawberry|strawberries]]. Many, but not all, of these plants can be (and often are) pollinated by other insects in the U.S., including other kinds of bees (e.g., [[squash bee]]s on cucurbits<ref>{{cite journal |first1=Vincent J. |last1=Tepedino |date=April 1981 |title=The Pollination Efficiency of the Squash Bee (''Peponapis pruinosa'') and the Honey Bee (''Apis mellifera'') on Summer Squash (''Cucurbita pepo'') |journal=Journal of the Kansas Entomological Society |volume=54 |issue=2 |pages=359–77 |jstor=25084168}}</ref>), but typically not on a commercial scale. While some farmers of a few kinds of native crops do bring in honey bees to help pollinate, none specifically need them, and when honey bees are absent from a region, there is a presumption that native pollinators may reclaim the niche, typically being better adapted to serve those plants (assuming that the plants normally occur in that specific area).{{Citation needed|date=January 2021}}

However, even though on a per-individual basis, many other species are actually more efficient at pollinating, on the 30% of crop types where honey bees are used, most native pollinators cannot be mass-utilized as easily or as effectively as honey bees—in many instances they will not visit the plants at all. Beehives can be moved from crop to crop as needed, and the bees will visit many plants in large numbers, compensating via [[saturation pollination]] for what they lack in efficiency. The commercial viability of these crops is therefore strongly tied to the [[beekeeping]] industry. In [[PRC|China]], hand pollination of apple orchards is labor-intensive, time-consuming, and costly.<ref>Partap, Uma Partap and Tej. Pollination of apples in China. 2 September 2005</ref><ref>{{cite journal |author1=Partap, U.M.A.|author2=T.E.J. Partap |author3=H.E. Yonghua|year=2001 |title=Pollination failure in apple crop and farmers management strategies in Hengduan Mountains, China|journal=[[Acta Horticulturae]]|issue=561 |pages=225–30 |doi=10.17660/actahortic.2001.561.32}}</ref>

In regions of the Old World where they are indigenous, honeybees (''Apis mellifera'') are among the most important pollinators, vital to sustain natural habitats there in addition to their value for human societies (to sustain food resources).<ref name=":0">{{Cite report|url = http://archive-ouverte.unige.ch/unige:32251|title = Global honey bee colony disorders and other threats to insect pollinators|date = 2010|last1 = Kluser|first1 = Stéphane |last2 = Neumann|first2 = Peter |last3=Chauzat |first3=Marie-Pierre |last4=Pettis |first4=Jeffery S. |last5=Peduzzi | first5= Pascal |last6=Witt |first6= Ron |last7=Fernandez |first7=Norberto |last8=Theuri |first8=Mwangi |publisher=[[University of Geneva]]|quote=Pollination services are provided both by wild, free-living organisms (mainly bees, but also to name a few many butterflies, moths and flies), and by commercially managed bee species. Bees are the predominant and most economically important group of pollinators in most geographical regions.}}</ref> Where honeybee populations decline, there is also a decline in plant populations.<ref name=":1">{{cite journal|title = Global pollinator declines: trends, impacts and drivers|date = June 2010|last1 = Potts|first1 = Simon|last2 = Biesmeijer|first2 = Jacobus|doi=10.1016/j.tree.2010.01.007|volume=25|issue = 6|journal=Trends in Ecology & Evolution|pages=345–53|pmid=20188434| bibcode=2010TEcoE..25..345P |citeseerx = 10.1.1.693.292}}</ref> In agriculture, some plants are completely dependent on honeybees to pollinate them to produce fruit, while other plants are only dependent on honeybees to enhance their capacity to produce better and healthier fruits. Honeybees also help plants to reduce time between flowering and fruit set, which reduces risk from harmful factors such as pests, diseases, chemicals, weather, etc.<ref name=":0" /> Specialist plants that require honeybees will be at more risk if honeybees decline, whereas generalist plants that use other animals as pollinators (or wind pollinating or self-pollinating) will suffer less because they have other sources of pollination.<ref name=":0" />

With that said, honeybees perform some level of pollination of nearly 75% of all plant species directly used for human food worldwide.<ref name=":0" /><ref name=":2">{{cite journal|title = Buzziness as usual? Questioning the global pollination crisis|date = July 2005|last = Ghazoul|first = Jaboury|doi=10.1016/j.tree.2005.04.026|pmid = 16701398|volume=20|issue = 7|journal=Trends in Ecology & Evolution|pages=367–73}}</ref> Catastrophic loss of honeybees could have significant impact, therefore; it is estimated that seven out of the 60 major agricultural crops in North American economy would be lost, and this is only for one region of the world. Farms that have intensive systems (high density of crops) will be impacted the most compared to non-intensive systems (small local gardens that depend on wild bees) because of dependence on honeybees. These types of farms have a high demand for honeybee pollination services, which in the U.S. alone costs $1.25&nbsp;billion annually.<ref name=":2" /> This cost is offset, however, as honeybees as pollinators generate 22.8 to 57&nbsp;billion Euros globally.<ref name=":1" />

== In the media ==
* A 2007 episode of ''[[Nature (TV series)|Nature]]'', "Silence of the Bees", offered several speculative reasons for the phenomenon.<ref>{{cite web|url=https://www.pbs.org/wnet/nature/silence-of-the-bees-introduction/38/|title=Silence of the Bees (2011)|website=[[PBS]]|date=16 February 2011}}</ref>
* The 2009 documentary ''[[Vanishing of the Bees]]'' pointed to neonicotinoid pesticides as being the most likely culprit, though the experts interviewed conceded that no firm data yet existed.<ref>{{cite news|last1=Jamieson|first1=Alastair|title=Pesticides blamed for vanishing bees|url=https://www.telegraph.co.uk/news/earth/agriculture/6245639/Pesticides-blamed-for-vanishing-bees.html|access-date=2017-08-20|work=Telegraph.co.uk|date=30 September 2009}}</ref>
* The 2010 feature-length documentary ''[[Queen of the Sun|Queen of the Sun: What Are the Bees Telling Us?]]'' featured interviews with beekeepers, scientists, farmers, and philosophers.<ref>{{cite web|url=http://www.queenofthesun.com/about/story/ |title=What Are the Bees Telling Us? &#124; The Story |publisher=Queen of the Sun |access-date=2012-05-24}}</ref>
* The 2012 documentary ''Nicotine Bees'' argued that neonicotinoid pesticides are principally responsible for colony collapse disorder.<ref>Pierre Terre Production, 2012, viewable on YouTube</ref>
* ''[[More than Honey]]'', a 2012 documentary, examined the relationship between humans and bees and explored possible causes of CCD.<ref>{{cite web|url=http://www.morethanhoneyfilm.com/about.html |title=More than Honey – about the film |access-date=2013-07-28}}</ref>
* In [[List of Elementary episodes#Season 3 (2014–15)|season three]] of the TV series ''[[Elementary (TV series)|Elementary]]'', CCD was a recurring theme with Holmes blaming pesticides in episode 10 and theorizing cures in episode 14. In episode 23 "Absconded", Holmes and Watson investigated the death of a USDA researcher undertaking field studies of a CCD outbreak in Northeast USA.{{Citation needed|date=January 2021}}
* The 2016 short film ''Colony Collapse Disorder: A Life Without Bees'', showed an exaggerated, dystopian future of a life after bees.<ref>{{cite web|url=http://www.spurgo.de/ccd/ |title=Colony Collapse Disorder – a life without bees |access-date=2016-10-27|date=2016-08-17 }}</ref>
* The ''[[Black Mirror]]'' episode "[[Hated in the Nation]]" showed a future in which mechanical bees were developed to combat CCD.{{Citation needed|date=January 2021}}
* In the ''[[Cloak & Dagger (TV series)|Cloak & Dagger]]'' episode "Funhouse Mirrors", Tandy Bowen and Mina Hess discussed the dwindling of [[American bumblebee]]s every few decades. The [[Cloak & Dagger season 1|season 1 finale]] was "Colony Collapse".{{Citation needed|date=January 2021}}

== See also ==
* [[Centre for Integrative Bee Research]] (CIBER)
* [[Beehives]]
* [[Pesticide misuse]]
* [[Pollinator decline]]
* [[Kakugo virus]]

== References ==
{{Reflist|25em}}

== Further reading ==
{{Refbegin}}
* {{Cite book|title=Fruitless Fall: The Collapse of the Honey Bee and the Coming Agricultural Crisis|last=Jacobsen|first=Rowan|publisher=Bloomsbury|year=2009|isbn=978-1-59691-537-4|location=New York|url-access=registration|url=https://archive.org/details/fruitlessfallcol0000jaco}}
* {{Skeptoid | id=4524 | number= 524| title=Colony Collapse Disorder: Science and Pseudoscience | date= June 21, 2016| guote= | access-date=}}
{{Refend}}

{{Pollination management}}
{{BeeColonyMemberTypes|state=collapsed}}
{{Authority control}}

{{DEFAULTSORT:Colony Collapse Disorder}}
[[Category:Bee diseases]]
[[Category:Bee ecology]]
[[Category:Environmental controversies]]
[[Category:Insect conservation]]
[[Category:Population ecology]]
[[Category:Unexplained disappearances]]