A Causal Analysis of Observed Declines in Managed Honey Bees (Apis mellifera)

Figures & data

Figure 1 Causal analysis approach used for assessing reduced overwinter survival of honey bee colonies. (Color figure available online.)

Table 1 List of candidate causes.

Stressor	Description	Reference
Viral diseases
Acute Bee Paralysis Virus (ABPV) and Chronic Bee Paralysis Virus (CBPV)	ABPV and CBPV are Aparaviruses, + single-stranded RNA viruses in the Dicistroviridae family. Both viruses cause uncontrollable trembling that prevents flight and causes paralysis.	EMBL-EBL (no date)
Black Queen Cell Virus (BQCV)	BQCV is a Cripavirus, a + sense, single-stranded RNA virus in the Dicistroviridae family. BQCV affects queen larvae, which die and turn black after the cell is sealed.	Oregon State University (2008)
Cloudy Wing Virus (CWV)	CWV is an icosahedral virus that causes the wings to become opaque due to crystalline structures of viral particles between muscle fibers; heavy infestation can cause mortality.	Biosecurity Authority Ministry of Agriculture and Forestry (2003)
Deformed Wing Virus (DWV)	DWV is an Aparavirus, + sense, single-stranded RNA virus in the Dicistroviridae family. DWV symptoms include vestigial and crumpled wings, bloated abdomen, paralysis, and severely shortened adult life span for worker and drone bees. DWV in combination with Varroa mites leads to immune suppression and subsequent disease from other pathogens.	Highfield et al. (2009)
Invertebrate Iridescent Virus (IIV-6)	IIV-6 is a double-stranded DNA virus in the Iridoviridae family. IIV-6 causes larvae to become inactive and die.	Bromenshenk (2011)
Israeli Acute Paralysis Virus (IAPV)	IAPV is an Aparavirus, a + single-stranded RNA virus in the Dicistroviridae family. IAPV causes wing tremors that progress to paralysis and then death outside of the hive.	Beeologics (no date)
Kashmir Bee Virus (KBV)	KBV is an Aparavirus, + single-stranded RNA virus in the Dicistroviridae family. KBV causes hairlessness, an oily appearance, an inability to fly, trembling, and eventual death.	British Columbia Ministry of Agriculture (2012)
Lake Sinai Virus 1 and 2 (LSV)	LSV I and 2 are RNA viruses discovered in 2011.	Runckel et al. (2011)
Sacbrood Virus (SBV)	SBV is an Iflavirus, + sense, single-stranded RNA virus in the Iflaviridae family. SBV infects larvae in the pre-pupa stage prior to cell capping and causes liquid to fill in the loose outer skin, resulting in death.	Agricultural Research Council (2010)
Varroa Destructor Virus 1 (VDV1)	VDV1 is an Iflavirus, a + sense, single-stranded RNA virus in the Iflaviridae family. VDV1 does not have a pathology description but appears to have the same effects as the Deformed Wing Virus.	Moore et al. (2011)
	Bacterial diseases
American foulbrood	American foulbrood is caused by Paenibacillus larvae subsp. Larvae, a rod-shaped, chain-forming bacterium. Larvae ingesting spores in their food can become diseased and die with as few as 35 spores.	Shimanuki and Knox (2000) and University of Georgia (2011)
European foulbrood (EFB)	European foulbrood is caused by Melissococcus plutonius, a short, non-spore-forming bacterium. These bacteria multiply and remain in the gut of larvae and compete for food, causing the larvae to die from starvation.	Shimanuki and Knox (2000) and Food and Environment Research Agency (2009)
Fungal diseases
Chalkbrood	Chalkbrood is caused by the fungus Ascosphaera apis. Infected larvae rapidly reduce food consumption and then stop eating altogether. Infected larvae are covered by white fibrous mycelium, which fills the entire cell, and the larvae usually die after the cell has been capped.	Calderone (2001) and Aronstein and Murray (2010)
Nosema apis and Nosema ceranae	N. apis and N. ceranae are microsporidian fungi that invades the intestinal tracts of adults. Worker bees ingest spores when they are <1 week old and will not digest food well and are not capable of producing brood food secretions. Their lifespan is reduced by up to 78% and infected queens are superseded with a month. Bees are unable to leave the hive to eliminate waste, and dysentery develops. Nosema ceranae is replacing Nosema apis, even though its spores are less durable.	Runckel et al. (2011); Mussen (2011), Fries (2010) and Canadian Association of Professional Apiculturists (no date)
Stonebrood	Stonebrood is caused by the fungus Aspergillus (A. flavus, A. fumigatus, A. niger, and other species). Fungal mycelia penetrate the larvae and after death, the infected larvae become hardened.	Shimanuki and Knox (2000)
Pests and parasites
Crithidia	Crithidia are flagellate protozoan parasites found in the lumen or attached to the epithelium of the hindgut and rectum of adults. Their role in honeybee health is unclear but infestations in bumble bees during stressful conditions affect behavior and life span.	Shimanuki and Knox (2000), Evans and Schwarz (2011)
Greater Wax Moth (Galleria mellonella) and Lesser Wax Moth (Achroia grisella)	Due to its size, the Greater Wax moth is a more important pest. Adult wax moths do not affect the colony or spread disease, but wax moth larvae damage the comb by obtaining nutrients from honey, pollen, etc.	Mid-Atlantic Apicultural Research & Extension Consortium (2000), Shimanuki and Knox (2000), and Sanford (1995)
Phorid fly (Apocephalus borealis)	The phorid fly kills the bee upon emergence of the larva. It causes infected bees to become disoriented and stranded away from the hive. Phorid flies can be potential vectors for Nosema ceranae and DMV.	Core et al. (2012)
Small hive beetle (SHB) (Aethina tumida)	SHB does not affect the bee directly but affects the quality of the honey and in turn, affects the colony. Yeast from defecating SHB cause fermentation of the honey; the queen ceases laying, and the infested colony may be absconded.	Ellis and Eillis (2010), Zawislak (no date), and Ellis (2012)
Tracheal mites (Acarapsis woodi)	Tracheal mites are parasites that feed on honey bee hemolymph by piercing the tracheae. Bees die due to respiratory disruption from mites clogging the tracheae, from microorganisms entering the hemolymph, and from the loss of hemolymph.	Eishen (1987), USDA BARC (2002), and Sammataro et al. (2000)
Varroa mite (Varroa destructor)	Varroa mites are ectoparasites that feed on the hemolymph of immature and adult honey bees. Infected pupae do not develop into adults, and those that emerge have shortened abdomens, misshapen wings, deformed legs, and decreased weight. Varroa can transmit viruses such as DWV, ABPV, CBPV, SPV, BQCV, KBV, CWV, and SBV.	LeConte et al. (2012), Shimanuki and Knox (2000), and Ellis and Nalen (2010)
Environmental
Availability and quality of water	Limited access to water or access to contaminated water can affect honey bee health.	USDA (2012)
Bacillus thuringiensis (Bt) pollen	Bt is a gram-positive bacterium with Cry toxins that are used in insect-resistant genetically modified crops. Bt proteins in pollen can affect the hypopharyngeal gland in nurse bees and affect the ability to make brood food.	Rose et al. (2007)
Cell phones	Cell phones and cell phone towers have been linked to honey bee health in the popular media, originating from a small study in Germany that looked at whether a base station for cordless phones could affect honey bee homing systems.	USDA (2012)
Loss of feral populations resulting in reduced diversity of drones	A decrease in feral populations reduces the genetic pool from drones, and in turn, reduces the genetic variability of the queen's progeny. Loss of genetic variability can result in offspring with low genetic quality that are susceptible to disease and other effects.	NC State University (no date)
Reduction of propolis (saps and resins)	Propolis are resin and sap mixtures from plant sources used by honey bees to seal open spaces in the hive. Propolis is used to reinforce the structure of the hive, for protection against disease and parasites, and reduction in vibration.	Simone-Finstrom and Spivak (2010)
Sun spots	Sun spots are temporary events on the sun caused by intense magnetic activity. Sun spots cause disturbances in the earth's magnetic field, altering the honey bee orientation system for navigation.	Ferrari and Cobb (2010)
Weather events	Extreme weather events such as cold snaps and storms can result in colony loss, threaten nutritional success and ability to forage, and affect immunocompetence of bees already weakened by other factors.	Underwood and van Engelsdorp (2007) and Oliver (2010)
Beekeeping practices
Aggregation of hives in large agricultural situations	The overcrowding in apiaries as honey bees are transported to agricultural areas for pollination services induces stress and causes poor nutrition.	USDA (2012)
Antibiotics	Antibiotics are used to prevent honey bee disease (e.g., tetracycline is used for American foulbrood). However, resistance to tetracycline has prompted the use of new antibiotics like Tylosin. It is suspected that new antibiotics can affect the beneficial bacteria in honey bee guts.	Hathaway (2012)
Fungicides (in-hive)	Some classes of fungicides, such as ergosterol biosynthesis inhibitors, can inhibit cytochrome P450-mediated detoxification of pesticides.	Johnson et al. (2010)
Genetics (telomere premature aging syndrome)	Telomeres are protective DNA structures that provide a buffer for incomplete DNA replication during cell division in somatic cells. The gradual shortening of teleomeres may limit the lifespan of these somatic cells, causing impaired tissue regeneration and compromised immune systems.	Stindl and Stindl (2010)
Miticides (in-hive)	Miticides such as fluvalinate, coumaphos, and thymol are used to control Varroa infestations. Miticides can cause honey bee mortality, affect reproduction, and result in physical abnormalities and atypical behavior. Miticides can also interfere with the ability to properly integrate stimuli that elicit feeding, mating, colony defense, and communication behaviors.	Burley (2007), Haarmann et al. (2002), and Frost (2010)
Poor queens	Queens are often replaced when they are no longer productive. Due to genetics and poor health, poor queens can produce progeny with compromised health and less than desirable genetic diversity.
Stress (e.g., transportation)	Stress, such as migratory stress during transportation, can compromise the immune system and increase disease susceptibility.	Johnson (2010)
Pesticides
Fungicides (external)	Fungicides are used to protect agricultural crops from fungal infections. For example, pyrethroids, organophosphates, carbamates, DDT, lidinale, etc. Neonicotinoids area sub-group of insecticides.
Insecticides (external)	Insecticides used on crops to prevent insect damage may have effects. For example, pyrethroids, organophosphates, carbamates, DDT, lindate, etc. Neonicotinoids are a sub-group of insecticides.
Neonicotinoids	Neonicotinoids are systemic neuro-active insecticides that can cause behavioral changes, reduce foraging activity, and increase foraging flight distance, and can cause acute mortality to honey bees at high doses.	Schneider et al. (2012)
Nutrition
Nutrition deficit (quality of food)	Pollen is a protein source and nectar is a carbohydrate source. The diversity and quality of food can affect a colony's number of pollen foragers.	Pernal and Currie (2001)
High-fructose corn syrup (HFCS)	HFCS is used in supplemental feeding. Problems associated with HFCS include toxicity due to hydromethylfurfural (HMF) if improperly stored.	Pernal and Currie (2001) and Alaux et al. (2010)
Starvation (quantity of food)	Nutrition is related to the proximity of the hives to available foods. The lack of adequate nutrition is partly a management issue. The lack of pollen resources just prior to winter may lead to immunosuppression, affect brood-rearing capacities, and decrease preparation for overwintering.	Mattila and Otis (2007)

Table 2 Weight-of-evidence for candidate causes and consistency of evidence.

			Cause–response relationship
		Co-occurrence			Known		Conclusions
Candidate	Time	(Spatial and	Sufficiency	Sufficiency	mechanism		of consistency
cause	order	temporal)	(laboratory)	(field)	of action	Alteration	of evidence
Viral diseases
ABPV + KBB + IAPV	−	+	+/0	+	+	0	Unlikely
BQCV + SBV +CBPV +LSV 1 2	0	+	0	0	0	0	Indeterminate
DWV in combination with other causes		++	++	+	+	++	Possible/contributor
IAPV	+						Possible/contributor
IIV–6 CWV VDV1				−			Indeterminate
Varroa Mites + virus	+++	+++	+++	+++	++	+++	Probable
Bacterial diseases
American foulbrood	−	−	+	−	+	——	Unlikely
European foulbrood	−	−				−	Unlikely
Fungal diseases
Chalkbrood	−	0				−	Unlikely
Nosema apis	−			+	+	+	Unlikely alone/ contributor
Nosema ceranae	+	+ / −		−	+	0	Unlikely alone/ contributor
N. apis + N. ceranae	+	−	+	+			Unlikely alone/ contributor
Stonebrood	−	−	−	−	+	−	Unlikely
Pests and parasites
Crithidia	0	+	0	0	0	0	Indeterminate
Phorid fly	0	−	0	0		0	Unlikely
Small hive beetle	−	−					Unlikely
Tracheal mites	−	−	+	−	+	NE	Unlikely
Varroa destructor	+++	+++	+	+	++	+++	Possible
Wax moth	−			−			Unlikely
Environmental
Availability and quality of water							Indeterminate
BT pollen	+	+	−	−	−	−	Unlikely
Cell phones	+	−		−	−		Unlikely
Loss of feral populations reducing diversity of drones	+	0	0	0	+	0	Indeterminate
Reduction of propolis							Indeterminate
Sun spots	−	−			−		Unlikely
Weather events (e.g., cold snaps, rain, or timing of warming) and availability to forage	−	++		++	+		Unlikely alone/ contributor
Pesticides
Fungicides (external)	+	−	+	+	+	0	Indeterminate
Insecticides (external)	++	−	+		+	+	Indeterminate
Neonicotinoids	+	−	+/−	−	+	0	Unlikely alone/ contributor
Beekeeping practices
Aggregation of hives in large ag situations	++						Indeterminate
Antibiotics	+	0					Indeterminate
Fungicides (in–hive)	+	−	+	+	+	0	Indeterminate
Genetics (e.g., telomere premature aging syndrome)							Indeterminate
Miticides (in-hive)	+	+/−	+	+/−	+	0	Possible/contributor
Poor queens	+	+	+	+	+	0	Possible/contributor
Stress (transportation)	++						Indeterminate
Nutrition
Nutrition deficit	+	+		+	+	+	Possible
Problems with supplemental feeding (HMF)	0	+	+	0	+		Indeterminate
Starvation	+	+	+	++	+	+	Possible
Due to time limitations, scoring was incomplete for some causes. Blank cells indicate that no score was assigned.
“+/−” indicates disagreement among workshop participants.

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