Key points
- BQCV kills queen larvae and pupae in their cells, and the cell wall turns black.
- It is one of the most widespread honey bee viruses, almost always symptomless in adults.
- It is closely linked to nosema: co-infection raises worker mortality.
- It spreads through nurse bee brood food, from queen to eggs, and between colonies.
- No treatment: strong, healthy cell builders, nosema and varroa under control, comb renewal.
Black queen cell virus (BQCV) kills developing queens inside their cells. After capping, the queen larva or pupa turns yellow, dies and then blackens, and the wall of the queen cell takes on a dark, almost oily look. It is regarded as the most common cause of death in queen larvae, and a well-known problem for anyone who rears queens.
The paradox is that this virus is everywhere. It is found in the great majority of colonies, almost always without any sign. It only becomes visible under certain conditions, especially when the colony also has nosema. This factsheet explains how to recognise it, how to tell it apart from other queen cell failures, and how to limit its impact in the apiary.
Black queen cell virus
Discovery and name
The virus was described in 1977 by Leslie Bailey and R.D. Woods in Britain. In July 1975 they had found many dead prepupae and a few dead pupae in queen rearing cells. The pupae were partly decomposed and darkened, and the cell walls looked almost black in patches. The symptoms resembled sacbrood, but serological tests did not recognise sacbrood virus: this was a new virus, made of spherical particles about 30 nm across1. Dead worker pupae carrying the same virus were also found the following spring1.
A dicistrovirus
BQCV is a small, non-enveloped, positive-sense RNA virus3. Its genome, sequenced in 2000 from South African bees, is about 8,550 nucleotides long. It carries two large open reading frames: the first codes for the replication proteins, the second for the capsid proteins2. This layout places it in the family Dicistroviridae6, the same family as the acute bee paralysis viruses. The structure of its capsid was described in 2017: it bears large surface protrusions that make it bulkier than most picornaviruses3.
An extremely common virus
BQCV is one of the most frequent honey bee viruses. In Belgium, a nationwide screening by real-time RT-PCR detected it in more than 95% of colonies8. In France, a study of samples taken in 2002 found it in most of the apiaries analysed10. It is not confined to the honey bee: in the bumble bee Bombus huntii it replicates in the gut and then reaches other tissues, probably through shared flowers11.
How the virus spreads
Through nurse bee brood food
The main route is food. Infected nurse bees pass the virus to larvae in the brood food they provide6, 12. A queen larva receives abundant food over a long period: if the royal jelly carries a lot of virus, the dose swallowed can be enough to kill it as a larva or pupa7.
Through the queen and drones
BQCV is present in queens and in their eggs, which points to vertical transmission7. Young and unmated queens are often carriers, and virus levels tend to rise with age, without any visible symptom in the adult queen7. The virus has also been found in the seminal fluid of healthy-looking drones. According to a conference presentation, virus particles may build up in the wax of queen cells, a hypothesis that still needs confirming7.
Through the environment and between colonies
The virus can stay infectious for up to four weeks in larval remains, honey or pollen. It also spreads through drifting bees, contaminated water and equipment, and the distribution of queens from infected colonies12.
The role of varroa is still debated
In the French study of samples taken in 2002, BQCV was never detected in the varroa mites analysed10. Yet in New Zealand, along the expansion front of varroa, BQCV levels in colonies shifted in step with infestation9. A recent experiment sheds some light on this: adult workers fed the virus died no more than healthy bees, but when the same dose was injected into their bodies, mortality reached 61% within ten days6. A vector that injects the virus, as varroa does with other viruses, could therefore make it far more dangerous. This role has not been demonstrated to date6.
The link with nosema
As early as 1983, Bailey and colleagues linked BQCV to the microsporidian Nosema apis, a gut parasite of adult bees4. When swallowed on its own, the virus multiplies poorly in adults1, 6. A commonly proposed hypothesis is that nosema, which damages the gut lining, makes it easier for the virus to get through; the exact mechanism is still under discussion.
With Nosema ceranae, now the dominant species in Europe, the interaction has been measured in the laboratory. In a cage trial, fewer than 5% of workers infected with BQCV alone had died by day 11. With N. ceranae alone, about 20% had died; with both agents together, about half. The effect of co-infection was greater than the sum of the two5.
The same study tested a neonicotinoid, thiacloprid, at a sublethal dose. It did not kill larvae on its own, but it increased mortality caused by BQCV, clearly so at a high virus dose5. These laboratory results do not predict what happens in a given colony, but they show that the virus weighs more heavily when other stresses are added. See also Pesticide poisoning in honey bees.
Impact on the colony
In queen rearing
This is where BQCV shows itself and where it costs most. It is considered the most frequent cause of death in queen larvae7. A batch of queen cells turning black means grafted larvae lost, cell builder time wasted and a delay in the rearing schedule. The more serious risk is spreading carrier queens to other apiaries12.
In a production colony
A colony replacing its queen, through supersedure or after swarming, can also lose its queen cells: it then stays queenless for longer, or ends up with no queen at all. In workers, the virus is almost always silent. Infected adults show no signs, and worker brood is only rarely affected1, 12.
Recognising black queen cell virus
Symptoms
- A capped queen cell that does not emerge on the expected date.
- A pale yellow larva or pupa whose skin forms a sac, as in sacbrood7, 12.
- Progressive darkening of the dead body, from brown to black7.
- A blackened queen cell wall, in patches or all over, with a dark, “oily” look1, 7.
- Normal-looking adult bees, the queen included.
- Less often, a few dead, darkened worker pupae1.
Do not confuse it with
Not every failed queen cell is caused by BQCV. Before drawing conclusions, rule out the more ordinary causes.
| Situation | What you see | Key clue |
|---|---|---|
| Black queen cell virus | Pupa yellow then black, cell intact, wall darkened | Closed cell, dead and blackened contents |
| Cell destroyed by a rival queen | Cell opened on the side, empty or contents torn out | Side opening, no blackening |
| Cell destroyed by workers | Cell chewed down or removed | Colony already had a queen or another cell had emerged |
| Chilled cell | Dead, greyish pupa, at the edge of the frame or cell bar | Cold snap, few bees covering the cells |
| Sacbrood | Worker larvae in a sac, head raised, gondola-shaped scale | Worker brood affected, scattered cells |
| American foulbrood | Sticky brown mass, smell | Rope test: elastic thread |
A queen cell from which a queen has emerged opens neatly at the tip, with a round cap cut away. If you suspect foulbrood, do the rope test: American foulbrood is a regulated disease.
Diagnosis
In the apiary
- Note the proportion of queen cells that failed to emerge and their position on the bar.
- Open a suspect cell with a blade: yellow or blackened pupa, sac-like skin, dark inner wall.
- Rule out other causes: side opening, chilling, abnormal worker brood.
- Check the cell builder colony for nosema, by examining bees under the microscope (see Nosema).
In the laboratory
RT-PCR, especially quantitative real-time RT-PCR, is the reference method: it detects the viral RNA and measures how much is present8. It is best to send affected queen cells, possibly with bees from the cell builder colony. A simple detection in adult bees means nothing on its own, since most colonies are carriers. It is a very high viral load in dead queen pupae that confirms the diagnosis.
Regulation
In France, black queen cell virus is not a notifiable disease. It is not on the list of bee diseases of the World Organisation for Animal Health (WOAH)13. Rules vary between countries, so check those that apply where you keep bees. A suspicion of American foulbrood, on the other hand, must always be reported.
Prevention and what to do
There is no medicine against BQCV, nor against any other honey bee virus. Prevention relies on the overall health of colonies and on hygiene in queen rearing12.
- Choose strong, healthy cell builder colonies. A populous, well-fed colony with a young queen generally keeps the virus in check12.
- Control nosema, which is closely linked to BQCV4, 5. Checking cell builder colonies under the microscope is a useful step.
- Control varroa and other diseases: this is the most effective strategy against viruses as a whole12.
- Make sure food is plentiful. A cell builder colony needs abundant pollen and nectar, or feeding when there is no flow.
- Renew the comb: replace old frames every three to four years12.
- Place hives in a warm, sunny spot from autumn to spring12.
- Remove suspect colonies from queen rearing. A cell builder or nucleus whose cells turn black should no longer be used to raise, sell or distribute queens12.
- Limit the movement of frames, queens and equipment between apiaries. See Apiary biosecurity and How to clean and disinfect a beehive.
In practice: what beekeepers actually do
Black queen cell virus is managed mostly upstream, when choosing and preparing the colonies that will raise queens. Here are the most common habits.
Hands-on steps
- Check the cells when distributing them, a few days before emergence: dark or misshapen cells are discarded.
- Open a doubtful cell rather than putting it into a nucleus: a queen from a problem colony is no gift.
- Keep a rearing log: cell builder colony, grafting date, number of cells accepted, emerged and blackened.
- Run a nosema check on cell builder colonies in spring, before the rearing season.
Common strategies
1. Switch cell builders. When several batches of cells turn black in the same colony, most beekeepers stop using it for rearing and replace it with another, stronger one.
2. Strengthen and feed. It is common to add capped brood and bees to a cell builder colony, and to give it syrup and pollen stores when forage is poor.
3. Start again on fresh comb. The cell builder’s frames are renewed, and reused cell bars and cups are cleaned or replaced.
4. Requeen colonies that show both nosema and repeated queen cell failures.
Useful kit
- A fine blade and a light to open and examine cells.
- A simple microscope and a mortar for nosema checks.
- A notebook or rearing record for each cell builder colony.
- Spare cups and cell bars.
Checklist
- Blackened, closed queen cells: black queen cell virus likely.
- Cells opened on the side: a rival queen, not the virus.
- Nosema in the cell builder: take it out of queen rearing.
- Low stores: feed the cell builder colony.
- Repeated failures: switch cell builders, renew the comb.
- Suspected foulbrood: rope test and laboratory analysis.
The most common mistakes
- Blaming the virus for every failed cell, without checking whether cells were opened on the side or chilled.
- Carrying on rearing in a colony whose cells blacken batch after batch.
- Ignoring nosema in cell builder colonies.
- Using a weak or poorly fed colony to raise queens.
- Selling or distributing queens from a suspect colony.
- Testing only adult bees and worrying about an ordinary positive result.
Frequently asked questions
Why are my queen cells turning black? If the cell stayed closed and holds a dead pupa, yellowish then black, black queen cell virus is the most likely cause. A cell opened on the side has been destroyed by a rival queen or by the workers.
Does black queen cell virus also affect worker bees? Adult workers are very often infected, but without symptoms. Worker brood is only rarely affected. However, co-infection with nosema clearly increases their mortality in the laboratory5.
Is there a treatment for BQCV? No, no medicine works against honey bee viruses. Prevention relies on strong, well-fed cell builder colonies, control of nosema and varroa, and comb renewal.
Will a queen from an affected colony carry the virus? She may: the virus is found in queens and in their eggs7. That is why queens from a colony whose queen cells turn black should not be raised, sold or distributed.
Is honey from a carrier colony safe to eat? Yes: BQCV is a honey bee virus and poses no risk to humans. Avoid feeding that honey or pollen to other colonies, though.
References
- Bailey L., Woods R.D. (1977). Two more small RNA viruses from honey bees and further observations on sacbrood and acute bee-paralysis viruses. Journal of General Virology 37: 175-182. repository.rothamsted.ac.uk
- Leat N., Ball B., Govan V., Davison S. (2000). Analysis of the complete genome sequence of black queen-cell virus, a picorna-like virus of honey bees. Journal of General Virology 81(8): 2111-2119. doi.org
- Spurny R., Přidal A., Pálková L., Kiem H.K., de Miranda J.R., Plevka P. (2017). Virion structure of black queen cell virus, a common honeybee pathogen. Journal of Virology 91(6): e02100-16. doi.org
- Bailey L., Ball B.V., Perry J.N. (1983). Association of viruses with two protozoal pathogens of the honey bee. Annals of Applied Biology 103(1): 13-20. repository.rothamsted.ac.uk
- Doublet V., Labarussias M., de Miranda J.R., Moritz R.F.A., Paxton R.J. (2015). Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environmental Microbiology 17(4): 969-983. doi.org
- Al Naggar Y., Paxton R.J. (2020). Mode of transmission determines the virulence of black queen cell virus in adult honey bees, posing a future threat to bees and apiculture. Viruses 12(5): 535. doi.org
- Amiri E., Strand M.K., Tarpy D.R., Rueppell O. (2020). Honey bee queens and virus infections. Viruses 12(3): 322. doi.org
- Matthijs S. et al. (2020). Nationwide screening for bee viruses and parasites in Belgian honey bees. Viruses 12(8): 890. doi.org
- Mondet F., de Miranda J.R., Kretzschmar A., Le Conte Y., Mercer A.R. (2014). On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathogens 10(8): e1004323. doi.org
- Gauthier L., Tentcheva D., Cousserans F., Colin M.E., Bergoin M. (2004). Étude des populations virales dans les ruchers français [Viral populations in French apiaries]. Abeilles & Cie no. 101. apiservices.biz
- Peng W., Li J., Boncristiani H. et al. (2011). Host range expansion of honey bee black queen cell virus in the bumble bee, Bombus huntii. Apidologie 42: 650-658. doi.org
- Bee Aware (Australia). Black queen cell virus (pathogen factsheet). beeaware.org.au
- WOAH (World Organisation for Animal Health). Diseases of bees (list of bee diseases in the Terrestrial Code). woah.org
- USGS Bee Inventory and Monitoring Lab. Apis mellifera, queen, side view (photograph, public domain). usgs.gov