Anatomy, Behaviour & Reproduction in the Male Honey Bees
The male honey bee is known for his role in reproduction and not much else. Ejaculate in the queen, rupture your abdomen, die a few moments later. This is an oversimplification, for drones produce pheromones for communication, and (perhaps) assist with hive heating during low temperatures.
Sexually-mature drones cluster in the sky, forming “drone congregation areas” to await the arrival of a virgin queen. Once Her Majesty arrives, they chase and mate with her mid-air. Apis mellifera queens mate with over a dozen drones, returning to her hive once the flight ends. Beekeepers can look for the tips of the drone organ (“endophallus”) protruding from the queen’s abdomen as a sign of successful mating.
Drone Congregation Areas (“DCAs”)
DCAs contain a highly mixed drone population that emerge from surrounding apiaries. Unlike colonies, establishing a DCA happens independently of queen presence – it is the queen who seeks DCAs. Once the area forms, drones will return to the DCA year after year. In general, the higher the number of colonies in the surrounding area, the greater the genetic diversity of a DCA, producing more diverse daughter colonies.
Factors that Determine DCA Formation
Studies into DCA formation are ongoing. One such factor is the landscape characteristics, such as geographical landmarks (used for drone orientation). Another, the distance from apiary, negatively impacts the drones and virgin queens – the longer they have to travel, the more energy expended and the greater risk of predation. Ruttner classifies this average distance as between 500m to 5km (Ruttner, 1976).
Loper and colleagues suggest that it is bee behaviour, not the landscape, that determines DCA formation (Loper et al., 1992). You could argue that it is also a feature of landscape – drones prefer areas with lower turbulence and relatively stable wind temperatures. Mating is also more likely to happen on the flight path (“flyway”) rather than at the DCA itself, on account of drones perceiving “more favourable conditions”.
Galindo-Cardona et al. conducted a landscape analysis of DCA formations in Central America and had a 25% success rate in identifying DCAs (8 out of 36 proposed locations; Galindo-Cardona et la., 2012). They suggest other factors could be involved, from the earth’s magnetic field (bees have iron granules in their abdomen that assist with navigation) to skyline presence and wind direction. The authors state that locating DCA would have been more successful if they looked for terrain with obvious landmarks such as slopes and urban developments.
What Happens at DCAs
Once the DCA forms in the afternoons, the drones await the virgin queen(s) to arrive. These sexually-mature drones spend hours, day after day anticipating for Her Majesty. Upon arrival, they chase her in an attempt to mate- either dying from success, or returning to the DCA the next day to try again. DCA formation is a daily occurrence during the spring and summer, decreasing in autumn and generally non-existent in winter.
A drone congregation area can be thought of as “drones following drones”. The mature drone produces an aggregation pheromone that guides other drones to him, and when a critical mass is reached, a DCA is established. After 10-12 days of age, drones are deemed “sexually mature” on the basis of sperm quality and flight capacity. Bastin and colleagues showed that attraction to drone aggregation pheromone is age-specific (Bastin et al., 2017). Young drones (2–3 and 7–8 days old) are uninterested in the aggregation pheromone, and thus will not take part in the DCAs, unlike their sexually-mature counterparts (10-15 days).
Enter the Queen
Virgin queens fly into DCAs and are pursued by the drones forming a “comet” appearance; a large number of drones chase the queen. Queens mate with multiple drones, with figures from 12 to 20, depending on your sources.
Mating occurs mid-flight. Drones approach the queen and grasp her abdomen. Upon successful docking, the drones positions himself by bending his abdomen and placing the tip of his endophallus with her open sting chamber. The haemolymph (“bee blood”) rushes from his head and thorax, concentrating in the abdomen. He is paralysed from the metaphorical “waist-up” during mating, later ejaculating and causing the endophallus to break off as it remains lodged in the queen bee. The drone dies shortly after, having completed his life purpose, and another takes his place. This newcomer uses his endophallus to remove the now-dead drone’s endophallus, and restarting the mating process (reviewed in Koeniger et al., 2010).
The Mating Flight is Terminated by the Drones, not the Queen
How does the queen know when to stop? A review by Woyke states that it is the drones who signal the end of the mating flight, and this is determined by the capacity of the queen’s spermatheca (Woyke, 2016). Each successive mating reduces available abdominal space, making it harder to remove the previous endophallus. When the final drone attempts to mate and cannot remove the mating sign, he signals the end of the mating flight, and the queen returns to her hive.
How do you know if your queen has mated successfully? Check for the remains of the drone endophallus- it will be a white-ish protrusion from the tip of her abdomen. This is the “mating sign”; it lasts a short while before the queen brushes it off when inside the hive. The second sign of a successfully-mated queen is the presence of a multiple (i.e. more than one, but not a dozen) eggs per cell in the early days – she is still learning how to lay, and these excess eggs are relocated by the worker bees, no stress.
Multiple Mating Flights by the Queen
Some queens mate multiple times (reviewed in Woyke, 2016). The number of mating flights is dependent on the success of her previous flights- the less successful, the more flights she takes. Sometimes a queen may be poorly mated but unable to fly again – perhaps due to poor weather. In this case, it would be due to the post-mating physiological changes, which transform her into a heavy queen with poor vision, amongst other things.
Recall that drones are the ones who terminate the mating process: “mating with more drones during a single flight is hindered because of the impossibility of removing the mating sign of the last successful drone from the sting chamber of the queens” (Woyke, 2016). If the conditions are ideal in this situation, the queen returns to the hive, rests, removes the lodged endophallus and flies out again.
The Role of Drones in Honey Bee Colonies
The drone’s body is specialised for mating: large compound eyes to detect virgin queens in flight, A large number of wing sensilla1, smaller mandibles and a (relatively) large endophallus. They have no stinger to defend the nest or themselves, and no hypopharyngeal glands to assist in brood rearing.
From Egg to Emergence: Drone Brood Development
Adapted from honey bees’ lifecycle
Under normal conditions, drones emerge from unfertilised eggs laid by the queen. This egg is placed in comb of a larger size (~6.4mm across) to account for the larger mass of drones. After three days, the larva hatches and is fed by workers – royal jelly at the start, then the standard bee bread – pollen and honey or nectar. After 6.5 days, the larva is large and the cell is capped with wax, commencing the pupal stage. Inside, the drone larva spins its cocoon and over 14 days undergoes metamorphosis. Cells and organs rearrange; shapes begin to form.
The young male emerges at day 24 from when the egg was first laid, and takes another 12-15 days to sexually mature. In this time, the drone is fed by his sisters, conducting orientation flights, and perhaps contributing to colony’s heating during the colder days of spring. Once mature, they fly to the DCAs and await the virgin queen.
Under abnormal conditions, the workers lay eggs that hatch into drones, as in queenless hives. The queen maintains reproductive dominance over her daughter workers via a combination of brood and queen pheromones. Should a colony be unable to raise a new queen following her loss, they become ‘hopelessly queenless” and start to lay eggs, competing with another. Go read the two articles for further details.
Diploid Drones, a Sign of Inbred Queen Mating
Drones can develop from fertilized eggs when the queen is inbred; a consequence of mating with her sons at the DCAs. These diploid drones usually do not survive to adulthood (Herrmann et al., 2005). The authors showed that young diploid drone larvae (and only young larvae) were removed by worker bees via cannibalisation. It’s assumed that the difference in cuticular hydrocarbon composition on the exoskeleton of younger diploid drone larvae raises the removal alarm. Their altered hydrocarbon pattern diminishes 72 hours after hatching, and older diploid larvae were reared as normal drones. When these pupa emerged, there was no difference in their weight or appearance (Herrmann et al., 2005).
However, these drones had smaller testes, fewer wing hooks and a higher sperm count (exactly 2x that of their haploid counterparts). Combining this diploid sperm with an unfertilised, haploid egg results in a chromosomal count three times the normal amount2, making the egg nonviable (“aneuploid lethal progeny”). As such, diploid drones do not contribute to the colony (the opposite, as they are a resource drain) – their sperm cannot be used by the queen.
Pheromones Produced by Drones
Extracted from “honey bee pheromones“
Drones don’t contribute much by way of pheromones. Their mandibular gland secrete chemicals that aid other drones in finding (and forming?) the DCAs (Villar et al., 2018). The gland produces pheromones up until 7-8 days of age, whereby their mating flights commence. The drones release pheromones as they fly to the congregation areas, attracting other drones over long distances.
However, Villar and colleagues do not suggest that the drone mandibular secretions are a “pheromone” on the basis of insufficient information: “[C]ontexts in which these compounds are secreted are still unknown and will need to be elucidated before a function can be ascribed. Identifying whether drones secrete the contents of the DMG [Drone Mandibular Gland] on their way to and/or at mating sites will be valuable in understanding whether they are using chemical cues in addition to landscape cues to arrive at and maintain a presence at congregation areas” – (Villar et al., 2018).
Drones Can Enter Other Colonies Without Harm
Drones can drift between hives without consequence. If a worker attempted to do that, the guard bees deny her entry, occasionally allowing a foreign worker allow if she begs hard enough. Currie and Jay found that drones were more likely to drift into colonies with virgin queens, or those that contain components of the virgin queen pheromones (Currie & Jay 1991). As we know by now, the older the drone, the more likely they were to drift off, on account of greater sexually maturity.
Drones drifted westwardly, assumedly in alignment with the sun’s path. They drifted even when their own colony contained a virgin queen (unsurprising, as it reduces the risk of mating with their mother queen), and were more attracted to virgins in neighbouring colonies (Currie & Jay 1991).
In the Asian honey bee A. cerana, drones rarely drift into other nests, and if this happens, they are not readily accepted like in A. mellifera (Hagan et al., 2023). The drifting of drone bees in A. mellifera could be a consequence of the unnaturally-large colony density in apiaries, which increases the chances of the males making navigational errors.
Drone Drifting and Varroa populations
Since Varroa mites are more common in drone than worker bees, could the drifting drones be a source of Varroa infestations into previously-uninfested hives? My local beekeeping club certainly thinks so. I did not find studies on this, so here are my thoughts: the drone leaves his infested hive and to the DCA. Drones are more likely to drift upon returning from a DCA. They spend 30-45 minute at the DCA, with the mite remaining on his body until he returns unsuccessfully to his hive. However, should he make a navigational error and drift into another colony, then the foundress mite dislodges off his body in search of a brood cell, beginning the colony infestation.
In light of the beekeepers’ emphasis on removing drone brood comb, it is possible that these drifting drones risk transmitting Varroa between hives.
Bonus: European Drone Honey Bees at DCAs Displace Africanised Drones
Africanised honey bee colonies are aggressive honey bee hybrids found in in the Americas. They swarm more frequently and produce more drones than a European colony, thus spreading rapidly. Africanised bees are more aggressive and undesirable for beekeeping operations, and preventing their spread involves removing africanised colonies and their genetics (drones).
Mortensen and Ellis propose to increase the number of managed European colonies in locations with high feral africanised bee populations (Mortsensen & Ellis 2016). As the European drones arrive at DCA, they compete with their Africanised counterparts. As the queens mate with multiple drones, there is an increased likelihood of insemination by the European bees, reducing the overall “Africanised” profile.
However, the authors state that future work will need to determine the ideal number of European colonies to have an acceptable impact. To reduce the chance of inbreeding, virgin queens attend more distant DCAs than drones (Jensen et al., 2005). This suggests that the density of European colonies would have be a lot higher than mated queens, or spread out over longer distances – future researchers, please advise.
Honey Bee Drone Congregation Areas & Colony Survival
DCAs form in the sky as drones get together. When the virgin queen arrives, they chase after her pheromone trail, and attempt to mate. Queens mate with over a dozen drones, and multiple times too, depending on the success of prior mating. Once mated, the drone dies, and the newly-mated queen attempts to (safely) return to her hive and lay eggs, building up her new colony.
By mating with multiple drones the queen has enough sperm to last her many years. The diversity in drone sperm is advantageous, as there will be no one disease to wipe them out, and some individuals may be more resistant to stressors than others. Even if the queen remains viable for several years, most beekeepers would choose to requeen after one or two years to maintain strong colonies.
Want more on drones? Here’s part 1 on drone biology.
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Footnotes
- These small sensory organs detect things like touch & vibrations (“mechanosensory” sensilla), temperature & humidity (“thermosensory” and “hygrosensory” sensilla) and chemicals (e.g. pheromones; “chemoreceptive” sensilla). A combination exists in drones, with mechansensory being dominant during flights, followed by chemoreceptors for virgin queen pheromone detection. ↩︎
- In general, we need one half from the mother and one half from the father to form an embryo (diplody). Exceptions exist of of course, like drones having only one half from the mother (haploidy). In the case of diploid drones mating with the queen, the equation becomes “one half from the mother and TWO halves from the father” – three halves, or 1.5 the genetic material, does not lead to embryogenesis. ↩︎