(Ed.Note: It has not been possible to add the photographs that accompanied this article to the web version)
What do we know about drones?
Although many aspects of honeybee biology have been studied extensively over the past decades, the males have always remained the neglected gender . This is partly due to the fact that honeybee drones do not participate in any of the colony’s tasks, and also because they are mostly present during a short season. Moreover, the most important event in a drone’s life (that is mating) is very difficult to observe, lasting only a few seconds and taking place far away from the hive, about 20 m above the ground.
Several researchers have attempted to study drone mating behaviour relying on different techniques, such as direct observations or marking experiments, the use of radars or pheromone traps to monitor drones on flight, and the employment of genetic markers to quantify paternity. Today we know that mature honeybee drones (Fig. 1) engage in mating flights, when they gather by the thousands in specific “drone congregation areas” (DCAs) that virgin queens visit to get mated. DCAs are formed irrespective of the presence of a queen, at selected sites delimited by conspicuous geographic landmarks, such as forest openings or valleys. Moreover, they are stable through time, with some locations known to have served as DCA for decades .
Under favourable weather conditions, drones can perform multiple mating flights in a single afternoon, staying in the DCA for up to 30 min before returning to the hives to feed. At these DCAs drones fly at 15 to 60m above the ground, following elliptical trajectories with 60-200 m of diameter . Whenever a virgin queen appears, dozens of drones pursue her forming a “mating comet” (during the drone season it is even possible to observe such mating comets by simply throwing dark-coloured stones into the air in the middle of a DCA). Inside these mating comets the drones seem to compete for more promising positions behind the queen, either by overtaking, leaving or entering the comet. After reaching a queen, guided by both visual and chemical cues, drones grab her abdomen, evert their endophallus into her vagina, ejaculate, and die shortly after; falling to the ground and leaving the queen free to mate again .
The use of pheromone traps in honeybee research
Pheromone traps have shown particularly useful in the study of drone mating biology. Formally designed by Jon L. Williams in 1987 to capture honeybee drones on flight (and hence also known as Williams traps), pheromone traps consist of a net cone with an opening at the bottom, provided with several “queen dummies” that hang from different sites. Queen dummies can be made out of black-painted cigarette filters impregnated with synthetic queen mandibular pheromone (9-ODA).
Attracted by the queen dummies, drones enter the bottom part of the net cone and stay trapped in the top (Fig. 2). Because the drones fly between 15 and 60 m above the ground when performing their mating flights, the traps need to be lifted. Williams initially attached the pheromone traps to a rotating mast firmly anchored to the ground. Later, other researchers have employed weather balloons filled with helium or hydrogen to lift the traps many meters from the ground (Fig. 3). Because these balloons do not need to be anchored to the ground, they are particularly useful when trying to locate the places where drones congregate.
Since Williams, pheromone traps have become common in honeybee research. The German honeybee researchers Nikolaus and Gudrun Koeniger employed several variations of such traps to study different aspects of drone mating biology. By marking drones from different apiaries with colour tags and recapturing them with pheromone traps in different DCAs, they found out that drones usually prefer to fly to the nearest DCA, even if they are able to fly to a more distant one . Similarly, based on the total number of captured drones and the number of recaptured marked ones, they found that more than 11,000 drones are present in a single DCA during a given day .
Keeping the pheromone trap at different altitudes, Dr. Koeniger and her collaborators found that drones of different honeybee subspecies (Carniolan and Italian bees) fly at different levels within the same DCA, the former preferring higher altitudes . The development of new molecular tools made possible more sophisticated analyses. Using genetic markers to identify the origin of drones collected with a pheromone trap in one DCA, Dr. Emmanuelle Baudry and his team demonstrated that more than 200 colonies can contribute drones to a single DCA .
Using a similar approach, a team of researchers led by Dr. Robin Moritz estimated the density of colonies surrounding a DCA . More recently I used genetic markers to analyse samples of drones collected from a single DCA over a period of three years, finding an extremely fast turnover of the colonies surrounding the DCA . Finally, within an international team of researchers, I used pheromone traps to sample drones across the native range of honeybees (Africa, Europe and central Asia), analysing them later with genetic markers to detect the presence of feral or wild colonies in locations with differing patterns of land use. My results show that while Africa hosts a large wild honeybee population, Europe has almost exclusively managed bees .
Using pheromone traps to improve honeybee breeding
Pheromone traps could be particularly useful to bee breeders that seek to mate their queens with particular drones. For example, this tool could be used to temporarily deplete an area from feral drones. If done before saturating the same area with managed drones, this could minimize the chances of getting unwanted matings. In Addition, because the drones caught in these traps have shown successful in performing their mating flights, they can also be regarded as potential queen mates. This makes them ideal samples to look for sexually transmitted diseases. By screening for such diseases in drones collected in different DCAs, it would be possible to identify particularly susceptible areas, where queens are very likely to become infected through mating.
Ongoing research of the Collaborative Initiative for Bee Research (CIBER), based in the University of Western Australia (UWA), is pioneering the use of pheromone traps in Western Australia to find DCAs, monitor the presence of managed and feral drones there, and study different aspects of drone quality and health. Two DCAs near the UWA have already been identified (Fig. 3) and drone samples collected. Hopefully, this tool will soon help both honeybee researchers and beekeepers of Western Australia take a closer look at the drones.
- Koeniger, G., The neglected gender - males in bees. Apidologie, 2005. 36(2): p. 143-143.
- Koeniger, N. and G. Koeniger, Reproductive isolation among species of the genus Apis. Apidologie, 2000. 31(2): p. 313-339.
- Loper, G.M., W.W. Wolf, and O.R. Taylor, The use of radar to document honey-bee (Apis mellifera) drone flight behavior, in Africanized Bees and Bee Mites, G.R. Needham, et al., Editors. 1988, Ellis Horwood: Chichester. p. 193-198.
- Koeniger, N., et al., Drone competition at drone congregation areas in four Apis species. Apidologie, 2005. 36(2): p. 211-221.
- Gary, N.E., Activities and behavior of honey bees, in The Hive and the Honey Bee, J.M. Graham, Editor. 1990, Dadant & Sons Inc. : Hamilton, Ilinois. p. 269-372.
- Williams, J.L., Wind-Directed Pheromone Trap for Drone Honey-Bees (Hymenoptera, Apidae). Journal of Economic Entomology, 1987. 80(2): p. 532-536.
- Koeniger, N., G. Koeniger, and H. Pechhacker, The nearer the better? Drones (Apis mellifera) prefer nearer drone congregation areas. Insectes Sociaux, 2005. 52(1): p. 31-35.
- Koeniger, G., et al., Assortative Mating in a Mixed Population of European Honeybees, Apis-Mellifera-Ligustica and Apis-Mellifera-Carnica. Insectes Sociaux, 1989. 36(2): p. 129-138.
- Baudry, E., et al., Relatedness among honeybees (Apis mellifera) of a drone congregation. Proceedings of the Royal Society B-Biological Sciences, 1998. 265(1409): p. 2009-2014.
- Moritz, R.F.A., V. Dietemann, and R. Crewe, Determining colony densities in wild honeybee populations (Apis mellifera) with linked microsatellite DNA markers. Journal of Insect Conservation, 2008. 12(5): p. 455-459.
- Jaffé, R., et al., Temporal variation in the genetic structure of a drone congregation area: an insight into the population dynamics of wild African honeybees (Apis mellifera scutellata). Molecular Ecology, 2009. 18(7): p. 1511-22.
- Jaffé, R., et al., Estimating the Density of Honeybee Colonies across Their Natural Range to Fill the Gap in Pollinator Decline Censuses. Conservation Biology, 2009.
Author: Rodolfo Jaffé Collaborative Initiative for Bee Research (CIBER: www.ciber.science.uwa.edu.au) Centre for Evolutionary Biology (M092) / ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Crawley, WA 6009, Australia.