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Original Research
The flight characteristics
of drones TN relation to
mating
Joseph R. Goelho
Department ol Biological Sciences
Western lllinois Univercity
Macontb' ,L 61455
USA
ABSTRACT
Flight characteristics of drones were compared to workers,
and sometimes queens, to gain insight into the
evolved design of drones with respect to mating opportunity
and competitiveness. Drones had inferior flight
endurance and range as compared to workers, but
similar maximum flight speed and maneuverability,
indicating these characteristics have limited significance
for drone fitness. Drones had superior kinetic
energy, which might provide an advantage in aggressive
encounters between males, but such encounters
have notbeen observed. Droneshad much greatertotal
force production, which might allow drones to carry
queens during mating. The evolutjon of drone size is
still a mystery, though this study suggests that investigators
should pursue further research into lift force and
the potential for intermale mate competition.
Received for publication: I September 1994
Acceptedfor publicotion: 20 November 1994
KEY WOBDS
Apis melifera, queen, drone, flight, mating
INTRODUGTION
In spite of the fact that honey bees (Aprs mellifera L.l
have been domesticated for over 7,000 years (Crane
1975), many aspects of their biology are unknown. The
dearth of information is especially acute for drones,
which have traditionally been ignored, perhaps because
of their lack of commercial value and simplified
social behavior relative to workers, queens and whole
colonies. In this study I address a perennial issue: why
are drones so large? I use informdtion integrated from
studies of drone flight physiology and honeybee mating
behavior to gain insight into the potential for either
sexual selection or natural selection to have influenced
the evolution of drone size in honeybees. This area has
suffered from a lack of direction and lack of data,
probably because of the difficulty of observing natural
mating. Such information is needed to address a number
of pending questions. For example, African drones
may be smaller than European drones (zunderer et 4/.
1985), but we have almost no idea what effect this may
have on the potential for hybridization.
It is clear that drones have not evolved to work.
They are poorly equipped for foraging, having rather
small mandibles, proboscis and honey crop (Snodgrass
1925). Dronesdo not forage, but fuel theirmating flights
by taking stored honey (Orosi-Pal I 959). Drones also do
nbt perform tasks within the hive, lacking wax glands
and most of the pheromone-producing and nutritional
glands (see review by Winston 1987).
Drone morphology is consistent with their almost
exclusive involvement in reproductive behavior. They
have extremely large eyes, which occupy most of the
head, and very sensitive anten nae, which have l0 times
the number of antennal plate organs as workers (Winston
1987). These are used in locating and orienting to
flying virgin queens (see Currie 1988 for review). Success
in mating is very likely to be the primary selection
pressure on drones. However, it is not always clear
what characteristics of drones must be optimized in
order to maximize reproductive fitness. A brief review
of honey bee mating behavior may allow some insight
into these questions.
Mature drones take flight during the afternoon in
suitable weather. There maybe large numbers of drones
at drone congregation areas or on flight paths leading
to and from them (Loper et al. 1987), so the operational
sex ratio at these sites is very skewed toward drones. If
a virgin queen appears the drones pursue her as a
swarm known as a "comet" (Gary I 953, Koenig er 1986a) . If insemination is successful, the tip of the
endophalius breaks off, the drone becomes paralyzed
immediately, fallstothe ground, and soon dies (Ruttner
1956, Gary 1963, Koeniger et al. 19791; therefore, a
drone can mate only once. Because mating opportunities
are rare, this limitation is probably not significant.
Nonetheless, selection pressure on drones must be
intense.
Because mating occurs in flight, drone characteristics
must be consistent with maximization of flight
performance. Few attempts to address these questions
have been made (except see Starr 1984) This study
examines drone flight performance characteristics, in-
BeeScience 1996 Vol. 4 No. 1 Page 21
cluding those that may affect mating opportunity (the
endurance and range of flight) and competitiveness
(flight velocity wl, kinetic energy [Ek], maneuverabiiity,
and load-carrying capacity). I have measured some
of these attributes directly, others I took from the
available literature. By comparing drone perlormance
with that of workers and queens, it should be possible
to understand how drone characteristics affect performance,
and to gain insight into how the morphology
and physiology of drones has evolved in relation tit
flight and mating.
FLIGHT ENDURANCE AND BANGE
A drone should be able to increase the probability of
encountering a queen by increasing the duration and
range of a mating flight. Energy-efficient flight and
iarge fuel storage would reduce transit time and refueling
time at the hive because drones must derive all the
energy for a mating flight from honey obtained at the
hive and carried in the honey crop. Su-h characteristics
would also be consistent with selection for flight range,
which might be important since the finite distance
covered by drones from a given colony limits the abiiity
of the queen from that colony to spread her genes
(Taylor and Rowell 1P88).
The fuel-carrying capacity of, drones was determined
by measuring the volume of,honey carried in the
honey crop. Drones were collected as they left the hive,
taken to the laboratory, and dissected. These individuals
were assumed to b-e sexually mature drones depart-
Tg on mating flights, having fllted their honey crops
from colony stores. The honey crop was removed intact
and weighed. Since the contribution of the thin-walled
membrane of the crop itself is negligible, the entire
mass was assumed to be honey.
Honey bee flight is fueled aerobically by carbohy,
drate metabolism (Beenakkers 1969, Kammer and
Heinrich 1 978, Beenakkers et al . 1984 , Nachtigall ef a1.
1989, Rothe and Nachtigall 1989) through rapid uprake
ofsugars frommidgut to hemolymph (Crailsheim 1!88).
Therefore, an oxycaloric equivalent for carbohydrate of
478 kJ/mol O, was assumed (Gnaiger 1983). Using
oxygen consumption data from published sources
(Coelho 199|a) and assuming l8.l l,zml honey (White
1975), the average theoretical mating flight times ol
drones were calculated. The average flight time of
workers was calculated in the same way, assuming a
modest honey crop volume of 25 mL, aithough the
maximum is considerably higher (Sylvester et al. 1983,
Schmid-Hempel et al. 19851.
The calculated average flight times were multiplied
by flight speed (Coelho 1991a and below) divided by
two to generate theoretical flight ranges, distances that
drones and workers should be able to travel if they flew
straight away from the hive and back.
Twelve drones leaving the hive averaged 215.8 I
3.0 mg (mean+ SE) body mass (Mb), and 15. I mghoney
crop contents with a maximum of 30 mg. The reproductive
tract weighed 27.8 x 1.0 mg. Based on these fuel
reserves and rate of utilization described above, a
drone should be able to fly for an average of -37 min at
a thorax temperature (\n) ol40'C. These estimates are
consistent with measured rates of food consumption
(Mindt 1962, as cited by Ruttner 1966, Berg 1988, as
cited by Nachtigall et al. 1989). A worker carrying 25 mg
of honeyin its crop should be able to fly continuouslyfor
i 05 min, almost three times longer than a drone. The
theoretical flight range of a drone with an average
honey crop load and average flight speed is 5.0 km. The
range of a worker is 38.2 km at average speed and crop
load, over 5 times that of a drone.
Most studies show that the average length of time
spent in a mating flight by a drone is -30 min. (reviewed
by Witherell 1971), which represents SlVo of the theoretically
available time. Drones routinely reach congregation
areas 5 km from the natal colony, and occasionally
as far as 5 km, while virgin queens probably fly only
2-3 km on mating flights (Ruttner and Ruttner 1966).
Yet matingsroutinely occurbetween drones and queens
whose natal colonies are l2 km apart, and occasionally
up to 17 km apart (Taylor, Kinsolver, and Otis 1986).
Drones return from mating flights with virtually empty
honey crops (Ruttn er 1966, Coelho, unpublished observations).
These observations suggest that drones commonly
use all of the time and range available to them
from their energy stores, perhaps retaining a small
amount of fuel as a safety lactor. The energetic strategy
of drones appears to be that ol utilizing nearly completely
the energy stores on a given flight, returning to
the hive, refueling, then taking another flight. In this
way as many as eight flights may be taken in one day
(Witherell l97l). Workers should be able to fly for a
much longer period of time than drones, though they
seldom do in reality (Gary 1975). These considerations
make it unlikely that drones are designed for endurance.
Similarly, flight range must not be the key drone
character for if drones were subject to strong selection
for maximal flight range they would be designed more
like workers-with smaller body mass, greater fuel
reserves, and faster flight.
FLIGHT SPEED
Koeniger ( I 985b) suggested that the fastest drone
reaches the queen lirst and copulates with her. Since
drones are larger and have a higher body temperature,
one might expect them to be able to fly faster than
workers. Hence, flight speed might provide the evolutionary
driving force for drone size. Although this scenario
is intuitively appealing, the data do not support it.
Flight speed values for drones and workers were
taken from Coelho (1991a), and kinetic energy was
calculated for drones and workers from values of Mb
and V therein. Mean V for drones (5.28 r 0.i0 m/s) is
significantly lower than that of workers (5.85 t 0.08 m,/
s) as measured by K-band radar lCoelho 1991a). The
maximum speed ls similar for drones and workers, -8
m/s.
Because V is more strongly correlated with Tth
than with body mass (Coelho i989) and drones have
higher Tth (Coelho 1991a, 1991b), one would predict
that they should be faster flyers than workers. The fact
that this is not the case indicates that drones have not
evolved large body size and high T,n simply as a means
of improving V.
Coelxo: Dnoxe Flrcxr
BeeScience 1996 Vol.4 No. I Page 22
Coelxo: Dnoxe Fucxr
Table I
Calculatedkinetic energsr of a drone and worker of average mass at mean and maximal flight speed.
Kinetic Energgr fl)
at mean flight speed
at maximum flight speed
Drone Worker
2.88 r.85
6.48 3.24
Note: mean body mass of drone = O.2 grworker = O.l g.
Mean flight speed of drone = 5.17 m/s, worker = 6.o8 m/s.
Maximal speed for both = 8 m/s.
KINETIC ENERGY
Male-male competition could provide an alternative
adaptive characteristic for drones. The ability to knock
aside a rival drone that is attempting to mount the
queen and to then supplant the rival's position depends
upon the usurping drone imparting sufficient kinetic
gne.rgy _to the incumbent drone. Kinetic energy (Ek)
during flight is related to body mass and flight speeit
according to a standard Newtonian equation:
Er = 0'5MuV2
The kinetic energy of a drone and worker of average
mass at mean and maximal V were calculated from
published values of Mo and V (Coelho t99ta) and are
presented in Table 1. In each case E* is substantially
higher in the drone.
The mean E* of drones used in flight speed experiments
was 3.25 ! 0.27 J, which falls between the mean
and maximal theoretical values for drones, and is much
greater than the mean value for workers.
In spite of their lower flight speed, drones generate
a great deal of kinetic energy during flight as compared
to workers, mostly because drones are larger. These
considerations would imply that drones are well suited
to aggressive, contact interactions with other drones.
Unfortunateiy, there is no evidence that they actually
engage in such interactions. Direct aggressive interaction
among drones attempting to mate with tethered or
artificial queens has not been observed, even with the
use of high speed {ilms (Gary 1953, Koeniger 1985b,
Coelho and Taylor 1994). Such contact would likely
cause injury, decreasing the odds of successful mating.
IIANEUVERABILITY
It is possible that maneuverability is important in determining
drone mating success. With an operational sex
ratio so heavily skewed to males, and the obvious
potential for competition, maneuvering for access to
the queen could provide the opportunity to mate. Maneuverability
can be defined as the ability to accelerate
and decelerate. Acceleration is equalto force divided by
mass; therefore, the acceleration of a flying insect is
equal to the force that it generates in flight divided by its
body mass, or mass-specific force production. Thus, an
index of maneuverability can be determined by measuring
maximal force production (F*u*) and body mass.
F-r* is largely determined by flight muscle mass, so
that a crude index of maneuverability is the ratio of
flight muscle mass to body mass (flight muscle ratio, or
FMR, [Marden 1987]).
The force produced by drones, workers, and queens
was taken from Coelho (1991b). On average drones
produce an F.r* (3.95 t 0.23 mN) over twice that of
workers (1 .73 t 0.13 mN). Mass-specific F*u* was not
significantly different between workers and drones.
Queens produced an F.r* intermediate between that of
workers and drones, but generated a mass-specific
Fn.r* significantly lower than that of the other two
groups.
Drones have higher FMR than queens, and as a
result have higher mass-specific Fmax (Coelho 1991b).
Drones should, therefore, have sufficient maneuverability
to catch a flying queen, and variation in maneuverability
may have important consequences for the
mating success of drones. Drones also had higher FMR
than workers, but mass-specific F*r* was similar between
the two. These results make it unlikely that drone
size has evolved solely in response to seiection for
maneuverability during mating, for it should be less
expensive for a colony to produce the same number of
small drones as large drones, and both would have the
same maneuverability.
LIFT FORCE
It is possible that absolute force production is more
important for drone mating success than mass-specific
lorce production. Since F*r* is strongly related to size
(Coelho 1991b), drones are weli constructed for it.
During mating the drone approaches the flying queen
BeeScience 1996 Vol.4 No. I PaEe 23
frombelow, and mounts her from above, grasping her
by the abdomen with all six legs {Gary 1963, Koeniger
d ol. 19791.It may be that the drone then carries the
queen in flight, although direct observations of natural
mating are not available to support or contradict this
possibility. Copulation occurs only after the queen
voluntarily opens the sting chamber, so that the drone
may have to car4l the queen for more than several
seconds {Gary 19631. Drone-queen pairs can fly freely
without losing altitude (Gary 1953), and drones can
carry a 148.5 mg weight in flight-approximately that of
a queen {Betts 1939).
The force required to lift a drone and a t5picalvirgin
is3.4 mN {Coelho 199lb). Drones can produce 3.95 mN
under optimal thermal conditions. Thus a drone of
average size need generate only 85% of F*., to lift
himself and a queen. The reverse cannot occur-a
queen cannot lift a drone and herself, for the queen at
best produces only 2.15 mN of force (Coelho l991bl.
Perhaps this is why on rare occasions a queen and dead
drone in copula are observed after falling to the ground
$ordan 1954, Ruttner 1956, Gary 1953). Normally the
explosive force of ejaculation results in the separation
of the dead drone from the queen (Gary 1953). If this
mechanism fails the queen cannot support the sum of
the drone's mass and her own, and falls.
For a queen to be carried aloft by a worker, 2.55 mN
of force are required. This is far above the force a
workeriscapable ofproducing, 1.73 mN (Coelho 199lb).
Total maximum force is strongly correlated with all
measures of size. Hence, the large siz-e of drones may
be a result of selection for absolute force production
during flight-the ability to carry a queen. If so, then the
support of large external loads is required. Internal
loads are, therefore, minimized: drones have low semen
volume (Harbo 1986) and honey crop volume,
even though these shortcomings result in brief flight
time, short flight range, and limited gamete delivery.
In an interesting contrast, workers have large honey
crops, but seldom fillthem completely when foraging,
an apparent constraint of energetic efficiency and lifespan
(Schmid-Hempel et al. 1985,Schmid-Hempel and
Wolf 1988, Wolf and Schmid-Hempel 1989). Hence,
selectionpressure for additional lift capacity in workers
is likely to be slight. Workers need not be any larger, at
least for the purpose of foraging.
CONCLUSION
I have attempted to identify key flight characteristics for
which drones are adapted. In that all organisms represent
a compromise among numerous selection pressures,
it seems likely that the flight design of drones is
a compromise among several needs, includingperhaps
all of those mentioned above and others. Nonetheless,
fruitful avenues of research might focus on some of
these areas, especiallylift force and male-male competition.
largerthan the females. The explanation ofthis anomaly
is that a marriage flight is absolutely necessary with
these species, and the male requires great strength and
size in order to carry the female through the air."
AGKNOWLEDGUENTS
I thank Allen J. Moore, Orley R. Taylor, Jr. and two
anon)nnous reviewers for their comments on the manuscript.
This work was supported in part by a grant from
the University Research Council, Westem Illinois Universigl.
COTITACT ADBESS
Joseph R. Coelho: Department of Biological Sciences,
Westem Illinois University, Macomb, 1L61455. BITNET:
MFrC@ECNUX A. BITNET, Internet : MFIC@ UXA.ECN.
BGU.EDU, Phone: 309-298-2521.
B'OGRAPH'CAL SKETCH
J. R. Coelho is Assistant Professor of Biological Sciences,
Western Illinois University, and has studied
flight, physiology, behavior and ecology ofhoney bees.
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