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First published online February 15, 2006
Journal of Experimental Biology 209, 978-984 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02085
Visual regulation of ground speed and headwind compensation in freely flying honey bees (Apis mellifera L.)
Centre for Visual Science, Research School of Biological Sciences, The Australian National University, PO Box 475, Canberra, ACT 2601 Australia
* Author for correspondence (e-mail: barron{at}rsbs.anu.edu.au)
Accepted 10 January 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: optic flow, wind tunnel, Apis mellifera, honey bee, ground speed
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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) observed that Drosophila flying in a tunnel
regulate their ground speed by holding the induced optic flow constant.
Srinivasan et al. (Srinivasan et al.,
1996) and Baird et al. (Baird
et al., 2005) obtained similar evidence for honey bees. How well
is ground speed regulated in the presence of wind disturbances? David
(David, 1982) found that
Drosophila flying upwind in a wind tunnel compensate for the headwind
by increasing their flight thrust to maintain the induced optic flow at its
still-air value, for wind speeds of up to 1 m s–1. Wenner
(Wenner, 1963) timed the
flights of honey bees flying outdoors from their hive to a feeder. He
concluded that the cruising speed of unloaded honey bees in natural outdoor
environments is 
7.5 m s–1, and that this value changes
very little even in the face of headwinds or tailwinds as large as 3 m
s–1. Riley and Osborne
(Riley and Osborne, 2001) used
sophisticated radar tracking methods to show that bumblebees only partially
compensate their ground speed against headwinds and tailwinds, and possibly
adjust altitude to maintain an innately preferred rate of optic flow during
flights disturbed by winds (Riley and
Osborne, 2001). If compensation for wind is indeed achieved visually – by monitoring the optic flow – how sensitive is it to variations in the visual environment? Are bees better able to regulate ground speed when flying in a richly textured environment that provides strong optic flow signals, as opposed to a sparsely textured environment that offers impoverished optic flow information? We have investigated this question using honey bees.
We began by examining how bees control their flight speed in visual environments that produce strong or weak optic-flow cues. We then investigated the ability of bees to compensate for headwind in these two, rather diverse, optical environments.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Bee training
In all of the experiments, bees were trained to enter and fly through a
narrow wooden tunnel and forage at a feeder placed at its far end, which was
sealed. The roof of the tunnel was covered with 1.5 m long strips of
transparent Perspex, and the walls and floor were lined with visual patterns,
described below. Training was commenced by placing a 2 mol
l–1 sucrose feeder close to the entrance of the hive in the
beehouse. Once the feeder had attracted a sufficient number of bees it was
moved gradually, first to a position at the entrance of the tunnel, and then
progressively further inside the tunnel to the final position, which was near
the far end. Bees that continued to visit the feeder regularly after the
feeder had been moved to its final position were marked with individually
distinctive coloured dots of acrylic paint on the thorax and abdomen.
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The patterns were generated on a computer, printed on a laser printer as a series of sheets of paper, and affixed to the walls using transparent mending tape, taking care to ensure that the junctions between adjacent sheets were true and as visually flawless as possible.
In experiment 4, ground speeds were measured under conditions in which the patterns on the walls were moved at various speeds, either in or against the direction of flight. In this case the bees were trained to fly into a tunnel 20 cm tall and 22 cm wide, with walls made of clear Perspex. This tunnel was placed between two motorized conveyor belts which could be moved at various speeds in either direction. The belts were 28 cm apart, and the tunnel was positioned centrally between them. The belts carried axial striped patterns, as described above. The object of this experiment was to examine whether axial stripes generated any residual optic-flow cues, as will become evident in the Results section. The distance from the tunnel entrance to the feeder was 3.23 m.
Tests in headwind
For experiment 2 a flow of air was generated through the tunnel by placing
a fan 170 cm behind the feeder (Fig.
1). The air flow passed through an array of thin walled (0.5 mm)
30 cm long plastic tubes (internal diameter 3 cm), which were also placed
behind the feeder. This honeycomb array reduced the vorticity and the
turbulence of the air flow in the tunnel. The speed of the fan was adjusted
using a variable voltage power supply. In this way we could alter the speed of
the headwind experienced by bees flying toward the feeder in the tunnel.
Fig. 1 illustrates the wind
speeds generated at five different fan voltages: 0, 60, 100, 140 and 180 V. It
shows that wind speed did not vary substantially along the length of the
tunnel. At maximum power, the fan created a headwind of 3.8 m
s–1. Estimates of honey bee ground speed in a natural, open
environment vary from 7.0–7.5 m s–1 for unloaded bees
to 5.3–6.5 m s–1 for bees carrying a load of nectar
back to the hive (Wenner,
1963). Given these estimates, we believe that the fan generated a
significant head wind for a flying bee.
Measurement of ground speed
Under each experimental condition, ground speeds were measured only after
individual bees had visited the feeder at least 10 times (1 h). Ground
speeds were measured by recording the durations of the bees' flights in the
tunnel when travelling toward the feeder. Using a manual stopwatch, bees were
timed from the point at which they entered the tunnel until they passed a
point 5 cm in front of the feeder. In effect, this procedure measured the
cruising time of the bee in the tunnel, discounting the time required to
finally alight at the feeder, which was variable. Very occasionally a bee
landed on the wall or floor of the tunnel en route to the feeder, or made a
U-turn and headed back toward the entrance. Such flights were not used in the
analysis. Only continuous forward flights were recorded.
Data analysis
Bees were marked individually, and several flights were recorded for each
bee. We first calculated the mean flight duration of each individual in a
given experimental treatment, and performed statistical analyses on these
means. Therefore each individual is considered only once per experimental
treatment in our statistical tests, to avoid pseudo-replication.
Experimental conditions
Since each experimental condition lasted several days, it was difficult to
use the same bees for each condition. However, the climate regulation of the
beehouse ensured that temperature conditions were stable throughout the series
of experiments that were run in this study.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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In one experimental condition, the walls and floor of the tunnel were lined with the checkerboard pattern, providing strong optic flow cues. The mean flight durations of trained bees in the tunnel were determined by recording at least five flights for each of 32 different bees. In another condition, the walls and floor of the tunnel were lined with the axial stripe pattern, which provided very weak or no optic flow. Ground speeds were recorded for a new set of 41 individual bees.
The results reveal that bees flew over three times faster in the axial striped tunnel, compared to the checkerboard tunnel (Fig. 2). This difference is highly significant (t-test, t=–19.5, d.f.=55, P<0.001).
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Clearly, then, optic flow is important in the regulation of ground speed:
reducing optic flow cues by changing the lining of the tunnel from
checkerboards to axial stripes resulted in a threefold increase in ground
speed. This finding is consistent with earlier, anecdotal observations that
bees fly noticeably faster in axial-stripe tunnels
(Srinivasan et al., 1996), and
consistent with the hypothesis that bees maintain a preferred image speed
across the eye during flight. If we imagine bees maintain a more or less
constant response from the movement-detecting neurons in their visual system
one might expect them to fly faster in the axial-stripe tunnel in order to
generate the same level of response from the neurons in this visually
impoverished environment. Further, the variation in ground speed observed in
the axial stripe tunnel was not much greater than in the checkerboard
environment (Fig. 2) suggesting
that bees could regulate flight speed perfectly well in this optically
impoverished environment.
Experiment 2: effect of headwind on ground speed in different optical environments
In this experiment bees were observed while they flew in the same two
environments as above, but in the presence of a headwind. If bees relied on
optic flow cues to compensate their ground speed against headwind, then one
might expect that compensation would be better in the checkerboard environment
(which produces strong optic flow cues) than in the axial stripe environment
(which produces weak optic flow cues).
Individually marked bees were trained to visit a 2 mol l–1 sucrose feeder placed inside a flight tunnel, 5.48 m from the entrance. The tunnel was 7.18 m long, 14 cm wide and 20 cm high. Multiple flights for each bee were recorded for each of five different headwinds, generated by setting the voltage to the fan at five different levels: 0, 60, 100, 140 and 180 V, which generated the wind speeds shown in Fig. 1. Observations were made over four consecutive days and, if possible, flight times for each individual bee were recorded for each wind speed on each of the 4 days. The order of presentation of wind speeds was varied randomly across the 4 days.
The results for the checkerboard environment are shown in
Fig. 3A. At each wind speed,
data was recorded from at least 30 individual bees. The results show that, in
this environment, the bees compensated extremely well for headwind speeds
right up to the strongest headwind that could be produced in the tunnel,
namely, 3.8 m s–1. There was no significant effect of
headwind on ground speed at any of the headwinds tested (ANOVA,
F=1.97, d.f.=160, P=0.10). Bees maintained a mean ground
speed of 0.4 m s–1, which is comparable to the value
recorded in still air in experiment 1.
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How were bees compensating for headwind in the axial-stripe tunnel, which offered very weak optic flow cues? One possibility is that the bees were able to extract enough image motion information even from the axial stripe patterns, to be able to regulate ground speed. Minor imperfections in the patterns, or visibility of the vertical joints between adjacent panels that carried the pattern, could have provided some optic flow cues. A second possibility is that the bees were able to use optic flow information from outside the tunnel. The ceiling structures of the beehouse were visible to the bees through the clear Perspex roof of the tunnel, and could have provided optic flow cues that were used by the bees to regulate ground speed. Since these structures were much further away than the walls and floor of the tunnel, one might expect the bees to fly at a higher speed to achieve the same rate of image motion across the eye, as they did. A third possibility is that bees possess an alternative, as yet unexplored mechanism for regulation of ground speed, which does not rely on visual information.
To distinguish between these possibilities, experiments 3 and 4 were designed to explore whether bees really use optic flow information from the axial stripes to regulate their ground speed.
Experiment 3: ground speed in axial-stripe tunnels of different widths
In this experiment, we compared ground speeds in axial stripe tunnels of
two different widths, namely, 21 cm and 11.5 cm. If bees were able to detect
optic flow information from the axial stripes in the walls and use it to
regulate their ground speed, then halving the width of the tunnel should
approximately halve the speed of flight. This is because, in a tunnel of half
the original width, bees would have to fly at half the original speed in order
to generate the same rate of image motion across the eye.
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The results (Fig. 4) reveal that halving the width of the tunnel does indeed reduce the average ground speed by almost exactly 50% (t=13.91, d.f.=60, P<0.001). This is consistent with the notion that the bees were indeed using optic flow information from the axial stripes on the walls, and not from the ceiling structures, to regulate their ground speed.
This possibility was tested more directly in the next experiment, where the axial stripes on the walls were moved to examine whether the motion affected the speed of flight.
Experiment 4: ground speed in axial striped tunnels with moving walls
Bees were trained to a feeder placed at the far end of a tunnel with
transparent walls. The tunnel was placed between two conveyor belts which
carried axial stripes that could be moved either in or against the direction
of flight, as described in the Materials and methods. The effective width of
the tunnel (the separation between the conveyor belts) was 28 cm. Flight
speeds were recorded for five different pattern speeds, including zero. The
entire experiment was conducted in still air, because the aim was no longer to
examine the effect of headwind, but simply to ask whether the bees were using
sparse optic flow information from the axial stripes to regulate their ground
speed.
The results are shown in Fig. 5. Pattern speeds in and against the direction of flight are shown as positive and negative, respectively. Motion of the axial stripe pattern had a significant effect on ground speed (ANOVA, F=15.1, d.f.=115, P<0.001). Bees increased their ground speed when the pattern was moved in the direction of flight: higher pattern speeds elicited higher ground speeds. Conversely, bees decreased their ground speed when the pattern was moved against the flight direction, and higher pattern speeds elicited lower ground speeds. This provides clear evidence that the bees were able to extract optic flow cues even from the axial stripe patterns.
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The changes in ground speed did not fully compensate for the movements of
the pattern. Two possible reasons for this may be (i) the presence of the
stationary Perspex walls between the bee and the pattern, which may not have
been totally invisible; and (ii) the presence of a `dead zone' in the
regulation of ground speed at image speeds that are close to the target value
(Baird et al., 2005).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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The ground speeds we observed in these tunnel studies were all far lower
than speeds observed for bees flying in the field. Even in the axial-stripe
tunnel, bees flew at 1.4 m s–1 (experiments 1 and 2) compared
to flight speeds greater than 7 m s–1 for bees in the field
(Wenner, 1963). Very probably
this is because in the flight tunnels bees are constrained to fly far closer
to the source of optical cues than in the field [field bees typically fly at
an altitude of 2 m (Riley and Osborne,
2001)]. Therefore bees experience a greater angular motion of the
image when flying in the tunnel than when flying outdoors. If bees indeed have
a preferred rate of image motion during flight, reducing ground speed in the
tunnel would be a compensation for this magnified image motion.
Earlier work, investigating a different question, namely visually mediated
odometry, reported that bees fly slower in headwinds, even when the headwinds
are relatively weak (Srinivasan et al.,
1997; Srinivasan et al.,
1996). The present findings are clearly different from the earlier
observations. Although the reasons for this discrepancy remain to be
ascertained, it should be noted that in the earlier studies the bees were
always trained in still air, and tested only occasionally and briefly in the
presence of wind. Therefore, they had no opportunity to learn to compensate
for the effects of wind in the tunnel.
Recent work in our laboratory suggests that, in still air, ground speed is
quite invariant to changes in the contrast and the spatial frequency content
of the patterns that line the walls and floor of the tunnel
(Baird et al., 2005). This
indicates that the neural mechanism that monitors the motion of the image in
the eye is capable of registering the speed of the image rather faithfully,
regardless of its visual texture. However, one can expect such robustness to
prevail only as long as the geometry of the texture is capable of inducing
horizontal optic flow in the eye. Examples of such textures are vertical
stripes, checkerboards or random dot patterns. An axial-stripe texture, on the
other hand, would theoretically induce no horizontal optic flow, because
flight is parallel to the direction of the stripes. The only horizontal flow
that such a texture could induce (if any) would arise from imperfections in
the construction of the pattern. Experiment 1 shows that bees fly about three
times as fast in an axial stripe environment, as in a checkerboard
environment, but bees are still able to regulate their flight speed in this
extreme condition of highly impoverished optic flow. Mean ground speeds in the
axial stripe tunnels were significantly less than ground speeds recorded for
bees in the field, and bees were able to regulate flight speed against
headwinds in the axial stripe environment as well as in the checkerboard
environment. These two observations indicate that flights were not
uncontrolled in the axial stripe tunnel, rather bees regulated ground speed at
a higher `set point' than in the checkerboard tunnel.
Ibbotson (Ibbotson 1991;
Ibbotson, 2001) has reported
the existence of visual interneurons in the honey bee, which respond
selectively to movements of patterns in the front to back direction on each
eye. The strength of this response is approximately proportional to the
velocity of the pattern, over a wide range of pattern velocities. They also
display the robustness to changes in contrast and spatial frequency content,
as discussed above. If bees adjusted their ground speed so as to maintain a
constant response (e.g. a constant spike firing rate) in these neurons, then
such neurons could be part of a neural circuit that regulates ground speed.
Although such a system would perform well at regulating ground speed in a
checkerboard environment rich in visual texture, in an axial stripe
environment, the bees would have to fly considerably faster in order to
generate the same firing rate from the neurons. Experiment 1 shows that bees
indeed fly considerably faster in an axial stripe environment.
Experiment 2 shows that bees display excellent compensation for headwind when flying in a checkerboard tunnel, which provides strong optic flow signals. This is in accordance with what might be expected from the schema described above, if one assumes that the movement-detecting neurons are sensitive enough to detect small deviations from the desired (target) image speed. Headwind compensation continues to be excellent even when the bees are made to fly in an axial stripe tunnel, which provides very weak optic flow cues. Although the bees fly much faster in this environment, their ground speed continues to be largely unaffected by headwind. We suggest that, in the axial stripe tunnel, bees are able to extract the weak optic flow information from this environment. They fly at a higher speed, which evokes a similar firing rate in the movement-detecting neurons as that evoked by slower flight in the checkerboard environment. In the presence of headwind, bees increase their thrust to maintain the same level of neural response. Thus, although the bees fly faster in the axial stripe environment, compensation for headwind continues to be excellent. The percentage variability in flight speed is approximately the same, regardless of whether flight is in the checkered tunnel or in the axial stripe tunnel, as can be seen from Fig. 2. This suggests that the visual movement-detecting neurons that underlie the regulation of flight speed respond to changes in the speed of image motion in a Weber-fraction fashion.
These findings are congruent with earlier observations in our laboratory
that bees are able to extract some optic flow information for the purpose of
estimating distance flown even when they fly in axial stripe tunnels
(Si et al., 2003). They are
also consistent with the observation that the honey bee's visually driven
odometer continues to register distance flown – albeit at a reduced rate
– even when flying over water surfaces, which provide only weak optic
flow cues (Tautz et al.,
2004).
In our flight tunnel studies honey bees responded to headwinds by
increasing their thrust to maintain a constant level of image motion
experienced during flight. However, observations of the flight paths of freely
flying bumble bees in the field suggest that compensation of ground speed for
headwinds is not perfect, and an additional response to wind is to change
flight height (Riley and Osborne,
2001). Riley and Osborne suggested that reducing altitude in the
face of headwind, and increasing altitude with tailwinds
(Riley and Osborne, 2001) would
be an energetically efficient way to maintain a preferred rate of optic flow
during flight (Riley and Osborne,
2001). If the maximum thrust that a bee can produce is not
sufficient to compensate fully for a headwind, flight at a lower height would
restore the optic flow experienced by the eye to its original value. This
response may have the added benefit of shielding the insect from the stronger
winds that prevail at greater heights
In our experiments, we have not observed any consistent wind-induced changes of flight height, but the dimensions of the tunnel could have prevented this response, and we were not able to measure subtle changes in height. Further, our experiments were all performed at relatively low wind speeds, compared to winds that can be encountered by bees flying in a field environment. Even so, our observations of flights in tunnels show that bees maintain a remarkably constant rate of optic flow during flight, and bees will increase thrust to compensate for headwind in a situation where they cannot (or do not) significantly reduce altitude. The questions we must now ask are: do bees also maintain a preferred rate of optic flow during flight in the field, and, if so, is this achieved by modulating thrust or altitude? Further experiments, using a combination of controlled conditions of a larger flight tunnel with higher wind speeds, and precise measurements of ground speed and altitude of bees in the field are needed to address this.
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Baird, E., Srinivasan, M. V., Zhang, S. and Cowling, A.
(2005). Visual control of flight speed in honeybees.
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David, C. T. (1982). Compensation for height in the control of groundspeed by Drosophila in a new `barber's pole' wind tunnel. J. Comp. Physiol. 147,485 -493.
Ibbotson, M. R. (1991). A motion-sensitive
visual descending neuron in Apis mellifera monitoring translatory
flow-fields in the horizontal plane. J. Exp. Biol.
157,573
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Ibbotson, M. R. (2001). Evidence for velocity-tuned motion-sensitive descending neurons in the honeybee. Proc. R. Soc. Lond. B Biol. Sci. 268,2195 -2201.[Medline]
Riley, J. R. and Osborne, J. L. (2001). Flight trajectories of foraging insects: observations using harmonic radar. In Insect Movement: Mechanisms and Consequences (ed. I. P. Woiwood, D. R. Reynolds and C. D. Thomas), pp.129 -158. Wallingford: CABI Publishing.
Si, A., Srinivasan, M. V. and Zhang, S. (2003).
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Srinivasan, M. V., Zhang, S. W., Lehrer, M. and Collett, T. S. (1996). Honeybee navigation en route to the goal: visual flight control and odometry. J. Exp. Biol. 199,237 -244.[Abstract]
Srinivasan, M. V., Zhang, S. W. and Bidwell, N. J. (1997). Visually mediated odometry in honeybees. J. Exp. Biol. 200,2513 -2522.[Abstract]
Tautz, J., Zhang, S., Spaethe, J., Brockmann, A., Si, A. and Srinivasan, M. (2004). Honeybee odometry: performance in varying natural terrain. PLoS Biol. 2, 915-923.
Wenner, A. M. (1963). The flight speed of honeybees: a quantitative approach. J. Apic. Res. 2, 25-32.
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