Visual control of flight speed in honeybees
1 Centre for Visual Science, Research School of Biological Sciences,
Australian National University, PO Box 475, Canberra, ACT 2601,
Australia
2 The Statistical Consulting Unit, Australian National University, PO Box
475, Canberra, ACT 2601, Australia
* Author for correspondence (e-mail: emily.baird{at}anu.edu.au)
Accepted 1 August 2005
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Summary |
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Key words: insect flight, honeybee, Apis mellifera, image motion, pattern motion, pattern texture, pattern contrast
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Introduction |
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Here, we investigate whether honeybees use visual cues to control flight
speed and attempt to uncover the properties of the underlying mechanisms. A
few earlier studies have suggested that flying insects use visual cues to
regulate flight speed. Heran
(1955) observed that tethered
flying bees altered their wing-stroke amplitudes when exposed to moving visual
patterns in the ventral visual field. While this suggests that flight thrust
is influenced by the image motion that is experienced by the eye, it does not
reveal how effective the motion-induced response is in regulating flight
speed. David (1982
) found that
Drosophila, flying in a wind tunnel with movable patterns on the
walls, adjusted their flight speed to maintain a constant velocity of image
motion in the eye. Srinivasan et al.
(1996
) found that bees flying
through a tapered tunnel slowed down as the tunnel narrowed, and sped up as it
widened. This suggests that the bees were adjusting their flight speed in such
a way as to hold the image velocity in the eye constant, despite the changes
in the width of the tunnel. Here, we test this hypothesized mechanism for
speed control in bees, directly and rigorously, by investigating the effects
of pattern motion on flight speed and examining the influences of pattern
texture and contrast on this behaviour.
Investigation of the influence of pattern texture and contrast on flight
speed is an important component of this study, given the current controversy
over the nature of the mechanisms that underlie movement detection. The
classical studies of optomotor behaviour
(Hassenstein and Reichardt,
1956; Reichardt,
1969
) and the electrophysiological investigations of the 1980s and
1990s on movement-detecting neurons in the fly have suggested that the
perception of movement depends strongly on the spatial texture and the
contrast of the moving image (Egelhaaf et
al., 1988
; Hausen,
1993
). In other words, movement detection does not involve an
accurate perception of image velocity. On the other hand, David's study of
flight speed regulation in fruit flies
(David, 1982
), and the
investigations of centring behaviour
(Srinivasan et al., 1991
) and
of visually mediated odometry (Si et al.,
2003
) in freely flying honeybees suggest that image velocity is
indeed sensed veridically by the visual system. These studies also show that
this velocity measurement is quite robust to variations in pattern texture and
contrast.
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Materials and methods |
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Experimental apparatus
All of the experiments were conducted in a rectangular tunnel that had
clear Perspex walls, which allowed bees flying through the tunnel to view a
variety of stationary or moving visual patterns (see below). The tunnel was
320 cm long, 20 cm high and 22 cm wide. A clear Perspex ceiling permitted
observation and filming of the bees as they flew in the tunnel
(Fig. 1A). The floor of the
tunnel was white and provided no visual texture. For each experiment, up to 20
bees were individually marked and trained to fly to a feeder containing sugar
solution placed at the far end of the tunnel. Flights to the feeder were
filmed in the central 1.45 m segment of the tunnel by a digital video camera
(Sony DCR-TRV410E; Sony Corporation, Toyko, Japan) positioned 2.5 m above the
tunnel floor (Fig. 1A). The
recorded flights were analysed by an automated tracking program developed
in-house, using Matlab software (v.6.5.0; The Mathworks Inc., Natick, MA,
USA).
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For Experiment 3 (described below), the tunnel walls were lined with a pattern of randomly placed black dots over one half of the length of the tunnel, such that the external, moveable pattern was occluded when a bee was in this section. Thus, half of the tunnel presented a stationary pattern on either side, while the other half presented moving patterns.
For Experiments 46 (described below), the side walls of the tunnel
were lined with various black-and-white patterns. These patterns were created
on a computer using a graphics program and were printed on a laser printer
using sheets of A4 paper. Adjacent sheets were joined and attached to the
walls using transparent adhesive tape. Care was taken to minimise visual
artefacts and flaws at the junctions. The contrasts of the patterns were
calibrated using a photodiode that had a linear intensity-response function.
Percentage contrast was defined as:
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Experiment 1. Measurement of the effect of pattern motion on flight speed
The flight speed of trained bees flying to the feeder was recorded for six
pattern velocities in each direction and for one condition in which the
pattern was static. When the pattern was moved in the direction of flight to
the feeder, the highest speed was limited by the maximum speed of the motor.
The speeds used for pattern motion in this direction were 15, 22, 30, 37, 45
and 52 cm s1 (these velocities were regarded as positive).
When the pattern was moved against the direction of flight to the feeder, at
high pattern speeds, the bees were unable to enter the tunnel. The maximum
speed used in this condition was therefore limited to the highest speed at
which the bees could enter the tunnel and fly to the feeder. The speeds tested
in this condition were 6, 12, 18, 24, 30 and 36 cm s1 (these
velocities were regarded as negative).
Experiment 2. Measurement of the effect of temporal changes of pattern velocity on flight speed
This experiment was designed to investigate how bees responded to temporal
changes in pattern speed. The flight speed profile of bees flying to the
feeder was recorded under two different conditions, stationary-to-moving and
moving-to-stationary. This was carried out for six different pattern
velocities. For the stationary-to-moving condition, the pattern motor was
initially stationary and was turned on as the bee approached the mid-point of
the tunnel. The pattern velocity profiles for this condition are shown in
Fig. 2A. For the
moving-to-stationary condition, the pattern was initially in motion at a
prescribed speed as the bees entered the tunnel, and the pattern motor was
turned off as they reached the mid-point of the tunnel. The pattern velocity
profiles for this condition are shown in
Fig. 2B. In each condition,
flights to the feeder were recorded for pattern speeds of 23, 30 and 37 cm
s1 with the pattern moving towards the feeder and for speeds
of 8, 23 and 30 cm s1 with the pattern moving away from the
feeder. In addition, there was one control condition in which the pattern was
stationary.
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Experiment 4. Measurement of the effect of pattern texture on flight speed
This experiment was designed to investigate how bees responded to changes
in the visual texture of the patterns lining the tunnel. The influence of
spatial texture was examined by measuring flight speeds with the tunnel lined
with vertical sinusoidal gratings of spatial periods 7.2 cm, 3.6 cm and 1.8
cm, in turn. For a bee flying along the midline of the tunnel, the spatial
frequency of these gratings as seen by the lateral field of the eye would be
0.03, 0.05 and 0.10 cycles deg.1, respectively. To enable
comparisons between the flight speeds with the various gratings, the 3.6 cm
grating (0.05 cycles deg.1) was arbitrarily designated as
the control pattern. This pattern was used throughout the course of the
training (24 h before testing began) and between the testing periods when the
other gratings were used.
Experiment 5. Measurement of the effect of pattern contrast on flight speed
This experiment was designed to investigate how bees responded to changes
in the visual contrast of the patterns lining the tunnel. The influence of
pattern contrast was examined by measuring flight speeds with the tunnel lined
with vertical square-wave gratings of various contrasts, in turn. Six
contrasts were tested: 100, 70, 50, 30, 10 and 0% (0% contrast being a
uniformly grey surface of luminance equal to the mean luminance of the other
gratings). The gratings had a spatial period of 1.8 cm, which, for a bee
flying along the midline of the tunnel, would present a spatial frequency of
0.10 cycles deg.1 as seen by the lateral field of the eye.
To enable comparisons between the flight speeds with the various gratings, the
50% contrast grating was arbitrarily designated as the control pattern. This
pattern was used throughout the course of the training (24 h before testing
began) and between the testing periods when the other gratings were used.
Experiment 6. Measurement of the effect of removing optic flow on flight speed
This experiment was designed to examine the contribution of optic flow cues
to the control of flight speed. The influence of optic flow was examined by
recording flight speeds when the tunnel was lined with two different types of
stationary pattern: vertical stripes and axial stripes. The vertical pattern
consisted of alternating black and white, vertically oriented stripes, with a
spatial period of 1.8 cm. The axial pattern consisted of alternating black and
white, horizontally oriented stripes, each of width 4 cm. The vertical pattern
was used as a control because the alternating black and white vertical stripes
would provide strong image motion cues to a bee flying along the tunnel. The
axial pattern, on the other hand, was used to create a condition in which the
optic flow cues were very weak. This is because flight in the direction of the
stripes would produce very little apparent motion of the images of the walls
on the retina. Because of the rather dramatic difference in texture between
the two patterns, it was necessary to place each pattern in the tunnel for
about 1 h before commencing flight measurements. This ensured that the bees
were accustomed to the change in the appearance of the tunnel environment.
Four testing periods were used for each pattern.
Analysis of flight trajectories
The number and frequency of trained bees that visited the apparatus were
usually such that, most of the time, only one bee was flying in the tunnel,
either towards the feeder or away from it. Only flights towards the feeder
were analysed. To avoid possible effects of interaction between bees, flights
in which more than one bee was flying simultaneously in the tunnel were not
analysed.
An automated tracking program was developed, using Matlab (v.6.5.0), to track individual bees and analyse the recordings of flights obtained in each experiment. For each flight, the program identified the position of the bee in consecutive frames (every 40 ms). The position of the bee was defined in relation to the tunnel co-ordinates x, y and z, where x denotes axial direction, y the transverse direction and z the vertical direction (Fig. 1B). Only x and y could be measured, as the system used a single camera (rather than a stereo pair). z was assumed to be constant. Visual observation indicated that, although bees decreased their height as they approached the feeder towards the end of the flight, this assumption was a good approximation within the segment of the flight that was filmed by the camera (Fig. 1A). The resolution of the tracking system, based on the pixel density of the camera is estimated to be 2 mm in x and 2 mm in y.
The data were analysed to calculate the component of the flight velocity in the axial (x) direction (Vx). The program generated plots of bee position (x,y) as a function of time, as well as plots of Vx as a function of time or position. It was also possible to calculate the mean values of Vx over any desired section of the tunnel or during any specified time window. Preliminary analysis revealed that the lateral component of flight velocity (Vy) was much smaller in magnitude compared with the axial component (Vx). In other words, the flight trajectories were essentially straight, with only small deviations from side to side. Given this, and the observation that flight height was reasonably constant within the filmed section of the tunnel (see above), it follows that Vx provides a good approximation of the actual magnitude of the flight speed.
Estimation of image velocities
It was of interest to estimate the angular velocity of the image (the speed
of the image on the retina) under various stimulus conditions. We estimated
the image angular velocity (; in deg. s1) in the
lateral field of view of the eye by using the relationship:
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Statistical analysis
Statistical models accounting for multiple levels of variation were
developed to assess whether covariates such as treatment, time, temperature,
light intensity or humidity affected bee flight speed and to eliminate their
effects. To account for the two principal levels of variation in the study
variation between bees and variation within bees linear mixed
models (McCulloch and Searle,
2001) were used, with bee identity as a random effect. The
response variables of flight speed, treatment, time, temperature, light
intensity and humidity were included in the models as fixed effects. The
significance of each explanatory variable was assessed using Wald tests, and
non-significant terms (at the 5% level) were deleted from models. Analyses
were performed using Genstat (release 6.1; VSN International Ltd, Oxford,
UK).
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Results |
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If bees regulate their flight speed by maintaining a constant rate of optic flow in the eye, flight speed should vary linearly with pattern velocity and the change of flight speed should be equal to the change of pattern velocity. Thus, the equation for the hypothesised flight speed adjustment (solid line, Fig. 3) takes the form: y=mx+c, where y is flight speed, x is pattern velocity and c is the flight speed that bees maintain when the pattern is stationary. If the bees maintain a constant optic flow in the eye, regardless of pattern velocity (i.e. if they compensate perfectly for changes in pattern velocity) then m=1. This assumes that at zero pattern velocity, flight speed is set to achieve the desired optic flow.
An analysis of the data indicates that a model that includes three lines of
different slopes provides a good approximation of the effect of large positive
pattern velocities, large negative pattern velocities and small positive and
negative pattern velocities (including zero pattern velocity) on flight speed.
To fit this model, the pattern velocities were classified into three
categories: high positive, near zero and high negative. A separate line was
fitted within each class. The allocation of data points to each category was
determined by comparing four possible groupings. At each of the two category
boundaries, there was one point that could be included in one of two possible
categories. Models were therefore created for each of the four possible
combinations with the two boundary points. The best model was chosen as the
one with the lowest Akaike's information criterion (AIC)
(Akaike, 1973). A comparison of
the AIC was also used to determine whether the three-line model provided a
better approximation of the data than a one- or two-line model.
For large positive pattern velocities, the model revealed a slope of m=1.36 (dotted line, Fig. 3). There is some evidence that this slope is significantly greater than 1 (two-sided t-test, t189=1.86, P=0.06). This result suggests that, when the pattern is moved in the direction of flight, the bees respond by increasing their flight speed by a greater amount, thus overcompensating for the changes in pattern speed.
For large negative pattern velocities, the slope of the model was m=0.68 (dashed line, Fig. 3). There is some evidence that this slope is significantly different from 1 (two-sided t-test, t189=1.78, P=0.077). Thus, when the pattern moved against the direction of flight, the bees were not making a complete adjustment of flight speed to counter the changes in pattern speed: they were experiencing increased optic flow.
For small pattern velocities about zero, the slope of the model was 0.27 (solid line, Fig. 3). This slope is not significantly different from zero (two-sided t-test, t189=0.63, P=0.53). Thus, at low image velocities, the bees were not adjusting their flight speed to compensate for the small changes in image velocity.
Experiment 2. Effect of temporal changes of pattern velocity on flight speed
This experiment was designed to investigate how bees responded to temporal
changes in pattern speed. Flights of bees flying to the feeder were recorded
under two stimulus conditions: stationary-to-moving and moving-to-stationary,
as detailed in Materials and methods. For each flight, the mean flight speed
was measured over two time windows: one window corresponding to the period
when the pattern was stationary and the other corresponding to the period when
the pattern was in motion. A minimum of 27 flights were analysed for each
experimental condition.
The results are shown in Fig. 4. In the stationary-to-moving condition (Fig. 4A), bees clearly change their flight speed in response to the onset of pattern motion. This is true regardless of the direction of pattern motion: in either case, the change of flight speed is such as to counter the effect of pattern motion. The effect of pattern velocity on flight speed is significant (Wald/d.f.=346.14, P<0.001) and the relationship is approximately linear for positive as well as negative pattern velocities. However, the compensation is not complete: the slope of the regression line is 0.63, a value significantly lower than 1 (two-sided t-test, t222=10.32, P<0.001). Thus, bees respond to temporal increases or decreases in pattern velocity by adjusting their flight speed in such a way as to partially compensate for such changes.
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Taken together, the results of Fig. 4 show that flight speed is sensitive to temporal changes of pattern motion and is equally responsive to changes in either direction.
Experiment 3. Effect of spatial changes of pattern velocity on flight speed
This experiment was designed to investigate how bees respond to spatial
changes of pattern motion. Flights of bees flying to the feeder were recorded
for two experimental conditions: one with the static pattern in the first half
of the tunnel and another with the static pattern in the second half. In each
condition, flights were recorded for a range of pattern speeds and directions,
as detailed in Materials and methods. For each flight, the mean flight speed
was measured in two sections of the tunnel: the static section and the moving
section. A minimum of 24 flights were analysed for each experimental
condition.
The results are shown in Fig. 5. In the static-to-moving condition (Fig. 5A), bees clearly change their flight speed in response to the existence of pattern motion in the second half of the tunnel. This is true regardless of the direction of pattern motion: in either case, the change of flight speed is such as to counter the effect of pattern motion. The effect of pattern velocity on flight speed is significant (Wald/d.f.=191.08, P<0.001) and the relationship is again approximately linear, for positive as well as negative pattern velocities. Again, the compensation is not complete: the slope of the regression line is 0.63, a value significantly lower than 1 (two-sided t-test, t208=8.29, P<0.001). Thus, bees respond to spatial increases or decreases in pattern velocity by adjusting their flight speed in such a way as to partially compensate for such changes.
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In summary, the results of Fig. 5 show that flight speed is sensitive to spatial changes in pattern motion and is equally responsive to changes in either direction.
Experiment 4. Effect of pattern texture on flight speed
This experiment was designed to investigate whether flight speed is
influenced by the spatial texture of the visual environment. Bees were trained
to fly to the end of a tunnel in which the walls were lined with patterns
displaying stationary sinusoidal gratings of various spatial periods, as
detailed in Materials and methods. A minimum of 20 flights were analysed for
each condition.
The results are shown in Fig. 6A. The data indicate that flight speed is largely insensitive to changes in spatial period. The mean flight speed varied by only 5 cm s1 over the three conditions and there was no strong evidence to suggest that the differences were statistically significant (Wald/d.f.=2.09, P=0.10). Thus, flight speed is relatively robust to variations in the spatial texture of the visual environment.
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Experiment 5. Effect of pattern contrast on flight speed
This experiment was designed to investigate whether flight speed is
influenced by changes in the contrast of the visual environment. Bees were
trained to fly to the end of a tunnel in which the walls were lined with
vertical gratings of different contrasts, as detailed in Materials and
methods. A minimum of 14 flights were analysed for each condition.
The results are shown in Fig. 6B. The data indicate that flight speed is largely insensitive to changes in the contrast of the visual environment. The effect of contrast on flight speed is not significant (Wald/d.f.=0.25, P<0.94). Flight speed is highest in the zero-contrast condition, although this value is not significantly different from that at any other contrast. The possible reasons for this outcome will be discussed below. Overall, this experiment reveals that flight speed is rather robust to variations in the contrast of the visual environment.
Experiment 6. Effect of removing optic flow on flight speed
This experiment was designed to examine the contribution of optic flow cues
to the control of flight speed. Flight speeds were measured when the tunnel
was lined with (1) vertical stripes and (2) axial stripes, as detailed in
Materials and methods. Forty-two flights were analysed for the vertical stripe
condition and 70 flights for the axial stripe condition.
The results are shown in Fig.
6C. The data indicate that bees fly substantially faster in the
presence of axial stripes (when optic flow cues are weak) than in the presence
of the vertical stripes (when optic flow cues are strong). The mean flight
speed is 96±23 cm s1 (±
S.D.) with axial stripes, compared with 42±10 cm
s1 with the vertical stripes. The difference in mean flight
speeds between the two conditions is significant at the P<0.001
level (Wald/d.f.=107.13). Furthermore, flight speeds are much more variable in
the axial stripe condition: the standard deviation is approximately twice that
in the vertical-stripe condition. We used a restricted maximum likelihood
(REML) test (Patterson and Thompson,
1971) to test the hypothesis that the variances for the two
conditions are the same. This test showed that there was strong evidence
against the hypothesis (P=0.0032), indicating that flight speeds are
significantly more variable in the absence of optic flow. It is possible that
absence of optic flow leads to greater variation in flight speed even within
individual trajectories, but we did not perform this analysis.
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Discussion |
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The phenomenon is clearest in Experiment 1, for pattern motion in the direction of flight. There, bees encountering the moving pattern increase their flight speed by an amount that is slightly greater than the speed of the pattern. When the pattern is moved against the direction of flight, bees decrease their flight speed by an amount that is slightly lower than the speed of the pattern. The changes in flight speed that are observed in response to the movement of the pattern suggest that the bees are holding the optic flow in the eye within a certain, preferred range. Interestingly, when the pattern is moved at slow speeds, either with or against the direction of flight, there is no associated change in flight speed. This suggests that the honeybee's flight speed control system responds only when the image velocity deviates from its `set point' by an amount that exceeds a certain threshold. From Fig. 3, we see that this threshold is between 10 and 15 deg. s1 (as calculated from the flight speed values at pattern velocities that are close to zero). However, once the deviation exceeds this threshold in either direction the flight speed is adjusted to reduce the deviation back to a level below threshold. As we see below, this `dead zone' in the speed control does not lead to statistically significant changes in the angular velocity of the image, except in two conditions.
In order to test whether the bees were maintaining a constant rate of retinal image flow, we estimated angular velocity as perceived by a bee flying along the tunnel when the patterns were in motion (Experiment 1). To calculate retinal image flow, we either added the pattern velocity to the bees' flight speed (when the pattern was moving against the direction of flight) or subtracted the pattern velocity from the bees' flight speed (when the pattern was moving in the direction of flight). Interestingly, statistical analysis using linear mixed models (as shown in Table 1) reveals that the estimated angular velocity for each pattern velocity does not differ significantly from that obtained when the pattern is stationary, except in two instances, namely when the pattern moved at 22 cm s1 in the direction of flight and at 30 cm s1 against the direction of flight. This suggests that, in all but a few cases, the bees were adjusting their flight speed to maintain a constant rate of image flow across their retina.
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We have seen that, in Experiments 2 and 3 (which examined the effects of temporal and spatial changes of pattern motion), the bees seemed to compensate only partially for the changes in motion. There could be a number of reasons for this. In Experiment 2, the bees would have required a finite time to respond to the change in pattern speed. Furthermore, the pattern did not change speed instantaneously from the stationary to the moving phase, and vice versa: the full transition required anywhere between 0.25 and 1.0 s, depending upon the magnitude of the final speed (see Fig. 4). A bee flying at a speed of, say, 56 cm s1 in the tunnel would be visible in the camera's field of view for only 1.25 s after the onset of pattern motion. Because of these delays and observation constraints, a simple comparison of the mean flight speeds during the stationary and movement periods (as we have done here) would tend to underestimate the magnitude of the full change in flight speed. A more accurate estimate of this total change could have been obtained by filming a larger section of the tunnel, using a longer time window and comparing the mean flight speed during the stationary phase with the flight speed well after the onset of pattern motion. However, such a measurement was not feasible owing to the experimental constraints described above.
A similar underestimation of the change in flight speed could have occurred in Experiment 3. Here, it is possible that the bees' response to the spatial change in pattern motion was not complete within the relatively short distance (70 cm) over which the mean flight speed in the moving section was measured. A better estimate of the change in flight speed could have been obtained by comparing the flight speed in the static section with that observed towards the end of the moving section. However this, again, was not practicable owing to the experimental constraints indicated above.
Experiment 3 reveals another phenomenon that is worthy of mention. When the pattern in the `moving' section was stationary, there was a small, but significant, increase of flight speed in that section compared with the `static' section (see Fig. 5). This is because the separation between the stationary patterns in the `moving' section (32 cm) was larger than in the `static' section (22 cm). Consequently, the bees had to fly faster in the wider section to maintain the same optic flow. This observation adds a further dimension to the results because it means that, when the external pattern was moving, the bees were responding to changes in optic flow that were caused not only by the changes in pattern velocity but also by the changes in pattern distance. In each case, the bees were responding by countering the resulting changes in optic flow.
The results of Experiment 4 reveal that flight speed is relatively insensitive to changes in the spatial texture of the patterns lining the tunnel walls (Fig. 6A). Specifically, when the patterns are sinusoidal gratings, the flight speed does not vary substantially when the spatial frequency of these gratings is changed by a factor of two or four. Because the flight speed is more or less constant at all of these spatial frequencies, it follows that each spatial frequency must induce a proportionally different temporal frequency of intensity fluctuations in the visual system. Therefore, we may conclude that flight speed is largely independent of the spatial as well as the temporal frequency of the gratings.
The results of Experiment 5 reveal that flight speed is relatively
insensitive to changes in the contrast of the patterns lining the tunnel walls
over a broad range of contrasts (100% through to 10%; see
Fig. 6B). When the contrast is
reduced to a nominal value of 0% (by lining the walls with uniformly grey
sheets of paper), the mean flight speed is somewhat greater than at other
contrasts, although the difference is not statistically significant. This
suggests that the visual system is capable of extracting motion cues even in
this impoverished condition. It should be noted, however, that the contrast of
the grey walls is not truly zero: rather, it is very low. Residual contrast
features arising from imperfections in the printing process, from light and
shade effects, and from the junctions between adjacent sheets must contribute
to the detection of image movement. Indeed, it is known that the insect visual
system is sensitive to motion at contrasts as low as 7%
(Dvorak et al., 1980). It is
possible that contrast adaptation a phenomenon whereby the contrast
sensitivity of the visual system is enhanced in the presence of low ambient
contrast and is suppressed in the presence of high ambient contrast
(Harris et al., 2000
)
plays a role in amplifying the sensitivity to low contrasts. This possibility
is supported by the finding that regulation of flight speed is better at zero
contrast (Fig. 6B) than when
the walls are lined with high-contrast axial stripes
(Fig. 6C). In the former case,
the absence of high environmental contrast would have made the visual system
highly sensitive to the low-contrast flaws in the stimulus, whereas in the
latter case the high contrast of the axial stripes would have made the system
insensitive to the flaws. Since the axial stripes, by themselves, carry no
horizontal image motion cues, it is reasonable to expect that, in the presence
of contrast adaptation, the motion signals will be weaker with the axial
stripes, causing the flight speed to be generally higher and more variable.
This is indeed what occurs (Fig.
6C).
Our findings suggest that the visual pathways that control flight speed are
capable of measuring and regulating the angular velocity of the images of the
walls in the eye, largely independently of the spatial texture and contrast of
the environment. A similar phenomenon has been observed in experiments
investigating odometry in honeybees. The perception of distance flown depends
upon the extent of image motion that is experienced by the eye but is largely
independent of the contrast or the spatial texture of the image
(Esch and Burns, 1995;
Hrncir et al., 2003
;
Si et al., 2003
;
Srinivasan et al., 1996
;
Srinivasan and Zhang, 1997
,
2000
). Robust perception of
image motion has also been observed in the context of another visually
mediated response the centring behaviour. Bees flying through a narrow
gap or tunnel maintain equidistance between the walls by adjusting their
lateral position so as to balance the image velocities in the two eyes
(Srinivasan et al., 1991
).
Bees continue to fly down the middle of the tunnel even when the spatial
frequencies or contrasts of the gratings on the two walls are substantially
different. This indicates that the visual pathway that mediates this behaviour
is again measuring image speed largely independently of the contrast or
spatial texture of the environment.
The movement-detecting mechanisms underlying the three behaviours discussed
above seem to have properties that are rather different from those of the
well-studied optomotor behaviour in insects. The optomotor response is a
behaviour in which a flying insect compensates for unwanted body rotations by
detecting the resulting rotations of the image in the eye and generates
motions to compensate for these deviations
(Reichardt, 1969). The
optomotor response appears to be characterised by a movement-detecting system
that is sensitive to changes in the contrast, spatial frequency and temporal
frequency of the moving image. This system appears not to encode image angular
velocity in a manner that is robust to variations in these parameters.
Therefore, it is very likely that the visual pathways that control flight
speed, mediate the centring response and generate the odometric signal have
properties that are different from the pathway that drives the optomotor
response. There is an extensive literature on the anatomy and physiology of
movement-detecting neurons in the insect brain, whose response properties
mirror the characteristics of the optomotor response (reviewed by
Egelhaaf et al., 1988
;
Hausen, 1993
). On the other
hand, there is relatively little evidence, so far, for the existence of
motion-sensitive neurons with response properties that meet the requirements
for centring behaviour, odometry and flight speed control. These latter
behaviours require movement-detecting mechanisms that measure image angular
velocity relatively independently of contrast and spatial texture. Future work
should identify the neural pathways that subserve flight speed control,
odometry and centring behaviour and investigate the response properties of
neurons in these pathways. Some reports of velocity-tuned neurons are now
beginning to appear (Dror et al.,
2001
; Ibbotson,
2001
), although it remains to be ascertained whether these neurons
indeed participate in the behaviours discussed above.
The present study has demonstrated that flight speed is regulated by holding constant the image angular velocity in the eye. What is the level of image angular velocity that is maintained? Table 2 shows estimates of the image angular velocities that the bees were maintaining under four different stimulus conditions. These angular velocities were calculated as described in Materials and methods. It is evident from the table that, despite the widely varying stimulus conditions, the bees were adjusting their flight speeds to hold the image angular velocity in the range of 215320 deg. s1 (the spread of angular velocities shown in this table is somewhat larger than in Table 1 because the data in Table 2 span a wider range of stimulus patterns and experimental conditions). Another way of evaluating the efficacy of this regulatory process would be to examine the extent to which the image angular velocities would vary between different stimulus conditions if the bees did not react to the various conditions and instead maintained a constant flight speed. For example, with a stationary random dot pattern, the average flight speed in the 32 cm tunnel is 68.3 cm s1 (average of flight speeds in rows 35 of Table 2), generating an average image angular velocity of 245 deg. s1 (average of image angular velocities in rows 35 of Table 2). If the bees were to maintain the same flight speed when the pattern was moving at 52 cm s1 in the same direction, they would experience an image angular velocity of only 58 deg. s1, a value substantially lower than that actually experienced (254 deg. s1; row 8, Table 2). Thus, the bees are compensating fully for the motion of the pattern by adjusting their flight speed by an amount that is appropriate to restore the image velocity to a level very close to its original value.
|
What are the consequences of maintaining a constant image angular velocity during flight? One outcome would be that flight speed would tend to be high when travelling in open fields, for example, and low during flight through densely cluttered vegetation. Thus, maintaining a constant image angular velocity in the eye would ensure that the speed of flight is automatically adjusted to a level that is safe and appropriate to the environment. The relative insensitivity of the underlying movement-detecting mechanism to the contrast or the spatial texture of the environment would enhance the robustness of this control system, ensuring that flight speed depends primarily on the distances to nearby surfaces and not on their visual properties such as contrast or visual texture.
A recent study found that bumblebees flying outdoors in natural
environments cruise at an average speed of 7.1 m s1, at a
height of 2 m above the ground (Riley
et al., 1999
), thus maintaining an image angular velocity of
200 deg. s1. This figure is very similar to that
maintained by bees during flight in our experimental tunnels. Thus, although
flight is fast in open environments, the image velocities experienced are very
similar to those experienced in the confined environment of the tunnel,
because flight in the tunnel is correspondingly slower.
Maintaining a constant image angular velocity would also simplify certain
difficult manoeuvres, such as making a grazing landing on a flat surface. If a
bee holds the image velocity of a surface constant whilst approaching it,
flight speed would automatically be reduced as the surface is neared, thus
ensuring a smooth touchdown. Indeed, bees performing grazing landings do hold
the image velocity of the surface constant. This image angular velocity is in
the range of 250750 deg. s1, with the value varying
depending upon the particular bee or the particular landing trajectory
(Srinivasan et al., 2000).
Interestingly, these image velocities are comparable with those maintained by
bees whilst cruising through tunnels (see
Table 2). Thus, the visual
mechanisms that regulate cruising flight speed may be similar, or identical,
to those used to control grazing landings.
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Acknowledgments |
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