The spectral input to honeybee visual odometry
Biozentrum, Zoologie II, Am Hubland, 97074 Würzburg, Germany
* Author for correspondence at present address: Biological Sciences, Queen Mary, University of London, Mile End Road, London E1 4NS, UK (e-mail: l.chittka{at}qmul.ac.uk)
Accepted 4 April 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: colour vision, dance language, motion vision, optical flow, waggle dance, odometry, honeybee, Apis mellifera
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Do bees use their trichromatic colour vision to measure the optic flow? In
fact, in several types of motion-related behaviours, such as the optomotor
response, edge detection and motion parallax, bees behave as if they were
colour blind (Srinivasan,
1989). These behaviours are driven entirely by a single class of
receptor: the long-wave or green receptor
(Giurfa and Lehrer, 2001
;
Horridge, 2000
;
Spaethe et al., 2001
). Here,
we investigate the spectral input channel that drives the bee odometer. We
evaluate not only the probability of waggle dances as a function of the visual
contrast experienced during flight but also waggle run duration, which in the
honeybee codes for the distance to a food source.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() | (1) |
|
|
The scaling factor k in equation 1 is given by:
![]() | (2) |
![]() | (3) |
When Apis mellifera ligustica workers fly through open territory,
they typically perform round dances (which are unspecific with respect to
direction) when the food sources are within a range of 50 m. Above this
threshold, bees switch to the figure-eight-shaped waggle dance, where the
duration of the central `waggle run' indicates flight distance as perceived by
the bees. When bees fly through a textured tunnel, they massively overestimate
flight distance. This is because flying through the narrow tunnel induces
translatory optic flow of a magnitude that is much higher compared with a
situation when the bee flies at the same speed but in the open field
(Srinivasan et al., 2000).
Thus, the tunnel can be used as a tool to investigate the colour parameters
used as input to the bee odometer. We determined the probability of waggle
dances performed for each colour pair displayed in the tunnel, as well as
waggle durations depending on the colours used. We tested whether any single
receptor (UV, blue or green) was solely responsible for driving the bee
odometer or whether bees use colour contrast for this purpose. We also
explored the possibility that bees might use the sum of the three
photoreceptors (brightness) as the input to the mechanisms that evaluate optic
flow.
A new group of 327 workers was trained for each new Julesz pattern (Table 2). The linings in the tunnel were replaced every 3 h to prevent bees from using scent marks or bee excrement as an additional visual cue. Dances of trained bees were videotaped with a digital Camcorder (Panasonic NV-DS35EG) at 25 frames s-1. Dancers typically switched between waggle dance circuits and round dance circuits during their dances; for each individual bee, we counted the complete waggle dance and round dance circuits. We determined the mean percentage of waggle runs performed for each Julesz pattern. This means that we first calculated the percentage of waggle runs for each individual, then calculated the mean of individual percentages. This procedure ensured that each individual bee entered the analysis with equal weight, regardless of how long it was observed. We also analysed the waggle duration of bees as a function of colour pattern in the tunnel using frame-by-frame video analysis.
|
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Correlation with green contrast is particularly strong in the range up to 0.15 and flattens off at higher values (Fig. 2C). The correlation coefficients above are determined for the entire range of contrast values; if we calculate rs for the range of green contrast from 0 to 0.15, the correlation becomes even more pronounced (rs=0.893, P=0.005, N=7). Note that this remains highly significant even after Bonferroni correction. For the other colour parameters, there is no such correlation even when only the lower range of contrast values (up to 0.15) is considered (UV contrast: rs=0.45, P=0.26, N=8; blue contrast: rs=-0.8, P=0.2, N=4; colour contrast: rs=-0.4, P=0.6, N=4). Since brightness contrast can vary over three times the range of the colour parameters, we recalculated the correlation between brightness contrast and waggle dance probability for contrast values up to 0.45; again, the correlation is not significant (rs=-0.196, P=0.61, N=9).
We therefore conclude that the decision to perform waggle dances rather than round dances is based on visual odometry driven by the green receptor. Because the effect of green contrast on dance probability is especially pronounced over low contrast values, we conjecture that bees have difficulties perceiving the contrast between adjacent squares in the tunnel when green contrast is low. We assume that the signal-to-noise ratio increases continuously over the range of contrast values from 0 to 0.15 and that at all values above 0.15, contrast is reliably perceived, so that waggle dance probability increases no further.
The evaluation of waggle run duration is consistent with this
interpretation. Whenever bees experienced green contrast sufficiently strong
for the waggle dance to be triggered, waggle duration was entirely independent
of the particular colour pattern presented in the tunnel
(Fig. 2F). There was no
significant difference in waggle duration between the different patterns
(KruskalWallis test; K=10.35, P=0.41, N=92).
Waggle runs invariably lasted about 400 ms. For bees foraging in natural
landscapes, this waggle run duration codes for food sources 100200 m
from the hive, depending on the particular territory passed in flight
(Esch et al., 2001). We
interpret this to mean that the bee odometer is sensitive only to the
integration of image motion over time, not to the amount of contrast
present in the image. This applies, of course, only if contrast is
sufficiently high to be detected.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
While the probability of waggle dances can clearly be influenced by the
visual scene passed en route, the duration of the waggle phase (a
component of the distance code) remains unaffected. This might be because
waggle phase duration (as opposed to waggle dance probability) is independent
of optic flow above a certain distance. However, in a new study, Si et al.
(2003) showed that waggle
dance duration can be influenced by the visual pattern passed in
flight and is influenced by distance beyond 6 m. We therefore conjecture that
the visual odometer relies only on the magnitude of optic flow
(Srinivasan et al., 2000
) not
the amount of contrast presented within the scene passed en
route.
Whether or not bees overestimate flight distance as a response to
experimentally increased optic flow depends, of course, on whether contrast in
the visual scene is detected in the first place. We assume that over the range
of low green contrast values from 0 to 0.15, several sources of noise
determine whether or not contrast between adjacent squares in the tunnel is
detected. It is noteworthy that in all patterns, even those with very low
green contrast, waggle dances are elicited at least occasionally. In the
blue4grey6 pattern, green contrast is only 3.7%, which corresponds to a
predicted difference in green receptor voltage signal of
V/Vmax=0.016. Vorobyev et al.
(2001) report a noise standard
deviation of 0.20.4 mV for the honeybee green receptor at daylight
intensity, and a Vmax of 38 mV for that receptor type. The
predicted signal difference for the blue4grey6 pattern is therefore
0.016x38 mV=0.61 mV, which is outside the noise standard deviation. We
would therefore predict that if receptor noise were the only limiting factor,
even the patterns with the lowest green contrast would be above detection
threshold. But noise of subsequent neuronal processing units, such as lamina
monopolar cells, can be substantially stronger than in photoreceptors
(de Souza et al., 1992
), so
limiting contrast detection more strongly than the peripheral (receptor)
level. In addition, the bees' flight speed and proximity to the tunnel walls
will determine whether or not low contrast between adjacent squares will be
detected. Small fluctuations in illumination might introduce additional
variation, although we expect them to be mostly compensated for by
photoreceptor adaptation (Laughlin,
1989
) and colour constancy
(Kevan et al., 2001
). We
assume that at a green contrast of 0.15, the signal reliably exceeds all forms
of noise, and contrast is reliably detected.
Our results are in line with those on other behaviours in bees controlled
by motion vision, all of which appear to be colour blind and entirely driven
by the long-wavelength or green receptor
(Giurfa and Lehrer, 2001;
Horridge, 2000
;
Kaiser, 1974
;
Spaethe et al., 2001
;
Srinivasan, 1989
). Even though
bees have excellent trichromatic colour vision, which they use, for example,
in flower identification (von Frisch,
1967
; Chittka et al.,
2001
), colour is not used for motion vision. Apparently, in bees,
colour and motion are processed strictly in parallel
(Lehrer, 1993
;
Zhang and Srinivasan,
1993
).
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Chittka, L., Shmida, A., Troje, N. and Menzel, R. (1994). Ultraviolet as a component of flower reflections, and the colour perception of hymenoptera. Vision Res. 34,1489 -1508.[CrossRef][Medline]
Chittka, L., Spaethe, J., Schmidt, A. and Hickelsberger, A. (2001). Adaptation, constraint, and chance in the evolution of flower color and pollinator color vision. In Cognitive Ecology of Pollination (ed. L. Chittka and J. D. Thomson), pp.106 -126. Cambridge: Cambridge University Press.
de Souza, J., Hertel, H., Ventura, D. F. and Menzel, R. (1992). Response properties of stained monopolar cells in the honeybee lamina. J. Comp. Physiol. A 170,267 -274.
Endler, J. A. (1993). The color of light in forests and its implications. Ecol. Monogr. 63, 1-27.
Esch, H. E. and Burns, J. E. (1995). Honeybees use optic flow to measure the distance of a food source. Naturwissenschaften 82,38 -40.[CrossRef]
Esch, H. E., Zhang, S., Srinivasan, M. V. and Tautz, J. (2001). Honeybee dances communicate distances measured by optic flow. Nature 411,581 -583.[CrossRef][Medline]
Giurfa, M. and Lehrer, M. (2001). Honeybee vision and floral displays: from detection to close-up recognition. In Cognitive Ecology of Pollination (ed. L. Chittka and J. D. Thomson), pp. 61-82. Cambridge: Cambridge University Press.
Horridge, A. (2000). Seven experiments on pattern vision of the honeybee, with a model. Vision Res. 40,2589 -2603.[CrossRef][Medline]
Kaiser, W. (1974). The spectral sensitivity of the honeybee optomotor walking response. J. Comp. Physiol. 90,405 -408.
Kevan, P. G., Chittka, L. and Dyer, A. G. (2001) Limits to the salience of ultraviolet: lessons from colour vision in bees and birds. J. Exp. Biol. 204,2571 -2580.[Medline]
Laughlin, S. B. (1989). The role of sensory adaptation in the retina. J. Exp. Biol. 146, 39-62.[Abstract]
Lehrer, M. (1993). Parallel processing of motion, shape and colour in the visual system of the bee. In Sensory Systems of Arthropods (ed. K. Wiese), pp.266 -272. Basel: Birkhäuser Verlag.
Peitsch, D., Fietz, A., Hertel, H., de Souza, J., Ventura, D. F. and Menzel, R. (1992). The spectral input systems of hymenopteran insects and their receptor-based colour vision. J. Comp. Physiol. A 170,23 -40.[Medline]
Si, A., Srinivasan, M. V. and Zhang, S. (2003)
Honeybee navigation: properties of the visually driven `odometer'.
J. Exp. Biol. 206,1265
-1273.
Spaethe, J., Tautz, J. and Chittka, L. (2001).
Visual constraints in foraging bumblebees: flower size and color affect search
time and flight behavior. Proc. Natl. Acad. Sci. USA
98,3898
-3903.
Srinivasan, M. V. (1989). Motion sensitivity in insect vision: roles and neural mechanisms. In Neurobiology of Sensory Systems (ed. R. N. Singh and N. J. Strausfeld), pp.97 -106. New York, London: Plenum Publishing Corporation.
Srinivasan, M. V., Zhang, S., Altwein, M. and Tautz, J.
(2000). Honeybee navigation: nature and calibration of the
"odometer". Science
287,851
-853.
Srinivasan, M. V., Zhang, S. W. and Bidwell, N. J.
(1997). Visually mediated odometry in honeybees. J.
Exp. Biol. 200,2513
-2522.
von Frisch, K. (1967). The Dance Language and Orientation of Bees. Cambridge: Harvard University Press.
Vorobyev, M., Brandt, R., Peitsch, D., Laughlin, S. B. and Menzel, R. (2001). Colour thresholds and receptor noise: behaviour and physiology compared. Vision Res. 41,639 -653.[CrossRef][Medline]
Waddington, K. D. (2001). Subjective evaluation and choice behavior by nectar- and pollen-collecting bees. In Cognitive Ecology of Pollination (ed. L. Chittka and J. D. Thomson), pp. 41-60. Cambridge: Cambridge University Press.
Wyszecki, G. and Stiles, W. S. (1982). Color Science: Concepts and Methods, Quantitative Data and Formulae, vol. 2. New York: Wiley.
Zhang, S. and Srinivasan, M. V. (1993). Behavioural evidence for parallel information processing in the visual system of insects. Jpn. J. Physiol. 43,247 -258.[Medline]