Primer

Dances as Windows into Insect Perception

Lars Chittka xperimental psychologists working with humans have a fundamental advantage over scientists studying the behaviour of other animals. This is because human subjects can give a verbal account of their experience. For example, they can report: These two lights of different colour look equally bright or This object looks further away than that one. Such direct reports facilitate studying how information from the sensory periphery, that is, the sense organs that actually interface with the environment, is processed in the brain. The perceptual world of animals is often very different from that of humans. Many animals have sensory facilities that we humans lack; for example, insects can see ultraviolet and polarised light. But how they actually perceive the world, based on information from their sensory periphery, is often beyond our grasp. Because animals cannot describe their sensations, our access to them is often based on indirect psychophysical tests, where animal performance depends fundamentally on motivation and training method (Chittka et al. 2003). However, some animals do in fact describe the world around them, but not necessarily in ways that we might intuitively understand. Perhaps the best example of this are the honeybees (genus Apis), which have a symbolic language that nestmates use to communicate with each other about protable food sources. By eavesdropping on this communication, scientists have recently obtained a unique perspective into the perceptual world of insects. How does the dance language work? A triumphant scout bee returns from the eld, and advertises the location of a newly discovered food source to nestmates. To do this, the forager performs a repetitive sequence of movements, the so-called waggle dance, which is one of the most intriguing examples of complex animal behaviour. The successful forager wiggles her abdomen provocatively from side to side, moving forward in a
PLoS Biology | http://biology.plosjournals.org

straight line. Then she runs in a half circle to the left, back to her starting point, performs another straight wiggle run along the path of her rst, and then circles to the right (Figure 1).

This pattern is repeated multiple times, and is eagerly attended by unemployed bees in the hive. Shortly after such dances commence, dozens of newly recruited foragers arrive at the food source being advertised. In the 1940s, Nobel laureate Karl von Frisch deciphered the code hidden in this seemingly senseless choreography performed on vertical honeycombs in the darkness of the hive (reviewed in von Frisch 1967). He found that the angle of the waggle run from the vertical is equal to the angle between the suns azimuth and the indicated food source outside the hive. For example, if a food source is found in the direction of the sun, the dancer will waggle straight up the vertical comb. If food is found 45 to the right of the suns direction, the waggle run will be oriented 45 to the right of vertical on the comb (Figure 1). The distance to the target, a ower patch with abundant nectar or pollen, is encoded in the duration of the waggle run: the longer the bee waggles, the larger the distance of the food from the hive. No other species (besides humans) uses a similarly symbolic representation to communicate information from the real world. But how do bees measure the ight distance that they communicate so precisely? It was previously thought they do this by measuring the energy used as they y (Heran 1956). However, doubts emerged when it was found that distance estimation by bees could be manipulated by altering the number of landmarks between the hive and a food source, suggesting bees were counting landmarks encountered en route (Chittka and Geiger 1995). In an elegant experiment, Esch and Burns

DOI: 10.1371/journal.pbio.0020216.g001

Figure 1. Figure-Eight-Shaped Waggle Dance of the Honeybee (Apis mellifera)

A waggle run oriented 45 to the right of up on the vertical comb (A) indicates a food source 45 to the right of the direction of the sun outside the hive (B). The abdomen of the dancer appears blurred because of the rapid motion from side to side. (Figure design: J. Tautz and M. Kleinhenz, Beegroup Wrzburg.)

Copyright: 2004 Lars Chittka. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Lars Chittka is at the School of Biological Sciences, Queen Mary College, University of London, London, United Kingdom. E-mail: [email protected] DOI: 10.1371/journal.pbio.0020216

July 2004 | Volume 2 | Issue 7 | Page 0898

(1995) tapped into the bees dance language to access their subjective assessment of ight distance. They let bees forage from a food source 70 m from the hive and recorded the dance distance code of the returning foragers. Subsequently, the feeder was attached to a weather balloon, and slowly lifted to an altitude of 90 mso that the distance between the hive and the food now increased from 70 m to 114 m. Correspondingly, foragers should have indicated a longer distance, by stretching their waggle run duration. But, in fact, the perceived distance (as indicated in the dance) decreased by more than 50%! This clearly shows that bee perception of distance cannot solely be based on energy expenditure, since a longer ight that cost more energy was danced as a shorter distance in the waggle run. So what actually drives the bee odometer? Because the landscape bees pass in ight moves more slowly when bees y at higher altitudes, Esch and Burns (1995) conjectured that foragers process the speed with which visual contours move across the eye (optic ow), and integrate this with travel time. To conrm this hypothesis, Srinivasan et al. (2000) further exaggerated the experienced image ow, by training bees to y through narrow chequered tunnels. These bees grossly overestimated actual travel distance, bragging to their nestmates that they had own 195 m when in fact they had own 6 m. Attendees of these dances promptly believed the highclass swindle, and searched for food at remote locations that the dancers had never even visited (Esch et al. 2001). The quality of information available about the velocity of the passing landscape will depend, of course, on the sensitivity of the eyes. The eyes of bees contain three types of colour receptors, with maximum sensitivity in the ultraviolet, blue, and green domains of the spectrum (Autrum and von Zwehl 1964). Their excellent colour vision is optimal for ower identication (Chittka 1996), but do they also use it to measure the image velocity of the passing landscape? Surprisingly, the answer is nobee odometry is in fact totally colour blind. Chittka and Tautz (2003) found that bees use exclusively the signal from their green receptors for measuring image velocity (Figure 2), conrming
PLoS Biology | http://biology.plosjournals.org

DOI: 10.1371/journal.pbio.0020216.g002

Figure 2. Bees Use Different Visual Cues When Viewing Flowers and Landscape Image Motion

Although bees see owers in colour, they do not analyse the colours of the landscape image that moves across the eye as they y. Their perception of landscape motion is colour-blind; motion vision is driven solely by a single spectral receptor type, the bees green receptor. This is reected in the distance code of the dance: the more green contrast is present in the scene, the further bees think they have own. (Figure design: F. Bock, Beegroup Wrzburg.)

earlier reports that motion vision in bees is mediated only by this receptor type (Giurfa and Lehrer 2001; Spaethe et al. 2001). Thus, the level of intensity contrast present in the scene strongly inuences the bees subjective experience of ight distance (Chittka and Tautz 2003; Si et al. 2003). With so many external variables inuencing distance estimation, it seems unlikely that the honeybee odometer would be very robust in natural conditions. Now, as reported in this issue of PLoS Biology, Tautz et al. (2004) have quantied the bees subjective experience of distance travelled when they y over natural terrain with varying levels of contrast. Specically, they compared the dances of bees ying over water (scenery with low visual contrast) with those of bees ying over land (scenery with relatively high contrast). They trained bees to forage at a feeder on a boat, which was paddled increasing distances from the hive, until it reached an island. All the while, observers at the hive deciphered

the dances of the bees returning from the feeder. Interestingly, bees ying 200 m over water hardly appeared to register an increase in travel distance, whereas the same increase in distance own over land resulted in a substantial increase in perceived ight distance. This is consistent with the hypothesis that the bees odometer is largely based on visual, external cues and demonstrates that this system is sensitive to visual contrast. But there must be something else beside visual cues. Navigation over water, in the near absence of visible ground features, is extremely difcult without a reliable internal instrument measuring travel speed. This is the case even for us humans with sophisticated measuring devices: malfunctioning air speed indicators have been responsible for several airplane crashes into water, for example Birgenair Flight 301 and AeroPeru Flight 603 in 1996. Heran and Lindauer (1963) likewise observed that honeybees ying over lakes sometimes lost altitude and plunged into the water. However, the new study by Tautz et al. (2004) also shows that most bees will reliably y over prolonged stretches of water without accident. Furthermore, even though bees experience only a small increase in subjective travel distance when ying over water, it is not zero. This indicates that bees do perhaps resort to an internal measure of ight distance when other cues fail. For example, bumblebees walking to a food source in absolute darkness, that is, in the complete absence of visual cues, are able to correctly gauge travel distance (Chittka et al. 1999), indicating that an internal odometer, possibly based on energy consumption, also exists. It appears that animal navigation, just like aviation, relies on multiple backup systems that support each other and can compensate if one system fails in a certain context. Spying on honeybee dances can not only tell us about the cues they use for navigation, but also allows insights into the cognitive architecture that governs other aspects of bee behaviour, such as the assessment of ower quality. Weve learned that bees prefer high over low nectar concentrations because this is reected in their dances. When bees nd better nectar, they dance more enthusiastically, that is, the number of dance circuits per minute increases
July 2004 | Volume 2 | Issue 7 | Page 0899

(Seeley et al. 2000; Waddington 2001). However, Waddington (2001) found that the relationship between actual and perceived nectar quality is nonlinear. In fact, it is a positive but decelerating relationship, so that an increase in sucrose concentration from 10% to 20% results in twice the difference in dance rate that an increase from 50% to 60% does. Interestingly, the perceived change in quality is stronger when there is a decrease than when there is an increase in nectar quality of the same magnitude. Such asymmetric perception of gains and losses is well known in humans, where it has been linked to risk-aversive behaviour (Tversky and Kahnemann 1981). Unfortunately, animal subjects often do not yield this type of information very readily. Only in their own language do they reveal many of their perceptual peculiarities. Using the bee language as a window into insect visual perception has been a wonderful tool and is a promising avenue for further research into the question of

how miniature brains encode the world around them.

References Autrum HJ, von Zwehl V (1964) Die spektrale Empndlichkeit einzelner Sehzellen des Bienenauges. Z Vergl Physiol 48: 357384. Chittka L (1996) Optimal sets of colour receptors and opponent processes for coding of natural objects in insect vision. J Theor Biol 181: 179196. Chittka L, Geiger K (1995) Can honeybees count landmarks? Anim Behav 49: 159164. Chittka L, Tautz J (2003) The spectral input to honeybee visual odometry. J Exp Biol 206: 23932397. Chittka L, Williams NM, Rasmussen H, Thomson JD (1999) Navigation without vision: Bumblebee orientation in complete darkness. Proc R Soc Lond B Biol Sci 266: 4550. Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Bees trade off foraging speed for accuracy. Nature 424: 388388. Esch HE, Burns JE (1995) Honeybees use optic ow to measure the distance of a food source. Naturwissenschaften 82: 3840. Esch HE, Zhang S, Srinivasan MV, Tautz J (2001) Honeybee dances communicate distances measured by optic ow. Nature 411: 581583. Giurfa M, Lehrer M (2001) Honeybee vision and oral displays: From detection to close-up recognition. In: Chittka L, Thomson JD, editors. Cognitive ecology of pollination. Cambridge: Cambridge University Press. pp. 6182. Heran H (1956) Ein Beitrag zur Frage nach der Wahrnehmungsgrundlage der

Entfernungsweisung der Bienen. Z Vergl Physiol 42: 103163. Heran H, Lindauer M (1963) Windkompensation und Seitenwindkorrektur der Bienen beim Flug ueber Wasser. Z Vergl Physiol 47: 3955. Seeley TD, Mikheyev AS, Pagano GJ (2000) Dancing bees tune both duration and rate of waggle-run production in relation to nectar-source protability. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 186: 813819. Si A, Srinivasan MV, Zhang SW (2003) Honeybee navigation: Properties of the visually driven odometer. J Exp Biol 206: 12651273. Spaethe J, Tautz J, Chittka L (2001) Visual constraints in foraging bumblebees: Flower size and color affect search time and ight behavior. Proc Nat Acad Sci U S A 98: 38983903. Srinivasan MV, Zhang S, Altwein M, Tautz J (2000) Honeybee navigation: Nature and calibration of the odometer. Science 287: 851853. Tautz J, Zhang S, Spaethe J, Brockmann A, Si A, et al. (2004) Honeybee odometry: Performance in varying natural terrain. PLoS Biol 2: e211 DOI: 10.1371/journal.pbio.0020211. Tversky A, Kahnemann D (1981) The framing of decisions and psychology of choice. Science 211: 453458. von Frisch K (1967) The dance language and orientation of bees. Cambridge (Massachusetts): Harvard University Press. 566 p. Waddington KD (2001) Subjective evaluation and choice behavior by nectar- and pollencollecting bees. In: Chittka L, Thomson JD, editors. Cognitive ecology of pollination. Cambridge: Cambridge University Press. pp. 4160.

PLoS Biology | http://biology.plosjournals.org

July 2004 | Volume 2 | Issue 7 | Page 0900