Honeybee navigation: critically examining the role of the polarization compass

Abstract

Although it is widely accepted that honeybees use the polarized-light pattern of the sky as a compass for navigation, there is little direct evidence that this information is actually sensed during flight. Here, we ask whether flying bees can obtain compass cues derived purely from polarized light, and communicate this information to their nest-mates through the 'waggle dance'. Bees, from an observation hive with vertically oriented honeycombs, were trained to fly to a food source at the end of a tunnel, which provided overhead illumination that was polarized either parallel to the axis of the tunnel, or perpendicular to it. When the illumination was transversely polarized, bees danced in a predominantly vertical direction with waggles occurring equally frequently in the upward or the downward direction. They were thus using the polarized-light information to signal the two possible directions in which they could have flown in natural outdoor flight: either directly towards the sun, or directly away from it. When the illumination was axially polarized, the bees danced in a predominantly horizontal direction with waggles directed either to the left or the right, indicating that they could have flown in an azimuthal direction that was 90° to the right or to the left of the sun, respectively. When the first half of the tunnel provided axial illumination and the second half transverse illumination, bees danced along all of the four principal diagonal directions, which represent four equally likely locations of the food source based on the polarized-light information that they had acquired during their journey. We conclude that flying bees are capable of obtaining and signalling compass information that is derived purely from polarized light. Furthermore, they deal with the directional ambiguity that is inherent in polarized light by signalling all of the possible locations of the food source in their dances, thus maximizing the chances of recruitment to it.

Keywords: compass; honeybee; navigation; polarization vision; waggle dance.

Figure 1.

Results of Experiment 1, in which bees flew in a tunnel with a view of the natural sky over a period of 1 day (13 March 2008) with the sun at various positions as shown in (a). The tunnel pointed in a direction 18° east of true North. The panels show orientation histograms of the waggle axes obtained on this day at various times of the day: (b) 7.56–9.09, (c) 9.15–9.30, (d) 10.47–11.10, (e) 11.10–11.20, (f) 12.41–12.46, (g) 14.13–14.25 and (h) 15.20–16.15. In each panel, the thin lines (blue in the online version) depict the dance orientation histogram. The thick continuous line (red in the online version) shows the mean dance vector. For clarity, the mean dance vector is shown as 6× the actual length. Thus, the maximum possible length of the mean vector as shown here would be 6.0, rather than 1.0. The thick broken line (green in the online version) denotes the dance direction expected at that particular time of day, calculated as described in §2. These values are 145.0°, 136.0°, 103.6°, 96.2°, 42.8°, 11.7° and –4.7°, respectively in (b) through (h), the angles being defined as positive counterclockwise with respect to the rightward horizontal direction. The length of this line has no significance, but it is shown equal to the length of the thick line to facilitate comparison of their directions. In this and subsequent figures each panel shows the magnitude (R) and direction (θ) of the mean vector calculated as described in §2, and the number of bees, number of dances and number of waggles analysed. (Online version in colour.)

Figure 2.

Results of Experiment 2, in which bees flew in a tunnel with transversely polarized illumination, as depicted by the lines on the ceiling in (a). This illumination mimics the pattern of polarized illumination that a bee would experience if it were to fly directly away from the sun, as shown in (b), or directly towards it. In (c), the thin lines (blue in the online version) depict the dance orientation histogram. The thick line (red in the online version) depicts the mean direction of the waggle axis, taking into account the up–down symmetry in the dance directions, as described in §2. This mean direction is oriented 91.7° counterclockwise relative to the horizontal rightward direction. (Online version in colour.)

Figure 3.

Results of Experiment 3, in which bees flew in a tunnel with axially polarized illumination, as depicted by the lines on the ceiling in (a). This illumination mimics the pattern of polarized illumination that a bee would experience if it were to fly in a direction such that the sun is 90° to the right, as shown in (b), or 90° to the left. In (c), the thin lines (blue in the online version) depict the dance orientation histogram. The thick line (red in the online version) depicts the mean direction of the waggle axis, taking into account the left–right symmetry in the dance directions, as described in §2. This mean direction is oriented 1.3° clockwise relative to the horizontal rightward direction. (Online version in colour.)

Figure 4.

(a–d) Four examples of dances of individual bees returning from a tunnel that provided transversely polarized illumination (Experiment 2). Each panel shows the waggle axis orientations recorded sequentially in a single dance. (Online version in colour.)

Figure 5.

Dance orientation histograms for bees flying in a tunnel with transversely polarized illumination (Experiment 2) between 12.55 and 13.14 on 1 May 2008 (a), and between 14.40 and 15.16 on 30 April 2008 (b). In each case, the mean orientation of the dance axis is shown (in the lower left corner) as the angle measured counterclockwise from the horizontal rightward direction. Other details are as in figures 2 and 3. (Online version in colour.)

Figure 6.

Results of Experiment 4, in which bees flew in a tunnel with transversely polarized illumination in the first half and axially polarized illumination in the second half, as depicted by the lines in the ceiling in (a). This arrangement mimics the overhead illumination that a bee would experience if it were to fly initially in a direction directly away from the sun, as shown in (b), or directly towards it, and subsequently in a direction such that the sun is 90° to the right, as shown in (b), or 90° to the left. In (c), the thin lines (blue in the online version) depict the dance orientation histogram. The thick continuous lines (red in the online version) show the four modal dance directions, computed as described in §2. The thick broken lines (green in the online version) show, for comparison, the four principal diagonal directions: 45°, 135°, 225° and 315°. (Online version in colour.)

Figure 7.

(a–d) Four examples of dances of an individual bee (bee no. 11) recorded in Experiment 4. Each panel shows waggle axis orientations recorded sequentially in a single dance. (Online version in colour.)

Figure 8.

Measurements of mean waggle durations in the dances of bees returning from a 12 m tunnel that was illuminated with axially polarized light (a), transversely polarized light (b), or transversely polarized light for the first 6 m and axially polarized light for the next 6 m, simulating flight through an L-shaped tunnel (c). The waggle durations measured under these three conditions are shown in (d) (mean ± s.e.). The upper dashed line represents the average of the mean waggle durations recorded in conditions (a,b), and the lower dashed line indicates (1/√2) times this value. (Online version in colour.)