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First published online October 21, 2005
Journal of Experimental Biology 208, 4123-4135 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01880

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Interactions of visual odometry and landmark guidance during food search in honeybees

Tony Vladusich^1,*, Jan M. Hemmi², Mandyam V. Srinivasan² and Jochen Zeil²

¹ Laboratory of Experimental Ophthalmology and NeuroImaging Centre, School of Behavioural and Cognitive Neurosciences, University Medical Centre Groningen, Groningen, The Netherlands
² Centre for Visual Science, Research School of Biological Sciences, Australian National University, Canberra, ACT 2600, Australia

View larger version (14K): [in a new window]   Fig. 1. Schematic illustration of the training and testing set-up. (A) Bees were trained to forage in a textured tunnel (the specific texture was varied throughout experiments) with a feeder at a designated location, and the landmark directly above. (B) In the test situation, bees entered the tunnel individually, and began searching for the removed feeder, repeatedly traversing the tunnel. The cross-section shows the trajectory over four -turns (note this is not a space-time diagram in the strict sense).

View larger version (30K): [in a new window]   Fig. 2. Results of Experiment 1. (A) Bees tested with no landmark conducted a broad search. (B) With the landmark at the training location, bees searched very accurately. (C) When the landmark was shifted to unit 14, bees searched either at the landmark or the training location. (D) Bees searched at the landmark when it was shifted to unit 4. Black bars, first -turns; grey bars, second -turns; coloured lines, search distributions; inverted triangles, training location; diamonds, landmark position; N=flight number. Note different y-axis scales in A,C and B,D.

View larger version (17K): [in a new window]   Fig. 3. Comparison between the `Landmark at unit 14' and `No landmark' conditions reveals the point at which bees were drawn towards the landmark (i.e. a beacon effect). (A) Reproduction of first -turn distributions. (B) Cumulative frequencies were tested statistically, and found to be different at unit 11 (see text), meaning that bees were drawn to the landmark from this point onwards.

View larger version (30K): [in a new window]   Fig. 4. Results of Experiment 2. Bees were trained and tested in an axially striped tunnel. (A) Bees tested without the landmark generally flew from one tunnel end to the other. (B-D) Bees tested with the landmark at the training site (B), shifted to unit 14 (C) and shifted to unit 4 (D), all made first turns near the landmark then tended to break visual contact on second turns (and often flew back to the entrance). For an explanation of figure layout and symbols, see Fig. 2.

View larger version (12K): [in a new window]   Fig. 5. Comparison of landmark fidelity, i.e. the tendency for bees to stay faithful to the landmark during search, with odometry (black line) and without odometry (grey line). Bees with odometry remained faithful on all four -turns, whereas bees without odometry progressively gave up searching at the landmark, in all conditions. (A) Landmark in place at the training site, (B) landmark shifted to unit 14, and (C) landmark shifted to unit 4. Numbers given indicate the number of bees considered when calculating the observed frequency.

View larger version (32K): [in a new window]   Fig. 6. Results of Experiment 3. Bees were trained without a landmark and tested with a landmark. (A) Bees tested without the landmark searched broadly in the tunnel. (B-D) Bees tested with the landmark (B) at the training site, (C) shifted to unit 14, and (D) shifted to unit 4, all tended to make first turns before reaching the landmark. This effect suggests that bees are repelled by the novel landmark placed along a familiar path. For an explanation of figure layout and symbols, see Fig. 2.

View larger version (22K): [in a new window]   Fig. 7. Assessment of the tendency for a novel landmark to repel bees. Ratios of bees turning just before the landmark to those turning at the landmark; black bars, familiar landmark; grey bars, novel landmark. The black line shows the ratios of bees turning before and after the landmark in Experiment 3 only. The conditions were `Landmark at unit 4', `Landmark at unit 9' and `Landmark at unit 14'.

View larger version (28K): [in a new window]   Fig. 8. Results of Experiment 4. Bees were trained at unit 21 with a landmark. (A) Bees tested without the landmark searched either near the training location or at the end of the tunnel. (B-D) Bees tested with the landmark (B) at the training site, (C) shifted to unit 30 and (D) shifted to unit 12, all tended to search at the landmark, or sometimes (as in C) before reaching the landmark. Note the different y-axis scales in A,C and B,D. For an explanation of figure layout and symbols, see Fig. 2.

View larger version (18K): [in a new window]   Fig. 9. Third and fourth -turns, plotted for two conditions of Experiment 4, show that bees that strayed away from the landmark often searched near the tunnel end. This occurred with the landmark (A) shifted to unit 12, and (B) in place at the training location.

View larger version (16K): [in a new window]   Fig. 10. Results of Experiment 5. Bees were trained at unit 21 with a landmark, and (A) tested without the landmark, or (B) with the landmark at the training site, searched in accord with odometry and landmark cues, respectively. (C) Bees trained without a landmark and tested without a landmark also showed no signs of the anomalous behaviour observed in Experiment 4. Note the different y-axis scales in A,C and B. For an explanation of figure layout and symbols, see Fig. 2.