Birds flying through a cluttered environment require the ability to choose routes that will take them through the environment safely and quickly. We have investigated some of the strategies by which they achieve this. We trained budgerigars to fly through a tunnel in which they encountered a barrier that offered two passages, positioned side by side, at the halfway point. When one of the passages was substantially wider than the other, the birds tended to fly through the wider passage to continue their transit to the end of the tunnel, regardless of whether this passage was on the right or the left. Evidently, the birds were selecting the safest and quickest route. However, when the two passages were of equal or nearly equal width, some individuals consistently preferred the left-hand passage, while others consistently preferred the passage on the right. Thus, the birds displayed idiosyncratic biases when choosing between alternative routes. Surprisingly - and unlike most of the instances in which behavioral lateralization has previously been discovered - the bias was found to vary from individual to individual, in its direction as well as its magnitude. This is very different from handedness in humans, where the majority of humans are right-handed, giving rise to a so-called ‘population’ bias. Our experimental results and mathematical model of this behavior suggest that individually varying lateralization, working in concert with a tendency to choose the wider aperture, can expedite the passage of a flock of birds through a cluttered environment.

Birds display a clear mastery of the skill of flying rapidly and safely through complex and cluttered environments. An example of this can be viewed at http://www.youtube.com/watch?v=p-_RHRAzUHM , which shows a bird flying at high speed through a dense forest. Such mastery requires the ability to determine, from moment to moment, which of several possible routes would provide the safest and quickest passage. Our study is one of the first to investigate how birds achieve this. Our experiments reveal that, when flying budgerigars are required to choose between two passages, they tend to favor the wider passage. However, this tendency is superimposed upon a bias that, surprisingly, varies from bird to bird: some individuals show an intrinsic preference for the left-hand passage, and others for the passage on the right. This is very different from handedness in humans, where the majority of humans are right-handed. We develop a mathematical model of the interaction between the birds' individual biases with their tendency to prefer the wider passage. The model reveals that this interplay is actually beneficial – it can expedite the passage of a flock of birds through a complex environment.

Funding: This research was supported by an ARC Centre of Excellence in Vision Science (Grant CE0561903), ARC Discovery Grant DP 110103277, and by a Queensland Smart State Premier's Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Copyright: © 2014 Bhagavatula et al. 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 author and source are credited.

What strategies do birds adopt to fly efficiently through complex environments? Here we investigate the behavior of budgerigars when they are offered a choice between two passages, presented side by side, through which they can fly. The relative widths of the passages are varied to investigate the rules that govern the birds' choices, and to examine whether these rules can facilitate rapid flight of a flock of birds through dense environments.

A bird flying through a complex and cluttered environment relies heavily on the use of visual cues to rapidly choose between alternative routes and avoid collisions with intervening obstacles. Goshawks, for example, display an impressive ability to fly through dense environments at high speeds [1] . Neural correlates of obstacle detection have been investigated in pigeons, where it was shown that neurons in the nucleus rotundus of the brain respond to a visual stimulus that depicts a moving object on a collision course [2] . While such neurons probably constitute part of an “early warning” system, it remains to be seen how the responses of such neurons contribute to the planning of an efficient and safe flight trajectory.

Results

We flew birds individually in a tunnel that presented a barrier with two apertures, positioned side by side halfway along its length, as illustrated in Fig. 1. The frequency with which the birds chose one aperture or the other was recorded, as the relative sizes of the two apertures were varied.

Some of the flights were filmed and reconstructed in 3D using high-speed stereo cameras, as described in “Methods”. Three examples of such flights, as viewed from above, are shown in Fig. 2. In Fig. 2A a bird selects the left-hand aperture (of width 60 mm) over the right-hand aperture (of width 40 mm). In Fig. 2B a bird initially flies toward the right-hand aperture (of width 10 mm), but possibly finds it too narrow and then chooses the left-hand aperture (of width 90 mm). In Fig. 2C a bird chooses the aperture on the right (of width 10 mm) because the left-hand aperture has zero width (i.e. is non-existent). [Birds can, and do occasionally choose to fly through very narrow apertures because the flanking panels, made of cloth, are compliant. The wings are then folded back to allow the bird to ‘projectile’ through the slit (unpublished observations)].

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larger image TIFF original image Download: Figure 2. Examples of birds choosing between two apertures. The red arrow denotes the direction of bird flight. The widths of the left- and right-hand apertures are respectively 60 mm and 40 mm in (A), 90 mm and 10 mm in (B), and 0 mm and 100 mm in (C). https://doi.org/10.1371/journal.pcbi.1003473.g002

A preliminary analysis of the birds' choices revealed the following general characteristics. When the apertures were very different in width, the birds tended to prefer the wider aperture, regardless of whether it was on the right side or the left. The birds appeared to be selecting the safest and quickest route. However, when the apertures were of equal (or nearly equal) width, some individuals consistently preferred the left-hand aperture, while others consistently preferred the right. Left-biased birds preferred the left-hand aperture, while right-biased birds preferred the aperture on the right. Thus – as we shall demonstrate in greater detail below – each bird had its own, characteristic, side bias.

What are the factors that govern the choice of aperture? We examined this question in greater detail by investigating how the bird's choices changed as the relative sizes of the two apertures were varied systematically. This was done by varying the position of the central panel that separated them, as described in the ‘Methods’ section. As the central panel was moved from its extreme left-hand position to its extreme right-hand position (in steps of 10 mm), the width of the left-hand aperture increased progressively from 0 mm to 100 mm, and the width of the right-hand aperture decreased progressively from 100 mm to 0 mm, as shown in Table 1.

Fig. 3A shows how the choice frequency for the left-hand aperture varied with its width, for one particular bird (bird One). When the two apertures were equally wide (or nearly so), the bird displayed a preference for the right-hand aperture, choosing it with a frequency of 74%. However, as the central panel was moved towards the right, making the right-hand aperture narrower than the left-hand one, the bird exhibited an increased preference for the left-hand aperture, eventually choosing it with 100% probability for left-hand aperture widths of 70 mm or greater. Conversely, when the central panel was shifted progressively towards the left, the bird showed a decreasing preference for the left-hand aperture, eventually not choosing it at all when it was 20 mm or narrower. Overall, the data suggest that bird One has a weak preference for the right-hand aperture, and that this bias is superimposed upon the bird's tendency to choose the larger of the two apertures (but see below).

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larger image TIFF original image Download: Figure 3. (A–E) Aperture choice profiles for birds One, Casper, Two, Drongo and Saras, showing choice frequencies for the left-hand aperture as a function of its width. The dashed vertical line represents the condition when both apertures are of equal width (50 mm). The dashed horizontal line represents the random-choice level of 50%. The symbols next to each data point indicate a statistically significant difference of the choice frequency from the random-choice level of 50%, calculated as described in ‘Methods’. [p<0.05: (*); p<0.02: (**) and p<0.00001: (***)]. The red dashed curve in each panel displays a fit of the data to a logistic function, as described in the Supporting Information. (F) Average preference for the left-hand aperture as a function of its width, obtained by pooling the aperture choice profiles of all 5 birds (Fig. 3A–E). The fitted values of the parameters B and Δd of the logistic function are shown in each panel. The horizontal red error bar in each panel represents the 95% confidence interval for the estimated value of B. https://doi.org/10.1371/journal.pcbi.1003473.g003

The results of a similar experiment conducted with a different bird (Casper) are shown in Figure 3B. This bird was left-biased: when the apertures were of equal width, the bird showed a greater preference for the left-hand aperture, choosing it 87.5% of the time. This choice probability was significantly different from the random-choice level of 50% (p<0.02).

Figs. 3C–E show data from three additional birds: Two, Drongo and Saras. Bird Two possessed a preference for the right-hand aperture. This bird chose the left-hand aperture only 12.5% of the time when the two apertures were equally wide, and this preference was significantly lower than the random choice level of 50% (p<0.02). Drongo (Fig. 3D) was also right-biased, but less strongly so than Two. Saras (Fig. 3E) was strongly left-biased.

The capacity of the birds to discriminate differences in aperture width can be quantified by fitting the choice frequency data to a logistic function that describes the choice frequency F L for the left-hand aperture as (1)where d is the width of the left-hand aperture. B is a bias parameter that specifies the bias of the bird, as estimated from the fitted function. It is the width of the left-hand aperture at which this aperture is chosen 50% of the time, i.e. the bird chooses randomly between the left- and right-hand apertures. If B = 50 mm, the random choice occurs when the two apertures are equally wide, and the bird is unbiased. If B<50 mm, the bird is left-biased, and if B>50 mm the bird is right-biased. α is a parameter which defines the sharpness of the bird's transition between the left-hand aperture and the right-hand one. The larger the value of α, the steeper the transition, and the sharper the discrimination of aperture width. The parameters B and α, and their confidence intervals were determined by performing a least-squares fit of the logistic function to the data for each bird and for the pooled data from all birds, as described in “Methods”. The computed values of B, and their 95% confidence intervals (Table 2) indicate that bird One has no significant bias, that Casper and Saras are left-biased (B<50 mm), and that Two and Drongo are right-biased (B>50 mm).

Table 2 also shows the increase in the width (Δd, in mm) of the left-hand aperture that is required for the choice frequency for the left-hand aperture to increase from 25% to 75%. This is derived from the value of α, as described in “Methods”. The smaller the value of Δd, the sharper the discrimination of aperture width. On this measure, bird Two displayed the sharpest discrimination (Δd = 3.2 mm) and bird One displayed the least sensitive discrimination (Δd = 19.7 mm). The mean value of Δd, averaged over all birds, is 13.0 mm, which indicates that, on the whole, the birds display an impressively sharp ability to discriminate aperture width.

What would be the behavior of the population as a whole? We examined this question by averaging the data from all of the birds, point by point, for each aperture width. The results are shown in Fig. 3F, which represents the average of the results obtained for all five birds, graphed in Fig. 3A–E.

The averaged curve shows no significant bias (B = 49.8; Fig. 3F and Table 2). This is as one might expect, given that in the group of birds that we tested, one bird had no significant bias, three birds displayed a right bias, and two others a left bias. Furthermore, while the relative preferences for the two apertures change sharply as a function of their relative widths for each individual bird (mean Δd = 13.0 mm), the relative preferences of the population as a whole change more gradually and smoothly (Δd for pooled data = 23.2 mm). The reason for this is that the sharp transition displayed by each bird occurs at a different point along the horizontal axis, because of the different biases possessed by the individual birds. This smoothing effect may have interesting implications for the behavior of a flock of birds, as we shall see in the Discussion section.

Fig. 3F suggests that the population, when considered as a whole, does not possess any net bias. A larger sample of birds would need to be examined before this statement can be made with complete confidence. Nevertheless, the spread of left and right biases that we have observed in the five birds that we have investigated suggests that, if there is a net bias at the level of the population (towards the left or the right), it is likely to be small.