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Authors: Tim Birkhead

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Most owls are nocturnal. Good night vision is therefore essential, mainly for negotiating obstacles rather than locating prey, since owls hunt mainly using their ears. The key issue for nocturnal owls is the sensitivity of their eyes. To establish the minimum amount of light they can detect, Graham Martin conducted some behavioural tests with tame tawny owls – one of only a handful of species for which such information currently exists. Over several months, the owls were trained to peck at a bar positioned in front of two screens through which lights of different intensity were projected. The birds were rewarded with a bit of food if they detected the light. Martin used exactly the same procedure (but without the food reward) with human subjects so that he could make a direct comparison. As we might expect, the owls were more sensitive than the human subjects and on average could detect much lower light levels than most humans, although a few human subjects were more sensitive than the owls.
34

The eyes of a tawny owl are enormous compared with those of most other birds, and in terms of their focal length they are remarkably similar to the human eye (they both have a diameter of about
17
mm). However, because the owl’s pupil is larger (
13
mm in diameter) than a human’s (
8
mm), it lets in more light, and the image on the owl’s retina is more than twice as bright as it is in humans – accounting for the difference in visual sensitivity. Tawny owls are woodland birds and Martin checked whether there were ever conditions when there would be insufficient light for them to operate efficiently. He found, not surprisingly, that under most circumstances there was sufficient light and only when the owls were under a dense tree canopy on a moonless night would they struggle to see clearly.

Comparisons with a bird that is strictly diurnal, the pigeon, for example, shows that the tawny owl’s sensitivity to light is about a hundred times that of the pigeon. That is, owls see much better in poor light than pigeons, and this explains how owls function so well at night. In full daylight, both the pigeon and tawny owl have similar levels of visual acuity, confirming that, contrary to what some people believe, tawny owls are at no disadvantage in daylight. Because the owl’s eyes are designed for maximum sensitivity rather than resolution they can see quite well at low light levels, but not very crisply. By comparison, the spatial resolution – the ability to discriminate fine detail – of diurnal raptors such as the American kestrel and the Australian brown falcon, is five times greater than that of the tawny owl.
35

 

 

The fact that birds use their right and left eyes for different tasks is one of the most extraordinary ornithological discoveries of recent times. As in humans, a bird’s brain is divided into two hemispheres, right and left. Because of the way the nerves are arranged, the left half of the brain processes information from the right side of the body, and vice versa. That different sides of the brain deal with different types of information was first recognised in the
1860
s by the French physician Pierre Broca, after examining a man with a speech defect and whose subsequent autopsy revealed that the left hemisphere of his brain was severely damaged – as a result of syphilis. A gradual accumulation of similar cases confirmed that the left and right hemispheres of the brain do indeed process different kinds of information. The effect is called ‘lateralisation’ – meaning ‘sidedness’ – and for a century or so was thought to be unique to humans. But in the early
1970
s, during a study of how canaries acquire their song, it was discovered that birds, too, have a ‘lateralised brain’. In canaries and other birds, their song emanates from the syrinx, a structure similar to our voice box. Fernando Nottebohm found that the nerves on the left side of the canary’s syrinx (and hence the right side of the brain) had no role in song production, whereas those of the right did – providing an important clue that song acquisition in birds, like human language, was more dependent on one side of the brain than the other. Subsequent research confirmed that this was exactly the case.
36

More than that, birds have continued to play a central role in understanding brain lateralisation and it is now recognised that sidedness in brain function enhances the processing of information, effectively allowing individuals to use several sources of information simultaneously.

Sidedness can be apparent into two different ways. First, in terms of the
individual
: humans, parrots and some other animals can exhibit sidedness, being either left- or right-handed or -footed (parrots). Second, entire
species
can exhibit sidedness, as in domestic fowl, which, as we’ll see, typically use their left eye to scan for aerial predators.
37

Humans are, of course, typically right- or left-handed; we also tend to have a dominant eye – in about
75
per cent of people it is the right eye – although we are not usually aware of using our eyes differentially. Yet in those birds whose eyes are placed ‘laterally’, that is, on the side of the head, the two eyes are used for different tasks. Day-old chicks of the domestic fowl, for example, tend to use their right eye for close-up activities like feeding and the left eye for more distant activities such as scanning for predators. What’s more, an ingenious behavioural test, in which one eye is temporarily covered with a patch, reveals that birds perform certain tasks much better with one eye than the other, including tits and European jays remembering where they’ve hidden food.
38

We even know how this differential use of each eye arises in birds. The leading researcher on lateralisation in birds, Australian Lesley Rogers, had often wondered how the phenomenon arose. Lesley told me this:

All of my colleagues assumed it was determined genetically but I was not
so sure. Then, one day [in
1980
] I was looking at photos of the chick embryo and noticed that, during the final days of incubation, the embryo turns its head to its left side so that it occludes [covers] its left eye but not its right eye. That gave me the idea that light reaching the right eye via the shell and membranes might establish visual lateralization. Therefore, I compared eggs incubated in darkness with those exposed to light for the last few days of incubation and showed that my idea was correct. Later I showed that you can even reverse the direction of lateralization by removing the late-stage embryo’s head from the egg and occluding the right eye while exposing the left to light
.
39

It is remarkable that the difference in the amount of light each eye receives during normal embryonic development (left: rather little; right: much more) determines the subsequent role of each eye. The chicks hatching from eggs that have been experimentally allowed to develop in complete darkness (so that there is no right-left bias in the amount of light each eye receives) show no such difference in eye use once they hatch. What’s more, those chicks were less competent at performing two tasks simultaneously (detecting predators and finding food) than chicks hatching from eggs incubated normally.
40

This remarkable discovery has enormous and as yet unexplored implications. Imagine a hole-nesting species which sometimes nests in deep, totally dark cavities, but occasionally nests in a shallow, light-filled cavity. In the first case there would be no opportunity for lateralisation, whereas in the second there would, and as a consequence the offspring would be of better ‘quality’ – because they would be more competent. If this is true, then differences in the environment in which they were raised could explain a lot about individual differences in behaviour and personality in birds. We might almost expect individuals to advertise – through display – how lateralised they are, since highly lateralised, more competent individuals will inevitably make better partners. A wonderful project for a budding ornithologist!

This bias in the role of each eye is difficult for us to imagine, but it may occur in all birds, albeit in different ways. Domestic fowl chicks, for example, use their left eye to approach their parent. Male black-winged stilts are more likely to direct courtship displays towards females seen with their left eye than with their right. The wrybill, a New Zealand plover, is unique among birds in having its bill curved laterally to the right, which it uses to flip over stones as it searches for invertebrates – either because the right eye is better for close-range foraging or because the left is better for spotting potential predators, or both. When peregrine falcons are hunting they home in on their prey in a wide arc, rather than in a straight line, and mainly use their right eye.
41
New Caledonian crows, famous for their construction of tools – making hooks from palm leaves – show a strong individual bias towards making tools from either the right or left side of leaves. Similarly, when actually using these tools to hook prey out of crevices they show an individual preference for their left or right side, but no bias exists towards left or right in the population as a whole.
42

Given how widespread sidedness is, it is natural to assume that it has a function. And indeed it has. Intriguingly, the more biased the sidedness is (at both individual and species level), the more proficient those individuals are at particular tasks. It has been known for centuries that parrots consistently prefer to use one foot to grasp food or other objects. The more biased parrots are towards using one particular foot (and it doesn’t matter whether this is the left or the right) the better they are at solving tricky problems – like how to pull up a food reward dangling from the end of a string. The same thing is true of fowl chicks – those with strong sidedness are much better at foraging (discriminating between food grains and gravel)
and
keeping an eye open for predators in the sky.
43

We’ll end this chapter by looking at how and why some birds are apparently able to sleep while still looking at the world through one eye. This ability was recognised as long ago as the fourteenth century when Geoffrey Chaucer in
The
Canterbury Tales
(
1386
) wrote: ‘. . . smale fowles . . . slepen [sleep] at the night with open ye . . .’ Sleeping with one eye open is something we now know birds share with marine mammals (which need to return to the surface to breathe), but certainly not with us.
44
It is not even true of all birds, and so far it is known that songbirds, ducks, falcons and gulls can sleep with one eye open, but a complete survey has yet to be undertaken. One-eyed-sleep is easiest to see in ducks roosting during the day beside urban ponds: with its head turned back towards the wing (often incorrectly described as ‘with its head under its wing’), the bird has one eye facing inwards towards its back and concealed, the other eye looking outwards and opening from time to time.

As you will probably have guessed, a bird sleeping with its right eye open is resting the right hemisphere of its brain (since information from the right eye is processed in the left hemisphere and vice versa), and there are two circumstances in which the ability to sleep with an eye open is incredibly useful. The first is when there is a predator about. Ducks, chickens and gulls often sleep on the ground and are vulnerable to predators like foxes, so it pays to keep one eye open. A study of mallard ducks showed that individuals sleeping in the centre of a group (where it is relatively safe) spent much less time with an eye open than those on the edge (where they are more vulnerable to predators), and that ducks on the edge of the group were more likely to open the eye facing outwards from the group in the direction from which a predator might approach.
45

The second circumstance in which it is extremely useful for birds to keep an eye open is when they sleep on the wing – that is, while flying. The idea that birds might sleep and fly simultaneously once seemed ludicrous, but was considered more than just a possibility by the ornithologist David Lack when he was studying European swifts. He and others noticed swifts ascending into the sky at dusk and not returning until the following morning, and inferred that they must sleep on the wing. More convincingly, a French airman on a special nocturnal operation during the First World War reported that, as he glided down across enemy lines with his engine off, at an altitude of around
10
,
000
ft: ‘We suddenly found ourselves among a strange flight of birds which seemed to be motionless . . . they were widely scattered and only a few yards below the aircraft showing up against a white sea of cloud underneath.’ Remarkably, two birds were caught and identified as swifts. Of course, neither Lack nor the French airman noticed whether their sleeping swifts had one eye open, but it is a possibility. Glaucous-winged gulls in North America, however, have been seen flying to their roosts with only one eye open, suggesting that they are already sleeping before even reaching the roost.
46

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