Authors: Tim Birkhead
The size of eyes is important precisely because the larger the eye, the larger the image on the retina. Imagine watching a
12
-inch television compared with a
36
-inch screen. Bigger eyes have more light receptors in the same way that larger TV screens have more pixels, and hence a better image.
Among diurnal birds, those that become active soon after dawn have larger eyes than those that become active later after sunrise. Shorebirds that forage at night have relatively large eyes, as do owls and other nocturnal species. The kiwi, however, is an exception among nocturnal birds, and, like those fish and amphibia that live in the perpetual darkness of caves, seems to have virtually given up vision in favour of its other senses.
The Australian wedge-tailed eagle has enormous eyes, both in absolute terms and compared with most other birds, and as a result has the greatest visual acuity of any known animal. Other birds might benefit from the eagle’s acute vision, but eyes are heavy, fluid-filled structures, and the larger they are the less compatible they are with flight. Flying birds are designed so that their weight is distributed in such a way that it does not interfere too much with flight. A heavy head is incompatible with flight and therefore sets an upper limit on eye size. Flight, and the need for large eyes, may also be responsible for the loss in birds of teeth, which have been replaced by a powerful muscular stomach, the gizzard (which birds use to grind up their food), located near the centre of gravity in the abdomen.
For early researchers, vision posed many puzzles. One was why we see only a single image, even though we have two eyes. After all, with either eye we see a perfectly good image, but with both eyes open we see just one image.
René Descartes identified another puzzle, noticing that on cutting a square hole in the back of a bull’s eye (that is, in the retina), and placing a piece of paper over the hole, the image projected on to the paper – through the eye – was upside down. Why, then, do we see images the right way up?
Writing about the eye in
1713
, William Derham presented this puzzle thus:
The glorious landskips [landscapes], and other objects that present themselves to the eye, are manifestly painted on the retina, and that not erect, but inverted as the laws of opticks require . . . But now the question is, how in this case the eye comes to see the objects erect?
He says that the Irish philosopher William Molyneux (
1656
–
98
) has the answer: ‘The eye is only the organ or instrument, ’tis the soul that sees by means of the eye.’
16
If we allow the ‘soul’ to be the brain, or acknowledge that the eye is merely an ‘instrument’, then Molyneux is correct. It is indeed the brain that sorts these things out, ‘seeing’ only a single ‘erect’ image. Amazingly, we train ourselves to ‘reverse’ the inverse image on our retinas. In a famous experiment conducted in
1961
, Dr Irwin Moon wore image-inverting spectacles that effectively turned the world upside down. At first he found it horribly disorientating, but after eight days of wearing the spectacles Dr Moon had adjusted and ‘saw’ the world the right way up again. To prove it, he drove his motorbike and took his plane for a spin – without mishap. Moon’s extreme experiment provided irrefutable evidence that we ‘see’ with our brain rather than with our eyes.
17
Although we tend to think of the brain as a discrete organ – a lump of squidgy tissue – it is better to think of it as part of an elaborate network of nervous tissue that reaches out to every single part of the body. Imagine the entire nervous system: the brain, the cranial nerves emanating from it, the spinal cord, with its pairs of nerves sprouting from each side, branching and branching again, becoming finer and ever finer – dendritic is the word – with the various sense organs at their tips. Information, gathered by the sense organs, the eyes, the ears, the tongue and so on, including light, sound waves and taste, is transformed into a common currency of electrical signals that travel along the neurons to the brain, where they are decoded.
How does a duck, whose eyes are located on the sides of its head, see the world: does it see one or two images? Does a tawny owl, whose two enormous eyes face forwards like our own, see a single image as we do? Graham Martin at the University of Birmingham, in the UK, has spent many years measuring the
3
-D visual fields of different bird species, and identified three broad categories of visual field.
Type
1
is what the typical bird, such as blackbirds, robins and warblers, sees: some forward view, excellent lateral vision, but (like us) no vision behind them. Surprisingly, the majority of birds in this group cannot see their own bill tip, but have just enough binocular vision to be able to feed their chicks and construct a nest.
Type
2
includes birds like ducks and the woodcock, whose eyes are high up on the sides of the head. They don’t have a great forward view and most don’t need to see their bill tip because they rely on other senses when feeding, but they do have panoramic vision, above and behind – helping them detect potential predators. Interestingly, the views from each eye barely overlap, so they probably see two separate images.
Type
3
birds are those such as owls with forward-facing eyes like ourselves, which have no vision behind. Because we rely so much on binocular vision for depth and distance perception, we automatically assume that all other organisms benefit in the same way. Our reliance on binocular vision may be one reason we have endowed owls with such symbolic significance, for they can look us in both eyes, with both of their eyes. But looks can be deceptive, and in fact owls’ eyes are much more angled with respect to each other than they appear, and their binocular overlap much smaller than our own. It has often been thought that the forward-facing eyes of owls is an adaptation to nocturnal living, but this isn’t so. Many owls are nocturnal, of course, but having a Type
3
visual field is not tightly associated with operating in the dark: oilbirds and nightjars are nocturnal, yet they have a Type
2
visual field. Martin has an interesting suggestion for why the eyes of owls face forwards. He thinks that it is associated with their need for very large eyes – associated with flying around in poor light – which, together with the need for very large external ear openings, means (as we’ll see in the next chapter) that the only possible place in the skull is in a forward-facing position. ‘Where else could they go?’ he asks. The lack of space for both eyes and ears (and brain) in the skull is illustrated by the fact that you can see the back of an owl’s eyes through its ear openings!
18
Readers of my generation educated in the UK in the
1960
s will remember having the basic structure of the human eye drummed into them at school from an early age: a ball-shaped organ roughly
2
.
5
cm in diameter; an opening (the iris) through which light enters; a lens that projects on to the retina, a light-sensitive screen at the back of the eye. Information from the retina is transmitted via a network of nerves through the optic nerve to the visual centres of the brain. We even dissected bulls’ eyes at what now seems like a very tender age: I was hooked!
When researchers first started to look into the eyes of birds and compare them with our own, they noticed a few striking differences. The first was that those of certain birds – like large owls – are more elongated than our own. The great nineteenth-century ornithologist Alfred Newton (
1829
–
1907
) described the eyeball of a bird as like ‘the tube of a short and thick opera glass’.
19
The second difference is that birds possess a translucent additional eyelid, whose existence was known for centuries by everyone who kept birds. Aristotle mentions it, as does Frederick II in his falconry manual: ‘for cleaning the eyeball there is provided a peculiar membrane that is quickly drawn across its anterior surface and rapidly withdrawn’.
20
The first formal description of this additional eyelid was – unexpectedly – of a cassowary, a gift to Louis XIV, that died in the Versailles menagerie in
1671
.
21
John Ray and Francis Willughby in their encyclopaedia of birds of
1678
say: ‘Most, if not all birds, have a membrane of nictation . . . where withal they can at their pleasure cover their eyes, though the eye-lids be open . . . and serves to wipe, cleanse, and perchance moisten . . .’ The term nictitating membrane comes from the Latin
nictare
, to blink. Our own nictitating membrane is a mere remnant – the tiny pink nub in the inner corner of our eye.
22
A bird’s nictitating membrane lies under its other eyelid and is most easily seen in photographs. If you have ever taken close-up pictures of birds at the zoo I bet you have images in which the bird’s eye seems to be milky or obscured in some way, even though it looked all right as the picture was being taken. Usually the milkiness is caused by the nictitating membrane moving rapidly across the eye, either horizontally or obliquely, in a movement almost too quick to be seen, but readily captured by the camera. As Frederick II recognised, the nictitating membrane’s function is to clean the eye, but it also protects it. Each time a pigeon puts its head down to peck at something on the ground, the nictitating membrane moves across each eye to protect it from spiky leaves and grasses. In raptors the membrane covers the eye immediately before the bird slams into its prey, and in exactly the same way the membrane covers the eye just before a plunging gannet hits the water.
The third difference between our eyes and those of birds is a structure called the pecten. So-named because of its resemblance to a comb (in Latin,
pecten
), the pecten seems to have been discovered in
1676
by Claude Perrault (
1613
–
88
), one of the great anatomists of the French Academy.
23
The pecten is a very dark structure with a pleated appearance, with the number of pleats varying between three and thirty in different species. At one point ornithologists hoped – as they had with so many other anatomical traits – that the pecten might provide vital information about the relationships between species. It didn’t. The pecten is, however, largest and most complex in those birds with the most acute vision, like raptors. Indeed, it was initially thought that the kiwi lacked a pecten altogether, but in the early
1900
s Casey Wood found that it possessed a small and very simple one.
24
At first sight the pecten looks as though it would impede rather than improve vision, sticking out like a large finger inside the rear chamber of the eyeball. Yet, on closer inspection, anatomists – including Casey Wood – realised that it is cunningly positioned so that its shadow falls on the optic nerve – or blind spot of the retina – and therefore does not interfere with vision. What is the pecten for, and why don’t we have one? The pecten in birds seems to be to provide the posterior chamber of the eye with oxygen and other nutrients. In contrast to humans and other mammals, there are no blood vessels in the avian retina, and the pecten, which is a mass of blood vessels, is little more than a clever oxygenation device – the pleating maximising its surface area and thereby facilitating the exchange of gases (oxygen in and carbon dioxide out) within the eye – effectively allowing it to breathe.
The human fovea – the crucial spot on the back of the eye where the image is sharpest – was discovered in
1791
. Over the following years foveas were found in a wide range of other animals, but it wasn’t until
1872
that they were discovered in birds.
25
Not long afterwards it was noticed that, while the majority of birds have a single circular fovea – as we do – some, like hummingbirds, kingfishers and swallows, as well as raptors and shrikes, have two. Remarkably, a few species, including the domestic fowl, have no fovea at all. Others have a linear fovea, and yet others have some combination of the two. Many seabirds, including the Manx shearwater, have a linear, horizontal fovea whose function may be to detect the horizon.
In birds like falcons, shrikes and kingfishers, the two foveas are referred respectively to as the shallow and deep fovea.
26
The shallow fovea is like that in birds with only a single fovea and provides monocular, and largely close-up, vision. The deep fovea, however, which is directed at about
45
o
to the side of the head, comprises a spherical depression in the retina that acts like a convex lens in a telephoto lens, effectively increasing the length of the eye and magnifying the image to provide very high resolution.
27
The position of the deep fovea in the eye also means that raptors have a degree of binocular vision, thought to be essential for judging the distance of fast-moving prey.
28
If you have observed captive birds of prey, you will see that they often move their head from side to side or up and down as they watch you approach. They do this because they are alternating your image on their two foveas, the shallow one for close up, the deep one for distance. Compared with our eyes, those of birds are relatively immobile in their sockets (space and weight are limited, and the reduction of muscles needed to move the eyes constitutes an important saving), so raptors and owls in particular have to move their head when they are scrutinising something.