Authors: Tim Birkhead
The size and basic design of birds’ eyes can tell us only so much, but the microscopic structure of the retina is more revealing. The wonderful visual acuity of raptors is largely the result of a high density of light-sensitive cells in the retina. The light-sensitive cells, or photoreceptors, come in two main types: rods and cones. Rods can be thought of as working like old-fashioned high-speed black and white film – capable of detecting low levels of light. Cones, on the other hand, are like low-speed (ISO) colour film (or a low ISO setting on a digital camera) – high-definition and performing best in bright light.
Our own single fovea is defined by a slight depression in the retina where the density of cone photoreceptors is very high, and where each photoreceptor has its own nerve cell sending information to the brain. Elsewhere in the eye each photoreceptor cell (i.e. both rods and cones) shares nerve cells, rather like lots of people having their computers connected to the internet via a single telephone line – frustratingly slow. The one-to-one relationship between photoreceptor and nerve cells in the fovea means that each cone sends an independent message to the brain, providing a signal whose origin is more accurately located, and explains why the fovea is the region of maximum resolution and colour imaging.
What a bird sees is dictated by the gross structure and size of the eye, the density and distribution of photoreceptors in the retina, and the way the brain processes the information transmitted through the optic nerve. Although all three aspects are correlated, any one of them on its own provides only a poor indication of a bird’s visual sensitivity, or how much detail a bird can see.
The raptor eye has excellent visual
acuity
– the ability to see fine detail. The owl eye, on the other hand, has excellent
sensitivity
– the ability to see at low light levels. No eye can do both, for the same reason that a camera cannot simultaneously have a wide aperture and a great depth of field. It is simply a law of physics. As vision biologists Graham Martin and Dan Orsorio say: ‘There’s always a trade-off between these two fundamental visual capacities [sensitivity and acuity]: if there are few quanta in the image [little visual information because the light is poor] the resolution cannot be high, and if the eye is designed to achieve high spatial resolution, it cannot do it at low light levels.’
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Visual acuity depends on the basic design of the eye, including its size (because this dictates the size of image projected on to the retina), and the design of the retina itself. The situation is analogous to a camera: the quality of lens determines the quality of the image, and the speed (grain) of the film (or the ISO setting on a digital camera) determines the accuracy with which the image is reproduced. Raptor retinas have a preponderance of cones, especially in each fovea, where the density is about one million cones per square millimetre (compared with some
200
,
000
in humans). As a result, a raptor’s visual acuity is slightly more than twice as good as our own.
Birds are among the most colourful of animals, which is, of course, one reason we find them so appealing. One of the most brilliantly coloured of South American birds (and there are many) is the Andean cock-of-the-rock. The male has the most intensely red body, a jet-black tail and outermost wing feathers, and unexpectedly silvery-white innermost wing feathers. So-named because it nests among rocks on cliff ledges, and because of its cocky Mohican-like crest, this pigeon-sized bird is a major draw to birdwatchers visiting Ecuador. The males display in groups, referred to as ‘leks’, deep in the rainforest, and it was with a group of some fifteen or so other birders that we made our way down a steep, slippery track towards a display area. Long before we saw them, the birds announced their presence with distinctive screeches, which the local Quechua people render as
youii
.
From the viewing platform on the valley side, the birds were surprisingly difficult to see. The vegetation was dense, and although the males were actively chasing each other from tree to tree, they came into view only occasionally and rarely remained long enough in one place to register a satisfying image on my retina. I kept willing them to perch in the sun so that I could see them properly. Eventually when one did, it was stunning and put me in mind of a fleck of glowing volcanic lava amidst a mass of green foliage.
The most memorable thing about my brief encounter with the cock-of-the-rock was that, despite the birds’ brilliant colour, as soon as they moved out of the sun they became almost invisible. It was like watching an actor step from out of a spotlight into the darkness, and disappear. This effect is no accident. Males choose sunny display sites to maximise the wonderful effect of their plumage. Evolution has designed these birds such that when illuminated by the sun they appear utterly brilliant, but in the shade, with the light filtered through green forest vegetation, their plumage has an almost drab quality, rendering the bird surprisingly well camouflaged.
As I watched the males flitting from perch to perch in the dense foliage, I wondered how the ornithological pioneers ever worked out what was going on at the cock-of-the-rock lek: I didn’t see a female, and consequently never saw the males in full courtship mode. Local people had obviously known about the birds and their leks for millennia, and used the males’ scarlet feathers in their headdresses.
The first description of a cock-of-the-rock lek came from Robert Schomburgk, a geographer charged by Queen Victoria with the daunting task of mapping British Guiana (now Guyana). On
8
February
1839
, during a tough day of climbing as he crossed the mountains between the Orinoco and the Amazon, Schomburgk and his colleagues watched a group of ten males and two females: ‘The space was four or five feet in diameter, and appeared to have been cleared of every blade of grass and smoothed as though by human hands. A male was capering to the apparent delight of the others.’ In
1841
Schomburgk’s brother, Richard, a botanist and ornithologist, went back and confirmed Robert’s extraordinary observations. On hearing the cries of the cock-of-the-rock, ‘My companions immediately sneaked with their weapons in its direction, when soon after one of them returned and told me to follow him carefully and lightly. We might have crept some thousand paces through the bush on our hands and knees when . . . on crouching down quietly besides the Indians, I witnessed the most interesting sight.’ A lek in all its glory, with birds ‘uttering the most peculiar notes . . . one of the males was cutting capers [dancing] on the smooth boulder; in proud consciousness of self it cocked and dropped its widespread tail and flapped its likewise expanded wings . . . until it seemed exhausted, when it flew back on the bush’.
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Like several other lekking bird species, male cock-of-the-rock choose their display sites with great care. The satin bowerbird of Australia selects sun spots, but some birds of paradise in New Guinea and manakins in South America actually create their own sun spot on the forest floor by pruning adjacent trees. It was once thought that this ‘gardening’ was to minimise the risk of predation, but as our understanding of avian vision improved, it became clear that the birds were manipulating the background colour to maximise the visual contrast of their plumage and the overall effectiveness of their sexual displays.
I was thrilled by the sight of male cock-of-the-rock and their brilliant colour in the sun, but I wondered whether a female would see them as I did. In fact, as we’ll see, females see them even more brilliantly.
As Darwin recognised, the bright colours of male birds, like those of the cock-of-the-rock, were unlikely to have evolved because they enhanced survival. Instead, such traits must have evolved because they increased reproductive success. Darwin imagined this happening in one of two ways: either males competing among themselves for females, or females preferentially mating with the most attractive males. It was an ingenious idea and neatly accounts for what are often dramatic differences in appearance and behaviour of the two sexes. Darwin called it sexual selection, to distinguish it from natural selection, recognising that even if bright plumage or loud songs rendered males more vulnerable to predators, if they were attractive enough to females and left enough descendants, they would still be favoured by selection. There were problems, though, especially with the second process, of female choice. Darwin’s contemporaries simply couldn’t imagine that females (human or non-human) were smart enough to make such informed choices. But by imagining that such choice required consciousness, they missed the point. A more serious problem was one raised by Alfred Russel Wallace, who pointed out to Darwin that he had not said
how
females benefitted from mating with particularly attractive males. Indeed, Darwin did not know.
These two objections effectively killed off the study of sexual selection, and in the several decades following Darwin’s death few researchers bothered to pursue it. Remarkably, it was not until a major shift in evolutionary thinking in the
1970
s that female choice became scientifically respectable again. The turning point was the recognition that selection operated on individuals rather than groups or entire species, and that as a consequence females could benefit in several different ways by choosing to mate with particular males. In the case of species like the cock-of-the-rock, where males make no material contribution to offspring other than through their sperm, the most likely benefits females obtain from choosing particular males is the acquisition of better genes for their offspring.
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To understand
how
females choose between different males, researchers in the last decade or so have started to consider the avian sensory system. In the case of the cock-of-the-rock one would need to see the world – or to see males at least – through a female’s eyes. While we cannot do this literally, we now know enough about how birds’ eyes work to be able to make a well-informed guess, simply (well, not so simply, actually) by looking at the microscopic structure of their eyes. The reason why this has been such a major step forward is that we now know that colour is a property of both an object, such as a bird or a feather, and of the perceiver’s nervous system that analyses its image thrown upon the retina. Beauty is, indeed, partly in the eye of the beholder: in fact, in the
brain
of the beholder, for that’s where images are processed. Without knowing about the nervous system we cannot really grasp how birds might ‘see’ each other, or, indeed, how they see the environment in which they live. It has taken a surprisingly long time to realise this, and as Innes Cuthill at the University of Bristol, in the UK, has said, while we readily accept that a dog has a much better sense of smell than we do, we have been incredibly reluctant to accept that birds, or any animals,
see
the world differently from ourselves.
Let’s consider the photoreceptors (cones) in the retina responsible for colour. Humans have three types, defined by the colour of the light they absorb: red, green and blue. These are directly equivalent to the three colour ‘channels’ on a television or video camera, which in combination produce what we consider to be the full spectrum of colour. Compared with most mammals, humans and primates have relatively good colour vision, because most others – including dogs – have only two cone types, which must be like having only two (instead of three) colour channels on a television. However good we (arrogantly) think our colour vision is, compared with that of birds it is rather poor because they have four single-cone types: red, green, blue and ultraviolet (UV). Not only do birds have more types of cone than ourselves, they have more of them. What’s more, birds’ cone cells contain a coloured oil droplet, which may allow them to distinguish even more colours.
The UV cone type in birds was discovered only in the
1970
s. Prior to that, UV vision had been known in insects since the
1880
s when Darwin’s neighbour John Lubbock noticed it in ants. Just a few decades later biologists discovered that honeybees use UV vision to discriminate between flowers. In the mid-twentieth century UV vision was assumed to be limited to insects, providing them with a private communication channel invisible to predators like birds.
This was wrong, and a study of pigeons in the
1970
s showed that they were sensitive to UV light. It is now known that many birds, probably most,
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have some degree of UV vision that they use to find both food and partners. The berries that some birds feed on have a UV bloom; and European kestrels can track their vole prey from the UV reflecting off the voles’ urine trails. The plumage (or parts of it) in hummingbirds, European starlings, American goldfinches and blue grosbeaks reflect UV light and often more markedly in males than females. In some species, like the blue grosbeak, the degree of UV reflectance also reflects male quality, so it is little wonder that females use this aspect of plumage to discriminate between potential partners.
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