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While conducting research on common murres on Skomer Island off the tip of South Wales, I constructed hides at various colonies to be able to watch the birds’ behavior at close range. One of my favorite hides was on the north side of the island, where, after an uncomfortable hands-and-knees crawl, I could sit within a few meters of a group of murres. There were about 20 pairs breeding on this particular cliff edge, some of them facing out to sea as they incubated their single egg. Being so close to the birds, I had the sense of being almost part of the colony and had become familiar with all their displays and calls.

On one occasion a murre that was incubating suddenly stood up and started to give the greeting call—even though its partner was absent. I was puzzled by this behavior, which seemed to be occurring completely out of context. I looked out to sea and visible, as little more than a dark blob, was a murre flying toward the colony. As I watched, the bird on the cliff continued to call and then, to my utter amazement, with a whirr of stalling wings, the incoming bird alighted beside it. The pair proceeded to greet each other with evident enthusiasm. I could hardly believe that the incubating bird had apparently seen—and recognized—its partner several hundred meters away out at sea.

Of all the avian senses, vision—and color vision in particular—is the area where the most spectacular discoveries have been made, mainly because this is where researchers have focused the most effort.

Compared with mammals, birds have relatively large eyes. In simple terms, a bigger eye means better vision, and excellent vision is essential for avoiding collisions in flight or for capturing fast-moving or camouflaged prey. Birds’ eyes, however, are deceptive—they are bigger than they look. As William Harvey (famous for discovering the circulation of blood) said in the mid-1600s, birds’ eyes “outwardly appear small, because excepting the pupils they are wholly covered with skin and feathers.”

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 screen 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 amphibians that live in the perpetual darkness of caves, seems to have virtually given up vision in favor 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. 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 scrutinizing something. 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 (used to grind up food), located near the center of gravity in the abdomen.

Birds are among the most colorful of animals, which is, of course, one reason we find them so appealing. One of the most brilliantly colored of South American birds 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 and other South American countries. The males display in groups, referred to as “leks,” deep in the cloudforest.

I was once watching some male cocks-of-the-rock from a viewing platform, and the birds were surprisingly difficult to see. The vegetation was dense, and although the males were actively chasing one another from tree to tree, they came into view only occasionally. 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 amid a mass of green foliage.

The most memorable thing about my brief encounter was that despite the birds’ brilliant color, as soon as they moved out of the sun they became almost invisible. It was like watching an actor step out of a spotlight into the darkness and disappear. This effect is no accident. Evolution has designed these birds so that when they’re 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.

Several other lekking bird species choose their display sites with great care. The satin bowerbird of Australia selects sunny spots, but some birds-of-paradise in New Guinea and manakins in South America actually create their own sunny spot on the forest floor by pruning adjacent trees. It was once thought that this “gardening” was to minimize the risk of predation, but as our understanding of avian vision improved, it became clear that the birds were manipulating the background color to maximize the visual contrast of their plumage and the overall effectiveness of their sexual displays.

I was thrilled by the sight of male cocks-of-the-rock and their brilliant color in the sun, but I wondered whether a female would see them as I did. In fact, females see them even more brilliantly.

Humans have three types of photoreceptors, or cones, in the retina, defined by the color of the light they absorb: red, green, and blue. These are directly equivalent to the three color “channels” on a television or video camera, which in combination produce what we consider to be the full spectrum of color. Compared with many mammals, humans and primates have relatively good color vision, because most others—including dogs—have only two cone types, which must be like having only two color channels on a television. However good we (arrogantly) think our color 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 cones, they have more of them. What’s more, birds’ cone cells contain a colored oil droplet, which may allow them to distinguish even more colors.

It is now known that many birds, probably most, have some degree of UV vision, which they use to find both food and partners. The berries that some 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 reflects UV light, often more markedly in males than females. In certain species, like the blue grosbeak, the degree of UV reflectance may also reflect male quality, though females don’t currently use this aspect of plumage to discriminate between potential partners.

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.

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 toward females seen with their left eye than with their right. 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. New Caledonian crows, famous for their construction of tools—fashioning hooks from palm-like leaves—show a strong individual bias toward 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 toward left or right in the population as a whole.

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 (at both the individual and species level), the more proficient those individuals are at particular tasks. It has long been known that parrots consistently prefer to use one foot to grasp food or other objects. The more biased parrots are toward using one particular foot (and it doesn’t matter whether it is the left or the right), the better they are at solving tricky problems—like how to obtain 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.

Sleeping with one eye open is something we now know birds share with some marine mammals (which need to return to the surface to breathe), but certainly not with us. 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. A complete survey has yet to be undertaken.

A bird sleeping with its right eye open is resting the right hemisphere of its brain, 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 an eye open. A study of mallard ducks showed that individuals sleeping in the center of a group spent much less time with an eye open than those on the edge, and that ducks on the edge of the group were more likely to open the eye facing outward from the group in the direction from which a predator might approach.

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 they might sleep and fly simultaneously once seemed ludicrous. But ornithologist David Lack and others noticed European 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 World War I reported that as he glided down across enemy lines with his engine off, at an altitude of around 10,000 feet, “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, at least one was caught and identified as a swift. 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.

Examining vision alone makes sense for convenience and clarity, but in reality, of course, birds use their senses in combination. Understanding how they work together increases our understanding of the way birds perceive the world. Take how migrating birds find their way. Biologists have long known that they use the sun and stars to navigate. More recently they have discovered that birds possess an internal magnetic compass.

It’s possible that a chemical mechanism based in the eye provides the compass, allowing them to “see” the earth’s magnetic fields, while magnetite (a magnetic mineral) receptors in the beak provide the map. The compass may detect the direction of the magnetic field, while the map detects the strength of the magnetic field, and by integrating both types of information the birds can find their way home, whether across a featureless ocean or a large land mass. At the present time we have a good basic understanding of at least some of the senses of birds, but the best is yet to come.

This story originally ran in the May-June issue as "Bird's-Eye View."