The eyes have it

A Bateleur with large, forward-facing eyes denoting its hunting lifestyle

Most higher animals (vertebrates) and many invertebrates too, need some visual ability to survive, find food, defend themselves from predators, seek shelter and interact with mates. There are only a few ways that an eye can be designed, and since the vast majority of animal species have eyes, that tells us that having eyes is really, really important. In the Cambrian period, when sophisticated eyes started to develop, they developed very quickly, and it may well have been the arms race between predators and prey that led to the rapid evolution of eyes.

Eyes sense light using nerves, and these then convert the light into electro-chemical impulses. In higher species, the eye is a complex optical system that collects light from the outside world, focuses it to shape an image by means of an adjustable lens assembly, transforms this image into a series of electrical signals and transmits these signals to the brain via complex neural pathways that link the eye via the optic nerve to the visual cortex and other areas of the brain.

Eye shape, position and lifestyle

Most vertebrate groups exhibit eye shapes that vary predictably with activity pattern. Activity patterns, the times of the day when an animal is awake and active, determine the amount of light available for vision, and as such becomes a key selective influence on the evolution of the vertebrate visual system.

Theoretically, all vertebrates could benefit from having larger eyes regardless of their activity pattern. However, differences do exist, not necessarily in absolute eye size, but rather as differences in cornea size. So, nocturnal vertebrates typically have large corneas relative to eye size as an adaptation for increased visual sensitivity. Conversely, diurnal vertebrates generally demonstrate smaller corneas relative to eye size as an adaptation for increased visual acuity. A recent study has argued that new statistical methods allow eye shape to accurately predict activity patterns of mammals, including cathemeral species (animals that are equally likely to be awake and active at any time of day or night).

Another difference in eyes when relating structure to lifestyle is that there is a strong link between the shape of the pupil and ecological niche. An interesting observation while on a very recent trip which coincided with research for this article was the discovery that mongooses have different pupils from other carnivorous mammals.

A very obliging Slender Mongoose with a group of Dwarf Mongoose in the Kruger National Park allowed some close-up photography. While editing and reviewing the photos it was suddenly very obvious (I am a bit embarrassed to admit this as a trained biologist, but the fun of learning is that it is a life-long process) that the pupils of both these herpestids and others from the family (Family Herpestidae) are horizontal.

Interestingly, pupil shape and orientation are very closely linked to the ecological niche an animal occupies. Animals with vertically elongated pupils are very likely to be ambush predators which hide until they strike their prey from relatively close distance. And while domestic cats have vertical slits, the larger predators, like lions and leopards, have round pupils. They also tend to have eyes placed forwards or on the front of their heads.

Strong binocular vision in both these animals – Vervet monkeys with large forward facing eyes and a lioness with forward facing eyes and the round pupils characteristic of larger predators.

In contrast, horizontally elongated pupils are nearly always found in grazing animals, which have eyes on the sides of their head. These are usually prey animals. This makes sense, because it gives prey animals a panoramic view, so they can scan all directions for danger. However, these animals are constantly pitching their heads down to graze and this leads to a far more fascinating discovery. These animals exhibit cyclovergence – their eyes rotate significantly to keep their pupils horizontal to the ground whether their heads are up or down.

In summary, vertically elongated pupils help predators capture their prey and horizontally elongated pupils help prey animals avoid their predators. So what does this mean in the case of my observations of the mongooses in Kruger? The eyes of these animals serve two purposes – to be hunters that capture prey (in general vertical or round pupils) and forward-facing eyes (yes) and also to help these smaller mammals to avoid their potential predators (horizontal). Basically, it seems likely that the position of the forward-facing eyes assists with depth perception during hunting while the horizontal pupils help to create a more panoramic field of view to scan for predators.

Now to focus on the birds which was the original point of this article.

Bird vision

Birds generally have excellent vision, surpassing humans in many ways. Their eyes are often the largest structures in their heads. The Common Ostrich has the largest eye of any land animal, not in the relative sense but in the absolute sense. And the bigger your eyes, the better you can see. One reason is because a large eye can let in more light than a smaller eye. And a large eye can pack in more light-sensitive cells.

The Common Ostrich has the largest eye of any land animal, not in the relative sense but in the absolute sense.

Birds can see a wider range of wavelengths (including ultraviolet!), track fast motion better, and see as much as 360 degrees at once in peripheral vision with multiple focal points. Some have the ability to see clearly underwater, some see more detail, some have excellent night vision or colour vision. So visual ability varies greatly between species. Many see less detail but make up for it with a wider field of view and better motion tracking than humans. Eagles see about five times more detail than we do, and about sixteen times more colour.

White-fronted Bee-eater. Bird colouration speaks to their abilities to see colour.

One of the amazing things about bird retinas is that they have four different types of cone cells, instead of only three as in humans. Having four types of cones is actually a primitive characteristic, shared by amphibians as well as reptiles. That fourth cone is sensitive to ultraviolet wavelengths of light, which humans can’t see. This is called the tetrachromatic colour space. Thus, many birds can see ultraviolet and have unsurprisingly also evolved ultraviolet plumage markings. Many birds may even be more sensitive to ultraviolet list than they are to what we know as visible light. Human eyes are UV-blind and yellow biased so we things somewhat differently. During the past three decades, a flurry of studies has tested the intriguing notion that mate choice and other bird behaviours may be shaped by secret visual signals humans cannot see. So, what might the world look like to a bird with UV vision? Since birds can detect more colours than humans can, scenes may appear more varied. And colours that already are bright to human eyes are—if amplified by UV reflectance—probably even brighter to birds. For starters, colours in the ultraviolet range are reflected by many flowers, fruits, and berries. So, birds that rely on these plant products for food can be more efficient and more successful in their foraging. Preliminary research has suggested that, for at least some species, females may prefer males with feathers that shine brightly in the UV part of the spectrum. The plumage of a male in UV light might be a signal of his overall health or fitness—useful info to females looking for a mate. So as colourful as many birds seem to us, they probably look even more dazzling to each other. Interestingly, this means that some species which we see as not being sexually dimorphic (male and females look alike) have differences between males and females that we can’t see. What an amazing world we live in…

Birds’ colours are key to social signalling.

Birds with relatively large eyes tend to have better low-light vision, which also allows them to be more active earlier and later in the day. This is a clear feature in those owl species which rely principally on vision for hunting and socializing. They can find mice in light 10 to 100 times dimmer than that needed by the human eye. Colour vision is not helpful at night, so they see mainly in black and white. Owl retinas are packed almost exclusively with rod cells. Cone cells are adapted for colour vision whereas rod cells are best for black-and-white vision.

Owls have large forward facing eyes which enable good night vision and accurate distance and space recognition. Pearl-spotted Owl (top) and Greater Spotted-owl (below)

Visual field

The majority of birds have binocular vision, similar to humans, in order to judge distance precisely – an obvious requirement for an animal that is flying through its world. Binocular vision is where both eyes are able to focus on the same object, if only one eye can see an object it is known as monocular vision. Binocular vision enables the bird, and us, to determine the size of an object and its distance.

Binocular vision is particularly well developed in raptors (eagles, owls, hawks), which tend to have their eyes positioned towards the front of the head; an owl actually has completely forward-facing eyes. Further adaptations enjoyed by owls are elongated eyeballs that are more tube-shaped, resulting in an increased focal length. This effectively turns their eyes into a pair of binoculars with large pupils that enable them to gather more light. This allows them to see even small prey at a distance and in dim light. It is only in complete darkness that this eyesight no longer helps and then their excellent hearing allows them to continue hunting. Owls’ eyes are aimed forward, can barely be moved within their sockets leaving a large blind spot behind them, which is one reason they need the ability to turn their heads through more than three-quarters of a circle. In some species each eye is bigger than the brain.

Smaller birds tend to have their eyes positioned more to the side of the head allowing them to have better all-round vision in order to detect danger all around them. Many birds have eyes on the sides of their heads, letting them see different things with each eye. This “monocular” vision allows birds to scan two large areas. Most birds have very little binocular vision (where both eyes overlap and see the same image), and generally it is not very sharp. This means that they have a very limited view of their own bill, in exchange for a wider view of their surroundings. You’ll often see birds with monocular vision moving their heads around and switching from one eye to the other as they inspect something. This is how they gauge the three-dimensionality, or the depth of their environment.

A male Red-crested Korhaan shows off its large eyes.

Many birds can see a full 360 degrees around, and 180 degrees overhead, at the same time, and see detail in a wide horizontal band along the horizon. Eagles see four separate focal points, two on each side. Because their sharpest vision is to the side, birds need to tilt the head sideways to look up or down with one eye. A newly discovered type of cone cell in the eyes of flycatchers is probably specialised for tracking fast motion, one of several adaptations that help these birds see and catch tiny flying insects in midair.

Cathemeral birds exhibit an intermediate morphology between nocturnal and diurnal birds, with relative cornea sizes that are larger than those of diurnal birds but smaller than those of nocturnal birds

Underwater vision

Some birds need to see in both water and air and have evolved flexible lenses to do so. Some birds hunt fish underwater at night or dive so deep that there is essentially very little to no light. Herons and egrets are able to correct for refraction at the water’s surface when they take aim at their prey. Birds that hunt like these are not thought to have any special adaptations for underwater vision. Prey is detected and located from the air and the ambush attack gives no time for a change of plans once contact with the water is made. They just need to correct for image displacement of the target produced by refraction at the water’s surface.

Other species of birds, like cormorants, and penguins are strictly submarine visual predators. Some float at the surface with their heads submerged, vigilant for passing prey which they then pursue underwater, powered by their feet or flippers in the case of penguins which perform the entire search, chase, and capture sequence in dives that can (in some species) exceed 200 metres in depth and nearly half an hour in duration.

Gannets plunge dive to catch fish below the surface. Gannets are large seabirds that hunt fish from the air, making a plunge dive followed by active swimming in pursuit of prey. These impressive birds, with wingspans approaching two meters, fold their wings as they sight their prey and plummet into the sea from heights of 10 or more metres like avian cruise missiles. A recent study shows that they convert from aerial to aquatic vision nearly instantly. If they miss their targets, they will often chase fish underwater by flapping their wings, penguin-style. Their eyes are specially adapted to adjust their focus instantaneously as they cross the boundary from air to water. They are capable of switching from well-focussed aerial vision to aquatic vision in less than 0.1 second — literally in the blink of an eye. The visual challenges in this situation are huge. First, the bird needs to see a fish below the surface, focus on it, and accurately gauge its depth and position. Then, when it dives at high speed, its eyes need to be protected from the impact with the water. If it has any hope of catching its prey, the bird needs to see with sharp focus underwater. Most animals can see well in either air or water, not both. Seabirds, however, have evolved a solution to this. Eyes specialised to see in water do not use corneal focusing at all — the lens assumes the entire function of forming a sharp image. Obviously, such a lens has to be far more powerful than that of a terrestrial eye, and the required power is gained both by having a spherical shape and a carefully shaped internal gradient in the f refractive index that decreases with the distance from the lens’s centre. Aquatic eyes, however, generally fail in air: being spheres themselves, their corneas are curved; on encountering air on their outer surface, their refractive power comes back into play and is added to the lens’s, thus focusing images well in front of the retina. The speed of the transition from aerial to aquatic vision is almost certainly achieved by actively reshaping the lens against the iris.

Other adaptations related to vision

When birds are walking, they appear to bob their heads to stabilise their view of the surroundings. While it may appear to be a bob this isn’t actually what pigeons are doing. Instead, as they move, their heads (and eyes) lock in place while their body catches up. Then the head darts forward again, locks onto something new, and the pigeon’s body keeps moving forward. This allows them to momentarily fix their eyes on objects and gives the photoreceptors in their eyes enough time—about 20 milliseconds—to build a steady scene of the world around them. This head bobbing is an instinctual behaviour that develops within 24 hours of a bird hatching.

Related to this is that many birds have a remarkable ability to hold their head at a fixed position in space while hovering, to keep their vision fixed on a target. This is very obviously seen when a bird is held in the hand and its body rotated or moved, the head often appears ‘locked in space’, and does not move with the rest of the body. To maintain this stable position the bird has to make complex compensatory movements of the neck. This can be seen clearly in pigeons, owls and many other bird species. It can also be seen in the natural behaviour of many birds; for example, when they land on a thin branch, or a power or telephone wire, their momentum will often set the branch or wire oscillating back and forth. Yet if one carefully observes their heads, by lining it up with a static distant feature of the environment, one can see that it is likewise ‘locked in space’ while compensatory movements of the body and neck are made to balance the bird. Kestrels and kingfishers, while hovering in mid-air before diving to catch their prey, also show remarkable stabilisation of the head relative to the much larger movements of their bodies. Also watch some of our heavier flying birds like Spur-winged or Egyptian Goose and you will notice that with each wing beat which produces upward thrust, their heads maintain a level path.

A hovering Pied Kingfisher

Birds have a nictitating membrane—a third eyelid—that protects the eye from damage. This ‘third eyelid’ crosses the eye in a horizontal direction and serves to protect the eyes from debris and keep them moistened.

Birds’ eyes also go through colour changes with maturity and also during the breeding season. One theory for these eye colour shifts is to signal maturity to other birds and thus mating availability. It is also coincidentally useful to birdwatchers as they attempt to identify immature and adult plumage birds.

The best is yet to come

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. Migrating birds for instance have long been known to use visual cues, the sun and stars to navigate and find their way. More recently however researchers have discovered that birds possess an internal magnetic compass based on a chemical mechanism which plays out in the eye which may even allow them to use and ‘see’ the earth’s magnetic field based on magnetite (a magnetic mineral) receptors in the beak to provide the “map”. By integrating all these types of information migratory birds can find their way “home” or to their breeding grounds, whether across a featureless ocean or a large land mass.

It appears that as we learn more…the best is yet to come!

About the author

Nicolette Forbes was born in Durban and is passionate about all things KZN and its environments. With an interest in all things living from a young age it was no surprise that her chosen career path ended with her becoming a professional biologist having studied biological sciences at the University of Natal, Durban (now University of KwaZulu-Natal). Studying was followed by a lecturing stint to both biology and medical students for nine years before leaving the university to put her knowledge into practice with an ecological consultancy specialising in coastal habitat assessments.

Birding has been a passion from her high school days and birdwatching, atlassing. photography and being in the bush are her favourite things. Currently the Chair of BirdLife eThekwini KZN, the club covering the Greater Durban area, Nicolette has also through the non-profit EcoInfo Africa, partnered with Kloof Conservancy to run environmental courses focussed on birds.