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Well after dusk, on the island of Skomer, off southwest Wales, a cacophony
of weird growling and moaning noises heralds the return of nearly 100,000
pairs of Manx shearwaters Puffinus puffinus to their nesting burrows. These
highly specialised seabirds, close relatives of the albatrosses, come ashore
only to breed. Outside the breeding season, they wander widely over the
Atlantic Ocean. But what makes Manx shearwaters particularly interesting
are their regular nocturnal habits, which are shared with only a handful
of other seabird species around the world. Although the birds feed by day,
they delay entry to their breeding colonies until nightfall, and may not
go to their nesting burrows at all on moonlit nights.

The birds probably seek the cover of darkness to avoid the attacks of
predators. Shearwaters are so well adapted to a life in the air and on sea
that their movements are slow and cumbersome on land, making them easy prey
to predatory birds active during the day such as great black-backed gulls.
But how do they manage to find their way about at night? Fifty years ago,
the French anatomist Rochon-Duvigneaud defined a bird as ‘a wing guided
by an eye’. While this is apt for most species, there is evidence that some
birds can rely upon other senses, especially hearing and smell, to guide
their flight. So whether vision plays an important part in the nocturnal
comings and goings of Manx shearwaters is not a trivial question.

Shearwaters could use smell to help them to find their burrows. The
structure of their nasal cavities and the parts of the brain associated
with this sense suggest that they have a well developed sense of smell.
We know that some species closely related to Manx shearwaters can locate
food in mid-ocean by smell alone. Moreover, shearwaters are smelly creatures,
and it is possible that personal odours wafting from a nest burrow could
help the birds to recognise home. The birds might also rely on the call
of the mate inside the burrow to home in on the right nest; Michael Brooke
of the University of Cambridge has recently shown that individuals can recognise
their mates’ calls. But birds can still find the correct burrow even when
its sole occupant is a silent chick.

The bulk of the evidence collected by Brooke, after studying the shearwaters
of Skokholm, suggests that most birds do in fact rely primarily on vision
when they come ashore under the cover of darkness. But Brooke has also observed
homecoming shearwaters sometimes crashing into each other and into rocks,
so the visual cues available to birds may, on occasion, be minimal. Their
familiarity with the landscape is probably an important factor.

Working with Brooke, I investigated the optical design of the Manx shearwater’s
eye, to look for signs that these birds have eyes uniquely adapted to their
unusual way of life. We also pooled our findings with those of Brian Hayes,
then working at the Institute of Ophthalmology in London, who looked in
detail at the structure of the retina in these birds.

We decided to compare the shearwater’s eye to that of the feral pigeon
or rock dove Columbia livia. We chose this species, familiar as a town bird
throughout much of the world, partly for convenience, but also because it
is at home flying around cliff faces, a habitat rather like the places where
shearwater’s nest. But the pigeon is entirely a day-time species, going
to roost around dusk. Our choice turned out to be particularly apt because
although the eyes of pigeons and Manx shearwaters are almost identical in
size and overall shape, their optical designs turned out to be quite different.

The placement of shearwaters’ eyes on the sides of their heads gives
them a wide field of view in the horizontal plane, which is useful to a
bird vulnerable to attack by aerial predators. But they do have a blind
spot behind the head – unlike mallard ducks, say, which can see everything
behind and above them. The shearwater’s blind region, which is 75 degrees
wide, occurs because the eyes are placed in the skull so that the visible
fields of the two eyes overlap to give an area of binocular vision in front
of the birds. This region is long and narrow, extending about 90 degrees
vertically, and with the beak placed at its centre, suggesting that vision
is used to guide the beak in pusuit of food.

Two aspects of its optical structure suggest that the eye of the Manx
shearwater is adapted to vision at night. In the shearwater’s eyes the lens
does most of the refraction, bendings or of light necessary to produce a
focused image on the retina. The cornea, the outer covering of the eye,
is relative flat and so of low refractive power. In pigeons, however, the
reverse is true. The cornea is highly curved and is the principal refractive
component (see Figure 1).

This difference in the optical structure of the two eyes is most easily
encapsulated by the ratio of the refractive power of the lens and the cornea
in the two eyes. The FL:FC ratio in the pigeon is 0.4 compared with 1.6
in the shearwater. If we plot these ratios for a range of different bird
and mammal eyes, we find that shearwater eyes fit neatly among those of
other nocturnally active creatures, while pigeons can be seen to have a
day-time eye design (see figure 2). The consequence of these subtle differences is that
pigeon and shearwater eyes differ in their focal lengths. The shorter focal
lenth of shearwater eyes give them a smaller, but brighter, image compared
with those in pigeons when viewing the same scene. In terms that will be
familiar to the photographer, the shearwater eye is ‘faster’, or has a lower
F-number, than that of the pigeon. Image brightness differs by a factor
of 1.5.

At bright day-time light levels, a pigeon’s eye scores over a shearwater’s.
The longer focal length of the pigeon’s eyes give it a larger image of the
same scene. Again, by analogy with photography, this gives the eyes the
potential to detect greater detail in the image. In other words, the visual
acuity of pigeons should be higher than that of shearwaters under identical
viewing conditions.

So the optical design of the eyes of Manx shearwaters would indeed give
the bird some night-time advantage over the eyes of strictly diurnal birds
such as pigeons. But the potential difference in sensitivity between the
two eyes is not dramatic, and could not of itself account for the shearwater’s
ability to come ashore at night under the darkest natural conditions. This
fits with the field studies, which suggest that cues other than vision might
also be used by homing shearwaters.

What of the retina of Manx shearwater eyes? Does this show any specialisations
linked to the shearwater’s way of life? The retina is the surface of the
back of the eye where the image produced by the optical system is first
analysed by the brain. It is a complicated layered structure, containing
many different types of cells. In every animal species looked at so far,
zoologists have found marked regional differences in the size and distribution
of these cells. No one is quite certain what these differences mean, but
small ganglion cells at a high density probably indicate a region where
much detail can be resolved. For example, in our retinas such cells are
particularly numerous in the region of the fovea, which serves the central
part of the visual field that we use for detailed visual tasks, such as
reading this text. Away from the fovea, ganglion cells become for less numerous
and visual resolution correspondingly falls in the peripheral part of our
vision.

So Hayes decided to look in detail at the distribution of ganglion cells
in the retinas of Manx shearwaters. We could then combine his data with
mine and be fairly certain where any specialised region of ganglion cells
were ‘looking’ in the shearwater’s visual field. Hayes’s data revealed that
as in many other birds, including pigeons, there is a small region of high
acuity which lies not directly in front of the bird but in the lateral fields
of each eye. In essence, for a shearwater to examine something in order
to see the greatest detail the bird must view the object ‘sideways’ with
one eye only, not binocularly as we ourselves would do in the same situation.

Hayes also found that Manx shearwaters have a dense region of ganglion
cells, and so heightened visual acuity, running in a narrow band right across
each retina and hence across the field of view of both eyes (see Figure 3). In flight,
Manx shearwaters hold their heads with the bill pointing down at an angle
of about 20 degrees to the horizontal. When we compensated for this by rotating
our visual field data, we found that this bird’s head is in the normal position.
The function of this linear area of heightened acuity is still unclear.
Pigeons do not have such an area, but it is not unique to shearwaters. Other
birds and even some mammals have such a band, and they are usually animals
that frequent wide open habitats where the horizon is nearly always in view.
The band of high resolution could represent a specialisation of the visual
system for detecting predators or prey, which often appear along the horizon.
It might also be a device for stabilising the position of the head to the
horizon, something that might be particularly useful in birds such as shearwaters,
which navigate long distances. Perhaps stabilisation to the horizon makes
it easier to measure the elevation of the Sun or stars to provide compass
cues. The Manx shearwater’s prowess as a long-distance oceanic navigator
was amply demonstrated 30 years ago. A bird taken from its breeding burrow
in Wales and released in Boston Massachusetts, 4500 kilometres way, returned
in twelve and a half days.

Although our findings on retinal structure raise many interesting questions
about the vision of Manx shearwaters, the most intriquing feature of Hayes’s
work has been the discovery of a new type of regional specialisation, never
before reported in any vertebrate retina. All previous regional specialisations
have involved small ganglion cells packed close together, and probably associated
with regions of high activity. But this new area cxontains extra-large cells
at low density aligned in a regular array. Again we used the visual field
data to find out just where this specialised region ‘looked’. It seems to
serve exactly the small area of binocular vision below the bird’s beak.

What aspects of the shearwater’s way of life are associated with this
unique feature of its retina? Is it something to do with nocturnal habits
or perhaps some aspect of the bird’s flight or foraging behaviour? Large
ganglion cells probably function to pool the responses from many receptor
cells and so such an arrangement could be a way of enhancing the sensitivity
of cells by summing the input from many receptors. But if this is the case,
why should such enhanced sensitivity be associated with just this particular
part of the frontal binocular field below the bill? Hayes suggests that
these types of ganglion cells could respond well to rapidly moving stimuli
and hence could serve to guide shearwaters over the ever changing surface
of the sea as they fly, literally a few centimetres above it, for hours
on end.

Further comparisons with other species will help to establish whether
any of these features are unique or represent more general adaptations.
What these findings do reveal is just how subtle the variations in the eye
design between different species of birds can be. Comparing the eyes of
pigeons and Manx shearwaters has shown that even eyes which look superficially
the same may harbour subtle differences that help us to understand sensory
aspects of an animal’s way of life.

Dr Graham Martin is a senior lecturer in the School of Continuing Studies,
The University of Birmingham.

Further reading, Brooke, Michael. 1990. The Manx Shearwater. Poyser,
London. Martin Graham. 1990. Birds by Night. Poyser, London.