Authors: Tim Birkhead
Around half of all bird species examined so far have a single fovea, like us, and the question is whether shrikes have one or two. When I asked my academic colleagues who specialise in avian vision, no one knew. But one told me where to look: ‘Check Casey Wood’s
Fundus Oculi
,’ he said. Remarkably, I knew of this obscurely titled book, published in
1917
, although I had never perused it. Wood’s
Fundus Oculi
is a study of the retinas of birds, as viewed through an optician’s ophthalmoscope. Its title – which guaranteed that it would never be a bestseller – refers simply to the back of the eye.
Casey Albert Wood (
1856
–
1942
) was already one of my heroes. Professor of ophthalmology at the University of Illinois between
1904
and
1925
, and probably the most eminent eye specialist of his age, Wood was also fascinated by birds, bird books and the history of ornithology. Recognising, for example, the immense significance of Frederick II’s thirteenth-century manuscript on falconry (and ornithology), Wood went to the Vatican Library, translated it and published it, making this extremely rare manuscript much more widely available. He also discovered, and purchased for his personal library, a unique hand-coloured copy of Willughby and Ray’s
Ornithology
(
1678
) that John Ray had presented to Samuel Pepys when Pepys was president of Britain’s Royal Society in the
1680
s. Another major achievement was Casey Wood’s
Introduction to the
Literature on Vertebrate Biology
, a remarkable reference book that I own and use regularly, that lists
all
known zoology books (including those on birds) published before
1931
.
Wood’s
The Fundus Oculi of Birds
(to give it its full title) grew out of his belief that a better understanding of the exceptional eyesight of birds would throw light on the biology and pathology of human vision. It was a stroke of genius and, employing the same equipment he used to examine the human retina, Wood described and catalogued the eyes of a wide range of living bird species. Such was his knowledge that it was said he could identify a bird simply from an image of its retina!
5
My first opportunity to look at Wood’s
Fundus Oculi
occurred during a visit to the ornithological Blacker-Wood Library at McGill University, Montreal, which I visited while searching for material for my book
The Wisdom of Birds
(
2009
). Casey Wood had donated his huge personal library to the university in honour of his wife. I went with my colleague Bob Montgomerie, specifically to look at the Pepys’
Ornithology
, and while I was there Eleanor MacLean, the librarian, asked if I’d also like to look at the
Fundus Oculi
. Stupidly, I declined, befuddled by its title and distracted by too many other more interesting old books.
Even if I had looked at it, there was no way I would have remembered whether Casey Wood had included shrikes in his survey, and when I later needed it I discovered that the book was scarce in British libraries. I eventually found one, and there, under ‘California Shrike
Lanius ludovicianus gambeli
’, now known as the loggerhead shrike, Wood writes: ‘There are two macular regions in the fundus of this bird.’ In other words, yes, there are two foveas (macular regions) on the back of the eye (the fundus) of the loggerhead shrike. Excellent! Just as I hoped, and as Wood says: ‘Birds with double foveae have exceptionally good eyesight.’
6
The human eye has long fascinated lovers, artists and physicians. The ancient Greeks dissected eyes, but struggled to understand how they worked, unclear as to whether they received or emanated light. The anatomical descriptions of the eye made by Galen – physician to the Roman gladiators during the second century
ad
– remained the standard until the Renaissance, when there was renewed interest in the natural world, and in the wonder of vision, inspired by translations of Islamic manuscripts from the thirteenth and fourteenth centuries. The German polymath Johannes Kepler (
1571
–
1630
) was among the first to create a theory of vision, later elaborated by Isaac Newton, René Descartes and many others. In
1684
Antonie von Leeuwenhoek, pioneer microscopist, got the first glimpse of what we now know to be light-sensitive cells – the so-called rods and cones – in the retina. Two hundred years later, using a much better microscope and a very clever way of staining different types of cell-different colours, Santiago Ramón y Cajal (
1852
–
1934
) provided a wonderfully detailed – and exquisitely illustrated – description of the way the cells of the retina connect to the brain, in a variety of animals, including birds.
In the
Origin of Species
Darwin refers to vertebrate eyes as ‘organs of extreme perfection and complication’. In a sense, the eye was a test case for natural selection because the Christian philosopher William Paley had used the eye in his
Natural Theology
(
1802
) as an example of the Creator’s wisdom. Only God, Paley asserted, could produce an organ so perfectly adapted for its purpose. Paley called it a ‘cure for atheism’. As an undergraduate at Cambridge, Darwin had enjoyed Paley’s book, when, believe it or not, he was training for the Church. But as Darwin said later, Paley’s ideas about the natural world (which were essentially about adaptation) all seemed quite plausible – before his discovery of natural selection. The recognition that natural selection provided a much more convincing explanation than God or natural theology for the perfection of the natural world was one of the fundamental shifts in our understanding of nature.
Paley was a creationist and an advocate of ‘intelligent design’, and the crux of his argument was that half an eye was of no use, and that therefore natural selection could not possibly create an eye. For Paley and the creationists the eye had to be fully developed to be of any use, and the only way that could happen was if God made it.
The flaw in this way of thinking has been exposed many times, but most tellingly in an ingenious reconstruction of the evolution of the eye by two Swedish scientists, Dan-Eric Nilsson and Susanne Pelger, in
1994
. Starting from a simple sheet of light-sensitive cells, they showed that a
1
per cent improvement in vision each generation could generate a sophisticated eye similar to that of a human or a bird in less than half a million years – a relatively short period in the history of life on earth. This evolutionary model not only showed that half an eye (or less) was better than no eye at all; it also revealed that the evolution of vision was nowhere near as complicated (or impossible) as Paley and his followers believed.
7
As I read more about the eyesight of birds, one particular phrase kept cropping up:
a wing guided by an eye
, meaning that a bird is no more than a flying machine with excellent vision. After a while I began to feel a twinge of irritation every time I read it, because it implies that vision is the
only
sense birds have: but, as we will see, nothing could be further from the truth. The expression comes from a book on vertebrate vision published in
1943
by a French ophthalmologist, André Rochon-Duvigneaud (
1863
–
1952
), for whom the aphorism captured the essence of being a bird.
Of course, long before Rochon-Duvigneaud, almost everyone who has written about birds has commented on their excellent eyesight. The great French naturalist the Comte de Buffon, for example, discussing the senses of birds in the
1790
s, said: ‘We find that of sight to be more extended, more acute, more accurate and more distinct in the birds in general, than in the quadrupeds’ and ‘A bird . . . that shoots swiftly through the air, must undoubtedly see better than one which slowly describes a waving tract’ – meaning a bird with a slower, more meandering flight.
8
Then, in the early nineteenth century, the ornithologist James Rennie wrote: ‘We have ourselves more than once seen the osprey dash down from a height of two or three hundred feet upon a fish of no considerable size, and which a man could with difficulty have perceived at the same distance’ and ‘The bottle tit [long-tailed tit] flits with great quickness among the branches of trees, and finds on the very smooth bark its particular food, where nothing is perceptible to the naked eye, though insects can be detected there by the microscope.’
9
In a similar vein, there is an oft-repeated observation that an American kestrel can detect a two-millimetre-long insect at a distance of
18
metres.
10
Unsure about what that meant in terms of human vision, I checked and, yes, at a distance of
18
m a two-millimetre-long insect is completely invisible, and in fact did not become visible until I had approached to within four metres – striking evidence of the kestrel’s superior visual resolution.
While conducting my PhD on guillemots on Skomer Island I constructed hides at various colonies to be able to watch their behaviour at close range. One of my favourite hides was on the north side of the island where, after an uncomfortable hands and knees crawl, I could sit within a few metres of a group of guillemots. There were about twenty 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 guillemot that was incubating suddenly stood up and started to give the greeting call – even though its partner was absent. I was puzzled by this behaviour, 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 guillemot flying towards 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 two birds proceeded to greet each other with evident enthusiasm. I could hardly believe that the incubating bird had apparently seen – and recognised – its partner several hundred metres away out at sea.
11
How can we establish scientifically how good avian vision is? There are two ways: by comparing the structure of their eyes with that of other vertebrates, and by devising behavioural tests to establish how well birds can see.
From the Renaissance onwards, researchers interested in human vision commonly studied the eyes of birds and other animals, and over time a picture started to emerge. Not surprisingly, it was a picture seriously biased by what was known about human vision.
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-
1600
s, birds’ eyes
‘
outwardly appear small, because excepting the pupils they are wholly covered with skin and feathers’.
12
As with many organs, the eyes of larger birds are generally bigger than those of smaller ones – obviously. The smallest eyes are those of hummingbirds, the largest are those of the ostrich. Those who study eyes use the distance between the centre of the cornea and lens to the retina at the back of the eye (the eye’s diameter) as a measure of eye size. The ostrich’s eye has a diameter of
50
mm, more than twice that of the human eye (
24
mm). In fact, relative to their body size, the eyes of birds are almost twice as large as those of most mammals.
13
Frederick II was an astute observer and in his manuscript on falconry, he commented: ‘Some birds have large eyes in comparison with their bodies, some small, some of medium size.’
14
The ostrich may have the largest eye of any bird in absolute terms, but, for its body size, it is actually smaller than we would expect. The largest eyes relative to body size occur in eagles, falcons and owls. The white-tailed sea eagle has an eye of
46
-mm diameter – not far off that of the ostrich (which is eighteen times heavier). At the other end of the scale, the kiwi has tiny eyes, both absolutely (an eight-millimetre diameter) and for its body size. To get some impression of just how tiny the kiwi’s eyes are, the Australian brown thornbill (which weighs a minuscule six grams) has an eye diameter of six millimetres. If kiwis had eyes proportional to their body weight (which is about two or three kilograms), their eyes would be
38
mm in diameter (similar to a golf ball) – a huge difference. The kiwi’s eyes have been described as ‘as degenerate as it is possible for an avian eye to be’.
15