Authors: Tim Birkhead
5
A brown kiwi. Thumbnails (
from left to right
): bill tip (
side view
) with numerous pits containing sensory nerve endings and nostril (
large opening
); cross section through the upper part of the bill showing the complex nasal region; a kiwi’s brain (
beak would be to the left
), showing the huge olfactory bulb (
darker shading
).
There are certain things in the realms of ornithology which commonly pass as instinct for want of a better name, but which really are a recognizable part of a bird’s economy
[way of life]
. All are at times rather incomprehensible, but the most perplexing is the capacity for scent – alleged by some, denied by others.
John Gurney,
1922
, ‘On the sense of smell possessed by birds’,
The
Ibis
,
2
,
225
–
53
In the mid-
1500
s, João dos Santos, a Portuguese missionary in East Africa (in what is now Mozambique), complained in his diary that each time he lit the beeswax candles in his tiny mission church, small birds would come in and eat the warm wax. The local people told dos Santos that the bird was ‘sazu’ – ‘the bird that eats wax’ (which he might have guessed). We now know that these were honeyguides and, writing four centuries later, Herbert Friedmann asked ‘how the bird becomes aware of the presence of wax in places where apparently there are no bees . . . To this there is no satisfactory answer as yet. The possibility of their finding it by smell is very slight as birds generally have but poor olfactory acuity.’
1
For some inexplicable reason ornithologists have found it hard to accept that birds might have a sense of smell. Ask almost any of them and they’ll turn up their noses and say, no, there’s not much going on in the olfactory department of a bird’s brain. They are wrong, and we have to thank John James Audubon, one of the greatest bird artists ever, for setting us off on the wrong track. As a child in the late
1700
s, Audubon had been told that the turkey buzzard (aka the turkey vulture) found its carrion food by means of ‘an extraordinary gift of nature’: an acute sense of smell. But as Audubon later observed, ‘nature, although wonderfully bountiful, had not granted more to one individual than was necessary and that no one was possessed of any two of the senses in a very high state of perfection; that if it had a good scent, it needed not so much acuteness of sight’. In other words, Audubon had the strange idea that it was impossible for a species simultaneously to have two well-developed senses. When he discovered that turkey vultures were unable to smell him when he approached them, concealed behind a tree, but ‘instantly flew away, much frightened’ when they saw him, any idea of an acute sense of smell evaporated, and he ‘assiduously engaged in a series of experiments, to prove to
myself
, at least, how far this acuteness of smell existed, or if it existed at all’.
2
A larger-than-life character, Audubon was the dynamic, erratic and charming illegitimate son of a French sea captain and a servant girl. Born in Haiti in
1785
, he moved to France at the age of six where he lived with his father and his childless wife, Anne. At eighteen his father sent him to Pennsylvania to oversee a plantation, but John James had no aptitude for farming, or, indeed, for anything that might earn him a living. Instead, he was passionate about birds, observing, shooting and drawing them. In doing so he discovered new species, made some original observations about bird behaviour and honed his artistic talents. He also found time to court Lucy Bakewell, the daughter of an English neighbour, whom he married in
1808
.
Determined to make a living from his bird illustrations, Audubon took himself to the east coast of America, where, despite making many useful contacts, he failed to convince anyone of the merit of his artistic efforts. Seeking fortune further afield, Audubon set off for England in
1826
, leaving Lucy and their small children behind. He was confident, cocky and proud of his skills as a field ornithologist, and his first exhibition in Liverpool was a success. No one painted birds like this – life-size, in realistic postures with every relevant feature illustrated. It was precisely because Audubon knew his birds so well that he was able to capture their essence so exactly.
Long before he set off for Britain, Audubon had tested the idea that turkey vultures had a sense of smell. His experiments consisted of hiding carcasses of various large animals and waiting to see whether vultures found them. Invariably they didn’t, and Audubon concluded that unless a carcass was visible the birds could not find it. So convinced was Audubon by his results that he decided to present the details of his vulture experiments to the Edinburgh Natural History Society in
1826
. The title of the subsequent paper – as long-winded as it was provocative – says it all: ‘An account of the habits of the turkey buzzard (
Vultur aura
), particularly with the view of exploding the opinion generally entertained of its extraordinary power of smelling’.
The effect of Audubon’s publication on the ornithological community was remarkable. It divided it, but not equally, for most of its members took Audubon’s side, considering his experiments ‘unanswerable’ – that is, utterly convincing.
3
His disciples included William MacGillivray, Audubon’s friend and ghostwriter,
4
and several other eminent ornithologists, including Henry Dresser, William Swainson, Abel Chapman, Elliot Coues and Lord Lilford. The latter two were ‘sportsmen’ and their evidence for ‘no sense of scent’ came directly from their experience as hunters. It seemed not to matter, they said, whether they approached birds upwind or not; in most cases it made no difference.
5
Among Audubon’s most enthusiastic supporters was the American Lutheran pastor and naturalist John Bachman, who repeated Audubon’s experiments in the presence of ‘a learned group of citizens’; they in turn then signed a document to the effect that they had witnessed the tests and were thoroughly convinced that the vulture lacked a sense of smell and was attracted to its prey ‘entirely by vision’. Science by committee!
6
Of Audubon’s critics the most vociferous was the astute but eccentric Charles Waterton who lived at Walton Hall, in Yorkshire. Waterton had spent many years in South America studying natural history and was familiar with turkey buzzards, and he was utterly convinced that Audubon’s experiments were flawed. Waterton was right, but his arguments were so convoluted, and his manner so strange, that the ornithological community ignored him.
7
Audubon’s experiments were indeed flawed. He made the mistake of assuming that vultures sought out putrifying, smelly carcasses and so these were what he used in his experiments. We now know that although these vultures feed on carrion, they prefer fresh carcasses and assiduously avoid those that are decomposing – hence Audubon’s erroneous results. Another problem compounded the confusion. Audubon said that he conducted his experiments on what he called the turkey buzzard – that is, the turkey vulture
Cathartes aura
– but in fact it appears that the bird he was studying was the black vulture,
Coragyps
atratus
, which, while similar in appearance, has a much poorer sense of smell than the turkey vulture.
8
Further investigations designed to establish whether birds had a sense of smell reinforced the view that they didn’t, even though, like Audubon’s, these experiments were appallingly designed. One such investigation, performed by Alexander Hill in
1905
, consisted of presenting a single domesticated turkey with two lots of food, under one of which was added some strong-smelling substance, including lavender oil, essence of anise and tincture of asafoetida.
9
The prediction was that if the turkey had a sense of smell, it would consume only the food uncontaminated by smell. Instead, the bird ate the lot. Hill’s final experiment consisted of presenting the unfortunate bird with food together with a saucer of hot, diluted sulphuric acid to which he added an ounce of potassium cyanide. The resulting reaction was extremely violent and produced a cloud of deadly prussic acid that killed the turkey. From these experiments, published in the journal
Nature
no less, Hill concluded that the turkey – and by inference all other birds – had no sense of smell.
While the ‘scientific’ evidence seemed to preclude the possibility of a sense of smell in birds, there was plenty of anecdotal evidence to suggest exactly the opposite. In Norfolk in the late eighteenth century, the blue tit was known as the ‘pickcheese’ for its habit of entering dairies and eating cheese; presumably they could smell it. Hardly convincing evidence: dairies are predictable in their location, so the birds could have learned; more telling would have been if the tits visited only when cheese was being made. We don’t know. In Japan some three hundred years ago, the closely related varied tit was taught to tell people’s fortunes. The fortune-teller read a poem aloud after which the (tame) bird picked out a card – placed face up on a table – that matched the poem. This was a particularly difficult trick to train the bird to perform, but the owners did so by placing something burned on the back of those cards they did
not
want the bird to pick. Since it worked, this suggests that the bird used its sense of smell to distinguish between the cards. Another anecdote refers to the ability of certain waders to smell mud. The Norfolk naturalist John Henry Gurney recounts that:
In Norfolk it is a common practice to ‘fye out’ a drain, that is to cleanse a ‘dyke’ or pasture water-course, and a very smelly operation it sometimes is. Again and again have I remarked how the attraction of the mud is sure to bring sooner or later the green sandpiper, by no means an abundant bird at any time . . . But how do they manage to discover the freshly-turned mire which is to provide them with a meal unless they smell it?
10
More convincing are the many anecdotes about ravens sensing death. This one in particular sounds like something from a Thomas Hardy novel:
11
In May
1871
, Mr E. Baker of Merse in Wiltshire was attending the funeral of two children who had died from diphtheria. The road to be followed lay along the Downs for a mile or more and the hearse had not proceeded far when two Ravens made their appearance. These sable birds . . . accompanied the mourners most of the way, and attracted attention by making repeated stoops at the coffin, leaving no doubt in Mr Baker’s mind that their powers of scent had detected what was inside them.
12
One commentator said: ‘After reading this narrative it is difficult to treat the long-established belief about ravens as a fable; here it is quite certain that sight could have been of no avail as the coffins were closed, and the ravens could only have realised what their contents were by scent.’
13
The widespread idea that ravens foretold death accounts for their appearance in Shakespeare’s
Othello
(Act IV, Scene I): ‘As doth the Raven, o’er the infected house, Boding to all.’
The anatomical evidence was stronger still. The nineteenth century saw huge advances in our understanding of animal anatomy. Dissection became a passion, especially among British and German zoologists. The most proficient in England was Richard Owen – later Darwin’s nemesis for rejecting natural selection, sticking instead to the Establishment view that God had created all life in its present form. Form was what it was all about, for Owen was a superb dissector and a shameless social climber, probing and slicing his way into the upper echelons of Victorian society.
The Victorian obsession with anatomy set the agenda for university zoology degrees for the following century and a half. As an undergraduate in the late
1960
s I dissected my way through much of the animal kingdom: earthworms, starfish, frogs, lizards, snakes, pigeons and rats. I loved it. The dogfish was our model organism; week in, week out we retrieved our personally labelled dogfish from a huge vat of stinking formalin so that we could continue our dissection. The cranial nerves were especially important, emerging from the brain to control most bodily functions, but whose significance I barely understood at the time. Despite the paralysing effect of the formalin on our nostrils, the dogfish was a delightful dissection. Its skeleton, made of cartilage rather than bone, allowed us to pare away the skull – it was like slicing beans – to expose the rope-like nerves leaving the brain. The fifth nerve, the trigeminal (so-named because it has three major branches), as in all vertebrates, carries information from the nasal cavity to the brain.