Authors: Tim Birkhead
It was this nerve that Richard Owen exposed in
1837
in a turkey vulture he dissected to check Audubon’s assertion that the species did not find its food by smell. Owen compared the turkey vulture with a turkey, which he felt was an appropriate comparison, being the same size and ‘one in which the olfactory sense may be supposed to be as low as in the vulture, on the supposition that this bird is as independent of assistance from smell in finding his food as the experiments of Audubon appear to show’. The dissection revealed the turkey vulture’s trigeminal nerve to be particularly large and Owen concluded that ‘the vulture has a well-developed organ of smell, but whether he finds his prey by that sense alone, or in what degree it assists, anatomy is not so well calculated to explain as experiment’. On the other hand, there were numerous anecdotes consistent with the turkey vulture having a well-developed sense of smell; one that Owen mentions came from a Mr W. Sells, a doctor in Jamaica:
The bird is found in great abundance in the Island of Jamaica, where it is known by the name of John Crow . . . an old patient and a much valued friend who died at midnight: the family had to send for necessaries for the funeral to Spanish Town, distant thirty miles, so that internment could not take place until noon of the second day, or thirty-six hours after his decease, long before which time, and a most painful sight it was, the ridge of the shingle roof of his house, a large mansion of but one floor, had a number of these melancholy-looking heralds of death perched thereon . . . the birds must have been directed by smell alone as sight was totally out of the question.
14
Owen’s anatomical evidence for an olfactory sense in vultures was ignored. Other zoologists, contemporaries who dissected the heads of fulmars, albatrosses and kiwis – all of which indicated that these birds have a well-developed sense of smell – were also ignored.
15
In
1922
John Gurney commented on the curious lack of evidence for a sense of smell in birds when it was well established in other animal groups. He says: ‘of the existence of a highly-developed scent in the mammals there can be no shadow of doubt’. In fishes, he writes, it is ‘fully acknowledged’ that they possess a sense of smell. More remarkably, even certain butterflies and moths are ‘credited with the enjoyment of the faculty of scent’. Birds were a puzzle, and olfaction the most perplexing of their senses: ‘It is curious that so important a matter should be still unsettled’.
16
Jerry Pumphrey, by now a professor of zoology at Liverpool, wrote a review of bird senses in
The Ibis
in
1947
, and said, after discussing vision and hearing: ‘Of the other sense organs, there remains little that is worth saying. The sense of smell is undoubtedly only very moderately developed by comparison with the more gifted mammals.’ Pumphrey acknowledged the anecdotal evidence for a sense of smell in some birds, but then pointed out that it was contradicted by other anecdotes.
17
Throwing his hands up in despair, he concludes that: ‘Indeed, in this field critical experiments are almost impossible, because human beings labour under the excessive difficulty of not knowing what to look for. There is no theory of smell which is even moderately consistent with the facts of human olfactory experience . . .’
18
A few years earlier Percy Taverner, curator of birds at the National Museum of Canada, had written a short article – a note, really – saying much the same and bemoaning how little was known about the sense of smell in birds: ‘These may be difficult subjects but it is time they were tackled. Here is a chance for some ingenious and ambitious post-graduate seeking fame and new worlds to conquer!’
19
Little did Taverner suspect that it would be neither a postgraduate, nor a man, who would launch the scientific study of the sense of smell in birds.
Enter Betsy Bang, a medical illustrator at Johns Hopkins University in the United States in the late
1950
s. Single-handedly, she transformed the study of avian olfaction, dragging it out of the academic shadows and into the limelight.
Betsy worked for her academic husband, illustrating his articles on respiratory disease in birds. This meant dissecting and drawing the nasal cavities of various bird species from her husband’s extensive anatomical collection. Betsy had only limited training in biology but was a keen amateur ornithologist, and she was smart. As she dissected and drew, she began to wonder why the design of nasal cavities differed so much in different species.
The structures inside the human nose that warm and moisten incoming air, but also detect odours, are called the conchae.
20
The term may be unfamiliar, but the conchae are the wafer-thin leaves of bone inside the harder upper part of the nose that are so easily broken during fights and less easily reshaped during nose jobs. In birds, air is drawn in through the two external nostrils, which in most species are mere slits in the upper portion of the beak. There are three chambers inside the upper beak of most birds; the first two warm and humidify the inhaled air, some of which passes into the lungs via the mouth. The third chamber at the base of the beak contains the conchae,
which
comprise a scroll-like roll of cartilage or bone. Air passes between the leaves of bone that are covered with a sheet of tissue and in which reside the many tiny cells that detect odours and relay information to the brain. The more complex the conchae – the more turns of the scroll – the greater their surface area and the greater the number of scent-detecting cells. The parts of the brain responsible for interpreting odour lie close to the base of the beak and because of their shape are referred to as the olfactory bulbs.
21
Looking at her dissections, Betsy simply could not accept that birds with large, complex nasal cavities had no sense of smell, as all the textbooks asserted. She was ‘deeply concerned that wrong information was out there about the olfactory abilities of birds and she wanted to correct this misunderstanding’.
22
The reason for the misunderstanding, she guessed, was a lack of communication between anatomists and those conducting behavioural studies. The few recent behavioural studies designed to establish whether birds could detect chemical signals had been conducted on pigeons, a convenient but biologically inappropriate study species which Betsy described as being ‘feebly equipped’ in the olfactory department. The other problem was that the behavioural experiments themselves were often poorly designed.
For her initial investigation Betsy focused on three unrelated species, each with greatly enlarged nasal conchae but each with a very different lifestyle. They were: (i) the turkey vulture, the species that Audubon thought he had studied, a diurnal carrion feeder; (ii) the black-footed albatross, a pelagic seabird that feeds on squid and whale carcasses (marine carrion), and (iii) the oilbird, a nocturnal, tropical, fruit-eating species that, as we have seen, nests in caves in complete darkness. The anatomical evidence seemed overwhelming – what other purpose could this elaborate nasal tissue have unless it is to detect odours? The resulting paper – her first – was entitled ‘Anatomical evidence for olfactory function in some species of birds’, and illustrated with slightly ghoulish yet revealing dissections of the heads of each species. The results were published in
Nature
in
1960
and, as one of her colleagues later said, ‘Bang’s paper made it impossible to deny the existence of a sense of smell in birds’; Betsy made ‘an essential contribution at a receptive time’.
23
Throughout the
1960
s Betsy continued to look at the anatomy of different birds, but it was a meeting with Stanley Cobb in the late
1960
s that provided the next big step. Betsy and her husband had a second home at Woods Hole at the southern end of Cape Cod, Massachusetts, where they spent each summer. At a dinner party one evening she found herself seated next to Cobb, a retired neuropsychiatrist with a passion for birds and brains. A few years previously Cobb had published a short article on the olfactory bulb in birds. He and Betsy hit it off immediately and joined forces to produce a massive comparative study of olfactory bulb size in the brains of
107
different species.
24
They measured the length of the olfactory bulb with a ruler, expressing it as a percentage of the maximum length of the brain.
25
They knew that this was a rough-and-ready measure of olfactory potential, but the only way they could have done anything better would have been to dissect out the olfactory bulb, weigh it and then calculate what this represented as a percentage of the remaining brain mass; but this would have been extremely time-consuming (it is a difficult dissection) and it would have meant destroying the museum’s specimens. For the time being at least, their simple index did the job.
Here are a few examples, in rank order: the higher the value, the greater the relative olfactory bulb size:
Snow petrel
37
Kiwi
34
Petrel – average
29
(varying from
18
to
33
)
Turkey vulture
29
Nightjar – average
24
(varying from
22
to
25
)
Hoatzin
24
Rail – average
22
(varying from
12.5
to
26
)
Feral pigeon
20
Shorebird – average
16
(varying from
14
to
22
)
Domestic fowl
15
Songbird – average
10
(varying from
3
to
18
)
Overall, Bang and Cobb’s comparative study revealed a twelvefold difference in the relative size of the olfactory lobe across different bird species – from the tiny bulb in the black-capped chickadee (a songbird), to the massive one in the snow petrel.
26
They also assumed that the relative size of the bulb reflects olfactory prowess, a link that was not formally verified until the
1990
s when researchers demonstrated an association between bulb size and the threshold for odour detection.
27
Overall, this is what Bang and Cobb were able to conclude: ‘Our survey suggests that in kiwis, in the tube-nosed marine birds, and in at least one vulture, olfaction is of primary importance, and that most waterbirds, marsh dwellers, and possibly echo-locating species, have a useful olfactory sense. In other species it may be relatively unimportant.’
28
Inspired by Bang’s initial papers, another American researcher, Kenneth Stager, decided to rerun Audubon’s behavioural experiments. The anatomical evidence for a well-developed sense of smell in the turkey vulture was convincing, but behavioural evidence was still needed. Stager confronted the problem with gusto, setting up some ambitious field experiments that, among other things, involved blowing air over concealed animal carcasses (and in other cases over nothing, as a control) to see the effect on turkey vultures. The effect was dramatic. The birds could clearly smell the carcass even though they were out of sight. A chance conversation with someone from the Union Oil Company of California resulted in a major breakthrough, enabling him to identify just what it was in the odour of animal carcasses that the vultures homed in on. Stager was told how in the
1930
s the company had noticed that leaks in natural gas pipelines attracted turkey vultures. The gas contained ethyl mercaptan (aka ethanethiol), a substance that smells like rotten cabbage (also responsible for the smell of bad breath and flatus); it is also released from decaying organic matter, including animal bodies. Union Oil therefore added higher concentrations of mercaptan to the gas to help them locate leaks. As early as the
1930
s the company knew that turkey vultures had a good sense of smell and, sure enough, when Stager blew mercaptan-laden air across the California hills, the vultures came flocking.
29
Not only had he obtained convincing behavioural evidence that turkey vultures use their sense of smell to find food, but he had identified the substance whose odour enabled them do this.
Bang’s pioneering anatomical research, together with the comparative study she did with Stanley Cobb on the olfactory bulb, was ground-breaking. But such is the truth-for-now nature of science that before long other scientists started to look at these results with new eyes. Science is always on the move and it was perhaps inevitable that new insights and new techniques would eventually expose the limitations of Bang and Cobb’s study. Indeed, this is exactly what Bang and Cobb had done in their own investigation which built on and improved the studies done in the nineteenth century.
30
Bang and Cobb’s study was in many ways exemplary science. They measured their specimens as carefully as they could, presented their results clearly but also acknowledged the fact that their estimate of olfactory bulb size was simply an index, modestly hoping that ‘these crude olfactory ratios may serve as a guide to its [olfaction’s] relative importance’. As we’ve seen, their main conclusion was that, in addition to the kiwi, tube-nosed marine birds (albatrosses and petrels) and the turkey vulture, ‘most waterbirds, marsh-dwellers and waders . . . have a useful olfactory sense’.