Bird Sense (23 page)

During the
1980
s there were major improvements in the way comparative studies were conducted. Armed with these new methods, two Oxford scientists, Sue Healy and Tim Guilford, decided to check Bang and Cobb’s results. When I asked Sue why she thought this was worth doing, she said that, as well as being interested in the new techniques, she also found the explanation that Bang and Cobb had for the variation in olfactory bulb size rather vague: ‘In those days being able to pin down one variable in a comparative analysis was much harder, I guess. Also, I’m a Kiwi and the kiwi has an extraordinarily large proportion of its brain given over to olfaction (and is nocturnal) so it seemed worth seeing if activity played a role in the rest of the variation.’ Significantly, she added: ‘I have been amazed ever since how little attention is paid to the role of olfaction in bird behaviour, not because people should have noticed our paper but because, once noticed, olfaction seems quite relevant to lots of things birds do.’
31

There were two main reasons for checking. First, Bang and Cobb had not considered the phenomenon of
allometry
– the way that organs scale with body size. Bang and Cobb implicitly assumed that brain size is directly proportional to body size. It isn’t. Larger birds have relatively smaller brains, in exactly the same way that adult humans have relatively smaller brains than babies. When the relative size of organs decreases with body size, this is referred to as negative allometry. Healy and Guilford were concerned that, by ignoring the fact that relative brain size decreases with body size, Bang and Cobb’s results might be wrong.
32

The other thing that Bang and Cobb were unaware of was the fact that, because many of the species in their comparison were closely related, their conclusions might be biased. Today, this type of bias is called a
phylogenetic
effect (phylogeny is the evolutionary relationship between species), and the way that phylogeny can potentially distort the results of a comparative study like Bang and Cobb’s may be seen by considering a different example. In the
1960
s two North American ornithologists, Jared Verner and Mary Willson, were looking for explanations for why certain birds had a polygynous mating system (i.e. one male paired with several females). After examining the literature, they concluded that marsh-nesting was the link, suggesting that, because a marsh habitat is highly productive and full of insects, female birds are able to feed their young without the help of the male, thus allowing polygyny to evolve. Since thirteen of the fourteen polygynous North American bird species nested in marshes, the effect of habitat seemed clear-cut.
33
But as later became apparent, there was a snag. Nine of these species belonged to a single family – the Icterids, the North American blackbirds whose ancestor may have been both marsh-nesting and polygynous. In other words, the fourteen species in their sample were not ‘independent’; nine shared the same evolutionary history, so the number of comparisons on which they based their conclusion that marsh-nesting is the ecological driver for polygyny was much less than fourteen, and, as a result, much less reliable. It was only in the early
1990
s that statistical methods for taking phylogeny into account in such comparative studies became available.
34

Healy and Guilford’s analysis showed that, after accounting for both allometry and phylogeny, the link that Bang and Cobb had found between lifestyle (i.e. living on or near water) and olfactory bulb size disappeared. The lifestyle effect was an artefact because most of the waterbirds came from just a few phylogenetic groups. Instead, Healy and Guilford found that it was mainly nocturnal and crepuscular birds that had relatively large olfactory lobes, consistent with the idea that olfactory prowess develops to compensate for reduced visual efficiency. Not all that surprising, you might think, but it is easy to be smart after the event.
35

When it was published in
1990
, Healy and Guilford’s study marked an important advance in our understanding of the ecological factors driving a good sense of smell in birds. But now, twenty years on, it looks like it is about to be overturned, or at least modified, as the truth-for-now process rumbles on. Healy and Guilford did not attempt to improve on Bang and Cobb’s simple linear index of relative bulb size – they simply used the original numbers because, without going back to the original specimens and doing a great deal of dissection, it would have been difficult to do otherwise.
36
However, by about
2005
high-resolution scanning and tomography (
3
-D reconstruction) started to become routine in medicine and biology, making it relatively easy (albeit expensive) to measure accurately the volume of different parts of a bird’s brain, including its olfactory bulbs.

Jeremy Corfield and colleagues at the University of Auckland in New Zealand have pioneered the use of
3
-D imaging to investigate the structure of birds’ brains, and have shown that Bang and Cobb’s index is sometimes well off the mark. To be fair, Bang and Cobb knew that this was a possibility and it was for pragmatic reasons that they assumed that, regardless of species, the basic design of birds’ brains is similar. The
3
-D scanning showed that this is not true. In the kiwi, which was the initial focus of Corfield’s work, the brain is unusual in its design: the olfactory lobe is not really a ‘bulb’ as in other birds, but is actually a flat sheet of tissue covering the foremost part of the brain, and the forebrain itself is unusually elongated. It was because of this that Bang and Cobb obtained a large index for the kiwi, so they got (roughly) the right answer (the kiwi does have a large olfactory region), but for the wrong reason.
37

The
3
-D studies have also revealed anomalies in some other species including the pigeon, whose olfactory bulb turns out to be much larger than anyone imagined,
38
and nicely consistent with its ability to navigate using its sense of smell, as we shall see in the next chapter.

Clearly, using Bang and Cobb’s index of olfactory bulb size is risky, and what are needed now are accurate measurements of the
volume
of the olfactory region of the brains of all the birds that Bang and Cobb studied. Given the work that this would entail, it might be some time before such information is available. Meanwhile, researchers have little option but to continue to use Bang and Cobb’s original values.

A recent study of the genes involved in olfaction in birds, so-called olfactory receptor genes, used nine species of birds that span the full range of Bang and Cobb’s olfactory bulb-size index, and showed that, overall, the total number of olfactory genes is positively associated with olfactory bulb size. In other words, the larger the bulb the more important the sense of smell is likely to be. Two nocturnal species, the kiwi and the kakapo, had the highest number of olfactory genes,
600
and
667
respectively, while the canary and blue tit, as expected on the basis of their relatively small olfactory bulb, had many fewer genes (
166
and
218
respectively). There was one anomaly, however: the species with the greatest olfactory bulb size, the snow petrel, had only
212
olfactory genes. It is just possible that a
3
-D scan might reveal this species’ bulb to be not as large as Bang and Cobb suggest, or possibly the snow petrel, which is diurnal, may be sensitive only to a limited range of odours and therefore require fewer genes.
39

Apart from the publication of Jane Austen’s
Pride and Prejudice
and the ongoing Napoleonic Wars, the most significant event of
1813
was Europe’s discovery of the kiwi. George Shaw, keeper of zoology at the British Museum, was given an incomplete skin – now known to be a South Island brown kiwi – by Captain Barclay, the captain of a convict ship. Barclay must have obtained the specimen from someone else, for he never visited New Zealand. Shaw described and illustrated this remarkable bird in
1813
, naming it
Apteryx australis
(wingless southerner). On Shaw’s death later that year, the specimen passed into the hands of Lord Stanley,
13
th Earl of Derby, whose enormous collection of natural history specimens at Knowsley Park in turn ended up in the nearby Liverpool Museum, where it has been ever since.
40

Despite its extraordinary appearance and incomplete nature, Shaw perceptively recognised that the kiwi might be a distant relative of the ostrich and emu (the ratites). Others erroneously imagined it to be either a kind of penguin or a species of dodo.
41

For over a decade Shaw’s was the only kiwi specimen available and some began to doubt the bird’s very existence. In
1825
, Jules Dumont d’Urville provided some tantalising new information. Recently returned from New Zealand, he described an encounter with a Maori chief wearing a cloak made of kiwi feathers. Following an appeal for more information, some New Zealand settlers put pen to paper and provided the first descriptions of kiwi behaviour, while others sent actual specimens. Once again Lord Stanley was a key player, passing the specimens on to Richard Owen at the British Museum, who, in his meticulous fashion, undertook detailed dissections. Owen noted the uniquely positioned nostrils at the bill tip and from the structure of the brain case recognised that a sense of smell might be important: ‘In the interior of the cranium the olfactory depressions are seen to be proportionately larger than in other birds’ and those cavities which in other birds are devoted to the lodgement of the eyes, are here almost exclusively occupied by the nose.’ Wrapping up, Owen concluded presciently: ‘The sense of smell must be proportionately acute and important in the economy [lifestyle] of the Apteryx.’
42

Observations of kiwis both in the wild in their native New Zealand and among birds brought to Britain and maintained in captivity revealed that they forage by snuffling around, literally, usually in the undergrowth, probing their long bills into the ground in search of their invertebrate prey – mainly earthworms. In the
1860
s the kiwi’s manner of finding food was accurately illustrated in a series of beautiful watercolour images by the Reverend Richard Laishley.
43

That kiwis regularly blundered into things when running away from human observers confirmed that their eyesight was poor, but the fact that they audibly snuffled as they foraged strongly suggested that kiwis found their prey by smell. Then, in the early
1900
s, W. B. Bentham of Otago University Museum, Dunedin, who knew of the kiwi’s large olfactory lobes from Owen’s publications, decided to see just how good its sense of smell was. Accordingly, he asked Mr Richard Henry, the curator of Resolution Island, a bird sanctuary off the south-west of New Zealand’s South Island, to conduct some simple experiments on a (tame) kiwi, which he referred to by its Maori name,
roa-roa
– meaning ‘long’ and presumably referring to its beak.

Following Bentham’s instructions, Henry presented the kiwi with a bucket that either did or did not contain earthworms buried beneath a layer of soil. The bird had no problem telling where the food was: ‘When I put down a bucket of earth without worms in it, the bird would not even try it; but the moment a bucket containing worms was put down the roa was full of interest and commenced to probe at once with its long beak.’ Bentham excuses himself for not having undertaken these experiments personally, pointing out the inaccessibility of Resolution Island and how ‘the uncertainty of getting back to the mainland in any reasonable time was so great that I had to give up the idea’. Admitting that many other experiments still needed to be done, he felt that his results afford ‘a certain amount of evidence for the existence in Apteryx of a keen sense of smell’.
44

In
1950
Bernice Wenzel joined the faculty in the School of Medicine at the University of California, Los Angeles. She had previously completed a PhD at Columbia University on the sensitivity of humans to smell, but by the time she reached California her research had shifted to the study of brains and behaviour. Even though she had changed direction, a colleague invited her to give a lecture at an olfaction conference in Japan in
1962
. She declined, pointing out that she was no longer studying olfaction. Refusing to take no for an answer, her colleague told her she’d ‘think of something’ and added her to the list of speakers. Bernice began to wonder what she might do and decided to see how pigeons, which she had in the lab, would respond to smell. Using a method commonly used by physiologists, she checked whether the pigeon’s heart rate changed in response to different stimuli. Bernice’s test involved exposing birds to a stream of pure air interspersed with brief periods during which an odour was added, and the bird’s heart and breathing rate were measured. On her very first test Bernice was amazed to see the bird’s heart rate soar as the odour was added. Here was unequivocal evidence that the pigeon had detected the smell. More studies quickly followed and at the meeting in Japan she presented her first paper on the sense of smell in birds.
45