Authors: Tim Birkhead
One of just a handful of female professors of physiology in the United States in the
1960
s, Bernice Wenzel’s great strength was to employ the combined tools and ideas of anatomy, physiology and behaviour better to understand olfaction. Examining birds as diverse as canaries, quail and penguins, she found that every species, including those with the tiniest olfactory lobes, was able to detect odours. Although all species responded, those with larger olfactory lobes showed a greater increase in heart rate. Despite these remarkable results, it was not known whether birds (other than the kiwi) used olfactory information in their daily lives.
The heart rate experiments were so successful that Wenzel decided to try the same approach with kiwis. In her previous investigations the birds simply needed to have their wings restrained for them to sit quietly during the experiment. Not kiwis. They are immensely powerful birds, and she quickly discovered that, with virtually no wings to constrain them and very strong legs, adult kiwis were ‘able to wiggle out of almost any system of restraint’. Instead, Wenzel took readings from a single young kiwi that was accustomed to being handled. To validate her results, she obtained a few readings from an adult – much more aggressive – bird.
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Curiously, and in contrast to all the other birds Wenzel had assessed, odour caused no change in the young kiwi’s heart rate, even when given a whiff of its favourite earthworms. Instead, it was changes in breathing rate and alertness that most obviously revealed the bird’s ability to detect odour. Wenzel then carried out some behavioural experiments to see if kiwis (five different individuals) could detect food by smell alone.
Employing an experimental design very similar to the one used by Bentham and Henry fifty years earlier, she presented the birds with metal tubes sunk into the ground. Some tubes contained strips of meat that the birds were used to eating, but covered with a layer of damp soil, while the other tubes contained only damp soil. In both cases the tubes were covered by a thin nylon mesh that the bird had to puncture with its bill so as to access the soil. This was essential because the birds foraged only at night and it would have been difficult or impossible to see which tubes they probed. The metal tubes provided no other cues to the presence of food and because the meat was inert it created no sound; there were no visual cues because the appearance of all the mesh-covered tubes was identical. The mesh covering also precluded any taste cues and left convenient evidence if the bird pushed its beak through it.
Just as in the earlier studies, the kiwis were interested only in the tubes containing food. Not only that, but they probed directly on to the food items, indicating that they could detect extremely subtle gradients in odour.
Other behaviours in her captive kiwis suggested to Wenzel a strong reliance on smell. One night while she was in the aviary, a kiwi woke up early and approached her. In her own words: ‘It was dark, the bird stopped very close to me and then methodically moved the end of its beak up and down my legs without actually touching them, as if outlining me . . . the behaviour is far more consistent with dependence on olfaction than vision.’
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Almost everyone who has watched free-ranging kiwis has commented on their audible sniffing, but it is generally recognised that this is as much to do with clearing the nostrils as with olfaction. Kiwis have nasal glands that secrete mucus when they are excited (by food) and, because the external nostrils are narrow slits, they become easily clogged with soil during probing.
During her studies, Wenzel noticed that lightly touching the bill tip of one of her captive kiwis would result in active searching movements, indicating that touch was also an important part of natural foraging behaviour. And in concluding her account she said: ‘there is probably a close interaction between the tactile and olfactory modalities, with little, if any, visual participation’.
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The northern hemisphere’s counterpart to the kiwi is the woodcock. Apart from its enormous eyes – which are essential for its crepuscular activity and flight, including nocturnal migration – the woodcock and kiwi are very similar. Both species have a similar lifestyle, probing for worms beneath the soil surface. As long ago as
1600
, Ulysses Aldrovandi tells us in his encyclopaedia of birds that woodcocks find their food by smell. This seems to have been well established since he quotes a poem on bird-catching by Marcus Aurelius Nemianus dating to
ad
280
, which mentions the bird’s enormous nostrils and its capacity to smell worms. Several later authors also refer to the woodcock’s sense of smell, but curiously, and in contrast to many other ornithological facts, they do so without citing or plagiarising earlier writers, suggesting that the woodcock’s sense of smell may have been independently discovered several times. Buffon, for example, quotes William Bowles, who in his book of
1775
,
An Introduction to the Natural History and Physical Geography of Spain
, describes how he watched a woodcock in the royal aviaries probing for worms in damp soil: ‘I did not see it once miss its aim: for this reason, and because it never plunged its bill up to the orifice of the nostrils, I concluded that smell is what directs it in search of its food.’ And then, citing his colleague René-Joseph Hébert, a hunter and naturalist, Buffon adds this: ‘But nature has given, at the extremity of its bill, an additional organ, appropriated to its mode of life; the tip is rather flesh than horn, and appears susceptible to a sort of touch, calculated for detecting prey in the mire.’
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The English ornithologist George Montagu, who dissected many woodcocks and observed one living in his aviaries in the late
1700
s, writes:
Thus when most other land birds are recruiting exhausted nature by sleep, these [woodcock] are rambling through the dark; directed by an exquisite sense of smelling, to those places most likely to produce their natural sustenance; and by a still more exquisite sense of feeling in their long bill, collect their food. . . . The nerves in the bill . . . are numerous, and highly sensible of discrimination by the touch.
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Writing about the senses of birds a century later, John Gurney had this to say:
The investigator has to be cautious not to confuse the organ of scent with that of touch, by means of which some birds feed – e.g. the woodcock. Thus it will be seen what an involved business it is for an experimenter to formulate any trial which appeals to a bird’s sense of smell, and which at the same time excludes sight, hearing and touch.
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When I checked, I was surprised to see that Bang and Cobb
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had obtained an olfactory bulb index of just fifteen for woodcock, which places it in the mid-range rather than close to the top. I wonder if this means that the olfactory bulb is an odd shape, as
3
-D scanning revealed for the kiwi, and that the index is wrong: given the woodcock’s unusually shaped skull, this is a possibility. Of course, the other thing to do is conduct some behavioural studies and put the woodcock through its olfactory paces to see how it compares with the kiwi.
Bernice Wenzel and Betsy Bang put avian olfaction on the academic map, partly through their independent research but also through a chapter of a book they wrote together in the
1970
s that has become the definitive account of the sense of smell in birds.
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Betsy Bang died at Woods Hole in
2003
at the age of ninety-one, and Bernice, now in her eighties, is an emeritus professor at UCLA. In
2009
, two other female pioneers of avian olfaction, Gaby Nevitt and Julie Hagelin, dedicated a symposium to their two predecessors. Bernice told me that she was overwhelmed by this gesture, and remarked on how different it was to the early comments on her research, many of which had questioned why she was even bothering to study smell in birds.
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What was it about the field of avian olfaction, that it should have been so dominated by women? Few other areas of research – except for primate behaviour – have such a preponderance of female researchers. Colleagues I have spoken to told me that as mentors Betsy and Bernice were extremely encouraging and more generous in sharing advice than most male researchers would have been, traits that may have been particularly appealing to younger female zoologists.
In
1980
, with colleagues Richard Elliot and Remey O’Dense, I visited a remote and little-known group of islands, called the Gannet Clusters, some twenty miles off the coast of Labrador. Our goal was to count the seabirds there. This was hardly a trivial task for there were tens of thousands of puffins and guillemots, and only slightly fewer razorbills, plus a few fulmars and kittiwakes (but no gannets – the name of the islands is misleading and its origin a mystery). On our first night, not long after we had settled down to sleep inside our tent, Richard sat bolt upright exclaiming, ‘Leach’s petrel!’
I woke and listened, and, sure enough, outside in the dark I could hear the distinctive gentle purring of a Leach’s storm petrel close by. The reason Richard was so excited was that this was the first record for this tiny, nocturnal seabird on these islands and one of the most northerly records for North America. The next morning we hunted around outside the tent for further signs, and there in the peaty soil was a nesting burrow, just five centimetres in diameter. Richard’s immediate reaction was to drop to his knees, stick his nose into the hole and sniff audibly. ‘Yes!’ he said. ‘It’s Leach’s all right’, for, like other members of the petrel family (which includes the albatrosses and shearwaters), Leach’s petrel has a distinctive musky smell.
Continuing to search, we found several more burrows, and, as luck would have it, inside one of them I found a mummified Leach’s petrel corpse, definitive evidence of their existence. In a somewhat macabre but entirely scientific gesture, I kept the dead bird: it was completely dried out and not in the least bit unpleasant. Years later, back in my office in Sheffield, I had only to sniff the bird to be transported back to the magic of the Gannet Clusters, so strong and so evocative was the bird’s aroma.
Bang and Cobb had not included Leach’s petrel in their comparative study, but they examined ten other petrel species, all but one of which had huge olfactory bulbs. Indeed, ever since the early days of commercial whaling, mariners had noticed how incredibly sensitive albatrosses, petrels and shearwaters appeared to be to the odour of whale offal. In the
1940
s, Loye Miller, professor of biology at the University of California, Los Angeles, conducted some simple but extremely telling experiments involving individually marked black-footed albatrosses – which he refers to as ‘goonies’ – off the west coast of North America.
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Within one hour of bacon fat being poured on to the sea surface, birds were drawn in – Miller estimated from a distance of
32
km. No birds were attracted to paint scum, an equally smelly substance used as a ‘control’. ‘Chumming’ is now used regularly by oceanic twitchers to attract seabirds, the olfactory equivalent of playing a recording of birdsong to attract land birds. The effect is remarkable, as I witnessed off the east coast of New Zealand’s South Island, at Kaikoura: being surrounded by fifteen different species of petrels and albatross just a few metres away counts as one of my best birdwatching experiences.
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Scientists refer to albatrosses, petrels and shearwaters as tubenoses. Despite their obvious link with odour detection, the function of their tube-like nostrils remains a mystery. Different species, which range in size from the
50
-g storm petrels to
8
-kg wandering albatross, feed on krill and squid, and sometimes on whale offal. Finding a decomposing whale carcass by smell might not be all that difficult – the aroma of rotting blubber is one that can stick in human nostrils for hours or days, as I can verify – and even we might not find it too difficult to travel upwind to such a feast. But krill and squid – do they smell strongly enough to allow tubenoses to find them in the vast, featureless ocean? That’s another story.
Gaby Nevitt, mentioned earlier, and a biologist at the University of California at Davis, started out studying how salmon relocate their spawning river after several years at sea. The idea that they might use smell to navigate once seemed preposterous, yet research in the
1950
s showed it to be true.
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Almost as unbelievable is the way albatrosses, flying across vast tracts of the ocean, are able to relocate their breeding colonies, tiny specks of rock in a featureless sea. There is no question that they can do so, but what wasn’t appreciated until the
1990
s was just how far they travelled from their colonies in search of food during the breeding season. Some wonderful pioneering work by French researchers Pierre Jouventin and Henri Weimerskirch showed, by means of what was then new satellite tracking technology, how wandering albatrosses covered thousands of kilometres in search of food, and still unerringly managed to find their breeding island.
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Gaby became interested in
how
albatrosses were able to find food and relocate their colonies so efficiently.