Authors: Tim Birkhead
John Weir’s observations were verified by the eminent entomologist Henry Stainton, who told Alfred Wallace in
1867
how, after ‘mothing’ [i.e. moth trapping], he was accustomed to throwing all the common species to his poultry. On one occasion a brood of young turkeys greedily consumed the moths he threw to them, but ‘among them was one common white moth. One of the young turkeys took this in his beak, shook his head and threw it down again, another ran to seize it and did the same, and so on, the whole brood in succession rejected it.’ The white moth, the ermine, was the adult of the larvae Weir’s birds had found so unpalatable.
The pioneering efforts of Wallace, Weir and Stainton have since been amply confirmed by more recent researchers, including Christer Wiklund, a behavioural ecologist (and Bob Dylan aficionado) from the University of Stockholm in Sweden. In the
1980
s Wiklund and colleagues used:
naive individuals of four different bird species, great tit, blue tit, starling and common quail, and showed that it seems a general phenomenon that birds do have a sense of taste and release distasteful and aposematic [warningly coloured] insects more or less immediately after taking them in their beak (and without harming the insect – presumably not out of sentimentality (or generosity) but rather so as not to get all that nasty stuff in their mouth).
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All these observations provide clear evidence that, using their sense of taste and vision, birds associate the appearance of their prey with its palatability. Warning colouration (also known as ‘aposematic’ colouration) has since been found in a wide range of animals, including insects, fishes and amphibia, and, as we’ll see, in birds as well.
Even by Darwin’s day, the issue of whether birds possess a sense of taste had long been debated. On the one hand, the hard beak of birds is so different from our own soft, sensuous mouth that it is difficult to imagine birds of any kind being able to taste much. The human mouth is a remarkable structure; soft and moist, with a large, fleshy tongue acutely sensitive to gustatory, thermal and tactile sensations, both while eating and during erotic kissing. The difference between our own mouth and that of birds could hardly be greater: the bird’s beak is hard, often sharply pointed, and the inside of the mouth itself looks distinctly unsensuous. In most species the tongue is a hard, understated, arrow-like structure, lying within the lower jaw, and at a first sight appears to offer minimal purchase for many taste buds. Also, because birds lack teeth and do not chew their food but swallow it directly, the impression is that they have no sense of taste. Add to all that the fact that a bird’s beak limits any facial expression associated with taste – pleasure or disgust – it is hardly surprising that the general impression is that birds have little or no sense of taste.
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Taste buds in humans were first described in the nineteenth century. Long before that, though, people had been fascinated by taste. Aristotle believed that the sensation of taste was transmitted from the tongue via the bloodstream to the heart and liver, which, in the fourth century
bc
, was considered both the seat of the soul and the source of all sense perception. The Roman anatomist Claudius Galen (
ad
129
–
201
) later debunked Aristotle’s idea by tracing the nerves in the tongue to their origin in the base of the brain. The discovery of taste ‘papillae’ (nipple-like structures) on the human tongue by the Italian anatomist Lorenzo Bellini in
1665
was almost certainly inspired by Marco Malpighi’s (
1628
–
95
) discovery of papillae on the tongue of an ox the previous year. Bellini’s description is wonderfully enthusiastic: ‘Many papillae are evident, I might say innumerable and the appearance is so elegant . . .’ He describes them as appearing like ‘innumerable mushrooms emerging between fine, densely standing blades of grass . . .’ True taste buds – microscopic nerve endings – were not discovered for another two centuries, in frogs and fishes and then in humans, in the
1850
s and
1860
s. The fact that they were associated with the papillae on the tongue strongly suggested they were involved with taste.
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The Scottish naturalist James Rennie, writing in
1835
in his book
The Faculties of Birds
, says that while ‘some birds at least are endowed with the faculty of taste’ this is ‘expressly or partially denied by certain authors distinguished for accuracy of observation, such as Colonel Montagu and M. Blumenbach because in several species the tongue is “horny, stiff, not supplied with nerves, and consequently unfit for an organ of taste”’. But, as Rennie perceptively points out, ‘it does not follow, that because the tongue in most other animals is the chief organ of taste, that birds . . . cannot discriminate their food by taste, since other parts of the mouth may perform this office.’
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Rennie was almost alone at that time in imagining birds to have a sense of taste, but a moment’s reflection makes it improbable that birds could function without one. Taste is essential for discriminating between edible and non-edible (or dangerous) food items. Nonetheless, sixty years later, writing in his massive
Dictionary of Birds
, Alfred Newton says:
The tongue is commonly supposed to be the chief organ of taste; but it is certainly not so in birds . . . It is true that the tongue of birds is very rich in sensory bodies . . . which are terminal organs of the sensory nerves; but these corpuscles are frequently embedded deeply in and beneath the impervious horny sheath, so that they cannot serve as organs of taste though they may act as organs of touch . . .
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Of course, taste buds were eventually found in birds – how could birds not have had a sense of taste? – and for a while the definitive overview of the field was one published in
1946
by Charles Moore and Rush Elliot. According to them, the few taste buds birds possessed were restricted to the tongue, a view that subsequent researchers accepted without question.
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Fast-forward to the
1970
s, and the University of Leiden in the Netherlands, where Herman Berkhoudt is a young PhD student. His research topic is the microscopic structures associated with the sense of touch in the beaks of birds. One day in January
1974
, while supervising two students engaged in the familiar anatomist’s exercise of constructing a
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-D image from a series of thin two-dimensional sections – in this case of a duck’s head – he made an exciting discovery.
Berkhoudt had enlarged the sections they were looking at by projecting them on to a table so that they could be easily traced, and, as one particular image appeared, he noticed something unusual. At the very tip of the duck’s beak there were ‘strange, ovoid clusters of cells leading to a pore inside the beak tip’. He told me: ‘At that moment I realised that I [had] found taste buds. It gave me quite a dose of adrenalin!’ This was new. All previous studies of birds’ taste buds said that they occurred only on the tongue or towards the back of the mouth.
Berkhoudt’s discovery diverted him from his original research topic of touch to taste. A few years earlier some colleagues in his own department had shown that mallard ducks possess a remarkable ability to discriminate between ordinary peas (which they loved to eat) and peas made to taste unpleasant, simply by grasping them with the bill tip. The ducks never got it wrong; they could always pick out the palatable peas. Figuring out precisely how they did this became the main objective of Berkhoudt’s studies.
Over the next few years, his meticulous microscopic examination of the mallard’s mouth revealed a total of some four hundred taste buds in the upper and lower jaws, with none – rather oddly, given previous studies – on the tongue itself. The taste buds occurred in five discrete clusters, four in the upper and one in the lower jaw. The next stage was to see why the taste buds were positioned where they were. To investigate this, Berkhoudt used an ingenious technique of high-speed X-ray filming of ducks picking up and swallowing food. This revealed that the points where the bird grasps food (the bill tip), and where food comes in contact with the inside of the mouth as it is moved towards the throat, coincides exactly with the position of the taste buds, providing a clear explanation for the birds’ ability to distinguish true peas from artificially unpleasant-tasting ones.
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An important part of any PhD study is the need to be thoroughly familiar with what has been published previously on one’s particular research topic. This is an essential part of scholarship, without which it is all too easy to end up reinventing the wheel. In addition, knowing what earlier researchers have done enables one to build on their discoveries and avoid the pitfalls identified by their work. Sometimes, though, if the earlier literature is in another language, it can remain inaccessible. Fluent in German, Herman Berkhoudt was amazed to find a series of papers from the first decade of the twentieth century that had been completely overlooked by all previous taste researchers. The first of the unknown papers was by Eugen Botezat at the University of Czernowitz in the former East Germany, who found taste buds on the tongues of young sparrows in
1904
. The second was Wolfgang Bath, at the University of Berlin, who confirmed the presence of taste buds in birds in
1906
and – significantly – showed that they were not confined to the tongue, as Botezat had said.
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A little disappointed that his own results were not quite as novel as he first thought, Berkhoudt was nonetheless intrigued by what these German anatomists had found. He also realised that his own discoveries opened up some exciting research opportunities, and he made good use of them. Employing new, efficient ways of finding and counting taste buds, Berkhoudt plotted their distribution in the mouths of ducks. Because earlier researchers were unaware of Botezat’s and Bath’s papers, and persisted in focusing their efforts on the tongue, they had seriously underestimated the total number of taste buds that birds possessed.
We now know that the chicken has
300
and, from Berkhoudt’s work, that the mallard has about
400
; Japanese quail have just
60
and the African grey parrot has at least
300
–
400
. But apart from these few species, we still have remarkably little information on the total number of taste buds possessed by birds. If you look at textbooks dealing with the senses, the numbers of taste buds for a variety of birds are listed, including the blue tit, bullfinch, ringed dove, European starling and an unknown species of parrot. Yet, as far as I can tell, these are all underestimations since they refer only to parts of the mouth.
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In most bird species the taste buds are located at the base of the tongue, in the palate and towards the back of the throat. Since saliva (or, at least, moisture) is crucial for the perception of taste, many taste buds are, not surprisingly, located near the openings of the salivary glands. Based on the limited amount of information available, birds have relatively few taste buds compared with humans (
10
,
000
), rats (
1
,
265
), the hamster (
723
) and a species of catfish (
100
,
000
).
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Despite the general assumption that there is a correlation between the amount of sensory tissue and how developed that particular sense is, the actual number of taste buds may not tell us very much about what birds can actually taste or how well they can discriminate between different tastes.
The ability of birds to distinguish different tastes was investigated in the
1920
s by the scientist Bernhard Rensch and the birdkeeper Rudolf Neunzig. They screened sixty species of birds for their taste perception, simply by presenting birds with a single water container dosed with various chemicals to create the four main taste stimuli – salt, sour, bitter and sweet – that humans respond to. The birds’ water consumption was compared with a ‘control’ group of birds provided with pure water. In later studies the experimental design was improved and the same birds were given two water containers, one in which the test substance had been dissolved, the other containing pure water. Preference for one or the other was taken as evidence that birds could taste the difference between the two containers.
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