Authors: Tim Birkhead
Spelled out like this, the study of avian hearing seems straightforward, but our understanding of hearing in birds still falls far short of what we know about vision. This is partly because birds have no external ears and because (as in most vertebrate animals) the most important part of the ear is deeply embedded in the bones of the skull. But perhaps most significant of all, there has simply been much less interest in hearing than in vision. At the time that John Ray and Francis Willughby were writing their ground-breaking
Ornithology
in the
1670
s, almost nothing was known about the structure of ears in birds. Even the great anatomists of the seventeenth, eighteenth and nineteenth centuries found dissection of the inner ear a major challenge.
The first serious investigations of the human ear were undertaken by Italian anatomists in the
1500
s and
1600
s. Gabriel Fallopius (
1523
–
62
) – after whom the Fallopian tube in the reproductive system of female mammals is named – discovered the semi-circular canals in the inner ear in
1561
. Batholomaeus Eustachius (
1524
–
74
) – after whom the Eustachian tube is named – discovered the middle ear in
1563
(the ancient Greeks already knew of the cochlea). Giulio Casserius (
1552
?–
1616
) discovered the semi-circular canals in the inner ear in pike in
1660
, and found that birds (i.e. the goose) have only a single bone (rather than three) in the middle ear. The French anatomist Claude Perrault was the first to describe the inner ear of any bird. His discovery was the result of dissecting a currasow, a turkey-like bird from tropical South America, which had died in the Zoological Gardens in Paris.
8
That was the descriptive phase. Discovering how the ear actually worked would take rather longer. Even by the
1940
s when Jerry Pumphrey (
1906
–
67
), a lecturer at Cambridge University, wrote a short but seminal overview of the senses of birds in
1948
, he summed up by saying: ‘It will have been noted that there is a sufficient body of knowledge of the avian eye to permit of intelligent speculation about its performance and the part it plays in avian behaviour. This is far less true of the ear . . . [and avian hearing offers] a most promising and unjustly neglected field for experiment and observation.’
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Since the
1940
s there has been increasing interest in what birds can hear, driven largely by spectacular advances in the study of birdsong, that has served as a general model for learning and for understanding human speech acquisition. It was once thought that children were able to learn any language they were exposed to because they started life as a blank slate. The study of birdsong dispelled this idea by demonstrating that, although young birds are capable of learning almost any song they hear, they actually possess a genetic template that dictates both what they learn and how they sing. The study of the way birds acquire their song has provided the most compelling evidence that there is no nature-nurture divide: genes and learning are intimately interconnected in both birds and babies. It was through the study of the neurobiology of birdsong that we began to realise the huge potential for the human brain to reorganise itself and form new connections in response to particular inputs.
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In both birds and mammals, the latter including ourselves, the ear consists of three regions: outer, middle and inner. The outer ear comprises the auditory canal (and in most mammals an external ear). The middle ear consists of the eardrum and either one or three middle ear bones. The inner ear comprises the fluid-filled cochlea. Sound (technically, acoustic pressure) is transmitted from the environment through the outer ear, down the auditory canal and on to the eardrum, then via the tiny ear bones to the inner ear, causing the fluid inside it to vibrate. The vibrations cause microscopic hair cells in the cochlea to send a signal to the auditory nerve and then on to the brain which decodes the message and interprets it as ‘sound’.
There are four main differences between human ears and those of birds.
First
and most obvious is the absence in birds of an external ear, or ‘pinna’ – the skin-covered bit of cartilage we call our ear.
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It isn’t always obvious where a bird’s ears are because, in all but a few species, they are covered with feathers known as the ear coverts. The ear opening lies behind and slightly below the eye, in roughly the same position as our own: it is obvious if you look at the sparsely feathered head of a kiwi or an ostrich, or the naked head of New World vultures, like the condor, or the aptly named bare-necked fruit crow.
12
In birds with feathered heads the ear coverts differ from adjacent feathers by being rather shiny, a feature that may ensure a smooth flow of air over the ears while the bird is in flight, or that may facilitate hearing by filtering out the sound of the wind passing over the ears.
13
In seabirds the feathers covering the auditory canal prevent water getting into the ear while they are diving, a potentially serious problem for species like the king penguin which dives to several hundred metres, where the pressure is considerable. In fact, the ears of king penguins exhibit a number of anatomical and physiological adaptations to protect them from the problems associated with deep-sea diving.
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The kiwi would clearly benefit from some additional protection of its auditory canal, for several of those I handled in New Zealand had ticks lodged inside their ear openings! I later wondered whether these ticks might be an unpleasant by-product of New Zealand’s relatively recent invasion by man’s domestic animals and their parasites, but it appears that the kiwi ticks I saw are native to New Zealand and an inconvenience that kiwis have been coping with for a long time.
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In
1713
William Derham, a colleague of John Ray, noted that the ‘outer shell or pinna is missing in birds, because it would impede their passage in air’. For Derham the perfect match between an organism’s design (in this case the absence of a pinna) and its lifestyle (flight) was evidence of God’s wisdom. In today’s terminology, we would simply say that this was an adaptation for flight. Whether the lack of a pinna really is an adaptation for flight is unclear, for the reptilian ancestors of birds had no pinna, so it is possible that the evolution of the pinna in mammals was an adaptation to improve hearing in a group that was primarily nocturnal. It is obvious that the presence of a pinna does not prevent flight, for many bat species have enormous external ears (yes, I know, they don’t fly as swiftly as birds). The other way of looking at this is to consider the fact that none of the fifteen families of flightless birds has an external ear; nor did the most primitive birds have external ears. My guess, therefore, is that the lack of a pinna is a consequence of the birds’ ancestry rather than an adaptation for flight.
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The value of our own pinna is all too apparent. By cupping our hand round our ear we increase the effective size of the pinna and the effect is dramatic. In much the same way, in recording birdsong (or anything else) a parabolic reflector on a microphone increases the amount of sound gathered. The lack of a pinna must potentially have a marked effect, not only on how well birds can hear, but also on their ability to pinpoint the source of a particular sound – although, as will become clear, birds have evolved other ways of doing this.
A
second
difference between birds and mammals is that mammals, including humans, have three tiny bones in the middle ear, whereas birds have only a single bone, as do reptiles, again reflecting their evolutionary history.
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Third
is the inner ear – the business part of the ear. It is embedded in bone, for protection, and comprises the semi-circular canals (concerned with balance, which we won’t discuss here) and the cochlea. In mammals the cochlea is a spiral structure (
cochlea
means snail in Latin), whereas in birds the cochlea is straight or slightly curved like a banana. Inside the fluid-filled cochlea lies a membrane – the basilar membrane – on which there are lots of tiny hair cells. Sensitive to any kind of vibration, the hair cells work like this. A sound occurs, producing a pressure wave which travels down the auditory canal in the external ear until it hits the eardrum. This now causes the bone(s) of the middle ear to vibrate, which in turn transmits a vibration to the beginning of the inner ear and then to the cochlea. A pressure wave occurs inside the fluid of the cochlea causing the hair of the hair cells to bend, firing off a signal to the brain. Sounds of different frequencies – which I’ll explain in a moment – reach different parts of the cochlea, stimulating different hair cells. High-frequency sounds cause the base of the basilar membrane to vibrate, and low-frequency sounds cause the far end of the membrane to vibrate.
The coiling of the cochlea in mammals allows a greater length to be packed into a small space, and, indeed, the mammalian cochlea is longer than that of most birds: about seven millimetres in mice and just two millimetres long in the similarly sized canary. One possible explanation for this difference is that a coiled cochlea enhances the detection of the low-frequency sounds used by many large mammals.
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One of the pioneers of the avian inner ear was the extraordinarily talented Swedish scientist Gustav Retzius (
1842
–
1919
). By marrying Anna Hierta, the daughter of a newspaper magnate, Retzius gained financial independence and almost complete freedom to pursue his studies, which ranged from the design of spermatozoa to poetry and anthropology. It is his work on the nervous system and the structure of the inner ear, however, for which he is best known. Retzius was one of the first to provide comparative information and beautiful illustrations of the inner ear of a range of animal species, including several birds. Poor Reztius! Nominated no fewer than twelve times for a Nobel Prize, he never quite made it to Stockholm. When Jerry Pumphrey later took stock of what was known about the senses of birds in the
1940
s, he put Retzius’s detailed descriptions to good use, speculating about the hearing ability of birds by dividing them into those whose cochlea was ‘conspicuously long’ (eagle owl); long (thrushes and pigeons); average (lapwing, woodcock and nutcracker); short (chicken); and very short (goose, sea eagle). Pumphrey wrote: ‘If we exclude the owl, we can perhaps imagine a correlation between the length of the cochlea and musical ability.’ He was not far off. We now know, first, that the ears and hearing of owls differ from those of most other birds, and, second, that if we interpret ‘musicality’ as its reciprocal, ‘the ability to detect and distinguish sounds’, then Pumphrey’s speculation is remarkably accurate.
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With the benefit of more information both on cochlea size and hearing ability, it is now apparent that the length of the cochlea (specifically, the basilar membrane inside it) is a reasonable index of a bird’s sensitivity to sound. As with other organs (brain, heart, spleen), larger birds have a larger cochlea, but, in addition, larger birds are also particularly sensitive to low-frequency sounds, and small birds more sensitive to high-frequency sounds.
Let’s put some numbers on this, so we can see the pattern – we’ll use just five species: the zebra finch (which weighs around
15
g) has a basilar membrane about
1
.
6
mm long; budgerigar (
40
g),
2
.
1
mm; pigeon (
500
g),
3
.
1
mm; gannet (
2
.
5
kg),
4
.
4
mm; and emu (
60
kg),
5
.
5
mm. The existence of this relationship means that researchers can predict how sensitive a bird is to particular sounds from the length of its cochlea. Indeed, biologists have recently done just that, using the dimensions of the inner ear of the extinct Archaeopteryx
–
derived from fMRI imaging of the fossil skull – to suggest that its hearing was probably much like that of a present-day emu – that is, rather poor.
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Owls are the exceptions. For their body size, their cochlea is, relatively, enormous and contains very large numbers of hair cells. The barn owl, for example, which weighs around
370
g, has a relatively enormous basilar membrane at nine millimetres, containing some
16
,
300
hair cells – more than three times what we would expect from its body size, and providing exceptionally good hearing.
Fourth
, the hair cells within the cochlea of birds are replaced on a regular basis, whereas those of mammals are not. Had the corncrake that called so close to my ear remained where it was and continued to call, and had I been silly enough to continue to lie there, the volume of its call would eventually have started to damage my ear and impair my hearing – irreparably. The hair cells responsible for detecting sound in the inner ear are so sophisticated and so delicate that they are easily damaged by too much noise. Ours is a sensitive system. It is so sensitive, in fact, that any further improvement and we would hear the sound of our own blood rushing through our heads. Rock musicians and their fans know to their cost the long-term damage to the ear caused by too much noise. Damaged hair cells are not replaced. This is also why, as we get older, we find it increasingly difficult to detect high-frequency sounds. Many birdwatchers over fifty that I know are oblivious to the goldcrest’s high-pitched song, or in the Americas are unable to hear the songs of species like the black-throated green warbler and the blackburnian warbler. And it is not just ageing rockers: Gilbert White, author of
The Natural History of Selborne
(
1789
), at the relatively young age of fifty-four, bemoaned how: ‘Frequent returns of deafness incommode me sadly, and half disqualify me for a naturalist.’
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