Authors: Tim Birkhead
Birds are different in that their hair cells
are
replaced. Birds also seem to be more tolerant of damage created by loud sounds than we are. This is currently an area of intense research, for if we can establish the mechanisms by which birds replace their hair cells, a cure for human deafness might be found. So far the prize is elusive but in their quest researchers have discovered a great deal about hearing, including its genetic basis.
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Fifth
, imagine what it would be like if our ability to recognise voices on the telephone disappeared each winter. Inconvenient? Yes, given our lifestyle, but birds’ hearing ability really does fluctuate throughout the year.
One of the most remarkable of all ornithological discoveries was the realisation that birds in temperate regions undergo enormous seasonal changes in their internal organs. The most obvious of these involves the gonads. In a male house sparrow, for example, during the winter the testes are tiny, no bigger than a pinhead, but during the breeding season they swell to the size of a baked bean. The human equivalent would be testes the size of apple pips outside the breeding season. Similar seasonal changes occur in females: the oviduct, which is a mere thread of tissue during the winter, becomes a massive, muscular egg-delivery tube during the breeding season.
These enormous effects are triggered by changes in day length, which stimulates the release of hormones from the brain, and in due course from the gonads themselves. The hormones in turn trigger the onset of song in the males. Perhaps the most far-reaching discovery relating to these changes was the finding in the
1970
s that parts of the brain also varied in size across the year. This was totally unexpected because the conventional wisdom was that brain tissue and neurons were ‘fixed’ – what you were born with you had to make do with until the day you died. Exactly the same was thought to be true of birds. The realisation that this was not the case in birds revolutionised and reinvigorated research in neurobiology and song learning, because, among other things, it has the potential to provide a cure for neuro-degenerative diseases like Alzheimer’s.
The centres in the avian brain that control the acquisition and delivery of song in male birds shrink at the end of the breeding season and grow again in the following spring. The brain is expensive to run – in humans it uses about ten times as much energy as any other organ – so, for birds, shutting down those parts not needed at certain times of the year is a sensible energy-saving tactic.
In temperate regions birds typically sing most in the spring; this is when males establish territories, which they defend via song, and when they acquire a partner, which they attract via song. A few temperate birds, like dippers and nuthatches, however, set up their territories in late winter and start singing earlier in the year. The hearing ability of songbirds is most sensitive at the time of year when song is most important.
This makes sense. If song is predominantly a springtime event, it follows that it might be advantageous if birds’ hearing ability is enhanced at this time. Males, for example, need to be able to distinguish territorial neighbours from non-neighbours who will pose more of a threat, and females need to be able to distinguish between potential partners of different quality. Studies of three North American songbirds, the black-capped chickadee, the tufted titmouse and the white-breasted nuthatch,
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show that seasonal changes occur in both sensitivity (the ability to detect sound) and processing (the ability to interpret those sounds). Jeff Lucas, who conducted this research, suggested thinking about this as if these three species were listening to an orchestra:
Chickadees show a broad-band increase in processing in the breeding season, so the orchestra really would sound better to them in the breeding season. Tufted titmice show no change in processing but they do show a change in sensitivity, so the orchestra wouldn’t sound any better, but it would sound louder. White-breasted nuthatches show a narrow-band increase, increasing processing of
2
kHz tones. So for them, the orchestra would sound better when the orchestra was playing a C(
7
) or B(
6
), but the timbre of the instruments wouldn’t be more enjoyable.
You might be surprised to learn that humans also experience predictable, regular changes in their hearing ability – or at least females do. Oestrogen is the key: when oestrogen levels are high, a man’s voice sounds richer. The effect is so subtle that most women are unaware of it, but, even so, it may play a vital part in mate choice.
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The sounds birds make vary from the deep booming of a bittern to the high-pitched tinkle of goldcrests and kinglets. The frequency (or pitch) of sound is measured in hertz – the number of sound waves going by at any one time, usually expressed in terms of thousands of hertz, or kilohertz (kHz). A bittern’s boom clocks in at around
200
cycles per second, or
200
hertz (Hz), or
0
.
2
kHz. In contrast, the goldcrest sings at a frequency of around
9
kHz. These two sounds cover pretty much the entire span of sound frequencies uttered by birds. A canary, a typical songbird, sings at a frequency of about
2
or
3
kHz. As we might expect, the frequency of the sounds birds make matches pretty closely what they can hear, or, to be more precise, the frequencies at which they are most sensitive. Humans hear best at about
4
kHz, but we can hear sounds as low as
2
kHz and as high as
20
kHz – when we are young. Birds are most sensitive to sounds in the region of
2
or
3
kHz and most are capable of hearing between
0
.
5
kHz and
6
kHz.
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What humans and birds can hear is usually illustrated by means of an ‘audiogram’ or ‘audibility curve’. This is a visual representation of the quietest sound an animal can hear at different frequencies throughout its range of hearing. It comprises a plot of frequency (in kHz) along the horizontal axis and loudness up the vertical axis. The fact that the graphs are U-shaped indicates that for both birds and humans the quietest sounds we can hear are those in the middle frequency range; for us to detect lower or higher frequency sounds they need to be louder. The audiograms of humans and most birds are rather similar, although humans have better hearing at mid to low frequencies. Owls have better hearing than most other birds (and humans) in that they can detect much quieter sounds, and songbirds have better hearing at high frequencies than other birds. Although only a few species have been tested, it seems likely that bitterns are most sensitive to low-frequency sounds, and goldcrests to high-frequency sounds.
Birds use their hearing to detect potential predators, to find food and to identify members of their own and other species. To be able to do all these things they must be able to identify where a particular sound is coming from; distinguish meaningful sounds from ‘background’ noise created by other birds and the environment; and discriminate between similar sounds, much as we can recognise the voices of different people.
Imagine you are alone in the dark in an unfamiliar place, and unsure about how safe you are. Suddenly there’s a strange sound, a footstep on gravel perhaps . . . but you cannot tell which direction it has come from. Is it behind you, in front, or off to one side? Knowing exactly where a potentially dangerous sound comes from is crucial if you are to prepare yourself for a quick escape. Being unable to localise a sound – especially in a dangerous situation – is one of the most disquieting of experiences. We are normally pretty good at localising sound and, of course, when it isn’t dark we use our eyesight to check and confirm the source of sounds.
We pinpoint sound by unconsciously comparing when it reaches each of our ears. Our heads are large enough, and our ears far enough apart, for a sound to reach our ears at slightly different times. In cool, dry air at sea level sound travels at
340
m per second, and that means that the maximum time difference in a sound reaching our two ears is
0
.
5
millisecond (one millisecond is
1
/
1000
th of a second). If we detect no difference in the time when sound reaches our ears we assume that the sound is coming from directly in front of (or directly behind) us. Birds’ heads are smaller than ours, and some, like hummingbirds, goldcrests and kinglets, have particularly tiny heads, which means that, everything being equal, they would have difficulty localising sound. Indeed, with just one centimetre between the ears, the difference in time of arrival of sound to the two ears would be less than
35
µm seconds (one microsecond (µm) is
1
/
1
,
000
,
000
th of a second). Small birds get around this problem in two ways: first, by moving their heads more than we do, effectively increasing their size, enabling them to detect time differences; and secondly, by comparing the tiny difference in the
volume
of noise reaching each ear.
The type of sound also influences how easy it is to identify its origin and birds have exploited this in the way they communicate. It has long been known that when birds like thrushes or chickadees spot a predator, such as a hawk, flying overhead, they utter a high-pitched ‘seep’ call. Their high frequency (8 kHz) may render these calls inaudible to the predator (given that most predators are larger than their prey and that larger birds hear higher frequency sounds less well). The structure of these warning calls, which start and end imperceptibly and thus make them especially hard to locate, is exactly what you might expect from a signal where the signaller does not want to draw attention to itself. In contrast, when those same species spot a roosting owl they utter a completely different type of call, characterised by a harsh, abrupt chattering: a much more easily located sound. That’s the whole point. When songbirds discover a non-hunting predator, they want to attract attention to it, recruiting songbirds to join in the mobbing and help drive the predator away. One of the interesting aspects of these two types of call is that they sound very similar across a range of species.
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The great French naturalist Georges-Louis Leclerc, better known as the Comte de Buffon, wrote this about owls in his history of birds of the mid-
1700
s: ‘[their] sense of hearing . . . appears to be superior to that of other birds, and perhaps to that of every other animal; for the drum of the ear is proportionately larger than in the quadrupeds, and besides they can open and shut this organ at pleasure, a power possessed by no other animal’. Buffon is referring here to the enormous ear openings of certain owls, which in some species span almost the entire height of the skull, as my experience with a great grey owl demonstrated.
The great grey owl’s greatness is partly an illusion; its enormous size is a consequence of its fabulous fluffy plumage. In reality, it is a midget in a vast, downy coat. The captive great grey owl whose ears I examined lay in the arms of his owner, looking up at me like a wide-eyed baby. As I carefully felt around behind his eyes, I couldn’t believe the depth of the feathers and the smallness of its skull. Fully ten centimetres of feather created the bird’s gigantic head. Around each eye the facial discs were bounded by a line of tawny feathers, conveniently marking the rear edge of the crevice in which each ear opening lay. Gently lifting the feathers forward on one side, the ear opening was revealed. It was huge – some four centimetres from top to bottom – and bewilderingly complex; the opening was covered by a moveable flap and bounded by unusual feathers. At the front edge, running from top and bottom, was a pallisade of rigid broad-shafted feathers, while the rear edge of the flap was lined with delicate filamentous feathers, behind which was a dense baffle of feathers that reminded me of a phalanx of Roman swords. The opening itself was huge, and contained lots of loose bits of skin, a bit like a grubby human ear. I then turned to the other side, and even though I knew that this species’ ears are asymmetric, the degree of asymmetry astounded me. Looking at the bird face-on, the right ear lay below the level of the eye at seven o’clock; the left ear was at two o’clock. The bird’s enormous head feathers are there simply to support the facial discs, gigantic reflectors whose purpose is to direct sound towards the ear openings.
One afternoon in the
1940
s Clarence Tryon came across a great grey owl hunting in the Montana woods. The bird was perched on the end of a branch about four metres above the ground:
Within a few minutes the owl made three swoops from its perch, apparently without catching anything. On the fourth swoop it hit the ground with considerable force and . . . flew away with a dead pocket gopher in its talons. The gopher was probably heard digging by the owl, which gave every indication of listening to some sound before swooping. Inspection of the spot . . . revealed that the owl had apparently broken through the thin roof of one of the feeding runways of the gopher’s burrow.
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