THE SCENE: Dawn in a sun-kissed country garden. A soft breeze stirs the dew
on the rose petals. As the first light washes over the eastern horizon, hundreds
of birds strike up a chorus, their tiny bodies filling the air with fortissimo
melodies.
Cut! This is a science magazine, not an over-the-top travelogue, and we need
go no further than those warbling warblers to find a research question worth
pondering, namely, how do those little birds produce such big, beautiful songs?
What instrument can craft such music? You鈥檇 think scientists would have figured
that out long ago. But as recently as a decade ago, biologists could offer
little more than guesses about what goes on in a bird鈥檚 throat as it shapes its
song.
But over the past few years researchers have enticed birds to sing with
fibreoptic scopes down their throats, with their beaks immobilised and even in a
helium-oxygen atmosphere. They have measured birds鈥� breathing and the activity
of their throat muscles during song. And they have shown how one group of birds,
the songbirds, exploits a feature that human singers can only dream
about鈥攖wo voice boxes, which means that a bird can do two different things
at once with its throat, even sing a duet with itself.
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鈥淚t鈥檚 a very versatile instrument,鈥� says Jeffrey Podos, an evolutionary
behaviourist at the University of Arizona in Tucson. 鈥淪ongbirds hit on something
big about 60 million years ago when they first evolved.鈥� But even today, the
experts can鈥檛 answer some basic questions, such as how birds can sing so
loudly.
To understand why progress has been so slow, you have only to look for a
bird鈥檚 syrinx, its vocal organ. Unlike the larynx of mammals, which sits in the
neck where researchers can reach it easily, the syrinx is buried deep in the
body. Birds do not breathe like mammals, but have air sacs that act like
bellows, pumping air through the lungs. Enclosed by one of these sacs, bound in
a tangle of muscle near the heart, is the nut-shaped syrinx. For a thrush, it鈥檚
about the size of a baby pea.
In ducks, chickens, parrots and other relatively primitive birds, the syrinx
sits in the windpipe just above where it branches into the bronchi that serve
the two lungs. But in songbirds such as warblers, larks and sparrows you鈥檒l see
a double structure that sits a little lower still, with one part in each of the
two bronchi (see Diagram).
The problem for avian anatomists is that its position makes the syrinx
virtually impossible to watch in action. For decades, researchers had to make do
with indirect approaches such as cutting this or that muscle and waiting to see
what effect this had on the bird鈥檚 song.
Duet for one
But in 1990 Roderick Suthers, a physiologist at Indiana University in
Bloomington, hit on a novel approach. He surgically implanted tiny devices to
measure airflow in the bronchi of two species of North American songbirds, the
grey catbird and the brown thrasher. When the birds resumed singing a few days
later, he could tell exactly which notes came from each of their two voices.
Since then, similar experiments by Suthers and his colleagues have shown that
the paired syrinx gives songbirds a varied bag of tricks for building complex
songs. Some birds, such as the thrasher, sing a true duet in which both voices
sound at the same time to add harmonic complexity. One side might sing a rising
note while the other sings a falling note, for example. Others, such as the
brown cowbird, sing rapid-fire bursts in which the two sides alternate notes, a
strategy that may give each side time to prepare its next note without ragged
transitions.
In many birds, the two sides act like the woofer and tweeter of a
loudspeaker, with the left side specialising in lower notes and the right side
in higher ones. One virtuoso performer, the cardinal, sings a note that sweeps
smoothly upward from about 1 kilohertz to 7 kilohertz, like the first note in a
wolf whistle. At about 3.5 kilohertz, the sound switches seamlessly from left to
right (see Diagram). Unlike speakers, however, a songbird鈥檚 woofer and
tweeter don鈥檛 differ much in size or construction. 鈥淵ou don鈥檛 see obvious
differences, but that doesn鈥檛 mean there aren鈥檛 some subtle ones,鈥� says Suthers.
Much of the specialisation could be accounted for by differences in muscular
force applied to the two sides, he speculates.
Canaries use their double syrinx in yet another way. Suthers found that they
sing through the left side and inhale through the right. Such a strategy is
possible because bird lungs interconnect so that a one-sided inhalation can fill
both lungs. This division of labour, Suther reckons, may help the birds to dash
off long runs containing as many as 30 鈥渟yllables鈥�, or short sound segments, per
second. To avoid running out of air, Suthers has found, singing canaries sneak a
quick breath after every syllable.
Speed, it seems, may be of the essence. One recent study found that female
canaries prefer males with faster songs. Males of other species may feel similar
pressure, says Podos. He tried to get swamp sparrows to sing faster by taping
wild songs and editing out the natural breaths between syllables. He then used
these breathless songs鈥攚hich sounded like the avian equivalent of 鈥渇ine
print鈥� in radio adverts鈥攖o teach young swamp sparrows that had never heard
a normal song. The birds did their best to copy, but couldn鈥檛 keep up for more
than a few syllables before stopping as if to catch their breath. 鈥淓ven a
relatively minor increase in trill rate seems to cause a backlash in
performance,鈥� says Podos. 鈥淭hat suggests that songs in the wild might already be
at the edge of what males can do.鈥�
Even as researchers began to understand how songbirds use the two halves of
their syrinx, though, they remained unsure of how either actually produced its
sound. For years, they guessed that birds either whistled like a kettle by
forcing air through a narrow passage in the syrinx, or buzzed like a kazoo by
vibrating the thin tympaniform membrane that lies flat against the side of each
air passage. Then, two years ago, Franz Goller of the University of Utah in Salt
Lake City and Ole Larsen of Odense University in Denmark managed to feed a
spaghetti-like fibreoptic scope down a songbird鈥檚 windpipe and watch its syrinx
as it sang. 鈥淲e had always felt that if anybody could find a way to do that and
still get the bird to sing鈥攚hich blows my mind鈥攖hat was the way to
handle it. And he did,鈥� says Abbot Gaunt, a morphologist, now retired, from Ohio
State University, who proposed the whistle hypothesis many years ago.
To their surprise, Goller and Larsen saw that the syrinx works not like a
kazoo or whistle, but much like the human voice. During song, muscles pull two
heavy folds of tissue鈥攖he internal and external labia鈥攊nto the
airway. Here, outrushing air sets them vibrating, just as happens with human
vocal cords. The kazoo-like membrane doesn鈥檛 affect sound much at all鈥攚hen
they destroyed it surgically, pitch and volume changed only slightly.
From birds to humans
Still, doubt remain. Goller and Larsen lacked a stroboscopic camera to see
the heavy folds vibrating during the song. And in a later study that did use
such a camera, Michale Fee of Lucent Technologies鈥� Bell Laboratories in Murray
Hill, New Jersey, saw only one of the two labia vibrating, along with the
kazoo-like membrane. Fee, however, did not study live birds but the excised
syrinx of a zebra finch, which lacked normal muscle tension.
Though this debate may seem academic, says Fee, there鈥檚 actually more at
stake than that. 鈥淚 think that by studying the syrinx we can learn something
about how the human vocal apparatus works,鈥� he says. Efforts to mimic human
speech with technology have not worked well, he argues. This is due, at least in
part, to our lack of understanding of how vocal apparatus works.
Fee and his colleagues also found an intriguing hint that the syrinx may run
on autopilot for at least part of a bird鈥檚 song. A live zebra finch鈥檚 song
includes points at which the sound changes abruptly from a pure tone to a noisy
buzz and back again鈥攁 hallmark of a system on the edge of chaos. Fee鈥檚
excised syrinx exhibited the same sudden transitions as he forced air through it
at gradually increasing speeds. This suggested that simple changes in airflow,
not delicate orchestration by the brain, may account for some of the richness of
zebra finch song. 鈥淭here鈥檚 a lot of structure in the song that seems to be
easily explained by the mechanics of the syrinx rather than by direct neural
control,鈥� says Fee.
If the syrinx is like the mouthpiece of a trumpet, a bird鈥檚 throat and mouth
play the parts of the tubing, valves and bell. Resonances here modify the
original sound enormously as it passes through. The effect is easy to hear in
humans, where the throat, mouth and lips form all the various vowel and
consonant sounds of speech, as well as many of the differences in timbre that
make every person鈥檚 voice unique.
It also explains why someone who talks after breathing in helium sounds like
a munchkin. Less dense than air, helium conducts sound faster and emphasises
resonances in the vocal tract at pitches that are higher than normal, even
though the frequency of vibration of the vocal cords changes very little.
Something similar, though less dramatic, happens with birds. More than a
decade ago, ethologist Stephen Nowicki, who is now at Duke University in Durham,
North Carolina, immersed members of nine songbird species in a helium-rich
atmosphere and recorded their songs. In every case, he recorded high-frequency
overtones鈥攚hich led to a squeakier sound鈥攖hat were absent when the
birds sang in air. This led him to suggest that the upper vocal tract acts as a
filter, helping to produce relatively pure tones by amplifying some pitches
generated by the syrinx and not others.
But since many birds鈥� songs leap about from octave to octave, they must
constantly adjust the filter to let the right pitches through. When Nowicki and
his colleagues filmed sparrows singing, they found that the birds opened their
beaks wider for high notes, thus shortening their vocal tract and making it
resonate at a higher frequency.
In a later experiment, which has yet to be published, researchers in
Nowicki鈥檚 lab immobilised sparrows鈥� beaks at a fixed gape by clamping them for
brief periods to a 鈥渂ite block鈥�. 鈥淎fter several days of training, you do get the
birds to actually sing with their beaks clamped,鈥� says Podos, who was then
Nowicki鈥檚 student. Sure enough, those birds sing squeakier songs with more
overtones.
As you might expect, the complex coordination needed to conduct syrinx,
throat and beak takes practice. 鈥淚t鈥檚 like a musician becoming proficient at
playing a song,鈥� says Podos. 鈥淎 trumpeter has to learn to match what they鈥檙e
doing with their hands with what they鈥檙e doing with their lips.鈥� Indeed, he
found that when young sparrows are learning to sing, they start by getting the
rhythm and pitch of the notes right. One of the last things they learn is how to
adapt their whole vocal tract to sing pure tones.
So the next time you find yourself in that country garden at dawn, listen
more closely to the chorus and see if you can sort the seasoned pros from the
beginners.
TALKING parrots have fascinated people for centuries, but only in recent
years have scientists figured out some of Polly鈥檚 tricks. Both parrots and their
smaller cousins the budgerigars mimic speech by copying the changing patterns of
frequencies that give each vowel and consonant its sound. But they do it in
totally different ways.
Ethologist Irene Pepperberg and her colleagues at the University of Arizona
in Tucson watched with infrared and X-ray cameras as Alex, a trained African
grey parrot, spoke a variety of English words. Alex uses the same basic strategy
as humans, they found. He creates a vibration with his syrinx (we use our
voicebox), then uses his throat, mouth and tongue to alter the dominant
frequencies, or 鈥渇ormants鈥�, to give the sound he wants. For example, Alex opens
his beak wider for an 鈥渆e鈥� than for an 鈥渁h鈥�, and probably pushes his tongue
further forward as well.
But Alex lacks lips and teeth, which are critical in forming human
consonants. 鈥淗e has to work harder to come up with a strategy for consonants,鈥�
says Pepperberg. She still does not know exactly how Alex does it, but some
evidence suggests he uses his oesophagus in making a 鈥渂鈥� sound.
Just as a small flute can鈥檛 sound a very low note, so smaller birds such as
budgies have trouble producing the deep pitches in human speech. 鈥淭he budgie has
a size problem,鈥� says Pamela Banta Lavenex, a former student of Pepperberg鈥檚 who
is now at the University of California, Davis. 鈥淚f they want to be heard,
they鈥檙e much better to go to a higher frequency where they can be louder.鈥�
To do this, Banta Lavenex found, budgies use amplitude modulation, the
principle behind AM radio. With their syrinx, they generate a 鈥渃arrier
frequency鈥� sound between 2 and 3 kilohertz. Then they produce a second
vibration鈥擝anta Lavenex is still not sure exactly where, but probably also
in the syrinx鈥攖hat modifies the carrier. As these two sounds add and
subtract, they produce additional frequencies just where the formants are for
human speech.