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First published online November 19, 2004
Journal of Experimental Biology 207, iv (2004)
Copyright © 2004 The Company of Biologists Limited
doi: 10.1242/jeb.01335
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Outside JEB

SINGING WITH SUPERFAST MUSCLES

Greg Crowther

University of Washington crowther{at}u.washington.edu


Throughout the animal kingdom, different muscles are specialized for different tasks. Among the most striking examples of extreme specialization are muscles that can contract and relax many times in the span of a single second. While a typical human limb muscle has a maximum contraction frequency of only 3-5 Hz, rattlesnake tailshaker muscles can contract at rates of 90 Hz, and toadfish swim bladder muscles produce a mating call by oscillating at 200 Hz. The rattlesnake and toadfish muscles turn on and off more rapidly than all others examined to date and, therefore, have been dubbed `superfast' muscles by the researchers who study them.

Although the superfast club is a rather exclusive one, researchers from Wageningen University (The Netherlands) and the University of Utah (USA) propose in the 9 September issue of Nature that the syrinx muscles of the ring dove (Steptopelia risoria) also belong in this elite group. The syrinx is birds' equivalent of the human larynx; whereas humans speak by moving the vocal cords in their larynx, birds vocalize by moving the membranes lining their syrinx. Two pairs of muscles are thought to adjust the membranes' position and tension, thus controlling sound production. Since doves' trademark cooing songs include trills of brief sounds repeated rapidly (up to 30 Hz), Coen Elemans and his co-workers reasoned that the syrinx muscles might have superfast properties.

To study these muscles further, the researchers attached electrodes to them and measured their electrical activity during cooing. Changes in electrical activity correlated with changes in the sounds emitted by the doves, suggesting that these muscles do indeed control the sounds. Elemans and his colleagues then removed the muscles to measure their contraction speed in response to individual pulses of electrical stimulation. On average, it only took the muscles about 4 ms to ramp up from 10% to 90% of their maximum twitch force and another 10 ms to drop from 90% back down to 10%. These extremely rapid changes put the dove syrinx muscles in the `superfast' category and are similar to those of rattlesnake tailshaker muscles.

Interestingly, the dove's superfast muscles are also super-weak; the need for speed apparently limits their ability to exert force. This trade-off between strength and speed is also seen with the rattlesnake tailshaker and toadfish swim bladder muscles, both of which are also quite weak. The low forces of the rattlesnake and toadfish muscles are due, in part, to the composition of the muscle cells, which include: relatively few force-generating proteins (actin and myosin) but lots of sarcoplasmic reticulum (which turns the contractions on and off) and mitochondria (which generate ATP aerobically so that the contractions can continue for many minutes). Presumably the dove syrinx muscle cells have a similar composition, although this was not addressed by the current study.

Are superfast syrinx muscles unique to ring doves? Elemans and co-workers suspect not. Since dove coos are relatively simple as bird songs go, they hypothesize that many other birds with more complex songs will also be found to have superfast syrinx muscles. With more data surely on the way, it is clear that Elemans' study is no swan song.

References

Elemans, C. P. S., Spierts, I. L. Y., Muller, U. K., van Leeuwen, J. L. and Goller, F. (2004). Superfast muscles control dove's trill. Nature 431, 146.[CrossRef][Medline]





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