The biology and evolution of bird songs.

Abstract

THE BIOLOGY AND EVOLUTION OF BIRD SONGS CLIVE K. CATCHPOLE* Introduction Bird songs are some of the most beautiful and complicated sounds produced by the natural world. No evening stroll in an English garden would be complete unless accompanied by the melodic sounds of blackbird , thrush, or even nightingale. The last bird so inspired Beethoven, Keats, and Shakespeare that they all helped to weave it deep into the fabric of our literature and music. How strange that such a subject should also become the focus of great attention from modern research biologists [I]. However, bird songs do share a number of important similarities with human speech. For example, in terms of sound communication , birds and people share the same wavelength. One reason we are so aware of bird songs is that we all transmit and receive through roughly the same "frequency window" (about 1—5 kHz)—and loudly, too. One reason why Keats was so impressed by the nightingale on Hampstead Heath was that he could hardly avoid hearing it. Indeed, small birds produce a remarkably loud sound signal for their size [2]. But dogs are also capable of producing loud sounds within our frequency range and yet have not endeared themselves to either the great composers or the public at large. Birds impress us because their sounds are both variable enough to be interesting and melodic enough to please the musical ear. The repetitive barking of a dog or the constant drone of an insect does not have this effect and is either irritating or even soporific. Quite simply, birds produce more complicated sound structures , and to understand why they do this is the main puzzle that evolutionary biologists find an irresistible challenge. But before attempting at least some answers to the puzzle, we must first understand exactly how they produce their sounds. *Department of Zoology, Royal Holloway and Bedford New College, University of London, Egham, Surrey TW20 OEX, England.© 1986 by The University of Chicago. AU rights reserved. 003 1-5982/87/300 1 -05 1 5$0 1 .00 Perspectives in Biology and Medicine, 30, 1 ¦ Autumn 1986 \ 47 Sound Production and the Neural Basis of Songs Birds share, with human beings and other mammals, the ability to produce sounds by using the respiratory system as the source of energy. Unlike mammals, they do not have a larynx, or voice box, at the top of the trachea. Instead, they have a special organ called the syrinx situated at the junction where the trachea bifurcates into the two bronchi. It is a complex structure, consisting of a resonating chamber (tympanum) and special tympanic membranes that vibrate to produce sound when air is forced over them from the lungs. There is considerable variation in syrinx structure [3], but the modern passerine birds—which include the oscines or true songbirds—have the most complicated syrinx of all. Apart from its position, the most obvious difference between this system and a mammal larynx is that there are two quite separate sound sources, one in each bronchus. Inspection of sonagrams (voice prints) has detected what appear to be two independently produced sounds occurring at the same time. This led Greenewalt [4] to suggest that the syrinx is a dual sound source responsible for the "two voice" phenomenon in birds. Detailed neurophysiological investigations have now shown how the syrinx is innervated and controlled by branches of the hypoglossal nerve. Furthermore, the left hypoglossal is usually dominant over the right, as shown by experiments on several different species. It appears that different segments of the same song are produced in each separate bronchus, acting under the control of different branches of the hypoglossal . These innervate the syringeal muscles, so controlling tension on the tympanic membranes. How this is orchestrated by the central nervous system is currently being unravelled by Nottebohm, who has pointed out a number of striking similarities between humans and birds [5]. Both have to learn complicated vocalizations, and both develop lateralization of control through dominance by the left cerebral hemisphere. Nottebohm has not only worked out the detailed brain circuitry involved but has also come up with something quite revolutionary, which forces us to reexamine our ideas about how the vertebrate...