Avian Song

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Avian song

Introduction

Many people have been captivated by the soaring melodies of a singing bird, or have been amazed by the diversity of sounds and the sheer noisiness of a dawn chorus in the rain-forest. Keen birdwatchers soon realize that listening more closely leads to an appreciation not only of the aesthetic beauty of song, but also of differences between songs: the whistles, warbles, trills, chirrups, squeaks, and buzzes that distinguish species. Following a single bird reveals even more; it may sing different songs when it interacts with its mate compared to to those it uses when it interacts with a neighbor, or give shrieking alarm calls when danger threatens. Detailed scientific studies of bird song have revealed the intricate complexity of communication in birds, and contributed to diverse fields such as ethology (study of animal behavior), neurobiology, evolutionary biology, and bioacoustics (study of sound and living systems).

There is tremendous variation in the sounds that birds produce. Some species produce non-vocal sounds in addition to vocalizations. Woodpeckers use their bills to drum loudly and rhythmically on tree trunks. Snipes have modified tail feathers that vibrate to produce a bleating sound as the bird plummets downward. The oscines, or songbirds, which comprise nearly half of all the species of birds in the world, are known for their well-developed singing abilities. Songs vary considerably, not only between species, but also at a finer level between different populations of the same species, between different individuals in the same population, and even within a single individual that sings a repertoire of different song types. Songs are sometimes distinguished from calls, a difference that is obvious in some species but not in others. Generally, calls are short, simple, stereotyped, and innate, while songs are longer, more complex and varied, and have to be learned. However, in some species, calls are also learned; two non-oscine groups, the parrots and hummingbirds, learn their vocalizations.

Bird species vary in who does the singing. In some species, only male birds sing. This is the case in many of the long-studied birds of the north temperate regions like Europe and North America, but it is not true of many tropical and south temperate species where it is quite common for females to sing as well. In some of the species where both sexes sing, breeding partners may coordinate their songs to produce duets that can be so precisely coordinated that it sounds as if only one bird is singing. Duetting is particularly common among the Thryothorus wrens of South America and the shrikes of Africa. Differences in the singing behavior of males and females are reflected in their brain structure. In species where only males sing, the song control regions in the brain are much larger in males than females, but in duetting species, females also have well-developed song control regions.

There are some patterns in when and where birds sing that are common to many species, and that hint at the function of song. Many species have what is known as a dawn chorus, where they start the day with high song rates, and some also have a smaller chorus at dusk. As well as this daily variation in song rates, there are also seasonal fluctuations. Spring is heralded in many parts of the world by a profusion of bird-song. This peak in song rates coincides with the time that many birds are establishing territories and finding mates, suggesting that song has a role in these activities. Birds often sing from a song post, where they have a clear view and may be near the border of their territory. When one bird sings, its neighbor often sings immediately afterwards, also suggesting that song is used in maintaining territory boundaries.

Methods of studying bird song

Looking and listening

Much can be learned about bird song using nothing more than a keen pair of eyes and ears, and a notebook. Many different vocalizations can be distinguished from one another by careful listening, though specialized sound analysis equipment may be necessary to detect some of the more subtle variation in form. Counting the number of songs given in different contexts allows variation in song rates associated with time of day, season, and stage of the breeding season to be identified. Observing the social context of singing can indicate whether song is directed at a partner, a neighbor, or an intruder, and what kind of response it elicits.

Recording song

Tape recorders and microphones are used to record bird-song so that it can be analyzed or used for playback in more detailed studies. Anyone can record the songs of a bird,

though getting a high quality recording can be challenging. Getting as close as possible to the bird without disturbing it is a good start. It is also important to choose a time when song rates are high and there is little other noise around; dawn is often best. Parabolic reflectors or highly directional microphones focused on the singing bird help to reduce background noise. Advanced recording techniques such as microphone arrays involve recording the songs of several birds simultaneously onto a series of microphones, and using differences in the time it takes a sound to reach each micro-phone to map the position and movements of the birds as they interact.

Analyzing song

Analyzing birdsong requires an understanding of some of the properties of sound. Sound consists of alternating waves of high and low pressure generated by a vibrating object, and the length of one complete cycle of high and low pressure is known as the wavelength of a sound. The number of cycles reaching an observation point per second depends on the wavelength and is called the frequency, measured in hertz (Hz). Frequency differences are heard as differences in pitch; for example, middle C has a frequency of 261 cycles per second while the C an octave higher has a frequency of 783 Hz. The amplitude, or intensity, of the pressure in the sound waves determines how loud the sound is. Georgia State University's Hyperphysics Web site (<hyperphysics.phy-astr.gsu.edu/hbase/hframe.html>) has more about the properties of sound.

For sound analysis, sound spectrograph machines and sound analysis computer software measure the physical properties of sound and convert them into pictures. These images allow different song types to be categorized by visual inspection of patterns, or by measuring particular features of the song such as length, frequency range, or maximum amplitude. Sonograms are images that show changes in frequency over time, while "waveforms" graph amplitude against time. Looking at a sonogram can give an idea of what a song sounds like, remembering that the vertical axis shows the pitch of the sound. A whistle at a single pitch appears as a horizontal line on a sonogram, while a descending whistle appears as a descending line. A very short sound spanning a wide frequency range appears as a vertical line, and sounds like a click, while buzzing sounds consist of a series of these clicks given in rapid succession.

Experimenting

Experiments are an important component of the scientific study of birdsong. One of the techniques used most commonly is playback, in which recorded songs are broadcast through a speaker and the response of birds to the song is monitored. Playback experiments allow responses to the song itself to be measured without any influence of other effects, like the behavior of the singing bird. Many birds respond dramatically to playback, flying toward the speaker and singing as if there were an intruder. Differences in the intensity of response to different playback suggest different levels of threat. The closer the speaker is to the center of their territory, the more aggressive the response. Even on the territory boundary, if an unfamiliar song is broadcast, it will elicit a more aggressive response than songs of a familiar neighbor. Also, if a neighbor's songs are not played from the appropriate territory boundary but from the opposite boundary, then they too will elicit a more aggressive response. Playback experiments have thus been used to show that birds can recognize different neighbors solely on the basis of their songs.

Innovative technology allows more advanced, interactive playback experiments to be conducted. Experimenters link a computer to the speaker and choose which songs to broadcast, depending on the behavior of the bird being tested. For example, the experimenter might choose to play a song that is the same length or the same type as the song the bird itself has just sung, to see how that influences its response.

The approach

Niko Tinbergen, a pioneer in the study of animal behavior, highlighted four approaches to answering questions about animal behavior. First, there are causal factors that can be studied, including both internal mechanisms and external factors such as the environment. Second, there is the developmental perspective, for example how birds learn to sing and who they learn from. Third, the survival value, or function, of a behavior can be studied, such as the role of birdsong in territorial defense and mate attraction. Fourth, the evolution of the behavior over time can be investigated.

Causes and mechanisms

Song production

Birds sing using an organ called the syrinx, which operates in much the same way as the mammalian larynx. Both are associated with the windpipe, or trachea; the larynx is at the top of the trachea, while the syrinx is at the bottom where it splits into two bronchi before entering the lungs. When they sing, birds push thin tympaniform membranes into the flow of air passing through the syrinx, causing the membranes to vibrate and generate sound waves. Because of the location of the syrinx at the junction of the bronchi, birds have two voices and can produce two harmonically unrelated sounds at once. Suthers implanted tiny devices for measuring air oscillations in each side of the syrinx to show that gray catbirds (Dumetella carolinensis) and brown thrashers (Toxostoma rufum) use both sides of the syrinx in producing their songs, while some birds, like the canary (Serinus canaria), use predominantly one side or the other.

Sounds generated in the syrinx are modified as they pass through the trachea and bill higher up in the vocal tract. The vocal tract selectively filters overtones produced by the syrinx, emphasizing some frequencies and filtering out others. Nowicki found that birds in helium-enriched air, which is less dense and allows sound to travel faster, produce songs with more harmonic overtones. So, like humans, higher pitched components of the sound that are normally filtered out by the vocal tract become audible in helium. Postural changes also affect song. When birds sing, they move their bills, puff out their throats, and stretch their necks, modifying the effective length of the trachea and influencing the resonance properties of their vocal tract and the frequencies of the sounds they produce. Trumpet manucodes (Manucodia keraudrenii) have greatly elongated trachea coiled in their breasts that give resonance to their loud, deep, trumpet-like vocalizations.

The production of diverse and complex sounds by the syrinx is achieved by an integrated system involving muscles, nerves, and hormones. The muscles of the syrinx control the tympaniform membranes to finely modify the physical properties of the sound. Syringeal muscles, in turn, are controlled by nerve impulses from specialized areas of the brain including the higher vocal center (HVC). Individual nerve cells in these areas are specialized and active only when particular songs are sung. Seasonal changes in song production are associated with seasonal changes in the size of the HVC, and also with changes in testosterone levels. Implanting males with testosterone in the nonbreeding season causes them to sing more, and females in species that do not normally sing can be induced to sing by injections of testosterone. The relationship between birdsong and hormones goes both ways; as well as hormones inducing song, hearing the song of male birds causes hormonal changes in females that induce them to start building nests.

Transmission of birdsong

The farther away the singer is, the fainter its song sounds. This attenuation (weakening) of sound is partly just because of a physical principle, the inverse square law. This states that sound radiates out in all directions from a source, so doubling the distance from the source causes a four-fold decrease in sound intensity, while trebling the distance decreases intensity nine-fold, and so on. The air itself also absorbs sound, thus windy, hot, or humid weather conditions cause sound to be attenuated more rapidly. Obstacles in the environment, such as vegetation, reflect and scatter sound waves, causing further attenuation. This attenuation by air and obstacles in the environment is frequency dependent; longer wavelengths do not attenuate as quickly, so lower frequency sounds travel farther than high frequency sounds. As well as becoming attenuated as it passes through the environment, sound is also degraded and the different elements of a song start to blur as sound is reflected off the ground, canopy, and tree trunks. Songs that have rapidly changing amplitudes or frequencies are especially susceptible to this degradation, known as reverberation.

These various constraints on sound transmission affect how, when, and where birds sing. Birds seem to have songs that are structured to transmit most effectively in their environment; for example, forest-dwelling birds have songs with acoustic properties that minimize the effects of reverberation due to vegetation. Song structure is also related to function, so species with larger territories have territorial songs that are louder and will travel farther. Many birds do a lot of their singing from special song posts in their territories, choosing a perch well above the ground with not much vegetation around, so that interference from these obstacles is minimized and the song will carry farther. Birds tend to sing less on windy days when their songs are less likely to be heard. They also avoid singing at the same time as other birds, and interactions between neighboring birds often take the form of countersinging where the song of one bird is followed almost immediately by a song from its neighbor, and then the first bird may sing again as soon as its neighbor finishes. In some species, overlapping a neighbor's song is a sign of aggression that can escalate into conflict.

Hearing songs

Bird ears are not very obvious because there is no outer ear funneling sound waves into the inner ear, and feathers cover the opening of the ear. Some birds have special feather structures that serve a similar purpose to an outer ear; the dish-shaped faces of owls concentrate sound waves on their ear openings. Internally, bird ears are similar to other vertebrates, with a thin tympanic membrane that detects sound waves. Vibrations of the tympanic membrane are transferred via a small bone, the columella, to the fluid-filled cochlea of the inner ear. Movements of fluid in the cochlea stimulate underlying hair cells that are sensitive to different sound frequencies. Generally, birds are most sensitive to frequencies in the range of 1–5 kHz, but there is variation between species that influences the design of signals. Prey species can produce vocalizations that take advantage of subtle differences in the hearing abilities of their predators, enabling them to communicate with members of their own species using frequencies that predators are less sensitive to, and reducing the risk of eavesdropping.

Signals from the inner ear are transferred by the nervous system to specialized areas of the brain that extract all sorts of information about the sound. Different frequencies activate different nerve cells so that certain song types only activate particular cells. The location of the sound is worked out by integrating the signals from each ear; comparing differences in arrival time and intensity of sound at each ear tells what direction it came from. Relative intensity, reverberation, and degree of attenuation of different frequencies provide information about the distance of a sound. Barn owls (Tyto alba) hunt in the dark, pinpointing prey by listening. A special arrangement of their ears, with one slightly higher than the other, and one pointing downward while the other points upward, increases the detectability of the differences between ears that the brain uses to locate the source of the sound with extreme precision in three dimensions. Again, mechanisms of sound perception have implications for signal design because aspects of the structure of a song, like timing and frequency range, influence how easily listeners can locate it. Song structure, whether its acoustic properties reveal or hide the location of the singer, can therefore reveal something about song function.

Learning to sing

Nature and nurture

Like human speech, birdsong in the songbirds (Oscines) is something that has to be learned. The way in which song develops is one of the most well studied processes in animal behavior, and illustrates the complex interactions between nature and nurture, or instinct and learning, that are involved in the development of behavior. Young songbirds make only simple begging noises at first to solicit food from their parents, but later they begin trying to produce adult-sounding songs that initially are wobbly and not very precise. This "sub-song" gradually improves with practice to become "plastic song," which sounds more like adult song but is still quite variable, before crystallizing to the stereotyped adult song.

Experiments have been used to identify various components of the normal song-learning process. Young birds raised in isolation in captivity develop songs that are crude approximations of normal adult song. Only if they hear adult song do they develop normal adult song. Some species copy songs heard from tapes, while others only copy songs heard from live tutors. Some species will copy adult songs of other species, but only if it is similar to that of their own. It seems that young birds hatch with a genetically determined template of song that enables them to recognize species-specific songs. The innate template allows them to produce something resembling a species-specific song even if they have never heard one, but memorizing songs they hear refines the template and enables them to produce normal songs. The second component in the process of song development is lots of practice, known as the sensorimotor phase because it involves both sound production and perception. Young birds deafened before they begin singing are unable to produce anything resembling a normal adult song. Auditory feedback is essential at this stage; in other words, they have to hear themselves sing to be able to match the sounds they produce to the songs they are copying.

When do they learn?

The timing of song learning varies considerably among species. Some have only a very short sensitive period, and if they do not hear adult songs during this period, they never develop normal songs. Other species, open-ended learners, continue learning new songs throughout their lives. Social influences are very important for facilitating learning. White-crowned sparrows (Zonotrichia leucophrys) exposed to taped song are sensitive only during the period from 10 to 50 days old, and do not copy songs of other species. However, when housed with live tutors, they learn songs after 50 days of age, and copy songs of other species. Changes in social circumstances at later stages in life can also lead to learning; captive budgerigars (Melopsittacus undulatus) moved to a new flock modify the structure of their calls to more closely match those of their new flock mates.

What do they learn?

Most birds copy the songs of their fathers or neighbors. Who birds learn from depends partly on when they learn. If they learn only after leaving the territory where they were born, then they may learn from other males in the neighborhood where they settle. Sharing song types with neighbors is important for communication in song sparrows (Melospiza melodia), and Beecher and his colleagues found that young males learn the songs of three or four neighboring males, selecting song types that are shared by the neighbors. In another population, where song sharing is less important, Hughes and her colleagues found that young birds copy parts of songs and recombine song segments, rather than copying whole songs.

The number of songs that each individual learns varies considerably among species, with some learning only a single song type, while others sing hundreds or even thousands of different songs. The number of song types that birds can learn seems to be related to brain space. Individuals with large repertoire sizes have larger song-control areas in the brain. Brenowitz argues that, rather than the size of song control areas being determined by the number of songs learned, it is likely that other factors such as genetic differences or early development may cause differences in the size of song-control areas that determine how many song types can be learned.

Some species are virtuosos when it comes to learning; they sing not only species-specific songs, but also the songs of other species. A survey by Baylis showed that a diverse range of birds engage in vocal mimicry. The function of vocal mimicry is not well understood, and may vary between species. Some mimicry is associated with brood parasitism, where females of one species lay their eggs in nests of another species, the host that then provides parental care. Male indigo birds (Vidua spp.) learn the songs of their host species. Single nestling cuckoos (Cuculus canorus) mimic nestling begging calls of a whole brood of host chicks to stimulate their host parents to feed at high rates, though this deceptive mimicry is innate rather than learned. Many accomplished mimics are not brood parasites. Lyrebirds (Menura novaehollandiae) sing the songs of many different species, and even incorporate other sounds into their repertoires. Once these sounds have been incorporated into a repertoire, they are learned along with species-specific songs by young birds. Male lyrebirds have display areas where they try to attract females with spectacular visual as well as vocal displays. It is possible that mimicry increases their repertoire sizes and makes them more attractive to females.

Functions of song

Signaling

Song is one of the most obvious and important ways that birds communicate with one another. Although birds also use visual signals like bright colors and displays, acoustic signals can often be heard from farther away than visual signals can be seen, and can be used to either avoid or mediate closer contact. Signals, of whatever variety, are used to convey information to others, and induce a change in behavior that benefits the signaler. Birds use song to convey information about themselves, such as identity or location. Birds may also convey information about the environment, for example, by using alarm calls to warn of approaching danger. Because song facilitates recognition, it plays an important role in mediating social interactions, hence what is known as the dual function of song in territorial defense and mate attraction.

Recognition

The immense variation in the structure of songs allows birds to recognize others as belonging to the same species, to identify their sex, and even to recognize particular individuals, be it a neighbor, mate, or offspring. Recognition at all these levels is vital for survival and successful reproduction. Sound analysis and playback experiments have been used to identify the features of song that permit recognition, and to show that recognition occurs. For example, in some species, males and females sing different song types, or there may be subtle differences in male and female renditions of the same song types. Birds respond differently to playback of their neighbors, their mate, and unfamiliar birds, indicating that they can distinguish between them on the basis of song alone. Vocal recognition is particularly important for parent-offspring recognition in species that breed in large colonies.

Defending a territory

Song is vital as a first line of defense for birds that hold territories. Many species defend a territory during their breeding season, and some species defend a territory throughout the year. Song serves as a long-distance proclamation of territory ownership, and as a threat to intruders that, if unheeded, may be followed up by physical aggression. The fact that birds respond to playback by singing suggests that song has a role in territorial defense. More direct evidence comes from experiments where birds have been removed from their territories and replaced by a speaker. Far fewer intruders are seen in territories where the speaker is playing their songs than where the speaker is playing control songs of a different species. Clearly, song alone, even without the physical presence of the bird, serves to deter intruders. A different type of experiment, involving temporarily muting birds, also shows that birds that are unable to sing are slower to establish territories and suffer more intrusions by other birds. Most studies on song have focused on male song, but research on song by female birds, reviewed by Langmore, indicates that their song also has a territorial function. It seems therefore that song is used to repel birds of the same sex.

Studies on interactions between birds occupying territories adjacent to one another have revealed some interesting details about the way songs are used in territorial defense. Birds save time and energy in defense by recognizing the songs of individuals living around them. In playback experiments, birds respond less aggressively to playback of their neighbors' songs than strangers' songs. Nevertheless, birds may direct song at neighbors, approaching the common boundary and singing in reply to their neighbor's songs, or countersinging. Birds also use their repertoires to communicate with neighbors; when individuals share song types with neighbors, they can direct songs to specific birds by matching song types. Burt and his colleagues used interactive playback experiments with song sparrows to show that song-type matching (replying with the same song type) elicits a more aggressive response than repertoire matching (replying with a shared song type other than the one just sung), and can escalate conflict between neighbors.

Although birds have ways of indicating that a song is intended for a particular recipient, McGregor and Dabelsteen argue that, because sound is transmitted in all directions, communication networks are set up where individuals can eavesdrop on signals between others. By eavesdropping on neighbors and listening to their vocal interactions with intruders, birds obtain an early warning if the intruder comes their way. They may also learn something about the competitive ability of the intruder by listening to how it fares in an interaction with a neighbor whose competitive ability is known. Females may also eavesdrop on singing interactions between males to assess their relative competitive abilities.

Attracting a mate

Male song rates are highest in spring, suggesting that song has a mate-attracting function. Consistent with this, males of some species stop singing once they have a partner, and experiments removing the female of a mated pair cause an increase in male song rates until the female is returned. More direct evidence that song attracts females comes from experiments on birds that breed in nestboxes. Nestboxes fitted with a trap to catch prospecting females and with speakers broadcasting male song catch more females than nestboxes from which no song is broadcast.

Male song can be quite elaborate, and it appears that females are not only attracted by song, but may choose between males on the basis of the amount or variety of song they produce. Males that have the time and energy to sing at high rates often have a good territory with a plentiful supply of food. Females also seem to prefer males with larger repertoires of song types. Female great reed warblers (Acrocephalus arundinaceus) pair with males that have better territories and bigger repertoires. They also sometimes mate with a male other than their social partner, and these males have larger repertoires. Hasselquist and his colleagues found that the offspring of males with larger repertoires of song types generally have higher survival rates, so it seems as if females are getting better quality males when they choose males that sing more song types.

As well as attracting females, male song also stimulates females to reproduce. Kroodsma played male song to captive female canaries, stimulating them to build nests and lay eggs. Again, larger repertoires seem to be better, because when he played large song repertoires to some females and small song repertoires to others, those hearing the larger repertoires built nests faster and laid more eggs than those hearing small repertoires.

Evolution of song

Regional variation

Fine-scale geographic variation is most obvious in species where each individual sings only one or two song types and neighbors share song types. Boundaries between song types are often sharp, creating dialect areas where males all sing the same song. Differences between areas are less obvious in species where each individual has large repertoires. Nevertheless, because birds generally learn their songs from parents or neighbors, songs tend to differ more between populations than within populations. Differences between populations can also be due partly to adaptations for sound transmission in different environments. Social influences might also contribute to differences between areas if individuals modify their songs to be more similar to their neighbors because there are benefits from sharing songs with neighbors.

Cultural change

Because there are slight changes every time birds learn songs, the songs in a population undergo a process of cultural evolution over time that is similar to genetic evolution. Also, because copying errors occur more frequently in the song-learning process than mutations occur in genetic evolution, birdsong provides an excellent system for studying evolutionary processes. Movement of birds between populations introduces new songs to a population and increases diversity within populations. Selection can act on song if habitats limit transmission of some songs, or if females prefer some songs.

Song and speciation

Because song is important in mate choice, it can be a powerful isolating mechanism leading to the formation of new species. Gradual changes in the form of songs could accumulate to the point where individuals no longer recognize one another as being from the same species, and therefore do not reproduce. In Darwin's finches of the Galápagos Islands, natural selection caused changes in bill size and shape, which in turn influenced the acoustics of song production. Podos suggested that these changes in the temporal and frequency structure of songs may have caused reproductive isolation and facilitated the rapid speciation that occurred.

Resources

Books

Baylis, Jeffrey R. "Avian Vocal Mimicry: Its Function and Evolution." In vol. 2 of Acoustic Communication in Birds, edited by D. E. Kroodsma and E. H. Miller, 51–83. New York: Academic Press, 1982.

Bradbury, J. W., and S. L. Vehrencamp. Principles of Animal Communication. Sunderland, MA: Sinauer Associates Inc.,1998.

Catchpole, C. K., and P. J. B. Slater. Bird Song: Biological Themes and Variations. Cambridge: Cambridge University Press, 1995.

McGregor, P. K., and T. Dabelsteen. "Communication Networks." In Ecology and Evolution of Acoustic Communication in Birds, edited by D. E. Kroodsma and E. H. Miller. Ithaca: Cornell University Press, 1996.

Periodicals

Beecher, M. D., S. E. Campbell, and P. K. Stoddard. "Correlation of Song Learning and Territory Establishment Strategies in the Song Sparrow." Proceedings of the National Academy of Sciences of the United States of America 91 (1994): 1450–1454.

Brenowitz, E. A. "Comparative Approaches to the Avian Song System." Journal of Neurobiology 33 (1997): 517–531.

Burt, J. M., S. E. Campbell, and M. D. Beecher. "Song Type Matching as Threat: A Test Using Interactive Playback." Animal Behavior 62 (2001): 1163–1170.

Kroodsma, D. E. "Reproductive Development in a Female Songbird: Differential Stimulation by Quality of Male Song." Science 192 (1976): 574–575.

Hasselquist, D., S. Bensch, and T. Vonschantz. "Correlation between Male Song Repertoire, Extra-Pair Paternity and Offspring Survival in the Great Reed Warbler." Nature 381(1996): 229–232.

Hughes, M., S. Nowicki, W. A. Searcy, and S. Peters. "Song-Type Sharing in Song Sparrows—Implications for Repertoire Function and Song Learning." Behavioral Ecology & Sociobiology 42 (1998): 437–446.

Langmore, N. E. "Functions of Duet and Solo Songs of Female Birds." Trends in Ecology and Evolution 13 (1998): 136–140.

Nowicki, S. "Vocal Tract Resonance in Oscine Bird Sound Production: Evidence from Birdsongs in a Helium Atmosphere." Nature 325 (1987): 53–55.

Podos, J. "Correlated Evolution of Morphology and Vocal Signal Structure in Darwin's Finches." Nature 409 (2001): 185–188.

Suthers, R. A. "Contributions to Birdsong from the Left and Right Sides of the Intact Syrinx." Nature 347 (1990): 473–477.

Tinbergen, N. "On Aims and Methods of Ethology." Zeitschrift für Tierpsychologie 20 (1963): 410–433.