INTRODUCTION

Striking parallels exist between the development of speech in human infants and the development of song in birds. Many sparrows, for example, learn their songs more readily during a sensitive period than at other times during development, require practice, and must hear themselves sing for normal song to develop (Baptista & Petrinovich 1986). These same features characterize both the earliest speech of human infants (see e.g., Ferguson et al. 1992) and second language learning, whether spoken or signed, among older individuals (Johnson & Newport 1989). Song production in zebra finches and canaries, like speech production in humans, is under lateralized neural control (Arnold & Bottjer 1985; Nottebohm 1991). Damage to any one of these areas, like damage to Broca's or Wernicke's area in (usually) the left temporal cortex of the human brain (for reviews, see Caplan 1987, 1992), produces highly specific deficits in the production or processing of communicative sounds.

As a result of these parallels in both behavior and neurobiology, studies of avian song development currently provide the best animal model for research on the mechanisms underlying speech development (Marler 1987). In contrast, while nonhuman primates are our closest living relatives and have often been used as animal models for the study of human social development (see e.g., Hinde 1984), their vocal communication is generally thought to provide no useful parallels with the development of human speech.

INTRODUCTION

In this chapter, we review work on the nature of vocal learning in human primates, comparing them en passant to nonhuman primates who share many of their capacities but are both less eager and less successful vocal learners. The basic question underlying this review is whether the precocious and prolific vocal learning of human primates can be explained by biological mechanisms that are specific to the language system or whether it relates to more general social capacities and to the particular social context of vocal learning in humans.

We know that young human primates are particularly good at vocal learning. One bit of evidence in support of this contention is that all national languages are spoken, even though extremely subtle articulatory and auditory discriminations are relied on to carry meaning in spoken languages. In addition, babbling and vocal play are early developmental activities universally observed in normally developing children (Locke 1992; Locke & Pearson 1992). Imitative vocal behavior is also universal in young children and common even in more mature language users. Furthermore, language learning, particularly word learning, by young children, is quite rapid and efficient.

Although there is much emphasis on children's preparedness for language learning, in fact children everywhere seem to enter the language system of conventional words use through the use of vocal forms that are more like adult forms in sound than in semantic or syntactic function. These early forms could be argued, though, to foreshadow a major function of oral language even in adulthood, namely to effect participation in social interaction rather than transmission of information.

INTRODUCTION

Vocal learning in birds has evolved independently in several different avian orders, but is common in only two groups, oscine songbirds and parrots. The diversity and complexity of vocal repertoire structure among the species in these two groups is enormous. However, much scientific attention in avian song learning has focused on a small group of songbirds, north temperate migrant species, in which song is restricted mainly to males and the occurrence of song and territoriality is seasonal. In addition to these birds there is also a vast number of laboratory studies on the development and neural control of male song in the zebra finch (Taenopygia guttata), an Australian species with an unusually compressed developmental period. This large body of research has resulted in general models of song and vocal learning drawn from only a small subset of the world's birds.

While these many studies have broadened our understanding of learned vocal communication, it is our contention that there is much to be gained by study of the vocal behavior of avian species with more complex social relationships. Such species exhibit long-term associations between well-acquainted individuals, and, for many, longterm associations are related to permanent residence in an area. Another important characteristic is the tendency to live in stable groups for at least part of the year. These groups could be, for example, a winter foraging flock of chickadees, a breeding colony of caciques, a foraging flock of cockatoos, or a permanently territorial pair of tropical wrens.

By consideration of common features of disparate groups that represent more fully the portion of the world's birds that learn vocally, we can approach a more truly universal model of vocal learning.

INTRODUCTION

Most studies of the effects of social interaction on the ontogeny of vocal communication in birds and primates concentrate on the normal course of development of species-specific codes: how birds learn conspecific song, how nonhuman primates develop their natural repertoire of calls, and how human infants develop language. The effects of social interaction, however, are probably even more important during exceptional learning (Pepperberg 1985): learning that is unlikely to occur in the normal course of events. Such learning, defined and described below, has been documented for a number of species, including humans. I have been particularly interested in examining how social interaction can influence a specific type of exceptional learning – the development of interspecies communication between humans and birds. My research on the effects of social interaction on the acquisition of a vocal, English-based code by grey parrots (Psittacus erithacus) clearly demonstrates how social and environmental input1 can engender learning that would not otherwise occur (e.g., Pepperberg 1990a). Interestingly, an analysis of research on ape language also demonstrates how social interaction may be a particularly effective means of teaching nonvocal human-based communication codes to nonhuman primates.

Although characterizing the effects of social and environmental influences on exceptional learning is not a simple task, my work has shown that a conceptual framework, social modelling theory, can be used (a) to characterize how social input influences learning and (b) to delineate the critical features of input necessary for exceptional learning.

INTRODUCTION

Marine mammals stand out among nonhuman mammals in their abilities to modify their vocalizations on the basis of auditory experience. While there is good evidence that terrestrial mammals learn to comprehend and use their calls correctly, there is much less evidence for modification of vocal production (Seyfarth & Cheney, Chapter 13). In contrast, vocal learning has evolved independently in at least two marine mammal taxa, the seals and cetaceans, and is widespread among the whales and dolphins. We concentrate our focus in this chapter on vocal learning and development in the bottlenose dolphin (Tursiops truncatus) because it is the marine mammal species in which vocal learning and imitation has been best studied.

Dolphins produce a variety of sounds. The two predominant sound types are clicks, which can be used for echolocation, and frequency-modulated whistles, which are used for social communication. In addition to whistles, dolphins produce short frequency upsweeps that have been called chirps (Caldwell & Caldwell 1970). The dolphin vocal repertoire also includes a variety of burst pulsed sounds and combinations of pulses and whistles.

Captive bottlenose dolphins of both sexes are highly skilled at imitating synthetic pulsed sounds and whistles (Caldwell & Caldwell 1972; Herman 1980). Once a dolphin learns to copy a sound, the novel sound can be incorporated into its vocal repertoire, and the dolphin can produce the sound even when it does not hear the model. Bottlenose dolphins may imitate sounds spontaneously within a few seconds after the first exposure (Herman 1980), or after only a few exposures (Reiss & McCowan 1993).

INTRODUCTION

Songbirds learn their songs by hearing others and then copying them, matching or improvising on the song theme (Slater 1989; Catchpole & Slater 1995). Their social behavior varies among species – they are migratory or resident, solitary or group-living, faithful partners to a single mate, polygynous or with no pair bond, and parental or nonparental in the care of their offspring (brood parasites lay in nests of other species, and their fosterers rear the young). All songbirds depend on parental care, and it has been suggested that this is the time when the young learn their songs. Later, when they are independent, the birds engage in a wider range of social interactions.

Field studies suggest that most songbirds learn their songs after the time of natal dispersal, when a bird moves from the site where it was reared to an area where it copies the song of a neighbor, rather than singing the song of its father: Bewick's wrens (Thryomanes bemickii), marsh wrens (Cistothorus palustris), saddlebacks (Philesturnus carunculatus), indigo buntings (Passerina cyanea), white-crowned sparrows (Zonotrichia leucophrys), and corn buntings (Emberiza calandra) (Kroodsma 1974; Verner 1976; Jenkins 1978; Payne et al. 1987; Baptista & Morton 1988; Petrinovich 1988; McGregor & Thompson 1988; McGregor et al. 1988). Song sparrows (Melospiza melodia) copy at least one song from three or four neighboring males when they settle on a territory, some time after the first four weeks of life (Nice 1943; Beecher et al. 1994). In two species males often copy their father (Darwin's finches (Geospiza fortis), zebra finches (Taeniopygia guttata); Millington & Price 1985; Gibbs 1990; Zann 1990), but not all individuals do this.

INTRODUCTION

A major focus in the study of bird song over the past three decades has been on the involvement of learning during development. At a basic level, two models of learning mechanisms have been proposed: instructive and selective (Jerne 1967; Changeux et al. 1984). In an instructive model, environmental stimulation adds information not already present in the behavioral repertoire. When a young bird memorizes a novel song, it is instructed. In contrast, in a selective model, learning consists of the selection of behavior(s) from a pre-existing repertoire as a function of experience. At the time of stimulation, the animal already possesses the potential or ability to perform the behavior. Therefore, the test to distinguish between the two models is to present a novel stimulus and to record whether it is learned.

Research on song learning has been guided largely by an instructive model of learning, embodied in the sensorimotor model first proposed in Konishi's (1965) study of song development in the white-crowned sparrow (Zonotrichia leucophrys). The sensorimotor model includes two stages: a sensory (instructive) phase in which songs are memorized, and a sensorimotor phase in which the bird compares its own song, via auditory feedback, to the memory trace acquired earlier.

One consequence of song learning is the formation of geographic “dialects” in which males at one location sing similar songs that differ from those of the same species at other locations. If vocal plasticity in birds is mediated solely by an instructive mechanism, then song matching dialects arise when males breed in the same area where they acquired their song(s).

INTRODUCTION

Experiments on song development have a long history dating from those performed by the Baron von Pernau with chaffinches (Fringilla coelebs), published in 1768 (Thielcke 1988). The Baron documented regional song dialects, showed that learning was restricted to a time window or “sensitive phase,” and demonstrated the bird's preference for learning songs of conspecifics over those of allospecifics or “stimulus filtering.” With the advent of instrumentation that allowed capture and analyses of sound, i.e., magnetic tape-recording and sound spectrographic technology, Thorpe (1958) was able to test these conclusions objectively. He played tape-recorded conspecific and allospecific songs to hand-raised, naive chaffinches reared in acoustic isolation. His experiments confirmed the existence of sensitive phases and stimulus filtering mechanisms during the song-learning process.

Thorpe's study set a standard for avian song ontogeny protocol: hand-raised naive experimental or pupil birds are isolated in sound-proof chambers and exposed to taperecorded vocalizations of model or tutor birds. An investigator is then able to: (a) control the number of songs played to the experimental birds to determine the minimum number of songs required to effect learning (Petrinovich 1985; Hultsch & Todt 1992; Peters et al. 1992; Hultsch 1993); (b) demonstrate that birds may recognize conspecific song by sound alone (Konishi 1985); and (c) test the effect of sound degradation on the choice of tutors by pupils (Morton et al. 1986).

That social factors could influence the choice of a song tutor by a pupil was first appreciated by Nicolai (1959). His work suggested that tape-tutoring experiments, although valuable, may in some cases test only what pupils can do under the conditions imposed by the investigator and not the pupil's actual or potential capabilities in nature.

INTRODUCTION

The study of vocal development in nonhuman animals has focused primarily on vocal production. However, vocal development involves not only production, but development of appropriate usage and appropriate responses to the calls of others. The relative neglect of usage and responses has led to a distorted view of vocal development as emphasized by Seyfarth & Cheney (Chapter 13) for monkeys and West et al. (Chapter 4) for birds. The argument is often made that nonhuman mammals differ fundamentally in vocal development from both birds and human beings but, as we have argued previously (Snowdon & Elowson 1992) and Seyfarth & Cheney (Chapter 13) argue, primates are similar to humans and birds if all three components of vocal development – production, usage and response – are evaluated.

In this chapter we argue that when functionally similar vocalizations are chosen from species that have similar social organization, then similar developmental processes will be found regardless of the taxon studied. We examine the idea that nonhuman primate vocal structures are fixed and review evidence that vocal plasticity may be quite common. We then provide three examples of phenomena from our research with marmosets and tamarins that illustrate how plasticity in pygmy marmoset trill vocalizations can be influenced by changes in social companions, how infant babbling in pygmy marmosets is a social interaction, and how the structure and usage of food-associated calls is acquired by cotton-top tamarins, and how social environments can inhibit the expression of these calls.

In the late 1960s a series of developments in linguistics, developmental psycholinguistics and animal communication led to a convergent model of vocal development in human and nonhuman species. As presented by Lenneberg (1967) and Marler (1970), the development of language and of bird song required exposure to species-specific codes during a sensitive period of development, after which subsequent learning was extremely limited. The amount of input required could be quite small, and this input could be effective regardless of social interactions. Both birds and humans needed intact hearing and an extensive time for practice (babbling for human infants, subsong and plastic song for birds) to acquire adult competence in vocal production. Subsequent to this practice crystallization occurred, and further changes in vocal structure were rare.

This paradigm has led to extremely productive research over the past 25 years, not only in the study of vocal development but also in the understanding of the neurological controls of vocal production. However, as researchers interested in the ontogeny of primate and avian vocal communication, we have become increasingly aware of the need to consider some modifications to this paradigm. Some forms of social stimulation can extend sensitive periods for song learning in birds, and songs and calls in some species can be modified throughout life, often in response to changes in social stimuli. Parrots, dolphins and great apes with exceptional training acquired codes with some similarities to human language. Yet at the same time there was little evidence of vocal plasticity in nonhuman primates, suggesting a gap in continuity of developmental processes in the evolution from birds to humans.

INTRODUCTION

The first studies of language acquisition by the child described mainly the developmental stages of this specific human ability From Piaget (1923) to Brown (1973), authors were interested mostly in the different formal aspects of the acquisition: for example, the age of onset, total amount of language at any age, mean length of utterance, and emergence of grammar. These studies considered the abilities of each child as representative of the general linguistic abilities of the human species at this ontogenetic stage.

More recently, new trends have appeared, where language is studied in a more pragmatic way: it is considered as a means, at each developmental stage, for a child to elicit real communicative interactions. Thus, while admitting that the general stages of language development are alike in any child (Locke & Snow, Chapter 14) such an approach to the development of communication implies integrating various aspects that are usually considered separately by different researchers.

On the one hand, to consider the emerging linguistic skill as part of the larger phenomenon of communication implies integrating the analysis of the linguistic competence of a child at a given stage with that of previous stages, in particular with babbling. It implies also the integration of other communicative behaviors: for example, approaches, emotional addresses, and object exchanges. It can be hypothesized that, when a child is communicating, it is both acquiring the human language and developing its personal communicative style with human beings.

INTRODUCTION

Vocal learning involves the ability to modify and acquire new signals in an organism's vocal repertoire through the use of auditory information and feedback. Humans and many avian species, particularly songbirds, have demonstrated similarities and analogous patterns in the vocal acquisition of their respective repertoires. These similarities include the importance of auditory input, feedback, and social influences on vocal structure and acquisition, and stages of developmental overproduction, selective attrition, and vocal babbling/subsong (for reviews, see Kroodsma 1982; Pepperberg & Neapolitan 1988; Locke 1990, 1993a,b). Finding such parallels in phylogenetically distinct species is striking and suggests a convergence in strategies of vocal learning.

Evidence for vocal learning in other species is rare. Studies of vocal learning in nonhuman primates have suggested that learning plays a role in vocal development of contextual use and comprehension (Seyfarth et al. 1980; Cheney & Seyfarth 1982; Seyfarth 1986; Hauser 1988; Gouzoules & Gouzoules 1989) but clear evidence for the learning of vocal repertoires by nonhuman primates has been slow to emerge. However, recent results of studies of nonhuman primates (Elowson & Snowdon 1994; Snowdon et al., Chapter 12; Mitani & Brandt 1994) and birds (Brown & Farabaugh, Chapter 7) suggest greater vocal plasticity than was previously described and point to an importance of social factors on vocal structure and acoustic variability of calls. Therefore, to more clearly elucidate the phenomenon of vocal learning it is important to make a distinction between vocal learning (the ability to acquire new elements in one's vocal repertoire) and vocal plasticity (the ability to modify signal structure due to social or environmental conditions).

THE SOCIAL FUNCTION OF LANGUAGE

This chapter analyzes alternative types of conversational action used to build social organization among girls and boys in an African-American working class neighborhood in Philadelphia. Participants work together to generate distinctive definitions of the situation appropriate to the task at hand, and the same individuals articulate talk and gender differently as they move from one activity to another. Making use of the same language system, children select alternative ways of putting these forms to use, constructing a range of diverse activites and social arrangements that can highlight either affiliation or competition.

From the perspective of ethology, Cullen (1972, p. 101) has argued that “all social life in animals depends on the coordination of interactions between them.” To achieve collaborative activity humans need to display to one another culturally meaningful behavior – articulating for their recipients what they are up to and how they expect others to respond. Sociologist Georg Simmel (1950, pp. 21–2) has stated that “if society is concerned as interaction among individuals, the description of the forms of this interaction is the task of the science of society in its strictest and most essential sense.” In that language provides the tool through which humans coordinate their behavior, then what is required for an adequate understanding of social organization is close attention to talk itself.

INTRODUCTION

In the mid-1960s Klaus Immelmann began a series of experiments with domesticated zebra finches (Taeniopygia guttata) that led to seminal contributions to two related fields, song learning and sexual imprinting. Immelmann (1969) manipulated the auditory and social experiences of young males in their first 100 days of life and found that those denied any contact with singing males failed to sing the normal zebra finch song at adulthood. He concluded that song in this species, like that of most songbirds, must be learned. When he isolated young from foster parents (Bengalese finches (Lonchura striata var. domesticaj) at different ages he found that the sensitive phase for song acquisition began as early as 25 days of age, about a week after fledging, and ended around 80 days of age, around the onset of sexual maturity. Furthermore, young males did not learn from just any singing adult, but preferred to copy from the male with whom they formed a personal bond. In most instances this was the father or foster father and the bond was based primarily on the provisioning relationship, the most basic filial bond. Immelmann (1969) hypothesized that wild zebra finches would be likely to learn the songs of their fathers, and an early end to the sensitive phase was necessary in order to prevent learning from heterospecific estrildines.

The experimental possibilities raised by Immelmann's intriguing study of song eventually stimulated a steady series of follow-up experiments by other researchers, in particular, by P. J. B. Slater and coworkers, who used song learning in domesticated zebra finches as a model for teasing apart the subtle interactions involved in the development of behaviour (for a review, see Slater et al. 1988).

INTRODUCTION

Vocal learning is a very widespread characteristic of songbirds, and a large variety of these learning processes has been described over the last decades. Learning can lead to different types of variation and results in song sharing that can be geographically localized and is then considered as “dialects.” The distribution of these variations can be limited to a few birds and/or cover large areas. Experimental studies have given precise information about the mechanisms involved, in particular in terms of “timing.” However, naturalistic validations may be necessary for us to fully understand the functional significance of vocal learning (see discussion of the sensitive periods, in the literature). There is a need for integrative studies and it is important to consider communication in its own context, which is that of social interaction (for language as a social act, see Goodwin 1990). A social organization needs an adapted communicative system, and comparative studies can give us hints about the evolutionary bases of vocal learning. Comparison can be made between species or phylogenetic groups but also between populations of a same species.

Likely candidates to help us to understand these processes are highly social animals that can adapt to different social environments. Starlings clearly correspond to this definition and here I examine through experimental and naturalistic studies the possible relation between song acquisition, song sharing and social organization.

The European starling (Sturnus vulgaris) occupies the largest geographic range of all the species of Sturnus (Feare 1984). It is present in Asia and in Europe from Scandinavia to Spain and Italy, and even in North Africa. It has also been introduced successfully in North America, New Zealand, and South Africa.

INTRODUCTION

It might seem odd to suggest that the study of bird song needs a social agenda. Isn't it obvious that birds sing to attract or to repel one another? Isn't it now clear that birds need social experience to develop species-typical repertoires? Although the answer to these questions is “yes,” we are convinced that only the surface structure of social influence has been uncovered – the deep structure remains to be explored. The purpose of the chapter is to defend this position by examining some of our own efforts to study social influences. We begin with an account of some of the formative experiences that shaped the directions of our research. We follow with some of the historical themes that guided us and others studying songbirds. Then, we describe some of our most recent efforts to examine new themes relevant to avian communication, themes quite familiar to those studying primates. In particular, we focus on the difference between communicative form and communicative competence. We wish to draw a greater distinction between the processes involved in developing a potentially communicative signal and the processes involved in learning how to use those signals effectively (Seyfarth & Cheney 1986 and see Chapter 13; Snowdon et al., Chapter 12). We conclude that analyses restricted only to the structural nature of vocal signals are inadequate to capture the developmental processes leading to vocal communication. We must go beyond studies of songs and focus on the singers, listeners, and the contexts framing communication.

FLASHBULB MEMORIES: A BIOASSAY OF SONG, A BIOASSAY OF SINGERS

In May of 1973, we witnessed an event that led to a series of studies spanning the next two decades.