Some Primordia for Communication

It is not easy to draw a firm line between stimuli produced by animals that are truly communicative and others that are not. The difficulty arises in part because so many cases fall on the borderline, having some of the attributes that we require for communication while lacking others. One elementary requirement is illustrated by the observation that telling a man to jump off a bridge is an act of communication, while pushing him is not (Cherry, 1966). The point here is not just that the use of force is hardly communicative in the fullest sense, but also that communicative behaviors are specialized for their function.

There are many examples of stimuli passing from one organism to another that qualify as specialized signals. Illustrations are by no means restricted to interactions between members of the same species. For example, many animal secretions are highly specialized for the chemical repulsion of predators (Eisner, 1970). Some are generalized irritants that cause pain when a predator touches them. Others are "for all intents and purposes natural imitations of histological fixatives, as for instance the spray of a whip scorpion, which contains 84% acetic acid" (Eisner, 1970). Insects subject to prédation may produce remarkably pure and concentrated secretions of such compounds as aliphatic acids, aldehydes, aromatics, quinones, and terpenes. The repellent effects on predators such as mice and toads are obvious, and sufficient to inculcate future avoidance of the prey. The specialization of secretions for such functions is clear, yet we may hesitate to label them as signals for communication in the fullest sense.

Clearly signal specialization can emerge in interactions between distantly related organisms. Plants have long been known to produce an enormous variety of chemicals, some shed into the environment, others retained within tissues of the plant. While some chemicals are involved in basic metabolic processes, many were long regarded as no more than excretory by-products. We now realize that many are specialized for functions in the realm of what we can begin to think of as "chemical ecology" (Whittaker, 1970).

Some plants secrete compounds that hinder the germination, growth, and survival of other plants. Leaves, fruits, and twigs of walnut trees, for example, produce hydroxyjuglone, which is carried from the leaves in raindrops to be released in the soil in the oxidized form juglone. This compound has the effect of inhibiting growth of seedlings of many other plant species, hence the sparseness of undergrowth under walnut trees. Another example of "allelopathic" compounds are the volatile terpenes produced by sagebrush and salvia in California chaparral. They too are said to discourage growth of other plants. Some chemical plant products, poisons, or unpleasant flavors are designed to discourage phytophagous predators. Such defenses may be aimed at vertebrate and invertebrate animals, and even at fungi and bacteria, the classical example being, of course, penicillin, evolved by a fungus as protection against bacteria.

Perhaps the most intricate case of chemical interchange between species was discovered by Brower in butterflies. Birds find monarch butterflies distasteful, and similar mimic butterflies gain vicarious protection as a result. Brower demonstrated that the protective agent, a cardiac glycocide, derives originally from milkweed, the food plant of the monarch larvae. Immune to the poison, they sequester it and pass it in turn to the imago in concentrations large enough to cause vomiting in a bluejay that eats the butterfly (Brower and Glazier, 1975).

Ironically, compounds probably evolved by plants originally for defense may eventually become key stimuli by which highly specialized phytophagous insects locate particular species as food for themselves and their larvae. In fact it seems to be the rule more than the exception that food plant location by insects depends on such idiosyncratic chemical characteristics of a host plant and not on a more direct perception of its nutritive characteristics (Dethier, 1970). Here we see specialization on the sensory side of the system, with insect chemical receptors especially tuned to compounds identifying their host plant.

Williams (1970) has discovered what is perhaps the ultimate in specialized chemical plant defense. Unsuccessful attempts to raise moth larvae to maturity in the laboratory were traced to a particular kind of hand towel paper. A compound eventually isolated from paper derived mainly from pulp of the balsam fir (Abies balsamea) proved to be a close replica of an insect growth hormone, withdrawal of which is necessary for metamorphosis from larva to adult— presumably evolved by the tree for its own chemical defense against plant-eating insects. "Present indications are that certain plants and more particularly the ferns and evergreen trees have gone in for an incredibly sophisticated selfdefense against insect control that we are just beginning to comprehend" (Williams, 1970).

This brief review of chemical stimulus exchanges between plants and animals demonstrates the widespread evolution of highly specialized stimuli, exchanged even between distantly related organisms. One criterion for social communication is surely satisfied—that there be evidence of evolutionary specialization of stimulus production and design for evoking particular responses from some other organism—but others are not. In particular, communication in the fullest sense implies evolutionary specialization of a mutualistic, cooperative nature lacking in the cases cited.

Communication as a Mutualistic Phenomenon

The richest elaboration of systems of social communication should be expected in intraspecific relationships, especially where trends toward increasing interindividual cooperation converge with the emergence of social groupings consisting of close kin. However, a close genetic relationship is not a prerequisite for the mutualistic evolution of systems of communication. The point is made by further consideration of relationships between plants and animals, on a more cooperative plane than those just considered. The relationship between plants and those animals that pollinate their flowers or disperse their fruits, with gain to both, is a cooperative undertaking.

The dispersal of many fruits is aided by their bright coloration, serving as a signal that the dispersing animals can detect at a distance. The adaptation of flowers to animal pollinators is ramified endlessly. Flower design and coloration are often well matched to the visual physiology of particular pollinators. Hummingbird-pollinated flowers are often red, a color attractive to those birds (Grant and Grant, 1968) but less so to bees. Thus, blue and yellow are more common in bee-pollinated flowers. Many bee-pollinated flowers are ornamented with ultraviolet designs, invisible to us though it is the color to which the bee's eye is most sensitive. The patterns serve to lead bees to pollen and nectar, rewarding them with food while pollinating the flower. Many insect-pollinators are also attracted to flowers by their scent. Scent is less common in flowers pollinated by the relatively anosmic birds. However, bats have a keen sense of smell, and flowers specialized for pollination by them often have a strong musky odor (Baker, 1963).

While there is extensive convergence in the design of flowers pollinated by the same classes of pollinators, there are counter-selection pressures for species-specific flower characteristics. This results from competition between flowering plants for the favors of pollinators that are in demand. Diversity in flower design encourages specialization in particular pollinating species, sometimes proceeding so far that plant and insect assume complete mutual interdependence. Alternatively, specific flower appearance and odor may encourage individual pollinators to persist in visiting one flower type for a period of time, whether a season or an hour of the day. This trend toward diversity in the flowers of animal-pollinated plants is evident in the use of flower features in botanical taxonomy. The classification of plants pollinated by birds or bees leans more heavily on the flowers than does the taxonomy of wind- or water-pollinated species— the latter depending more on vegetative characteristics.

Plants may encourage specialization of a particular pollinator by evolving a floral structure that excludes other pollinators, insuring in return for pollination a guaranteed food supply for the particular symbiont. Adaptations to different pollinators occur even within closely related plants such as the phlox family (Grant and Grant, 1965).

All of these interspecific relationships are mutualistic in the sense that cooperative adaptations have been evolved in both partners, another step toward communication in the fullest sense. We should distinguish another kind of species relation in which one is essentially parasitic on the communication system of the other. The orchid family is rich in species, with intense competition for pollinators. Perhaps more than any other plant family, orchids have gone to excess in encouraging specializing by particular pollinators. Their flowers may differ not only in structure but also in odor, known to attract particular species of bees (Dodson, 1970). Some that are pollinated only by males of certain bee species mimic the female bee in flower structure, inducing pollination by the attempts of the insect to mate with the flower. Some of the flowers go so far as to mimic not only female appearance but also odor, varying with the species of the bee (Kullenberg, 1956).

Some of the insects that live parasitically within the colonies of social insects go to remarkable lengths in mimicking signaling behaviors of the host (Hölldobler, 1967, 1970). Perhaps the most remarkable example of parasitization, by one insect (in this case a predator) on the communication system of another has been discovered in fireflies, some of which prey on other fireflies (Lloyd, 1975). Females of one species, Photuris versicolor, attract males of other species to their death by mimicking the flash responses of the prey's own female. They are even able to vary their flash patterns according to the species of the prey. Commenting on the efficiency of the process, Lloyd notes that a female seldom answers more than ten males without catching at least one of them.

Genetics of Social Cooperation

Imagine a hypothetical "kinship" series of animal interactions ranging from distant relatives at one extreme to very close relatives at the other. At one end are relationships between distinct and distant species. Next comes interplay between related species, then conspecific but interracial interactions. Relationships between a single population of a species will follow, then those within family or kinship groupings, with the other extreme represented by within-group interactions of social insects such as honeybees, where most members of a society are sisters.

The more similar two animals are to each other, the more likely they are to depend on similar resources—to have similar hiding and nesting places, to obtain similar foods in the same ways at the same times. Since genetic similarity implies sharing of morphological, physiological, and behavioral characteristics, the hypothetical series indicated above manifests a trend toward increasing competition, though not necessarily toward increasing competitiveness, in the sense of active interference of one individual's resource exploitation by another. A close genetic resemblance also has other implications for social evolution.

The proper focus for theories of social evolution is not on individual animals but on genotypes. If an animal is living together with close genetic relatives, then natural selection will tend to minimize aggressive interference with them despite their dependence on virtually identical resources and their potentially potent competitive relationship. Here then is a countertrend to the effect of competition, exerting an opposite influence on the likelihood of cooperative relationships emerging. At some point along the kinship series the trends are likely to achieve a kind of balance, varying with circumstances, but nevertheless tending to hover around a level that will be characteristic of a species, and perhaps different from one species to another, depending upon the degree of intraspecific genetic diversity. In a genetically homogeneous species cooperative relationships are likely to prevail in all intraspecific relationships. In a species that is genetically more heterogeneous, the balance is more likely to be found with smaller social groupings, perhaps at the level of a social group or family.

Communicative behavior will be of paramount importance in achieving and modulating cooperative relationships. Thus, the genetic makeup of a typical social group is likely to bear on the degree of elaboration that the communication system of a species exhibits. The most advanced accomplishments should evolve in animals whose societies are so constructed that groups of very close genetic relatives live together in social contact. Where then should we look but among the social insects, where entire colonies may be composed of the children of a single mother, as in the honeybee (Wilson, 1971)? We should not be surprised in hindsight that one of the most remarkable examples of social communication was discovered by von Frisch (1967) in the dancing behavior of the honeybee. Remarkable for the precise correlations between circumstances of food found and various characteristics of the dance, conclusive proof of its communicative significance, independent of olfactory characteristics of the food source and its environs (Wenner, 1971), was obtained only recently. By ingenious experimentation Gould (1974) was able to modify the dance in such a way as to send foragers in new directions where none had been before, thus establishing that they can be guided by the dance alone.

It is hard to know where to look among vertebrates for comparable examples, for so little is known about the genetic structure of their populations in nature. Theorizing about the origins of vertebrate social behavior is seriously hindered as a result. There are suggestions that some vertebrates, such as house mice and some other rodents, live in quite inbred social groupings (Selander and Yang, 1969; Anderson, 1970). There is evidence that troops of wild baboons with adjacent home ranges are somewhat separated genetically (Buettner-Janusch, 1963, 1965). However, we need data on species differences in genetic composition before theorizing can advance significantly.

Given the importance of kin groupings in the evolution of social communication and other aspects of social cooperation, it would be advantageous for populations to evolve means of discriminating kin from others, of refraining from interaction with non-kin, or even of repelling them aggressively from the social group.

For species such as primates that are born into a close-knit group in which everyone knows everyone else and that grow up within it, discrimination of strangers is a step toward discrimination of kin from non-kin. It is surely more than coincidental that strange conspecific individuals provide the strongest stimuli for aggressive repulsion in a variety of species (e.g., Bernstein, 1964; Southwick, 1967, 1970; Rosenblum et al., 1968; Scruton and Herbert, 1972; Marier 1976).

A more complex vehicle for discriminating kin from others is provided by learned dialects in bird song (Marier and Mundinger, 1971). Several attempts have been made to explain their functional significance, such as the theory that population markers encourage birds to settle and mate with members of the birthplace population, perhaps perpetuating local physiological races (e.g., Marler and Tamura, 1962; Nottebohm, 1969, 1975; Nottebohm and Nottebohm, in press; Nottebohm and Selander, 1972). Learned bird song dialects may also favor kinship groupings as a step in social evolution. There is evidence that both male and female white-crowned sparrows are more sensitive to the dialect they learned in youth and that a dialect boundary does indeed block gene flow to some extent (Baker, 1974, 1975; Marler, 1970b; Milligan and Verner, 1971). Playback studies with recorded bird songs also reveal a tendency for strangers' songs to evoke more intense attack and repulsion than the familiar songs of immediate neighbors (e.g., Falls, 1969; Kroodsma, 1976).

Assuming that young birds are prone to settle near their birthplace, repulsion of birds with strange songs may also favor the integrity of local kinship groupings. One may hypothesize that the cooperative interactions between neighbors that are thus favored increase efficiency of the local population in competition with others, and in turn contributes to the increased fitness of its members. The same may be true of primate troops. It is conceivable that a significant amount of social behavior is directly or indirectly concerned with the genetic structuring of local populations. Only long-term studies of the genetics of natural vertebrate populations can test the validity of this proposition.

Choosing a Sensory Modality for Communication

Depending on the biology of the species, signals of one animal may help others to reproduce effectively, to avoid prédation, to get more efficiently to food and water, or simply to find their way about in their environment. By controlling the pattern of individual interactions, and tendencies of animals to cluster or disperse depending on what they are doing, communication will also serve the particular societal structure of the species.

Spacing is a critical issue. Imagine the requirements for a signal that aids in spacing apart adjacent social groups. Efficient exchange requires signaling over a distance with a stimulus that a respondent can localize in space. The possibilities will depend in part on the particular sensory modality chosen—whether visual, auditory, chemical, or even electrical. The phylogenetic history of species will involve many such evolutionary choices, made within limits set by the basic sensory and motor endowment. The nature of the environment will play a role. For forest birds or monkeys that require signals to maintain intergroup spacing, auditory signals are appropriate. Auditory exchange is less hindered by obstacles than is vision, and sound frequencies and temporal coding of auditory signals offer many features on which distinctive categories may be based. Playback of recorded vocalizations of the African mangabey Cercocebus atrogalaris has shown that one of them, the distinctively patterned "Whoop-gobble," does indeed play a role in mutual avoidance of adjacent groups (Waser, 1975). The "Whoop-gobble" provides for identification of both species and individual, as well as remarkably accurate localization of the caller, as Waser has been able to demonstrate under field conditions.

For communication within a monkey troop rather than between groups, the odds seem to shift in favor of vision as the best medium for diurnal signaling, though sounds serve as well. In a crowd, visual signals are easier to locate than sounds; it is hard for an animal with any but the most primitive visual receptors to avoid locating the source of a visual stimulus in the very process of perceiving it (Marler and Hamilton, 1966).

The elaborate spatial coding that is readily achieved with visual stimuli as a result of their inherent directionality and separability is harder to envision with sounds. Simultaneous signaling is possible with several independent varying expressions of face and body, and perhaps with independent elements within an area such as the face, and human ethologists and anthropologists are beginning to explore the nature and communicative role of such visual signals (Eibl-Eiblesfeldt, 1970; Ekman, 1973).

Vision obviously has limited value in dim light or at night, except for special cases such as fireflies, which provide their own light source (Lloyd, 1966). In the many organisms that are active in the dark or that lack well-developed directional eyes, chemical signals are more important. The lack of dependence on ambient light is not the only advantage. Chemical signals have a durability that sounds lack. Durable visual signals are rare in animals, except for trails, rubbing posts, nests, and the like, although our own species makes extensive use of them.

The potential control of rates of fading, which adds an important dimension to chemical signal diversity, is another reason for the choice of a chemical signal when animals require durable signals. There is an abundant literature on animal marking behavior, by which chemical secretions placed on some other animal or on objects in the environment continue to be transmitted in the absence of the original marking individual (Ralls, 1971; Eisenberg and Kleiman, 1972). Chemical secretions on an animal's own body may have a profound impact on its social interactions with others. An aggression-eliciting pheromone is produced by male mice whose testes are actively producing androgens, radically changing their valence as stimuli for aggression in other mice (Lee and Brake, 1971 ; Lee and Griffo, 1973; Mugford and Nowell, 1971). The remarkable energetic efficiency of chemical communication is also relevant. It has been calculated that a receptor cell on the male silkworm moth's antenna requires only one molecule of the female sex substance, bondecal, for her presence to be detected (Schneider, 1965; Wilson, 1971).

When it comes to location of chemical signals, however, there are problems. It is one thing for a male to detect a female's presence and another to locate her. As long as the intervening medium is still, whether it is air or water, location of the source of a chemical signal is only possible by reference to the diffusion gradient. At more than a meter or so from the source the gradient is so gradual that orientation is difficult. With a moving medium it is much easier, and animals using olfactory signals over a distance make use of such movement. Release of a female moth's sexual attractant may be delayed until there is a breeze blowing of a certain speed, not strong enough to generate excessive turbulence, but strong enough to carry the scent downwind (Kettlewell, 1946). As the searching male moves upwind, backing when he loses her, he can get close enough to switch to other strategies.

Thus, each sensory modality has drawbacks and advantages. For certain fish there is still another choice, electrical signaling, originally discovered to be a system of object location and general orientation to the environment (Lissmann, 1958). More recently it has been shown to sustain a system of social communication (Hopkins, 1972, 1974) permitting electric fish to identify species, sex, and age of a partner and also providing some information about its motivational state.

When communicants are close to one another or in contact, other sensory modalities such as touch and taste become available for communication, with distinctive properties of their own. Perhaps for the reason that it requires contact, touch often seems to assume special social functions. Violent tactile contact may cause pain and social disruption. Gentle touching, on the other hand, especially as manifest in social grooming, recurs repeatedly among animals in situations where it can promote peaceful contact and at the same time reduce the likelihood of social violence (Sparks, 1964, 1967; Morris, 1971; Simpson, 1973).

Are Animal Signals Arbitrary?

The words in our language are arbitrary in two senses. Most words are semantically arbitrary, bearing no resemblance to their symbolic referent, other than in onomatopoeia. The word food does not resemble anything we eat. Thus, there is no obstacle other than inertia to the exchange of meaning of two words in the course of cultural evolution. Words exhibit another kind of arbitrariness in that there is nothing intrinsic to the process by which a word conveys information about food. Our speech does not require a word to have any particular acoustical properties, even those affecting locatability, for example.

Semantically, many animal signals are also arbitrary. The grunting sound by which chimpanzees announce discovery of a choice meal and readiness to share it has no morphological relationship to its referent—perhaps a cluster of ripe palm fruits.

African vervet monkeys have a repertoire of distinct alarm calls for different types of predators (Struhsaker, 1967). While some of the associations are rather general, others are specific enough to invite the speculation that they have wordlike properties. In particular, of the three that announce danger from (1) a venomous snake crossing the territory, (2) an eagle overhead, and (3) an approaching leopard, each evokes a different response functionally appropriate to the particular threat. Such calls have no iconic resemblance to the predators they symbolize. In this sense many though not all animal signals are semantically arbitrary (cf. Altmann, 1967).

Nevertheless, animal signals often possess physical characteristics that make them uniquely suited for the particular function they serve. Thus the exchange of meaning between words that we can easily imagine taking place in the evolution of speech patterns is often less likely with animal signals. In this sense the physical structure of many animal signals is far from arbitrary.

Some sounds require transmission over considerable distances, while others operate at close range, and their loudness varies accordingly. Among forest monkeys of East Africa, sounds males use to space troops apart are louder than those used within the group for coordinating foraging movements (Marler, 1973). The transmission distances of different sound frequencies vary with different habitat structure, and there is some evidence that male birds compose their songs of sounds that travel farthest in their habitual environments (Morton, 1975; Chappuis, 1971). Woodland bird songs, often consisting of medium-pitched pure tones, probably illustrate such adaptations.

Whales provide what is perhaps the most remarkable case of adjustment of vocal behavior to long-distance transmission. By using very low-pitched sounds, barely audible to our ears, and placing themselves at an intermediate depth in the ocean, in the so-called "deep sound channel," humpback whales are thought to be able to hear each other calling over distances measured in hundreds of miles. Because of the refraction of sounds by the thermocline near the ocean's surface and by compression layers deep in the ocean, sound waves are trapped within the channel, retaining much more of their energy than they would if they impinged on the surface or floor of the ocean (Payne and McVay, 1971; Payne and Webb, 1971).

The physical structure of the animal signals is related to their function in many ways. The importance of sound localization has already been indicated, and many bird signals are designed to provide an abundance of cues that permit localization by companions to be accomplished quickly and accurately. Other sounds are structured to minimize the clues available for localization, still serving to spread alarm to companions, while giving only a minimum of localization cues to a predator (Marler, 1955). By experimenting in the laboratory with owls trained to strike at sounds, Konishi (1973) could demonstrate that sounds like the hawk alarm calls of small birds are hard for an owl to locate.

The chemical signals of insects illustrate other kinds of adaptation to signal transmission. The molecular properties of pheromones often correspond nicely with functional requirements (Wilson, 1970). Using a ratio of the emission rate in molecules per unit time in relation to the behavioral threshold concentration as a frame of reference, a low ratio of the former to the latter indicates a slowly emitted signal with a very small "active space"—a three-dimensional volume enclosing the space where the threshold level for behavioral response is exceeded by the pheromone concentration. Such characteristics would fit well with a substance to be used in trail marking, by fire ants for example (Wilson, 1970). For a pheromone designed to transmit alarm different characteristics would be appropriate, with a larger active space and a more rapid diffusion rate, a prediction that can also be verified. The largest active space is found in the sex attractants of female moths, required to function over distances much greater than would be appropriate for communicating danger.

One could continue recounting examples of adaptations of signal structure to function. This review is not intended to be exhaustive, only to establish the point that in this rather special sense the structure of many animal signals is by no means arbitrary.

The Triggering of Signal Production

In spite of the logical difference in the symbolic or semantic significance of an alarm call and a sexual call, one with an external referent, the other without, the production of both must be associated with particular physiological states of the signaling animal, one externally triggered, the other generated endogenously. The process of symbolization would be easier to grasp if we knew more about the nature of these physiological states and the way they are engendered. If the soliciting female bird is signaling about physiological events that preface ovulation, such events are largely endogenous and cyclic in nature, arguing against the need to invoke an immediate trigger from the environment that one could then think of the solicitation call as symbolizing. The same might be said of other signals such as the begging call of a nestling bird. While this call may be triggered by approach of a parent, it often occurs without external provocation, as the nestling becomes hungry. The same duality is found in the singing of many birds, sometimes externally triggered but often starting without any precipitating event in the environment.

This distinction between signals that are externally and internally triggered, at first sight rather basic, may be less radical than it seems. Consider an alarm signal, usually triggered by an environmental event. One might be tempted to think that the role of internal physiology in its production is minimal. However, a bird that is alert or nervous is more likely to give alarm when danger threatens than one that is sleepy or relaxed. Thus, the physiological state at the time of confrontation with a predator cannot be ignored if we are to understand the process of alarm call production. Similarly the response evoked by an alarm signal in another bird will vary according to its state of arousal at different times or its previous learning experiences.

One may carry this line of thinking further and suggest that no reaction of an organism to an external stimulus can be understood without taking its current physiological state into account. Some stimuli evoke similar reactions across an array of physiological states so broad that one is tempted to ignore the significance of internal events. But these are cases where the particular reaction has high biological priority, so that the necessary physiological machinery must be in readiness much of the time. One may assert that the proper way to think of all stimulus-response relationships is as interactions between the organism and its environment (Marler and Hamilton, 1966). While the environment may provide a trigger responsible for orientation and timing of a reaction, the particular structure of the response, its coordination, its internal timing, and often even its orientation and intensity can be understood only by reference to the prior history of the subject (cf. Bullock, 1961). The responsiveness of an animal at the time of a particular stimulus event is the result of convergence of a multitude of past events reflecting the previous experience the individual, its genotype, and the particular pattern of environmental interaction experienced up to the instant of stimulus confrontation.

According to this view, physiological considerations are as important in the interpretation of a signaling action that has an external trigger as they are with internally triggered signals. One can also assert the converse, that signals endogenously triggered should not be thought of as completely independent of the external world. They are independent only in the sense that no immediate outside trigger is detectable. The precipitating endogenous event in the signaler's physiology reflects a history of innumerable prior environmental interactions, some closely related to the signal, others only remotely.

The sexual calling of a receptive female bird may lack an immediate environmental trigger, but it is nevertheless dependent on many prior environmental interactions, some with only a general bearing on the timing of ovulation, such as the requirements for normal growth, and others with a specific bearing such as increasing day length, social stimulation, and sensory feedback from nest-building activities.

The conclusion may be drawn that to speak of a signaling act as being "internally" or "endogenously" triggered implies no more than that its timing and structure are functions of prior events in the history of the individual, their influence being conveyed to the present by physiological means.

"Affective" Signaling: A Valid Category?

It is a commonly expressed view that the signaling behavior of animals is more susceptible to control by the kind of physiological states known in common parlance as "affective" or "emotional." The judgment that a state is emotional can be based on a number of different interpretations. Recurring themes are that the states are generalized, affecting many patterns of behavior; that autonomic arousal is often involved; that there is often some connotation of emergency in the tempo, intensity, and demeanor of the signaling animal; that there is often strong "momentum" to the behavior so that once begun it tends to continue for a period of time, resisting rapid change; that it is involuntary, or toward that end of a continuum with voluntary actions; that it is less susceptible to modification by learning or conscious effort; and that it can be placed somewhere on a dimension of pleasantness to unpleasantness.

Human signaling behavior, or at any rate, speech, is said to contrast with animal signaling in that it is voluntary, detached from any necessary linkage with pleasantness or unpleasantness, readily modified by learning or conscious decisions, not necessarily tied to autonomic arousal or other generalized physiological states, not necessarily associated with behavioral emergencies, and involved with physiological states that can change very rapidly.

The contrasts listed above, attempting a brief summary of a complex and difficult subject (e.g., Arnold, 1970), undoubtedly point to a significant difference between animal and human signaling behavior. In most of the circumstances in which animal signaling occurs, one detects urgent and demanding functions to be served, often involving emergencies for survival or procreation. To the extent that physiological states of emotion or affect are indeed distinguishable from other substrates for behavior, they have surely evolved to organize actions and responsiveness to stimulation in complex spatiotemporal terms, serving a variety of functions (e.g., Plutchik, 1970), not the least of which is to avoid inefficient vacillation in the face of conflicting environmental demands (cf. Pribram, 1970). Their pervasive influence on our own behavior is obvious, especially in social situations.

Firm resolution of this problem is difficult, but it is worthwhile to consider whether all animal signaling is as dominated by affect as is supposed. To take one example, we have already considered the vervet monkey's sound using different alarm calls for different types of predator (Struhsaker, 1967). The calls do not intergrade, and it is not obvious that they fall on a continuum of differing levels of arousal. To explain the vervet monkey's complex alarm-signaling behavior several different underlying physiological states must be postulated, seemingly more specific in nature than the emotional condition usually denoted as "fearful." However, these alarm calls do conform with another common attribute of emotional behavior, namely regular association with a complex of other, more directly functional behaviors. But it is usually the case that an animal signaler is itself engaged in the same functional behavior that is being signaled about. Insofar as monkeys are not known to engage in relaxed discourse about events in the distant past or future, there will be few if any occasions when a signal is likely to be dissociated from the other overt responses to a situation. Indeed, a monkey prone to such reflective signaling in the presence of a predator would probably not survive very long. Thus the issue of signaling about events remote in time, for which our speech seems more specialized than animal signaling, is much entwined with the issue of freedom from affective physiological control.

One circumstance in which such dissociation can be detected in animals is during play. Among the diagnostic criteria for play behavior are several that are reminiscent of distinctions between human speech and animal sounds (Marler and Hamilton, 1966). Separation of the behavior from its normal emotional substrate is sometimes mentioned, and there is correspondingly more freedom in switching from one pattern to another or reversing social roles than in the adult emotional version of the behavior. During play, signals are sometimes separated from the other ongoing behaviors that normally accompany them. Investigation of the distinctive physiological characteristics of play may well throw light on this distinction between affective and nonaffective signaling behavior.

One may also ask whether our speech is altogether free from emotional constraints. Autonomic arousal is a common accompaniment of speaking behavior, as is evident from the use of polygraphic lie detectors. Some psychoanalytic practices rest on similar assumptions. One does not need a galvanometer or an electrocardiograph to be convinced that speech uttered in social circumstances often has strong emotional components. Furthermore, some research on the physiology of human emotions seems to contradict the old notion that only a few simple physiological dimensions are involved. Two distinct components have been proposed, even for the most basic emotions (e.g., Schachter, 1970). One component incorporates many of the autonomic and hedonic functions imputed to emotion, and it is associated with the level of arousal; the other "cognitive" component seems to specify more precisely the particular emotion that will be subjectively experienced. While the cognitive is to some extent restricted to a particular emotion, the other may be shared by several emotions. To the extent that this model is indeed a correct one for human emotions, it may also be relevant to animals—at least the autonomic physiology of higher vertebrates seems similar to our own.

Thus, the distinction between generalized and specific physiological substrates for signaling behavior is not always clear. Whatever distinction we are groping for between speech and animal signaling (and it is hard to be sure that we are even asking the right questions), it is my own conviction that the underlying physiology of signaling will prove to be different in degree rather than in kind between animals and ourselves. If only to provoke some reappraisal, I would assert that no firm proof has yet been advanced of any fundamental differences between animals and man in this regard.

Signal Variation: Discrete and Graded Repertoires

That many patterns of animal behavior are stereotyped, especially those with communicative functions, is a deep-rooted notion in ethology, as shown by the concept of "fixed action patterns" (Lorenz, 1935, 1950; Schleidt, 1974). The stereotypy of some is indeed remarkable. Variability of the strutting display of the sage grouse is unusually low by some measures, as are the claw-waving displays of fiddler crabs, and some duck displays (Dane and Van der Kloot, 1964; Hazlett, 1972; Wiley, 1973). Some animal sounds such as certain bird songs and the loud calls of some adult male monkeys are also highly stereotyped (Marler, 1973).

Presumably this unusually narrow range of biological variation reflects some functional requirement. Accurate identification of a signal at a distance, without support by other cues and under noisy conditions, must be easier with stereotyped than with variable signals. However, quantitative description has revealed that extreme stereotypy is by no means a general rule. While some signals are almost fixed, others are exceedingly variable, as some monkey calls (e.g., Rowell, 1962, Rowell and Hinde, 1962; Green, 1975; Marler, 1965, 1970a; Marler and Tenaza, chapter 36, this volume).

What interpretation can be placed on this variation in degrees of stereotypy? Should it be viewed as a consequence of poor developmental control, or can some communicative significance be attributed to it? The problem that exists in interpreting variation in individual signals recurs at the level of entire signal repertoires, some of which are organized discretely, while others are highly graded. Within the repertoire of the African blue monkey, loud calls of the adult male, though superficially similar, proved to be categorically distinct (Marler, 1973). "Growls" and "pulsed grunts" grade into one another, however, by a series of intermediates.

The sound repertoires of certain animals contain few if any discrete sound types at all. The most extreme cases studied thus far are certain primates, notably the red colobus (Marler, 1970a), rhesus, and Japanese macaques (Rowell, 1962; Green, 1975), the talapoin monkey (Gautier, 1974), and the chimpanzee (Marler and Tenaza, chapter 36). In these species a major part, if not all, of the vocal repertoire consists of a single graded acoustical system. The grading may occur in several acoustical dimensions independently, such as frequency, tonal structure, and duration, each varying continuously, making it unrealistic to subject the sounds to a strict categorical classification.

Even in discrete signals, fine variation in morphology probably has communicative significance. The "chip" alarm call of female blue monkeys is discretely separate from other sounds in the repertoire. Nevertheless variations in intensity, frequency, morphology, and timing have the potential for conveying information to others, although presumably animals will be less sensitive to within-category variations than to variations between categories. The extent of within-category variation may differ from one signal to another in the same repertoire. The point is illustrated by vocalizations of the black and white colobus (Marler, 1969, 1972). The roaring of the male probably serves functions similar to the male loud calls of the blue monkey, namely the maintenance of territorial spacing and the rallying of group members. It is discretely separate from, for example, a system of squeak-screams used by adults and juveniles. Unlike roaring, where variability in structure and timing occurs but within limits, squeaks and screams vary along a number of dimensions. It is notable that they are used primarily for communication within the troop, whereas roaring includes an inter-troop function. Similarly the growl-pulsed grunt continuum of the blue monkey functions at close range within the troop, while that part of the repertoire especially concerned with distance communication, whether within or between troops, tends to fall into discontinuous, discrete categories.

If a species living in dense forest is socially organized in territorial groups, with a significant part of the vocal repertoire addressed to problems of intertroop communication, signaling must take place over appreciable distances in environments noisy from wind and sounds of insects, birds, and other primates. There must be strong selection pressures in such circumstances in order for a discrete type of signal organization to operate as the most efficient means of unequivocal conveyance of information to an adjacent troop. Any potential that graded signals might otherwise have for communication of more refined information over such long distances would surely be lost by signal degradation and masking. Pressures for specific distinctiveness would also favor discrete acoustical morphology and patterns of delivery.

Within the troop circumstances differ. Signaling is likely to occur over a shorter range. Even in a forest full of obstacles communicants in the same troop can often see as well as hear one another, ançl visual signals emitted in tandem with sounds may aid communicants in detecting and identifying the subtleties of graded signaling.

This line of argument can be brought to bear on those species that show excessive emphasis on signal grading in their vocal repertoire. In the absence of territoriality, greater group size, and more complex troop organization resulting from the presence of several adult males, we see a shift in emphasis toward intratroop communication, and a corresponding increase in the degree of grading of vocal repertoires. Far from representing disorderly erratic variation, as though from poor developmental control or relaxation of the relationship between vocal morphology on the one hand and ongoing behaviors and their physiological substrates on the other, this variation is in fact highly ordered, as demonstrated in both the Japanese macaque and the West African tala- poin monkey (Gautier, 1974; Green, 1975). There can be no doubt that the graded repertoire of the Japanese macaque has the potential for conveying subtle and complex information about the circumstances of sound production. Further work is required to establish whether or not these variants are responded to differently.

It is intriguing that the constellation of behavioral and ecological traits that, with some exceptions, tends to characterize those primates with a graded repertoire—large, nonterritorial, multi-male groups with a tendency to move on the forest floor and to invade open country—is consistent with speculations about the probable ecology and social organization of early man (Washburn, 1961; Campbell, 1972). Notably the list of primates with a predominately graded vocal system includes the chimpanzee, the closest of all other surviving primates to human ancestry in its behavior, social organization, and temperament, as well as its tool preparation and use and its habit of hunting and eating mammalian prey (van Lawick-Goodall, 1971; Teleki, 1973). It is all the more intriguing to note that sound spec- trographic descriptions of the structure of speech reveal that many adjacent speech sounds do in fact grade into one another in their acoustical morphology although they are heard as discretely distinct (e.g., Lisker and Abramson, 1964).

Specific Distinctiveness of Animal Signals

Behavior can be as revealing as external morphology in the diagnosis of difficult species, as every naturalist knows. However, the application of behavior to taxonomy is not easy. While their behavior may differ in some respects, species can be exceedingly similar in others. In trying to understand why some signals are so much more specifically distinct than others, it is important to remember that species do not live alone but in communities that include many other organisms. While it is an advantage for a species to possess "private" signals for functions most efficiently performed in interaction with conspecific animals, as with reproduction and often with aggression, the kind of "privacy" achieved by a high degree of signal species-specificity can also be a disadvantage. Alarm calls are often similar in groups of species living together. In both birds and monkeys interspecific communication has been found to occur frequently (Marler, 1957, 1973). Interspecies similarities in the calls used can only facilitate such interchange, thus serving a definite function. By contrast, the songs of male birds and the loud calls of male forest monkeys, serving reproductive isolation and spacing apart of conspecific troops, are specifically distinct from those of cohabiting relatives. The point serves as a reminder that the characteristics of the community in which a species lives may bear on its communication system. Thus, the resemblance in male songs and aggressive display calls of certain cohabiting bird species makes sense when one appreciates the possibility of special cases of interspecies competition as an influence on communication system design (Marler, 1960; Cody, 1973).

The Experimental Value of Modified or Synthetic Signals

Although few zoological studies of animal communication have gone farther than signal description, some investigations point the way to more analytical approaches. Once the functional role of a communication signal has been established, it is desirable to establish which components of the signal are necessary for a given response and which are redundant. Having answered this for one context, one must explore others because it is likely that a different subset of components assumes significance in other situations, with other recipients, which has proved to be the case with bird song (e.g., Falls, 1969; Emlen, 1972). The ideal approach to such problems is to synthesize signals artificially so that their structure can be changed systematically in one direction or another, along natural or unnatural lines of variation, to establish the limits of effectiveness in different situations. The approach has proved fruitful in studies of speech perception (e.g., Liberman et al., 1967) and may work as well in studies of animal communication.

An illustration is provided by Hopkins' (1972, 1974) studies of communication in electric fish in Guyana. In one of ten species living together, Sternopygus, he found the discharge pattern to be distinctly different from those of other fish present, the pulse repetition frequency being unique. Male and female frequencies were found to differ consistently, and, by working in the field during the rains when the fish breed, he found males embarking on courtship as the electric signals of an approaching female Sternopygus became detectable. Having hypothesized that the frequency difference was fundamental, he synthesized songs in which the only remaining natural property was the frequency, carried by a sine wave. Males courted the electrodes as long as the frequency fell within normal female range. If it was too low, approaching that of male Sternopygus, or too high and approaching the range of another species, Eigenmannia, the courtship ceased. Thus, although the electric discharges have other distinctive properties such as pulse shape, frequency seems to be the key property in this case (Hopkins, 1974).

The croaking of a bullfrog is another synthesizable animal signal. Capranica (1965, 1966) found that male frogs in a terrarium would readily croak in reply to recordings of their species, but not to sounds of thirty-three other frogs. Choosing to concentrate on the spectral structure and wave-form periodicity of the croaking, Capranica experimented with many synthetic calls. He demonstrated three key frequency characteristics that an optimal call must satisfy. Two spectral peaks are needed for maximum responsiveness, one around 200 Hz and another at 1,400 Hz. A sound with energy in only one of these regions is less than optimal in evoking a male bullfrog's response. In addition the call should have a minimal amount of energy in the mid-frequency region, around 500 to 600 Hz. The optimum periodicity in the temporal waveform should be around 100 per second. A mating call with all of these spectral and temporal features will evoke the greatest response from another male bullfrog.

Rigorous definition of the significant stimulus parameters prepares the way for exploring the physiological mechanisms underlying such specific responsiveness (Capranica and Ingle, in press). A fascinating correspondence is found with the pattern of sensitivity of the peripheral receptor systems in the bullfrog's auditory system. Detection of the mating call seems to involve excitation of both the amphibian and the basilar papilli of the inner ear. The low-fre- quency peak around 200 Hz seems to be the one that best excites the complex sensory units tuned to this part of the spectrum in the amphibian papilla. The high-frequency peak, around 1,400 Hz, excites the simple units of the basilar papilla. The further requirement that the optimal call should lack energy in the mid-frequency region, around 500-600 Hz, was identified with the inhibition of the low-frequency complex units of the amphibian papilla by sounds of this frequency. The maximum response of both simple and complex units to pulsed stimuli was obtained with a periodicity of 100 pulses per second, thus explaining the temporal wave-form of the optimal bullfrog call.

The bullfrog's detection of the species call is a direct reflection of the response characteristics of the amphibian and basilar papilli of his ear. Carrying this approach to study of sensory mechanisms in other frog species with different patterns of calling has revealed species differences in the sensitivity of these same sensory units. Thus, species differences in the peripheral stimulus filtering properties of the ear go far to explain the species-specificity of their calling behavior. As Capranica and Ingle indicate, such species differences in the sensitivity of hearing are less obvious in the peripheral auditory organization of birds and mammals, probably because their biology requires the detection of a greater variety of sounds from the environment than the biology of frogs does.

The general functions required of sense organs will have an inevitable influence on the type of physiological stimulus filtering evolved to meet the requirements for specific stimulus responsiveness. If such functions are simple and restricted, dominated by some particular function such as seeking out the opposite sex, then highly specific responsiveness can be imposed at the level of the receptors. Where more versatile sense organs are required, then more complex solutions to the physiological problem of stimulus filtering must be found (Marler, 1961).

Animal Signals as Predictors

The question of how animal signals came to have survival value for members of a species can be approached in different ways. One is to assume that a signal from animal A helps animal B to "anticipate" or "predict" future events. As a simple illustration, an alarm call given by a bird that sees a hawk permits other birds within earshot to behave as though they were anticipating or predicting a future approach of the predator, so they also rush for cover. If this reaction evoked by the signal has some regular and exclusive relationship to a particular environmental situation or referent—a hunting predator in this case—one may think of the signal as serving as a "sign" or "symbol" for it. The food call of chimpanzees, known as "rough grunting" (Marler and Tenaza, chapter 36, this volume), can be interpreted similarly. Other chimpanzees that hear it approach quickly, eager to partake of a preferred food, as though the call serves as a symbol for it.

Such a semantic interpretation by an animal seems appropriate when production of the signal is contingent upon a particular environmental situation or object that serves as an external referent. However, many animal signals are produced in circumstances where no external referents exist, such as those signals associated with agonistic behavior or copulation. Responses to such signals seem better interpreted on the basis of a prediction of how the signaling animal is likely to react on approach of the respondent. If the utterance of a sexual solicitation call by a female bird triggers full courtship in a responding male, it seems more appropriate to interpret his actions as based not on some external circumstance she is signaling about but rather on her anticipated or predicted response to his approach—assuming that the solicitation call is unique to the period of female sexual receptivity.

Selection of a Subset of Respondents by a Signal

When a respondent receives a given signal from a distance, its behavior may change in a specific, qualitative fashion. But often the first response that an observer can detect is no more than a change in its spatial relationship to the signaler. Thus, two signals that may eventually elicit very different responses—attack or copulation, for example—may first elicit an identical response, namely approach to the signaler. Sometimes a keen ethological eye detects other behaviors that permit a more specific prediction of the final response; an aggressive approach might be distinguishable from a sexual one for example. Such additional cues are often lacking, however, which makes the specific end point of a sequence initiated by signal-elicited approach difficult to predict. It may become predictable only later in the sequence, after further stimuli have been received. The culmination of an aggressive approach, for example, can vary widely, depending on further stimuli exchanged between sender and receiver.

Thus, while it is sometimes useful to speak of sexual signals, aggressive signals, alarm signals, and so on, it is often difficult to distinguish the responses that such categories of signals do in fact elicit. Both aggressive and alarm signals may elicit withdrawal of a respondent in some circumstances. In spite of the difficulties it is intriguing to consider approaching the analysis of signal function by a classification of the types of behavior that are evoked (Marler, 1967).

If a respondent withdraws in response to a signal, we usually classify this withdrawal as a form of escape behavior, our confidence in this judgment increasing if we see signs of autonomic arousal and excitement. Locomotion may be followed by tense immobility in a place of concealment. It remains as something of a paradox that the active and inactive phases of withdrawal are classified in the same behavioral category. Nevertheless, the number of respondent behaviors that succeed withdrawal from a signaler is relatively small.

By contrast, approach to a signaler can be followed by many possible types of respondent behavior, including genital contact; suckling, nursing, and other parent-young behaviors; food sharing, exchange, or stealing; competition for resting or breeding sites, or sharing of them; attack on the signaler or on another animal close by, such as a predator; or a variety of social activities such as standing close, sleeping together, grooming, and so on. We can exclude activities like foraging that may continue irrespective of changes in relative spacing of signaler and respondent. It is implicit in much of our thinking that the alternative response selected by the receiver of the signal is specified by that same signal that elicited the initial approach. In fact it seems likely that the specification is often partly or largely a function of further signals received during the approach or after it.

If the first response to many signals is approach with other signals responsible for further specification, one might question what advantage a species gains from having many different signal types for long-distance signaling. Would not one signal type suffice to elicit the approach? However, we must bear in mind that not all who hear a given signal will respond by approaching —this is obvious if one thinks of an infant signaling for its mother or a female soliciting for copulation. Diverse signals are still required to specify the appropriate class of respondent. The need for such diversity stems directly from the many different communicatory roles that individuals may play in a society, such roles being by no means interchangeable.

The thrust of this discussion is that some signals function not so much to impose a qualitative change on the behavior of respondents but rather to select a particular class of respondents that may be already predisposed to perform the response in question. A female monkey who has recently given birth will have a different set of response predispositions than an adult male engaged in consortship behavior. This fact greatly complicates the experimental analysis of communicative behavior, requiring exploration of the presence or absence of responses to a signal in all possible classes of recipients, some responding, others not, some inclined to respond in one mode, others differently. One may imagine the appropriate respondent being specified along several dimensions, including species, sex, age class, dominance status, individuality, and recent social history. The specification might also be made indirectly, addressing potential respondents that find themselves in a particular environmental context, as when vervet monkey alarm calls elicit different responses from animals out in the open and others already deep in cover. The specification might also be made according to a transitory physiological state—e.g., a food signal evoking a response from hungry animals but not from satiated ones.

Natural selection is likely to favor contrasting trends in the evolution of signals functioning to select different classes of respondent. Where restriction to members of the same species is favored there will be a strong tendency for emphasis on species-specificity. The converse will be true when the facilitation of interspecific communication conveys some advantage, the specification of appropriate respondents being broadened to cover several species. The similarity of alarm calls across species of birds and monkeys has been interpreted in this way (Marler, 1957, 1973). If specification of a particular class of respondents is facilitated by use of a signal that shares attributes with signals used by that class, then we can see how the specification of sex, individual, or age class of respondent may become reflected in the type of signal used for this function.

In the course of this brief discussion of respondent specification, we have concentrated on signals evoking approach from a distance. As the distance between signaler and respondent shrinks, the specification of alternate response patterns is likely to narrow. At closer range some of the difficulties of communication are eased, with less chance of error in identifying signals. The opportunity to receive compound signaling through several sensory modalities is increased. And if problems of species or individual specificity have been resolved earlier in the sequence, less emphasis is needed at closer range, and the release from stringent demands for species-specificity may permit further exploitation of other signal characteristics. I have argued in an earlier section that the increased exploitation of signals that are highly graded in structure rather than discrete is favored in such circumstances.

Signal Development: Genetic Control and Learning

Modifiability through learning, for which our speech has such rich potential, is sometimes thought to play no significant role in animal signaling behavior, and in some interpretations innateness becomes coupled with the presumption of an emotional basis. Genetic programs for neural outflow from the central nervous system to the signaling equipment have been reported in some organisms, the most striking example coming from the development of calling songs in crickets. In an elegant series of experiments Bentley and Hoy (1972) have shown that hybrid male crickets produce songs distinctly different from either parental song in a pattern that is directly attributable to genetic factors. Even more remarkable is the predisposition of hybrid females to be more responsive to the calling song of their hybrid sibling males than to the song of either parental species (Hoy, 1974), raising the question whether sensory mechanisms may not be involved in the motor development as well. However, there is no evidence that sensory control in insect song development goes so far as to permit modification through learning.

Birds, like humans, rely heavily on communication by sounds in maintaining the structure of their societies. Many songbirds learn their song (Marler and Mundinger, 1971) and at least some other vocalizations in their repertoires as a matter of course (Mundinger, 1970; Marler and Mundinger, 1975). Much has been learned in recent years about the nature and significance of vocal learning processes in birds.

One revealing approach has been study of the effects of deafening a bird surgically early in life upon its vocal development. A dove or chicken deafened soon after birth vocalizes at the normal time, and analysis of the sounds reveals a normal morphology (Konishi, 1963; Nottebohm and Nottebohm, 1971). Thus, a dove or chicken needs no access to an external model to develop normal vocalizations. Nor does such a bird need to hear its own voice in order to generate the normal vocal repertoire.

A contrast is struck with the song sparrow. Taken from the nest and reared as a group in acoustical isolation, young males of this species develop normal song, notwithstanding its greater complexity as compared with dove and chicken vocalizations. Like them, male song sparrows have the ability to generate the complex motor output of singing without the prerequisite of an external model, even though abnormalities are sometimes apparent (Kroodsma, in press). However, if a young male song sparrow is deafened early in youth, his subsequent singing, unlike that of doves and chickens, will be highly abnormal. All of the fine morphology is lost, and instead there is a burst of about two seconds of very noisy, erratic pulsed sounds with a rather insectlike quality. The song sparrow must hear its own voice if normal development is to occur (Mulligan, 1966).

Yet another condition is illustrated by the white-crowned sparrow. Here a young male taken from the nest and reared in isolation in a soundproof chamber will develop a highly abnormal song. Although this song is outside the set of normal patterns for the species, certain qualities of the species' typical song persist. Playback of a recording of normal song to a young male at a certain phase of life, between ten and fifty days of age in this species, results in the subsequent production of a close copy of the external model presented (Marler, 1970b). If a male white-crowned sparrow is deafened early in youth, the song he then develops is rather like that of a deafened song sparrow. It is much more abnormal than that of an intact male reared in social isolation. Almost all species-specific characteristics are lost, including those few that are still retained by an intact isolated male (Konishi, 1965). When deafened, both song sparrow and white-crowned sparrow males behave as though their songs were reduced to the lowest common denominator, perhaps the basic output from the passive syringeal apparatus with air flowing through it. This interpretation is reinforced by the similarity of songs of early deafened white-crowned sparrows, song sparrows, and another relative, the Oregon junco (Konishi, 1964), three species whose normal songs are highly divergent. The inference is drawn that hearing is significant in the divergent pathways normally taken by song development in these three species, not only for hearing external models but also for hearing their own voices.

The discovery that species differences in sparrow songs seem to originate with sensory mechanisms rather than with motor ones led to speculation about the existence of auditory templates. Visualized as lying in the neural pathways for auditory processing, embodying information about the structure of vocal sounds, and having the capacity to guide vocal development, they appear to have a more dominant influence on vocal development than structure of the sound-producing equipment or the characteristics of hearing in general, although they too can have an effect (Konishi, 1970). According to this view, the young male beginning to sing strikes a progressively closer match between his vocal output and the dictates of the auditory template. The transitions he goes through from subsong, to plastic song, and finally to full song are consistent with this interpretation. Species are thought to differ in the competence of the auditory template to guide song development in a fully normal fashion. In the song sparrow the template seems more or less adequate to guide normal development. However, in the white-crowned sparrow the template of a naive male is less adequate, although it may well still be sufficient to focus the male's attention on an appropriate class of external models, thus explaining the finding that a male will reject inappropriate models while he is learning. While the selectivity of learning might depend on a different mechanism, it seems economical to assume that the same one produces both effects. We presumably see in the song of an intact socially-isolated male white-crowned sparrow a picture of what the unimproved template of a naive bird embodies.

Given access to an appropriate external model during the critical period, the template becomes more highly specified, eventually embodying all of the instructions necessary for normal singing, including the characteristics of the particular dialect to which the male was exposed. Note that this learning precedes singing by a hundred days or more, permitting Konishi (1965) to deafen males both before and after learning, but before singing. The outcome was the same, the very elementary song of the trained and then deafened bird revealing no trace of the auditory learning that had already taken place. Thus, hearing is still required for the information incorporated in the improved template to be translated into motor activity. One may also postulate the existence of a similar sensory mechanism in the female white-crowned sparrow, who doesn't normally sing but who is responsive to the male song at the time of sexual pairing (Milligan and Verner, 1971). Konishi (1965) demonstrated that a female induced to sing by injection with androgens is in possession of the same information about song as the male. Not only will she sing, but, if exposed to normal song during early life, she will sing the particular dialect to which she was exposed.

While we can conceptualize song templates as single functional mechanisms, they may involve several physiological components that serve together as stimulus filters. Components that are modifiable through experience might be separate from components that underlie the selective perception of a naive, untrained male. The two sets might operate in series or in parallel, with control shifting from one to the other after training. There may be species differences in the nature, number, and mode of coupling of templates. As with other "feature detectors," one should be prepared for the likelihood that similar behavioral ends may be achieved by different physiological mechanisms.

Most intriguing of all is the possibility that a similar mechanism might underlie the learned development of speech. The studies of Eimas and his colleagues (1971, in press) have shown that some normal perceptual processing of speech sounds occurs in infants as young as a month of age, long before they have begun to speak or even to babble. This result suggests that human infants may possess auditory templates for certain speech sounds. Although they may have heard a lot of speech even by the time they are a month old, the early age raises the possibility that certain speech sounds can be processed without the need for prior exposure to them.

Auditory templates for certain speech sounds could serve a child well in more than one respect. They would focus an infant's attention on an appropriate class of external stimuli for social responsiveness, much as the auditory templates of the white-crowned sparrow restrict responsiveness to members of its own species when they are living in a community where many others are present. Auditory templates could also provide an orderly frame of reference for the infant's developing responsiveness to the speech of others, drawing attention to the particular subset of speech properties that retain valence into adulthood (Mattingly, 1972). The templates would become both modified and multiplied as a result of experience gained in the very process of aiding the infant's perception and analysis of the sounds of the language in which it participates. The number of parallels between song learning in birds and the acquisition of speech by a child is striking. We may press the parallel further and suggest that speech sound templates also function in the development of speaking. Improvements in a child's babbling, as with a bird's subsong, perhaps reveal growing skill in matching vocal output to auditory templates. Possibly most remarkable is the discovery by Nottebohm (1971, 1972) that the neural control of some bird songs is lateralized, with a tendency for one side of the brain to assume dominant control, an echo of the dominance of the left hemisphere in the control of our speech.

There may in fact be a basic set of rules for the organization of vocal learning to which any species might be expected to conform if the design of its societies depends on a series of complex, learned traits. Though full exploitation of the advantages of learning requires freedom, the provision of too much latitude in the morphology of signaling behavior would result in patterns so divergent that communication would be impeded and the structure of a society disrupted. Therein, perhaps, lies the survival value of genetic predispositions that a species brings to the task of vocal learning from its past history, interacting with environmental stimuli to extract and abstract from those models presented by experienced adults from which it must derive the norms for its own social behavior. Notwithstanding the fact that a child and a young bird put their capacities for vocal learning to entirely different functions, the processes underlying learning still have many attributes in common (Marler, 1970c).

Animals with Language?

Though the process of learning to speak is paralleled in many respects by avian vocal learning, it is obvious that birds lack language. A search for primordia for this attribute of our communication system, regarded by many as uniquely human, would surely require investigation of monkeys and apes, which have so much else in common with us. However, laboratory and field study seems to confirm that their patterns of vocal development are very different from our own. Whereas children and birds begin to show an almost irrepressible tendency toward vocal imitation at a certain age, no one has yet discovered a comparable tendency in any other mammal. In contrast with human children and young song birds, other primate young are not known to "babble."

It is true that when raised in a home like children are, and after much time and effort on the part of both subject and experimenter, chimpanzees learned to utter a few words (Hayes and Hayes, 1952; Hayes and Nissen, 1971). But the process of acquisition, requiring laborious step- by-step assemblage of the necessary mouth movements with rewards at each stage, had little in common with the vocal imitation of bird and child. Remarkable though chimpanzee Vicki's breathy and unvoiced renditions of "cup," "papa," and "mama" were, they served as further confirmation of the gap between ape and man.

It was tempting to infer that the chimpanzee's inability to imitate speech reflects its lesser intelligence. Lieberman (1968) and Lieberman, Crelin, and Klatt (1972) analyzed the chimpanzee vocal tract and concluded that it would not be capable of producing the full array of human sounds; hence the failure to imitate. However, if an inappropriately structured vocal tract were the only obstacle, chimpanzees would attempt imitation, but the renditions would be imperfect, as occurs with the abnormal but still intelligible speech of persons suffering from laryngectomy or cleft palate. But chimpanzees make no attempt at all. For an explanation one must look rather to deficiencies in neural mechanisms that engender the predisposition for vocal learning.

The fact that no simple intelligence deficit was responsible emerged from several remarkable investigations setting out to teach chimpanzees language like communication systems that did not require the imitation of sounds. Aware of the extent to which chimpanzees use their hands in natural communication, Gardner and Gardner (1971, 1975) and Fouts (1973) have used the hand sign language of the deaf, American Sign Language. With various training techniques, including shaping, guidance, and observational learning, as well as imitation, they were able to teach the young female chimpanzee Washoe to perform eighty-five signs, each equivalent to a word, in a three-year period. Included were many nouns, such as flower, dog, and toothbrush, adjectives such as red and white, prepositions such as up and down, verbs such as help, hug, and go. Many words were used in appropriate combinations such as the invitation for a walk, You me go out hurry, or the request Please gimme sweet drink. The appropriateness of combinations of actions and objects indicates a grammar not very different from that of young children in early two-word sentences (Brown, 1970; Gardner and Gardner, 1974). Recently another young chimpanzee, Lana, has demonstrated similar prowess with a languagelike system based on keyboard signals to a computer, which talks back to her in a similar fashion (Rumbaugh et al., 1973).

The third chimpanzee, Sarah, accomplished in the use of a languagelike system, was trained by Premack (1971) to use colored plastic shapes instead of words, these shapes serving as symbols for objects and actions. A blue plastic triangle served as the symbol for apple. The one for banana was a red square, and so on. The relation between symbol and referent was noniconic, the shape lacking any physical resemblance to the object to which it referred. After Sarah was trained to present the appropriate shapes when she wanted a piece of fruit, other nouns and then verbs were introduced such as give, wash, and insert, each performed by the experimenter when Sarah presented the appropriate symbol.

Within her repertoire of about 130 words were not only many nouns, verbs, and adjectives, but also more complex constructions such as same, and different, questions, and the conditional if-then. A particular word order was required of Sarah in arranging the symbols on a board. Premack aimed more to test the conceptual abilities of Sarah than to see whether she could use language, reasoning that in our own species the one is closely mirrored in the other.

Can one infer that Sarah thinks in the language of these plastic shapes? Premack says yes. One test, he feels, is the ability "to generate the meaning of words in the absence of their internal representation." Premack asked Sarah to perform a feature analysis of an apple, using the plastic words to name its color and shape, the presence or absence of a stalk, and so on. Asked to perform a similar analysis on the plastic word for apple, the blue triangle, she answered by describing an apple once more and not the blue shape. This test bears on a further point, Sarah's ability to consider something that is not there at the moment—an illustration of the critical language requirement of displacement in time.

The importance of appreciating the natural motives of a subject in trying to understand its use of language is well illustrated by errors Sarah made in the use of shapes for different fruits. Required to present the appropriate shape for a fruit before she was allowed to eat it, she chose the wrong word surprisingly often. In a moment of inspiration Premack wondered whether Sarah was asking for what she preferred rather than for what was before her. An independent series of tests on her fruit preferences provided the explanation. The word for banana offered when confronted with an apple was not an error but an attempt to get the experimenter to give her something else, suggesting again that she truly understood the symbolic significance of the shapes.

The accomplishments of chimpanzees using languagelike systems of signaling to converse with an experimenter are surely the highest animal attainments demonstrated so far. Yet they also raise a curious dilemma. If a chimpanzee can indeed achieve some elementary competence with language when provided with an appropriate vehicle, why has this not been demonstrated in nature? It may well be that our knowledge of natural communication in animals is in such infancy that we can hardly judge whether such abilities are demonstrated in nature or not. However, it is also possible that the social organization and ecology of wild animals is so structured that they have little use for the special patterns of communication that our language makes possible.

From a biological viewpoint, symbolic communication is highly specialized, working most efficiently with particular kinds of problems. For many of the uses to which animals can put their signals—largely social in nature and taking place within groups in which members are familiar with one another over a long history of acquaintanceship—other kinds of signals can probably do the job better. Indeed it is conceivable that other types of communication other than language in the purest sense play a much more important role in our own biology than we are inclined to acknowledge. One of the benefits of a comparative approach to human communication may be a better appreciation of the rich potential of affective signals in performing the great variety of functions that sustain the organization of a complex society.

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