Chapter 2

EXPANDING HORIZONS IN ANIMAL COMMUNICATION BEHAVIOR

Donald R. Griffin

During the past thirty years we have been repeatedly surprised by discoveries about animal behavior, especially in the area of orientation and communication. The behavioristic tradition of Jacques Loeb (1964), John B. Watson (1929), and C. Lloyd Morgan (1894) had not prepared us for the possibilities that grew in this period from hesitant speculations to well-accepted facts. (For concise reviews of the historical background for current ideas about animal and human behavior see Klein, 1970, and Klopfer and Hailman, 1967.) Outstanding examples of eye-opening discoveries about orientation behavior are: (1) The orientation of birds by means of the sun or stars with at least approximate compensation for the apparent motions of these heavenly bodies across the sky (Matthews, 1968; Emlen, 1975). (2) The ability of bats and two species of cave-dwelling birds to orient rapid and agile flight through darkness by echolocation, including the ability of insectivorous bats to intercept flying insects by echolocation (Griffin, 1958; Griffin, Webster, and Michael, 1960; Simmons, Howell, and Suga, 1975). (3) The evolution in several different groups of insects of specialized auditory organs that warn them of approaching bats in time for successful evasive maneuvers (Roeder, 1970). (4) The orientation of certain electric fishes by sensing with their lateral line receptors changes in the electric fields produced by their own electric organs or by bioelectric potentials from other animals (Lissmann, 1958; Lissmann and Machin, 1958; Kalmijn, 1971; Bullock, 1973). (5) The ability of honeybees and many other invertebrate animals to orient themselves by the polarization patterns of the blue sky (von Frisch, 1950, 1967).

Comparable surprises have come from research on the communication behavior of animals. These were reviewed in Animal Communication (1968), and other chapters of the present volume bring the whole subject up to date. Of all these new discoveries about animal communication the two most impressive and significant are the "dance language" of honeybees (von Frisch, 1923, 1946, 1967, 1972, 1974), discussed along with the communication behavior of other insects in the chapter by Hölldobler, and the recent experiments on gestural communication with chimpanzees, reviewed in the chapter by Fouts. This improved understanding of communication among animals has profound implications that call into question some of our basic assumptions about the relationship between men and animals. This chapter will discuss some of these implications and advance tentative suggestions for their future analysis.

The waggle dances of honeybees are coded gestures used most commonly to signal the location of a food source, but they are also used under special conditions to convey information about the location of other things required by the mutually interdependent colony of bees. The dances specify not only quantitatively the distance and direction but also qualitatively the desirability of what a scout bee has located. The degree of desirability may reflect the sugar concentration of the nectar, or, as discussed below, other desiderata. It is not adequately appreciated that these communicative dances are not always exhibited in rigid fashion. When food is plentiful the returning foragers often do not dance at all. Odors are always important in recruiting the worker bees to newly available food sources: the odors of nectar and pollen and other odors from the area where food was gathered that are carried back by the dancing bee, as well as scents secreted by special glands that are often used to mark food sources. These odors always help to direct recruits to the exact location of new food sources, and often they appear to be sufficient. Sounds or vibrations are also involved, at least in conveying the arousal level of the dancing bee. Independent searching by individual foragers also seems to be adequate under many conditions when food is plentiful. Thus the dance communication system is called into play primarily when a colony of bees is in great need of food or something else.

It is important to recognize, as many readers of von Frisch's early writings did not, that the system is not rigidly linked to one kind of material needed by the colony. The same signaling system is used for such different things as nectar, pollen, water, and resinous exudations from plants (propolis) that are used to repair portions of the honeycomb. But most significant of all, scout bees from a swarm that has moved outside its former cavity use the same coded gestures to convey to other bees the locations of cavities suitable to serve as future locations for the entire colony (Lindauer, 1955). As in other situations where the dances are employed, the response of potential recruits varies with the vigor and intensity of the dance. Scout bees that have found a relatively poor cavity dance with reduced intensity and sometimes also pay attention to other, more vigorous dances. They may be strongly enough influenced to fly out to the cavity whose location has been indicated by the more intense dance of another scout, and after visiting this cavity may dance in a pattern and with an intensity indicating both its location and its quality. Thus the same bee can alternate within a short period of time between acting as a transmitter and a receiver of information, using the same gestural code.

The discovery of such complex communication behavior would have been surprising enough among mammals, but to find it in an insect was truly revolutionary. It is one thing for one of our closest phylogenetic relatives to share some of our basic patterns of communication behavior and be able to learn others, but bees are as distantly related to mammals as any animal; our closest common ancestors lived at least 500 million years ago. The use of symbolic communication by insects thus implies that flexible communication behavior is not restricted to any one phylogenetic group of animals. This discovery was such a surprising one that, as von Frisch (1972) so succinctly put the matter, "No good scientist should believe such a thing on first hearing." Many were skeptical at first, but convinced themselves by repeating von Frisch's basic observations that the properties of the waggle dances were indeed closely correlated with the location of a food source.

Some years later Wenner (1971) and his colleagues (Wells and Wenner, 1973) raised a more serious question—whether the evidence presented by von Frisch and his colleagues is sufficient to demonstrate the communication of information about distance and direction. They contend that site-specific odors account for the results of von Frisch's experiments and that bees simply convey to one another these odors, for which the recruits then search. They concede that the dance patterns are correlated with the distance and direction of the food source but interpret this as a sort of accidental epiphenomenon. This of course leaves them in the embarrassing position of having no explanation at all to offer for this remarkable coincidence. These critics also underemphasize the fact that many years previously von Frisch had described extensive experiments showing that odors are of great importance in recruiting bees to new food sources. Indeed, Wenner set up a sort of straw man by implying that von Frisch claimed that bees always dance or that they locate food only by information conveyed through the dances. Wilson (1971) is clearly correct that "the basic thrust of the criticism was wrong," and Michener (1974) concurs, even though he had previously been swayed by Wenner's criticisms. Yet the publication of Wenner's views has had the constructive effect of stimulating new and improved experiments that have established even more solidly that von Frisch was correct in his original interpretations of the dances. Gould (1974, 1975, 1976) has recently developed a new experimental technique by which he can cause dancing bees to signal a different location from the actual feeding place from which they have just returned. The result is that most recruits fly to the place indicated by the dances rather than the actual feeding place from which the dancer has carried back odors.

The intensity of the skepticism expressed by Wenner and his colleagues, and probably felt by many others, is related to the fact that the dance communication system of honeybees edges embarrassingly close to human language in its symbolism and flexibility. Many writers have objected to von Frisch's use of the term language for what can be more conservatively described as communication behavior. But the important point is not one of semantic detail but rather the basic philosophical question of what distinguishes human language from the communication behavior of animals. The prevailing view expressed by many linguists, philosophers, and even biologists is that human language is the primary, qualitative difference in kind that distinguishes human beings from animals (Anshen, 1957; Dobzhansky, 1967; Simpson, 1964; Thass-Thienemann, 1968). Indeed many philosophers base their fundamental definitions of humanity on very definite assertions (of a negative sort) about the communication behavior of animals (Adler, 1967).

Perhaps the most thoughtful of these philosophical discussions has been provided by Bennett (1964), who argues with charming erudition that bees are not rational, although he concedes that their dance communication has many attributes of language. In discussing what imaginary bees would have to do in order to satisfy his criteria of rationality, Bennett requires convincing evidence that they know what they are doing. Since his discussion seems to be based on the evidence presented by von Frisch up to 1950, he does not consider the implications of Lindauer's discovery that swarming bees exchange information about potential locations for a new colony. Bennett and others place much weight on the lack of any evidence that the dance communication system is used by one bee to deny a statement made by another. But the exchanges of information between scout bees returning to the swarm from more or less suitable cavities could be interpreted in terms of assertions and denials. Von Frisch and Lindauer have thus provided data that are critically important for the arguments of such philosophers as Bennett, but not sufficiently complete or detailed to answer the questions they have raised. This means, for one thing, that whatever students of animal communication have learned, or can learn in the future, about communication behavior in other species is directly relevant to major fundamental questions about linguistics and philosophy.

There is, of course, no question about the enormous difference in complexity, subtlety, and versatility that separates human speech, to say nothing of written language, from anything known or even speculatively suggested in the communication behavior of other species. But it has seemed of fundamental importance to many scholars and philosophers to insist on a "radical difference in kind" in the terminology, for example, of Adler (1967), rather than a quantitative difference in degree of elaboration. Hockett and Altmann (1968), Thorpe (1972), and others have struggled to formulate objective criteria by which human language can be qualitatively distinguished from animal communication. But this task has become increasingly difficult as more and more is learned about the communication behavior of honeybees, chimpanzees, and other animals.

These considerations force us to face squarely the question of behavioral and even mental continuity between animals and men. Hardly anyone doubts the historical fact of biological evolution. Continuity is a fundamental assumption underlying the use of animals as surrogates for studies of anatomy, physiology, bio-chemistry, and many types of behavior—investigations that are expected to throw some light on comparable phenomena in our own species. For example, it would be folly to draw any conclusions about human learning from studies of rats or pigeons if one believed that human learning was radically different in kind from that found in other animals. But when questions of language and communication behavior are under consideration, even hard-nosed behaviorists often seem to believe in a lack of continuity or perhaps a radical difference in kind that separates human language from the communication behavior of other species.

Close examination of most assertions that human language differs radically in kind from animal communication shows that this belief is based largely if not entirely on the assumption that human beings use language with conscious intent to convey information while animals are mechanical systems responding to stimuli but lacking any awareness of what they are doing. Similar assumptions, not limited to communication behavior, are thoughtfully stated by Dobzhansky (1969) and Eccles (1969). Recognition that this is a key assumption raises the question: On what do we base our opinions about the mental experiences or consciousness of other animals? The conventional position is either that animals have no mental experiences or, more cautiously, that we have no way of gathering information about the mental experiences of animals if these exist, and hence that the entire question lies outside the proper concerns of science. In either case the evidence is essentially negative, and logically it supports only an agnostic position. Lacking convincing evidence pro or con, we simply do not know what mental experiences animals may have.

While subjective experiences are vivid to each of us individually, all the deepest reflection and most thoughtful eloquence of philosophers have not sufficed to provide methods by which such experiences can be studied except through introspection and verbal reporting. This has heretofore made it appear out of the question to discover anything about mental experiences that animals might have, since it has been taken for granted that a language or communication system adequate for any sort of introspective report was impossible. Furthermore the behavioristic climate of opinion that banished even consideration of human mental experiences from psychology, together with faith in Occam's razor and Morgan's canon, has been so influential since the 1920s that behavioral scientists are now highly uncomfortable at the very thought of mental states or subjective qualities in animals. When such notions intrude into our scientific discourse, as they do remarkably often, we feel sheepish. And when we find ourselves, in spite of these inhibitions, using such words as fear, pain, pleasure, or the like we attempt to shield our reductionist egos behind a respectability blanket of quotation marks.

Yet as Fouts (1973, 1975) has pointed out, our gut feeling of species superiority has suffered a series of intellectual setbacks beginning with the Copernican and Darwinian revolutions, the second having a far more basic impact than the first. Moreover, when evidence is presented that some other species has achieved a previously proposed criterion for distinguishing human language, the list of such criteria is lengthened to exclude the threatening interloper. There is an obvious danger here that our attempts to buttress our anthropomorphic feelings of superiority will lead us into indefensibly circular reasoning.

If we examine the background of our current viewpoint, it is clear that it stems from a critical reaction roughly seventy years ago to an earlier tendency to ascribe human feelings to a wide variety of animals on the basis of anecdotal reports. This behavioristic reaction has served our science well, but so much has now been learned about animal behavior, and especially about orientation and communication, that it is perhaps time to reexamine this basic viewpoint and inquire whether what was once healthy and disciplined restraint may not now be limiting our perspectives and causing us to overlook important opportunities for further advances. There has been a tendency for what was originally an essentially agnostic position about mental experiences in animals to drift into a de facto denial that mental states or consciousness exist outside our own species. Here it seems appropriate to follow the example of Holloway (1974) and quote Daniel Yankelovich ("Smith," 1972), "The first step is to measure whatever can easily be measured. This is okay as far as it goes. The second step is to disregard that which can't be measured or give it an arbitrary quantitative value. This is artificial and misleading. The third step is to presume that what can't be measured easily isn't very important. This is blindness. The fourth step is to say that what can't be easily measured really doesn't exist. This is suicide."

Suppose that the discoveries of von Frisch about honeybee communication or those of the Gardners and Fouts about gestural communication with chimpanzees had been known in, say, 1910? Would Loeb, Watson, and others have taken such an adamant stand against considering animal behavior in terms more complex than reflexes, tropisms, and the like? The history of von Frisch's studies of the honeybee dances may also be considered in this light. In the early 1920s he noticed that under certain circumstances round dances occurred when he offered sugar solution in dishes, while waggle dances were exhibited by bees carrying pollen. Only twenty years later did he discover the far more significant correlation of dance pattern with distance and direction. Might not the dance communication of bees have been discovered in the 1920s if complex communication among insects had not been so utterly unthinkable?

The lack of any conceivable means of obtaining introspective reports from animals has always seemed to place hopelessly beyond our reach any fruitful study of the existence or nature of conscious intention in other species. But recent discoveries of versatile communication behavior in animals have changed the situation by opening up the possibility of investigating the fundamental question of mental continuity between animals and men. For it is now thinkable that communication with animals might eventually be developed to the point that it could be used to obtain from them simple but nevertheless significant introspective reports, if, contrary to prevailing opinion, they have mental experiences and are capable of conscious intentions (Griffin, 1976a, 1976b).

Indeed the two-way communication between investigators and chimpanzees has already progressed a small but significant step in this direction. Questions have been asked by Gardner and Gardner (1971) and others about short-term desires such as wanting to go out for a walk or wanting a particular type of food. And questions of this sort have been clearly answered by the chimpanzees. It may be objected that all such behavior can also be described in terms of stimuli and responses, but the same can be said of all human communication. The reason we tend to reject a strictly stimulus-response explanation of our own behavior is that we are convinced of our own conscious intentions. Most of us accept the existence of mental experience and conscious intention in our fellow human beings even though our only source of information about them comes through the imperfect channel of introspective verbal reporting. A similar channel is now potentially available to us for the same basic purpose, at least with chimpanzees. It is even possible that suitable methods can in time be developed to achieve two-way communication with other species. Models, mirror images, and tape recordings can elicit elements of communication behavior. But more versatile models will be needed to carry out significant two-way exchange of messages sufficient to ask questions and obtain introspective answers.

To many readers these suggestions will seem farfetched or even outrageous. One objection that can be anticipated with confidence is the exaggeration of the mere suggestion that animals may have any conscious awareness and intentions at all, into a sort of straw-man assertion that they can equal the richness and versatility of human thinking. But the question I am raising is a much more limited one: Do animals have any sort of mental awareness of probable future events, and do they make conscious choices with the intent to produce certain results? The traditional view is that animals have no such mental experiences or that if they do we can never hope to gather significant and meaningful information about them. I am simply suggesting that the recent developments discussed above open the way to asking animals direct questions about their mental experiences and intentions. If successful, this would bring the whole question within the reach of experimental testing. While new and difficult techniques will have to be perfected, it seems reasonable to hope for significant success if the problem can be attacked with experimental ingenuity comparable, for example, to that devoted in recent years to studies of learning. Once such experiments begin to yield consistent results we can begin to inquire how extensive and elaborate the mental experiences and intentions of animals may be. At this stage there might even begin to emerge, for the first time, a true science of comparative psychology.