Communication: Basic Principles
What is communication? Let me try to cut through the Gordian knot of philosophical discussion that surrounds this word in biology by defining it with a simple declarative sentence. Biological communication is the action on the part of one organism (or cell) that alters the probability pattern of behavior in another organism (or cell) in a fashion adaptive to either one or both of participants. By adaptive I mean that the signaling, or the response, or both, have been genetically programmed to some extent by natural selection. Communication is neither the signal by itself nor the response, it is instead the relation between the two. Even if one animal signal and the other respond, there still has been no communication unless the probability of response was altered from what it would have been in the absence of the signal. We know that in human beings communication can occur without an outward changes of behavior on the part of the recipient. Trivial or otherwise useless information can be received, mentally noted, and never used. But in the study of animal behavior no operational criterion has yet been developed other than the changes in patterns of overt behavior, and it would be a retreat into mysticism to try to add mental criteria. At the same time there exist certain probability-altering actions which common sense forbids us from labeling as communication. An attack by predator certainly alters the behavior patterns of the intended victim, but there is no communicating in any sense in which we would care to use the word. Communication must also be consequential to some reasonable degree. If one animal simply pauses to watch as another moves by unknowingly at a distance, the passing animal has altered the behavior pattern of the first. But the passing animal was not really communicating in any way that could alter its own behavior or affect its relationship to the observing animal in the future. Perception occurred in this case but not communication.
J.B.S Haldane once said that a general property of communication is the pronounced energetic efficiency of signaling: a small effort put into the signal typically elicits an energetically greater response. This cannot be a universal prescription, but it is faithful enough to out intuition to permit the explicit exclusion of certain kinds of interaction. Two animals goring each other during an escalated territorial bout can be said to have commenced fighting. But to lift a friend from the ground in a abrazo is true communication that surely violets Haldane’s principle.
To finish drawing the boundaries of our definitions, consider the following two unusual examples that involve microorganisme. When bioluminescent bacteria of the genus Photobacterium are inoculated into a fresh medium, they are unable to produce a sufficient quantity of luciferase to generate light. After a while the growing bacteria secrete an activator substance of low molecular weight that promotes the synthesis of luciferase in bacteria of the same strain (Eberhard, 1972). Is this chemical synergism a form of communication? It can be designated as such or not, according to convenience. Lower organism such as Photobacterium, the interactions of which tend to be strictly physiological rather than behavioral, often create a grey zone of phenomena in which communication cannot be sharply demarcated. The second example includes three links in the communicative chain rather than the usual two. Hoyt et.al (1971) discovered that the sex attractant used by females of the grass grub beetle Costelytra zaelindica is the manufactured by symbiotic bacteria. These organism live in the beetle’s collateral glands, which are located beneath the vagina and serve the primary function of secreting a protective coating for the eggs. In this example, who is communicating with whom? Of course the question is basically frivolous: the beetles have simply added an entire organism to their biosynthetic machinery. The serious point to be made is that communication is an adaptive relation between the organism that signals and the one that receives, regardless of the complexity and length of the communication channel.
Human versus Animal Communication
The great dividing line in the evolution of communication lies between man and all of the remaining ten million or so species of organism. The most instructive way to view the less advanced system is to compare them with human language. With our own unique verbal system as a standard of reference we can define the limits of animal communication in terms of the properties it rarely—or never—displays. Consider the way I address you now. Each word I use has been assigned a specific meaning by particular culture and transmitted to us down through generations by learning. What is truly unique is the very large number of additional objects and concepts. This potential is quite literally infinite. To take an example from mathematics, we can coin no sense word for any number we choose (as in the case of the “googol,” which designates a I followed by 100 zeros). Human beings utter their words sequentially in phrases and sentences that generate, according to complex rules also determined at least partly by the culture, a vastly larger array of messages than is provided by the mere summed meanings of the words themselves. With else messages it is possible to talk about the language itself, an achievement we are utilizing here. It is also possible to project an endless number of unreal images: fiction or lies, speculation or fraud, idealism or demagoguery , the definition depending on whether or not the communicator informs the listener of his intention to speak falsely.
Now contrast this with one of the most sophisticated of all animal communication system, the celebrated waggle dance of the honeybee (Apis mellifera), first decoded in 1945 by the German biologist Karl von Frish. When a foraging worker bee returns from the field after discovering a food source (or, in the course of swarming, a desirable new nest site) at some distance from the hive, she indicates the location of this target to her fellow workers by performing the waggle dance. This pattern of her movement is a figure eight repeated over and over again in the midst of crowed of sister workers. The most distinctive and informative element of the dance is the straight run (the middle of the figure eight), which is given a particular emphasis by a rapid lateral vibration of the body (the waggle) that is greatest at the tip of the abdomen and least marked at the head.
The complete back and forth shake of the body is performed 13 to 15 times per second. At the same the bee emits an audible buzzing sound by vibrating her wings. The straight run represents, quit simply, a miniaturized version of the light from the hives to the target. It points directly at the target if the bee is dancing outside the hive on a horizontal surface (The position of the sun with respect to the straight run provides the required orientation.) if the bee is on a appropriate angle away from the vertical, so that gravity temporarily replaces the sun as the orientation cue (see figure 8-1).
The straight run also provides information on the distance of the target from the hive, by means of the following additional parameter. The farther away the goal lies, the longer the straight run lasts. In the Carniolan race of the honeybee a straight run lasting a second indicates a target about 500 meters away. During the dance the follower bees extend their antennae and touch the dancer repeatedly. Within minutes some begin to leave the nest and fly to the target. Their searching is respectably accurate: the great majority come down to search close to the ground within 20 percent of the correct distance.
Superficially the waggle dance of the honeybee may seem to posses some of the more advanced properties of human language. Symbolism occurs in the form of the ritualized straight run, and the communicator can generate new messages at will by means of the symbolism. Furthermore, the target is “spoken of” abstractly: it is an object removed in time and space. Nevertheless, the waggle dance, like all other forms of nonhuman communication studied so far, is severely limited in comparison with verbal language of human beings. The straight run is after all just a reenactment of the flight the bees will take, complete with wing buzzing to represent the actual motor activity required. The separate messages are not devised arbitrarily. The rules they follow are genetically fixed and always designate, with a one-to-one correspondence, a certain direction and distance.
In the other words, the messages cannot be manipulated to provide new classes of information. Moreover, within this rigrid context the messages are far being infinitely divisible. Because of errors both in the dance and in the subsequent searches by followers, only about three bits of information are transmitted with respect to distance and four bits respect to direction. This is the equivalent of a human communication system in which distance would be gauged on a scale with eight divisions and direction would be defined in terms of a compass with 16 points. In reading single messages, northeast could be distinguished from east by northeast, or west from west by southwest, but no more refined indication of direction would be possible. A through account of the work of von Frisch and his student is given in his master work Tanzsprache und Orientierung der Bienen (1965) or its English translation by L.E Chadwick (1967). A briefer review, including critiques and more recent studies, is provided by Wilson (1971a). the design features of human language as opposed to communication In animal, particularly, honeybee, were first systematically analyzed by Hockett (1960) and Altmann (1962b) and have been more recently evaluated by the same authors (Altmann, 1967b,c Hockett and Altmann, 1968). The main points o their formal system are included in the looser, more flexible account that follows.
DISCRETE VERSUS GRADED SIGNAL
Animal signal can be partitioned roughly into two structure categories: discrete and graded, or, as Sebeok (1962) designated them, digital and analog. Discrete signals are those that can be presented in a simple off-or-on manner, signifying yes or no, present or absent, here or there, and similar dichotomies. They are most perfectly represented in the act of simple recognition, particularly during courtship. The steel-blue back and red belly of the ,ale three-spined stickleback (Gasterosteud aculeatus) in an example of a discrete signal. Another is the ritualized preening of the male Mandarin duck (Aix galericulata), who whips his head back in a striking movement to point at the bright orange speculum of his wing. Still other examples are provided by bioluminescent flashing sequences of fireflies (Figure 8-2). Disreteness of form also characterizes the communion signals by which members of a group identify one another and stay in contact, such as the duetting of birds and certain grunting calls of the ungulates. Discrete signal become discrete through the evolution of “typical intensity” (Morros, 1957). That is, the intensity and duration of a behavior becomes less variable, so that no matter hoe weak or strong the stimulus evoking it, the behavior always stays about the same.
In contrast, graded (analog) signal have evolved in a way that increase variability. As a rule the greater the motivation of the animal or action about to be performed, the more intense and prolonged the signal given. The straight run of honeybee waggle dance denotes rather precisely the distance from the hive to the target. The “liveliness” or “vivacity” of the dance and its overall duration increase with the quality of the food find and the favorableness of the weather outside the hive. Graded communication is also strikingly developed in aggressive displays among animals. In rhesus monkeys, for example, a low intensity aggressive display is a simple stare. The hard look a human being receives when he approaches a caged rhesus id not so much a sign of curiosity as it is a cautious displays or hostility. Rhesus monkeys in the wild frequently threaten one another not only with stares but also with additional displays on an ascending scale of intensity. To the human observe these displays are increasingly obvious in their meaning. The new component are added one by one or in combination: the mouth opens, the head bobs up and down, characteristic sounds are uttered, and the hands slap the ground. By the time the monkey combines all these components, and perhaps begins to make little forward lungs as well it is likely to carry through with an actual attack (Figure 8-3). Its opponent responds by retreating or by escalating its own displays. These hostile exchanges play a key role in maintaining dominance relationships in the rhesus society.
Squirrels reveal gradually rising hostility by tail movements that increase from a slow waving back and forth to violent twitching. Birds often indicate aggressive tendencies by ruffling their feathers or spreading their wings, movements which create the temporary illusion that they larger than they really are. Many kinds of fish achieve the same deception by spreading their fins or extending their gill covers. Lizards raise their crest, lower their dewlaps, or flatten the side of their bodies to give an impression of greater depth. In short, the more hostile the animal, the more likely it is to attack and the bigger it seem to become. Such exhibitions are often accompanied by graded changes in both color and vocalization. And even by the scaled release of the characteristic odors (See Figure 8-4).
Gradation in one form or another characterizes most of the major categories of communication in animal societies. Birds and mammals transmit a rich array a messages, some of which are qualitatively different in meaning, by gradually varying postures and sounds (Andrew, 1972). Ants, to cite a very different king of organism, release quantities of alarm substances in approximate relation to the degree to which they have been stimulated. Fire ants deposit trail scent in amounts that reflect both the hunger of the colony and the richness of the food find (Hangartner, 1969a, Wilson, 1971a). the amplification of a signal can be accomplished simply by the gradual increase of the power output movement, melanophore contraction, or whatever component contains the information. Or it can be achieved by adding wholly new components. A striking example of the second method is found in the mobbing calls of certain birds (See Figure 8-5).
THE PRINCIPLE OF ANTITHESIS
One of the most general principles of animal communication was first recognized by Charles Darwin in The Expression of the Emotions in Man and Animals (1872). Labeled by him the principle of Antithesis, it can be expressed in an oversimplified manner as the following duality: when an animal reverses its intentions, it reverses the signal. The signal antithesis are most sharply defined in aggressive interactions. An animal that approaches another in a conciliatory mood, or else has lost a fight and is trying to appease the victor, uses postures and movements that are the opposite of aggressive displays. Darwin’s own description of antithetic signaling in dogs (see Figure 8-6) is graphic and precise:
When a dog approaches a strange dog or man in savage or hostile frame of mind he walks upright and very stiffly; his head is slightly raised, or not much lowered, the tail is held erect and quite rigid; the hairs bristle. Especially along the neck and back, the pricked ears are directed forwards, and the eyes have a fixed stare. These actions, as will hereafter be explained, follow from the dog’s intention to attack his enemy, and are thus to large extent intelligible. As he prepares to spring with a savage growl on his enemy, the canine teeth are uncovered, and the ears are pressed close backwards on the head, but with these latter actions we are not here concerned. Let us now suppose that the dog suddenly discovers that the man he is approaching, is not stranger, but his master, and let it be observed how completely and instantaneously his whole bearing is reversed. Instead of walking upright, the body sinks downwards or even crouches and is thrown into flexuous movements; his tail. Instead of being stiff and upright, is lowered and wagged from side to side; his hair instantly becomes smooth; his ears are depressed and drawn backwards, but not closely to the head; and lips hang loosely. From the drawing back of the ears, the eyelids become elongated, and the eyes no longer appear round and staring.
When displaying aggressively, a gull stretches its head forward, the ritualized intention movement by which the bird indicates it is ready to pack at its enemy. But in order to appease an opponent, a gull turns its head 900 to the side. Two gulls attempting to conciliate reciprocally will stand side by side, or face each other with their bodies, but they will momentarily gazing in opposite direction (N.Tingbergen, 1960). Dominant male rhesus monkeys raise their tails and heads and display their testicles by lowering them, subordinates lower their tails and heads and raise their testicles. The dominant males also mount their subordinates in ritual pseudocopulation, the subordinates present themselves in a pseudofemale posture to be mounted. Although such example can be multiplied at length, not all displays opposite in meaning are also antithetical in appearance to the human observe. Even appeasement displays sometimes incorporate wholly new elements unrelated to hostile signaling. Hyenas, for example, rely heavily on penis displays to conciliate one another, even the females are equipped with pseudopenes which they use with convincing skill (Kruuk, 1972). Rodents and primates routinely utilize grooming, while some birds and mammals revert to begging and other juvenile postures (Wickler, 1972a).
SIGNAL SPECIFICITY
The communication systems of insect, of other invertebrates, and of the lower vertebrates (such as fishes and amphibians) are characteristically stereotyped. This means that each signal there is only one response or very few responses, that each response can be evoked by only a very limited number of signal, and that the signaling behavior and response are nearly constant throughout entire populations of the same species. An extreme example of this rule is seen in the phenomenon of chemical sex attraction in moths. The female silkworm moth draws males to her by emitting minute quantities of a complex alcohol from glands at the tip of her abdomen. The secretion is called bombykol (from the name of the moth, Bombyx mori), and its chemical structure is trans -10 cis-12 hexadecadienol.
Bombykol is a remarkably powerful biological agent. According to estimates made by Dietrich Scheneider and his coworkers at the Max Planck Institute for Comparative Physiology at Seewiesen in Germany, the male silkworm moth start searching forfemales when they are immersed in as few as 14,000 molecules of bombykol per cubic centimeter of air. The male catches the molecules on some 10,000 distinctive sensory hairs on each of his two feathery antennae. Each hair is innervated nerve and ultimately through connecting nerve cells to centers in the brain. The extraordinary fact that emerged from the study by the Seewiesen group is that only a single molecules of bombykol is required to activate a receptor cell. Furthermore, the cell will respond to virtually no stimulus other than molecules of bombykol. When about 200 cell in each antenna are activated per second, the male moth starts its motor response (Schnider, 1969). Tightly bound by this extreme signal specificity, the male performs as little more than a sexual guided missile, programmed to home on an increasing gradient of bombykol centered on the tip of the female’s abdomen—the principal goal of the male’s adult life.
Such highly stereotyped communication system are particularly important in evolutionary theory because of the possible role, they play in the origin of new species. Conceivably one small change in the sex-attractant molecule induced by a genetic mutation, together with a corresponding change in the antennal receptor cell, could result in the creation or a population of individuals that would be reproductively isolated from the parental stock. Persuasive evidence for the feasibility of such as mutational change has been adduced by Roelofs and Cemeau (1969). They found two closely related species of moth (members of the genus Bryotopha in the family Gelechidae) whose female’s sex attractants differ by only the configuration of a single carbon atom adjacent to a double bond. In other words, the attractants are simply different geo metric isomer. Field tests showed not only that a Bryotopha male respond solely to the isomer of his own species but also that his response is inhibited if some of the other species’ isomer is also present. An even more extreme case—the ultimate possible, in fact—has been reported by Minks et al (1973). The two tortricid moth species Adoxophyes orana and Clepsis spectrana utilize the same twi isomers, cis-9 and cis-11 tetradecenlyacetate, as their female sex attractant. However, they manufactured and release them in different blends are sufficient to affect the male responses and hence isolate the species from each other.
For each such case extreme specificity there exist others in which signals are shared by more than one kind of animal. Among moths of the families Saturniidae and Tortricidae, specificity of the sex pheromone often exist at the species group level, meaning that the males respond to the pheromones emitted by females of both their own and closely related species (Priesner, 1968; Sanders, 1971). Under natural conditions the species depend on other kinds of prezygotic isolating mechanism to avoid hybridization, particularly differences in preferred habitats, seasons of emergence, and times of peak matting activity.
Other kinds of signals are known which are clearly not designed to impart specificity. The alarm substances of ants, termites, and social bees consist of an astonishing diversity of terpenes, hydrocarbons, and esters, most of which have low molecular weights. In spite of the fact that they differ in composition and proportionality from one species to another, they are generally active across broad taxonomic groups. When an agitated honeybee worker discharges isoamylacetate or 2 – heptanone, it alarms not only her nestmates but also any ant or termate that happens to be in the near vicinity. This phenomenon is precisely what the evolutionist would expect. Privacy is not a requirement of alarm communication, and when the communication is coupled with interspecific aggressive behavior, signals should be expected to affect enemies as well as nestmates. The same differences in breadth of activity are found among the communication system of bird and are subject to the same explanation. Territorial and courtship displays, including advertising songs, are characteristically elaborate and species-distinct. Their exceptional complexity and repetitive patterning are in fact the reasons why human beings consider them beautiful. But esthetics are not the primary consideration of birds. The displays are sufficient, in the great majority of cases, to isolate the members of each species of bird from all other species breeding in the same area. Where “mistake” occur, resulting in interspecific territorial combat or hybrids, they are usually limited to closely related species and most often to those that have come close contact only in the most recent geologic time. In contrast, the mobbing calls of small birds, which assemble other birds for cooperation in driving a predator from the neighborhood, are very similar from one species to another and are understood by all. The gulls (family laridae) provide an excellent capsular illustration of the specificity rule. The sequence of courtship displays of each sympatric species is distinctive in one species the long call is followed by mewing, in another the choking displays is followed by the long call, and so forth. The precise forms of the separate components also vary. During the lengthy exchanges leading to pair bonding, these signals make it unlikely that any gull will choose a partner of the wrong species. In contrast, the displays of aggression and appeasement are simple in execution and uniform across species. In a closely parallel manner, the intergroup spacing and within-group rallying call of Cercopithecus monkeys are species-specific, but their alarm call are relatively constant and can be understood from one species to the next (Marler, 1973).
Even though much convergence of signals exists in aggressive interactions, there is no universal code to which all species of a group subscribe. In the mammals, for example, we find appeasement behavior following much the same form in species after species : the animal tends to crouch, often rolling over to expose its flank or belly. Konrad Lorenz suggested that in some mammals such as the dog the exposure of these most vulnerable part cancel the aggressive impulse of the opponent. However, the belly-up posture does not invariably mean submission. Among shrews it signifies hostility and dominance-with good reason, since the shrew’s best fighting position is on its back (Ewer, 1968). Two points should be stressed : first, that evolution is entirely opportunistic and not bounded by any goal-directed rules, however intuitively appealing they may seem; and second, that display behavior are among the most evolutionarily labile of all phenotypic traits.
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