Do prosimian primates communicate? A cursory glance at the relevant literature might well raise doubts. "Olfactory information may be expected to play a more important role . . . ," "patterns of scent deposition are perhaps . . . ," "a gesture which may originally ..." are common statements. A more general, if equally cautious, contention is that
Communication is, in fact, such a problematical phenomenon that its exact meaning with respect to animals needs very careful statement. A correct formulation of the terms in which it is to be conceived is likely to hold implicitly the concepts that will automatically rearrange our empirical and theoretical views of mental evolution. The numerous inconclusive attempts to link human and non-human mentality in a continuum, which fill many serious books today, are perhaps all obstructed by the same weakness, the lack of adequate ideas of the animalian forms of perception and action from which our own development has taken off in its great expansion. A coherent view of animal mentality, without immediate reference to our own, might provide a foundation for surer insights into the fateful evolutionary shift that has taken place in the hominid stock. [Langer, 1973:108]
Is it really so difficult to formulate the terms? The simplest procedure is to consider all instances of information transfer as communication (Sebeok, 1968). However, simple though this is, it eclipses the very distinctions we would make. "Interactions" include phenomena as diverse as the control of protein synthesis by chromosomal DNA and echo location by bats. It is more useful and no more difficult to note finer differences and to consider the various classes of interactions separately. Mere perception by one organ or organism of signals emanating from another is thus best not termed communication. It is more useful to restrict the term to interactions dependent on a shared code, with the further provision that this sharing be of mutual benefit (note Klopfer and Hatch, 1968). This excludes prey-predator interactions. When a predator "communicates" his presence to his prey, only the latter benefits. We should also distinguish between a command, "Jump in the lake," and a push off the pier. This can be done on the basis of the energy required to achieve the identical results, for the command requires very much less than the push.
Other distinctions could, of course, be made (see Hinde, 1972), but these seem as useful and adequate as any. Of course, we do not thereby distinguish between intentional and nonintentional communication. Fortunately, that distinction becomes important only with human linguistic behavior. The implication of this last point—that mechanisms can be ignored when we consider function—needs to be stressed. If the fitness (in the Darwinian sense, i.e., the proportion of one's genes carried by future generations) of an organism is enhanced by an integration or synchronization of its behavior with that of others, synchronizing or integrating mechanisms are likely to arise. Where the organisms concerned are consanguinous, i.e., have some of their genes in common, the selective pressure for such mechanisms will be even greater. Thus, while my fitness is partially measured by the proportion of my offspring in future generations, it may also depend on the proportion of my brother's children in that generation. (My brother and I hold approximately 50 percent of our genes in common. Hence, his offspring will also contribute to my fitness, albeit it will take four of them to equal only one of mine.) This notion of "inclusive fitness" (Hamilton, 1964) provides a basis for altruistic behavior (since the survival of three of my siblings, even at the cost of my own life, will still increase my fitness to 3 × 50 percent) and, coincidentally, for the evolution of codes that are mutually useful and thus serve social ends.
The design features of the resulting communication systems may even include feedback controls that correct signals that are misunderstood, or adjust for inadequate signal/noise ratios, or switch signals or even codes as contexts change. Such controls may produce results that appear similar to the cognitively controlled, intentional acts involved in a conversation between two of us. No matter, the issue of intentionality may still be ignored so long as a communicative function is served. Natural selection could produce automatons whose behavior is functionally identical to that of willful men even while underlying mechanisms differ. If behavior is classified in terms of its function, the fact of a difference in ontogeny or mechanism is irrelevant. A leaf-eating insect may be cryptically colored and thus equally well protected whether it is born with green pigment or with scales that differentially refract different wavelengths, or whether it wraps a green leaf around itself.
It must be added that the issue of similarity in behavioral mechanisms may be important to those concerned with the reconstruction of the history or evolutionary past of an organism. Phylogenetic studies have traditionally leaned heavily on the identification of homologies, though some biologists as well as philosophers consider this a risky technique (Klopfer, 1973; Langer, 1973). Fortunately, we can sidestep this issue here, while admitting to its existence, and focus on the question of whether extant primates, particularly the prosimian primates, do communicate, how they do so, and the sorts of information they can convey. The issue of how they came to do so and what their relatives made of their talents we shall ignore.
Indications of Communication
The fact that many prosimian primates (Table 1) do show integrated patterns of social behavior may be considered a prima facie ground for suspecting the occurrence of some kind of communication. The existence of seemingly stereotyped (species-characteristic) movements, odor-producing glands, and distinctive sounds further suggest that these are the vehicles for a communicative code. A detailed list of the sounds, gestures, and odor source of prosimians, and the context in which they occur, is provided by Doyle (1974). It is as long and varied as that for any other primate. Note Table 2. The more insistent questioner, however, will demand to know how we can be certain that the behavior we assume to be communicative truly meets the criteria for communication, i.e., that (1) it entails a code (a stereotyped convention); (2) the "meaning" is at least specific in particular contexts (the effects on conspecifics are predictable); (3) the exchange mutually enhances fitness (i.e., this must not be a zero-sum game); and (by way of further distinguishing those instances of communication that appear to involve cognitive or purposive elements) (4) it entails a feedback control such that the sender adjusts his signal as he perceives the recipient is unable to receive it or is responding inappropriately.
The following classification of the prosimians is generally accepted, though there are disagreements as to the status of particular groups—whether L. fulvus is a distinct species or a subspecies of L. macaco. These issues are not important here, but they need to be kept in mind in using this table. Species marked with an asterisk are mentioned in the text.
some common communication signals of lemur catta
Other important questions concern the communicative patterns that serve particular functions—can one generalize about signals that enhance reproduction or group movements and distinguish them, as a class, from those involved in communicating the presence of predators or of food? For instance, Marier (1955) has proposed that the calls produced by songbirds in response to aerial predators share characteristics that hinder localization of the source of the sound, while calls given during casual feeding share different features, ones that aid in localization. Are there evolutionary trends or patterns with respect to the degree to which "codes" are linked to morphologic structures or perceived atomistically (the specific "releaser" of the ethologist) rather than holistically (note Nelson, 1973)?
The evidence for communication among nonhuman primates is inferential, though compelling. An excellent example of its character is to be found in van HoofFs (1972) account of the phylogeny of laughter and smiling. The movements or displays in question are seen to be stereotyped, with slight variations from species to species; there is a close correlation between the appearance of the display and certain other behavior patterns (i.e., the context of the act is predictable); there is a further correlation between the display and the response evoked in other animals. The specificity of this result and its dependence on the display itself are further supported by the experiments of Miller et al.(1964), who demonstrated that a televised facial expression was sufficient (at least in macaques) to convey affect.
Among the prosimian primates, unfortunately, correlational studies as exemplified by van Hooff (1972) are as yet unknown. As previously mentioned, Doyle (1974) has listed in considerable detail all the acts, movements, sound production, and scent deposition committed by prosimians that might be involved in communication. He summarizes as well the situations in which these acts most frequently occur. But, to date, there have been few rigorous experimental studies of prosimian communication. One exception is Harrington's (1971) analysis of olfactory communication in Lemurfulvus, while others have noted responses to particular calls (Andrew, 1964; Jolly, 1966; Doyle, 1974). All the criteria listed above have not been shown to apply.
Evidence for Olfactory Communication
The olfactory modality has been assumed to be of particular importance to prosimians because of (1) the nocturnal habits of many species (which presumably reduce the effectiveness of visually perceived signals in favor of acoustic and olfactory cues); (2) the abundance of skin glands, some with strong-smelling (to us!) secretions; (3) the presence of a substantial olfactory lobe as part of the brain; and (4) behavioral responses to objects marked or areas traversed by other individuals. It is the existence of the behavioral responses that has permitted tests to demonstrate the existence of a communicative system based on scents.
The anatomy of the olfactory organs of the Prosimii is described by Hill (1953); that of the specialized skin glands by a variety of authors, but particularly Montagna and his coworkers (Montagna, 1962). Deposition of scents by prosimians is described by Andrew (1964), Doyle et al. (1967), Ilse (1955), Jolly (1966), and Petter (1962). A review is provided by Johnson (1973). The often elaborate rituals associated with marking behavior inevitably suggest that there is some significance attached thereto, such as a role in territorial demarcation (Jolly, 1966), synchronization of breeding (Doyle et al., 1967), spatial orientation (Seitz, 1969), and individual identification (Clark, in prep.).
Specific tests of the ability of individual Lemur fulvus to discriminate among individuals of the same and different subspecies and species, and between sexes, as well as of the territorial function of scents, were conducted by Harrington (1971). His subjects were, for the most part, captive-reared Lemur fulvus. Scents were collected from the animals by rubbing sterile gauze over their glands or by allowing spontaneous marking of gauze or lucite rods left within the animals' quarters. Scents were presented to the animal being tested by successively placing scentimpregnated gauzes into its cage for 30 seconds at a time, until the subject ceased to respond or its responses (specifically, sniffing or marking of the gauze) waned. Once this criterion for habituation had been attained, the test animal was either presented with a new series of marked gauzes (from a different donor) or, in the case of the "control" subjects, another series from the original donor. If discrimination of scents was occurring, responses would be expected to reappear in the first instance, but not in the second. Apparently, individuals, sexes, and taxa can be identified by scent, though which scents are most important (assuming the products of different glands differ), or whether sexual condition or season alters the result could not be stated. Lemur catta respond differently to the secretions of the antebrachial (forearm) gland of different males (A. Rosenkoetter, pers. comm.).
Harrington also substituted clean and scentmarked rods on sections of rod paths on which the animals traveled within their large enclosures. These substitutions had no apparent effect on the manner in which the animals used their space, raising doubt that scent trails are of particular importance. Of course, in a natural setting, scent trails may be of consequence. This is currently under investigation by Rosenkoetter (pers. comm.), who is seeking to correlate marking sites, territorial boundaries, and paths of movement of Lemur catta (living free in Madagascar!). No data are available as of this writing, however.
In sum, olfactory signals could be used for communication, but the evidence in hand supports no more than this possibility. Perhaps olfactory and visual information must be presented simultaneously in order for the former to be employed. Marking behavior, as noted before, is associated with conspicuous, often stereotyped, movements. Perhaps, too, the role of olfaction is evident only in particular contexts or particular locales. In galagos, A. Clark (pers. comm.) reports that urine marking is performed on conspicuous branches, while chest rubbing occurs against vertical trunks. The context-dependence of so much behavior should alert us to the importance of spatial and temporal context (Shettleworth, 1972).
Other considerations also lend credence to the view that olfaction is relatively important to the communicative systems of prosimians. Five of these have been summarized by Harrington (1971):
(1) The relatively small home range of prosimians as opposed to other primates enhances the effectiveness of olfactory signals. An L. fulvus, for instance, has a range of circa 7 ha, compared with 18-78 ha for Cercopithecus aethiops (which, in turn, has a much smaller range than most other monkeys or apes).
(2) The predominantly nocturnal habit of prosimians, compared to other primates, also would favor olfaction in signaling.
(3) The more highly seasonal breeding behavior of prosimians would necessitate synchronization of behavior within troops, which could be assisted by olfactory cues (note Michael et al., 1971).
(4) The relatively simple forms of agonistic behavior shown by prosimians, which are largely confined to the four weeks of the breeding season, are less dependent on a complex (multimodal) signaling mechanism.
(5) Finally, the habit of mutual oral grooming, so marked in prosimians, whose teeth and tongue appear to have been especially adapted therefore, provides a ready mechanism for the transmission of scents.
If these correlatives of olfactory communication do stand in a causal relation to one another, one would expect those ceboidea that most resemble lemurs in having a highly developed olfactory communication system, e.g., the Hapalidae, to resemble lemurs in these other features, too (Harrington, 1971). This point has yet to be investigated.
Evidence for Acoustic Communication
Several descriptions of the vocalizations of prosimians are available (note Jolly, 1966), but systematic studies of their role in communication are far more rare. It was shown that Lemur catta could be made to vocalize in an operant-conditioning paradigm (Wilson, ms.), supporting the view that acoustic signaling is not altogether alien to these animals. Though this has been generally accepted, there is some further significance to Wilson's study. Studies of vocalization in experimenter-controlled situations have many advantages over post hoc analyses of spontaneous utterance, particularly for the study of the behavioral and neural organization of vocalization. Hence, Wilson's demonstration that discriminative vocal conditioning is possible in lemurs is of substantial methodological significance. To date, however, this approach has yet to be exploited.
One attempt to correlate laboratory and field findings, though not utilizing operant methods, is being made with the mouse lemur, Microcebus murinus (McGeorge, 1973, and work in progress). McGeorge first described the full range of sounds produced by captive animals and correlated them with the social situation and behavior that they accompanied. She then reasoned that there must exist a maximum distance between animals beyond which a sound signal would not be perceived. This distance would be expected to vary with seasonal (and other) changes in ambient noise and foliage density. Hence, if mouse lemur sounds are communicative, entailing both an emitter and a receiver/responder, then there should be systematic variations in the frequency and amplitude (i.e., carrying capacity) of the sounds that are related to the sound-propagation (or, conversely, sound-absorption) characteristics of the animal's environment. The specific tests involve measuring the acoustic properties of the environment, the animal's vocalizations, and the distances between (and reactions of) the individual animals. This work is in progress at this time.
In Lemur variegatus there is a form of ritualized, synchronized "duetting," which also implies communication, or at least a mutual responsiveness to calls. In pairs or small troops of animals (wild or captive), a seemingly spontaneous, raucous, and very loud call erupts a dozen or so times in a day. While several voices repeat a basso cadence for ten to thirty seconds, a single voice provides a tenor counterpoint. The timing and rhythm of the voices appears to be fixed, though this has yet to be confirmed by audio-spectographic analysis. Curiously, in one group of two animals and one group of six, it was generally (solely?) a particular male who chimed in with the tenor line. For instance, in the larger group, of 168 recorded occasions of duets, "Mars" took the solo line 164 times; on the remaining four occasions the solo singer could not be identified with certainty but might have been "Mars." Of the pair, "Mercury" took the tenor line 99 times out of 100; on the hundredth occasion, the identity of the singer was unconfirmed. During the song, the members of the chorus are often lying prone on branches, muzzles pointed upwards, while the solo singer points his downward. No particular function or relation of the song to other activities is known.
The Need for Holistic Analysis
In most experimental studies of communication, including those described here, the "signals" are treated atomistically: a particular scent or sound produces a certain response. Occasionally, one finds that the signal is compounded of two or more sensory modalities, or has meaning only in a given context. Thus, it would not be surprising to discover that the scent from a Lemur catta's brachial gland has one effect when exuded while the tail is elevated and shaken behind its head, and another when the tail is tucked against the back (Jolly, 1966; the general effect of "context" on meaning has been dealt with extensively by Smith, 1968). The issue I wish to raise here is more complex. It is the problem of devising research strategies for dealing with complex systems that must be treated holistically.
To begin, it is necessary to document the claim that the communicative system of prosimians does indeed require treatment as a whole, rather than analytically. Apart from prejudices favoring a Gestalt Weltanschauung, are there empirical grounds for a holistic approach? The outstanding successes of analytic and synthetic approaches in the study of the "language" of birds (e.g., Thorpe, 1961; von Frisch, 1965) certainly would support a negative response. However, some studies of mammalian communication lead to a different conclusion, in particular a study of the precopulatory display of jackals (Golani, 1973). A jackal's behavior patterns can be described as a sequence of configurations, each composed of a group of discrete and simultaneously occurring events (position of ear or tail, body orientation, etc.). Any particular configuration recurs infrequently, though within brief periods of time there is a higher degree of regularity. Golani explored the degree to which the "events" of a particular configuration are seen as discrete phenomena by the jackals themselves. He found the significance of specific events to lie in their relation to other simultaneously occurring events and in their temporal relations. However, the shifts in the composition of configurations over longer stretches of time imply a change in the significance of specific events. In Golani's words, "This indicates that it is necessary to trace the nature of the change from one significance to another, rather than to look for stable, unchanging significance" (1973:111).
The sophisticated computer techniques (Guttman-Lingoes Multidimensional Scalogram Analysis) employed by Golani have not been applied to other mammals. The assertion that the peculiar "stable instability" of the jackal communication system is true of mammals in general, or even of another mammal, let alone prosimians, is perhaps premature. Yet I would not gainsay the likelihood of this assertion's being validated, not the least because of the great plasticity displayed by primates faced with novel communicative tasks (Premack, 1970).
Holistic systems are those "whose behavior is constrained by important nonlinearities," wrote Nelson, in a provocative essay on the future of holistic studies of behavior. "We should try to understand its components, of course, but if we are to understand the system we must consider it as a totality or not at all" (1973:310).
This means that an enormous amount of care is going to be needed, both to arrive at the specific hypothetical mode of functioning and to determine just how it is to be sought in the physiology of the neuromuscular system. One of the implications, I believe, is that the "controlled experiment" will be of limited usefulness in elucidating neural function, and it is going to play a much-reduced role in the behavioral study of the near future. This need not be entirely a bad thing. Controlled experiments are costly, usually, in time, money, animals, and effort which might at this stage of our knowledge be applied more productively in finding out just what it is that is worth doing experiments on. I hesitate to use the examples of astronomy and geophysics, but they may prove to provide better research paradigms for us than physics has. The difficulty inherent in subjecting the earth and stars to controlled experiments has perhaps made astronomy a different sort of science, but not necessarily one lacking in rigor or success.
We may, if we like, subject animals to controlled experiments, but there is no law that they must divulge their secrets to us thereby. My personal opinion is that the greater priority is on the development of new modes of behavioral description, based on rigorous notions (where such are possible) of harmony and conflict, part and whole, simple and complex, containment and change. . . .
I expect considerable dissent from some quarters over these points. It seems not to be generally realized that the subjects of most controlled behavioral experiments are analog models of "real animals in real situations" just as a collection of neuromimes is. As a minimal assumption, the experimenter counts on Nature's having no intentions of resisting his invasion of her privacy, and we really have no means of determining how often he mistakes her intentions. Kavanau (1967) has catalogued as a cautionary tale for us some instances of the contrariness of well-bred mice.[1973:311]
It is a tale all of us might ponder.
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