Signals That Individualize The Social Units within the Population

Distribution of monkey populations into social units is the rule among Old World species, even though the concept of the group as a definite entity is not always easy to grasp. The existence of relatively stable groups in a population, in contrast to a nomadic life with labile groups, as in chimpanzees (Goodall, 1965; Sugiyama, 1968a), does not mean that these social units have no exchanges among themselves: most studies show, on the contrary, that a fairly important part of specific signals occurs in intergroup relationships. As Rowell (1972) notes, monkeys of neighboring groups "are intensely interested in whatever they can see and hear of them; in a communicative sense, each monkey belongs to the whole local population of his species as well as to his immediate group."

This spatial distribution presupposes a certain number of mechanisms by which groups are individualized. According to Kummer (1971b), three imperatives are required: "to keep members of each group together; to separate the groups; and to tie each group to a piece of land." They are assumed by communication mechanisms.

The cohesion of group members can rest on two different modalities of signal action: (1) All individuals exchange signals permitting them to maintain contact; this type functions at close range (see intragroup communication). (2) Wide-range signals, uttered by a few individuals, gather the members of the group around the vocalizers. This pattern of signal generally has a sufficiently wide range to be perceived by neighboring bands; thus it simultaneously assumes the intergroup communication function of maintaining distance (Marler, 1968). Increase in distance can be accomplished either by wide-range signals, if the groups do not come into visual contact, or by proximity exchanges, if the nature of the relationships tends to draw the groups together.

Generally speaking, these signals are characteristic of adult males. Their nature depends on the distance at which the exchange takes place and on the structure of the habitat in which the species is evolving. It is possible to classify monkeys into two categories: (1) Species in which there is no visual contact between groups, either because of the size and/or shape of their home ranges or because of habitat density. In the former there are few or no exchanges of species specific signals (patas [Erythrocebus patas]: Hall, 1968b; talapoin [Miopithecus talapoin]: Gautier Hion, 1971a); in the latter the exchanges are essentially of an acoustic nature (as in most forest guenons). (2) Species for which the wanderings of individuals from different groups lead actively or passively to a closed proximity; such encounters, favored by open habitats, permit all sorts of exchanges, particularly visual ones. The existence of species-specific signals depends on the individualization of groups and their mutual tolerance, and it becomes difficult to be precise about the concept of social unit when the exchange and mingling of individuals happens without any specific manifestation (the case in the geladas [Theropithecus gelada]: Crook, 1966; and in the hamadryas: Kummer, 1968). In other cases, individualization depends on mutual avoidance (olive and chacma baboons [P. anubis and ursinus]: DeVore and Hall, 1965) or on an intergroup hierarchy of dominance (rhesus monkey [Macaca mulatto]: Southwick et al., 1965): the signals exchanged are those of the usual aggressive repertoire.

The olfactory capacities seem little used in intergroup relations (see below). Olfactory markings appear to be a form of vestigial behavior and operate with other kinds of signals.

VOCAL SIGNALS

Carpenter (1934) was the first to point out the vocal mechanisms used for group spacing, along with the roaring of male howlers (Alouatta palliata). Subsequently, many authors have emphasized the existence of powerful vocalizations acting in intergroup communication in Old World monkeys. Such signals exist in langurs (hanuman langur and ceylon gray langur [Presbytis entellus]: Jay, 1965a; Sugiyama et al., 1965; Ripley, 1967; Yoshiba, 1968; Vogel, 1973; nilgiri langur [P. johnii]: Tanaka, 1965; Poirier, 1968, 1970a, 1970b; lutong [P. cristatus]: Bernstein, 1968), in the African Colobus spp. (black and white colobus [Co. guereza¹]: Ullrich, 1961; Schenkel and Schenkel-Hulliger, 1967; Marler, 1969, 1972; black colobus [Co. satanas]: Sabater Pi, 1970; angolan colobus [Co. angolensis]: Groves, 1973), in the macaques (Japanese macaque [M. fuscata]: Itani, 1963; lion-tailed macaque [M. silenus]: Sugiyama, 1968b; crab-eating monkey [M. fascicularis or M. irus]: Shirek-Ellefson, in Marier, 1968; Kurland, 1973; pig-tailed macaque [M. nemestrina]: Chivers, 1973), in the baboons (P. ursinus: Hall, 1968a), in the patas (Hall, 1965, 1968b), in the mangabeys (grey-cheeked mangabey [Ce. albigena]: Chalmers, 1968; Waser, 1975; agile mangabey [Ce. galeritus]'. Quris, 1973), and finally in a large number of other species of Cercopithecus (spot-nosed guenon [C. nictitans], moustached monkey [C. cephus], crowned guenon [C. pogonias]: Gautier 1969; Struhsaker, 1969; mona monkey [C. mona], Campbell's monkey [C. campbelli], red-eared guenon [C. erythrotis], l'hoest's monkey [C. l'hoesti], lesser spot-nosed guenon [C. petaurista]: Struhsaker, 1970; C. campbelli: Bourlière et al., 1970; red-tailed monkey [C. ascanius], blue monkey [C. mitis]: Aldrich-Blake, 1970; Marler, 1973; de Brazza's monkey [C. neglectus]: Gautier, 1971).

The most obvious general characteristic of these calls is their exceptional intensity and range: the roaring of the guereza can be heard for more than a mile, and the "Pml" of the spot-nosed guenon carries as much as a kilometer. Despite their diversity, these vocalizations are all of a pure, low-pitched structure and seem particularly adapted for penetrating a woodland habitat.

They are uttered primarily by adult males. Ontogenetic development studies show that they do not appear in males before sexual maturity, between five and seven years of age (C. nictitans, pogonias, neglectus, petaurista, Ce. albigena, galeritus: Gautier, 1971, 1973, and pers.obs.). Fig. 1 illustrates these facts in several species raised in captivity.

Fig. 1. Ontogeny and spectrographic analyses of the "loud calls" of five five cercopithecus species. The period of sexual maturation in males indicated by a break in the weight curve. Loud calls are emitted for the first time at the end of this period, be it at 5, 6, or 7 years of age. A: C. pogonias: Mml, boom-type call, type 1 loud call; Mm2, unitary and binary barks, type 2 loud call. B: C. neglectus: Bml, boom-type call, type 1 loud call; Bm2, unitary barks, type 2 loud call. C: C. nictitans:PmO, boom-type call, seldom manifested; Pml and Pm2, barks, types 1 and 2 loud calls. D.E.Ce. albigena and Ce. galeritus: whoop gobble, type 1 loud call.

Depending on the species, there can be from one to four vocalizations of high intensity; in intergroup relations, however, only one or two types are used.

Type 1 Loud Calls

In addition to their intensity, these calls are notable for their structural originality, in contrast to other vocalizations of specific repertoires, and for their slight variability in structure, which is stereotyped and discrete (Marier, 1972), as much at the species as at the individual level. Thus the ''booms" of a male C. pogonias or the barks of a C. nictitans maintain great stability in their fundamental structure, in spite of aging of the animals, the only change being an increase in intensity and a modification of timbre. In some species, on the other hand, the calls of different individuals can be distinguished by ear (Cercopithecus spp.: pers.obs.). This interindividual variability, which supposedly enables congeners to identify the vocalizers, rests on slight transformations of fundamental or accessory structures. Waser (1975) has shown through playback experiments that in the grey-cheeked mangabey males can distinguish "whoop gobbles" uttered by stranger group males from those emitted by members of their own band. Other monkeys, like the guereza, have such stereotyped vocalizations that individual recognition of emitters seems improbable (Marler, 1972).

The diversity of structures at the interspecific level is great, but schematically four categories can be recognized: (1) calls of the "boom" type, given principally by representatives of the su-perspecies mona (Mml, Fig. 1 A); (2) "barks" of various guenons and some macaques (Pml, Fig. 1 B); (3) "whoops," sometimes followed by "hiccups" (langurs) or by "gobbles" (mangabeys; Fig. 1 D, E); (4) "roaring" of the colobus. The category of barks is by far the most heterogenous.

Proceeding from these categories one notes: (1) Calls of similar structure occur simultaneously in phylogenetically close species (same genus) and relatively remote species (different genera), e.g., the booms of the superspecies mona are observed in de Brazza's monkey and to a lesser degree in C. mitis and C. nictitans (Gautier, 1971, 1973; Marler, 1973) (Mml, Pml; Fig. 1 A, B, C); and the bark of C. nictitans is practically indistinguishable from the "pyow" of C. mitis (Gautier, 1969; Aldrich-Blake, 1970; Marier, 1973) and seems close to the Dl calls of the Japanese macaque (Itani, 1963) if one refers to Itani's phonetic transcription. Furthermore the complex call structure of the mangabeys described by Chalmers (1968) for Ce. albigena and by Quris (1973) for Ce. galeritus, and which probably exists in Ce. torquatus (Struhsaker, 1970), includes a whoop of pure structure (pitch: 200-300 Hz) that seems to correspond to the whoop of the langur, is close in pitch (300-400 Hz: Vogel, 1973, for P. entellus), and is perhaps comparable to that of M. silenus (Sugiyama, 1968b). Furthermore, the hiccup that follows the whoop in P. johnii (Poirier, 1970a, 1970b) may be related to the gobble of the mangabeys.

(2) Conversely, phylogenetically close species can possess very different loud calls. This is the case in the two monkey pairs C. nictitans-C. cephus and C. mitis-C. ascanius, the usual vocalizations of which are very similar (Gautier, 1969; Marler, 1973). Generally speaking, species possess increasingly differentiated loud calls in direct proportion to their degree of sympatry, and a fortiori when actually living in polyspecific association (Gautier and Gautier-Hion, 1969; Gautier, 1973). These calls would therefore have an important role in speciation.

In addition, species differentiation is brought about through temporal patterns and emission sequences. In various species, loud calls are in effect uttered in series whose temporal organization is often elaborate (Marier, 1968). These sequences can include from one to three different vocalizations, sometimes associated with nonvo-cal sounds. Fig. 2 illustrates these sequences in three sympatric species, C. nictitans, neglectus, and pogonias. In the last two, the calls are similar, species differentiation being based on emission sequences.

Fig. 2. Spectrographic analyses of the emission sequences of loud calls in Cercopithecus neglectus, C. pogonias, and C. nictitans. A, B: C. neglectus inserts tree shaking and a sound produced by inflating the vocal sac between two booms (see also Fig. 3), whereas C. pogonias can emit only one or several booms. The barks (type 2 loud calls, Bm2 and Mm2) also have different structures and temporal emission patterns, which accentuate sequence-specificity. C: In C. nictitans, type 1 loud calls (Pml) and type 2 loud calls (Pm2) each have different emision rhythms during stereotyped sequences.

Another frequently emphasized characteristic is the diurnal periodicity in the emission of these calls. The rhythm may be monophasic, with calls being uttered predominantly in the morning: P. entellus ("morning whoops," Jay, 1965a), Ce. albigena (Waser, pers. comm.), Ce. galeritus (Quris, 1973); or in the evening: C. mona (Struhsaker, 1970). It can be biphasic, the calls being more frequently given morning and evening, as in C. nictitans (Gautier [Beiinga region], 1969) and Co. guereza (Marler, 1972); or polyphasic, as in C. nictitans and C. pogonias living in a mixed troop (Gautier-Hion and Gautier [M'passa region] 1974). Thus the same species can, according to the region, present different emission rhythms or none at all (cf. Struhsaker [Cameroun], 1970 for C. nictitans). The increase in the frequency of the emission of loud calls in the morning and evening shows that they are principally uttered close to sleeping sites (Hall, 1968b; Aldrich-Blake, 1970; Gautier-Hion and Gautier, 1974).

From the work of Stark and Schneider (1960) and Kelemen (1963) it is known that the phonation organs of the primates are among the most highly developed. Hill and Booth (1957), working with Colobus spp., and Gautier (1971), studying various African guenons, have offered evidence suggesting that males of species that emit strong vocalizations possess either a well-developed larynx (Colobus spp. except the red colobus, Co. badius, which does not utter any loud calls: Marler, 1970), or hypertrophied vocal annexes (other species).

Itani (1963) has noted a distension in the submaxillary region in Japanese monkey males during the emission of DI calls. Our observations in C. neglectus, pogonias, and nictitans show that vocal sacs in effect play an active role in the emission of some loud calls. Fig. 3 analyzes the emission behavior of boom-type calls in a C. neglectus male, in which the inflation of the vocal sac precedes the emission. If a hole is punched in this sac, the call will be of low intensity for the sac acts as a resonator and amplifier (Gautier, 1971). The participation of these annexes is less evident in other species. In most cases, however, the loud vocalization, preceded by a lowering of the head, is uttered when the head is thrown back violently (Fig. 4).

Such complex vocal behavior necessitates a certain amount of "concentration" from the vocalizer and indicates, on the behavioral level, the relative quietude and weak motility of the animal. These characteristics differentiate loud calls of the first type from those of the second.

Each monkey group has one or several male emitters, e.g., there are several in Ce. albigena (Waser, 1975), various langurs, and M. fuscata, but only one in groups of Colobus or Cercopithecus spp. There is no doubt that these individuals have the status of social leaders. Hunkeler et al. (1972) estimate that in C. campbelli, the emitter of loud calls must be the exclusive genitor. In fact, when dominance relations are established between two adult males in species where a single vocalizer is observed in natura, the loud calls of the subordinate male can be totally or partially inhibited (Gautier, 1971). This throws a new light on the social structure of harems, which would only in some cases correspond to one-male "status" group.

The ritual character of loud calls, resulting from their stereotyped nature and their daily rhythm of occurrence, is reinforced by the fact that it is often difficult, especially for the morning and evening emissions, to find evidence of any stimuli provoking them (Marier, 1968). For this reason, numerous authors employ the term "spontaneous," an adjective used to describe other calls of mammals (e.g., the bell of the deer: Kiley, 1972).

Fig. 3. Behavioral sequence accompanying the emission of booms (type 1 loud call) in Cercopithecus neglectus. 1-3: preparatory phases; 4-7: inflation of vocal sac accompanied by sound (spectra a, b); 8-10: emission of boom with deflation of the vocal sac (spectra c, d). (From Gautier, 1971, in Biologia gabonica.)

Fig. 4. Emission behavior of type 1 loud calls in an adult male Cercopithecus nictitans. (Paimpont; from photographs.)

For most species, what most often provokes the emission of type 1 loud calls is the production of the same calls by males from neighboring groups. Nevertheless, the existence of phonoresponses varies. They have never been observed in C. cephus or C. ascanius (Gautier, 1969; Marler, 1973) and are also rare in C. pogonias. These variations are a result of both population density and differences in call function (e.g., absence of territoriality in C. cephus: Struhsaker, 1969).

Type 1 loud calls are also heard at the time of close-range intergroup exchanges, in which they are produced predominently at the end of an encounter, when calm has been restored. Thus the roaring of guereza, like the Pml of C. nictitans, appears after interactions between groups, when the vocalizer has left the area of conflict (Marler, 1972; Gautier, 1969). Similarly, the D1 of the Japanese macaque (Itani, 1963) is uttered by the male only after the other members of the group have taken cover.

Furthermore, these vocalizations are given following numerous stimuli that are not specific; the lists of these stimulations, given by various authors, are astonishingly similar. Some are social, such as those produced by alarms from congeners; while others result from various happenings—breaking branches, falling trees, thunderclaps, rifle reports, birds of prey, approach of humans—prompting Struhsaker (1970) to state that these calls are evoked by situations "all of which seem to have in common, the potential to disrupt the coherence of the social group."

Here again, these loud calls appear only as deferred responses to those stimuli that are immediately followed by type 2 loud calls or various aggressive alarms (see below). Type 1 calls are therefore uttered by animals that have returned to a lower state of excitation.

Experiments aimed at provoking these vocalizations in captivity have shown that any disturbance threatening the integrity of the group will release them. This always happens if a female is removed from the group. Type 2 loud calls are uttered during her capture, and upon her réintroduction, the male leader immediately tries to copulate with her and emits a long series of type 1 loud calls.

According to the literature, loud calls seem to fulfill two types of function (see Marler, 1968): (1) An intragroup function of cohesion and rallying. Not only do such calls permit localization of the vocalizers but also, by provoking a new outbreak of contact calls from congeners, they facilitate interindividual localization, especially after a disturbance. Furthermore, the calls given in the morning and evening clearly have the function of orienting movement—they are followed by the group's either getting under way or stopping its activity (Itani, 1963; Jay, 1965a; Shirek-Ellefson, in Marler, 1968; Gautier, 1969; Gautier-Hion and Gautier, 1974). (2) A function of maintaining intergroup distance, assumed principally by the phonoresponses between males of adjacent groups. Thus in areas of high density, as is the case for groups of C. nictitans in northeastern Gabon, it is not rare for the males of three or four adjacent groups to exchange their loud calls upon awakening. In this way the groups are informed of the position of their neighbors before beginning any activity. Aldrich-Blake (1970) notes than in C. mitis the response of a male varies according to whether he is at the center of his home range. In the langurs, on the other hand, there is an active search for close contacts between groups, the males going several hundred meters away from their own groups in order "to challenge each other" vocally and visually (Ripley, 1967; Poirier, 1970b).

The fact that loud calls depend on hormonal mechanisms (see above, ontogeny) implies a more or less direct correlation with the phenomenon of reproduction. Hill and Booth (1957) thought that the loud calls of the colobus were an "assertion of status." Going back to the ideas of Darling, Poirier (1970b) suggests that inter-group spacing displays are simultaneously the social stimuli necessary for success in reproduction. This seems confirmed by the observations of Hunkeler et al. (1972, see below) with a group of monas. The vocal "outbidding" observed in males of various species in mixed troops (Gautier-Hion and Gautier, 1974) should also be understood as an assertion of status. With these males, it is not a question of distancing and spacing, since they live in permanent association, but rather a mutual yet somewhat competitive affirmation of their identity (in terms of species, age, sex, and status) (see also Marler, 1973).

The strict species specificity of the loud call structures and/or sequences for sympatric species and especially for those living in association, leads one to think that these vocalizations are behavior patterns adapted to assure individualization of social groups and species isolation in reproduction. The loud calls of male monkeys who are social leaders of their groups would thus play a role close to that of the songs of birds, in which females select males on the basis of vocalizations (Hinde, 1970).

VOCAL SIGNALS

Some vocalizations linked with the general routine of the group act without the support of visual information. In interindividual close range exchanges, on the other hand, the overlapping of vocal, visual, and tactile signals is great.

Signals Associated with the Routine Activity of the Social Unit

A group of monkeys is most often silent during rest. Vocal activity resumes slightly before individuals begin to stir and continues during their movements. The calls emitted are often nasal, of short range, and uttered without modification of facial expression. They do not appear to be addressed to specific receivers, but nevertheless evoke identical vocal responses in adjacent monkeys. Occurring as individual reactions, they are diffused throughout the group thanks to phonoresponses, which permit reciprocal individual localization and the general cohesion of the social unit. This kind of signal has been reported in most species, except the African colobus, which are particularly silent (Booth, 1970, 1972). They are the "grunts" of the baboons (Hall, 1962; Andrew, 1963b; Hall and DeVore, 1965; Rowell, 1966; Aldrich-Blake et al., 1971), the drills and mandrills (Struhsaker, 1969; Gartlan, 1970), the langurs (Jay, 1965a; Poirier, 1970a; Vogel, 1973), the "deep muffled grufF' vocalizations of M. mulatta (Altmann, 1962), "the calling sounds" of M. fuscata (Itani, 1963), the "basic grunts" and "A-calls" of M speciosa (Bertrand, 1969), and the "grunts" of the mangabeys (Andrew, 1963b; Chalmers, 1968; Quris, 1973; Deputte, 1973), the guenons (Haddow, 1952; Struhsaker, 1967b, 1970; Aldrich-Blake, 1970; Marier, 1973) and the talapoin (Gautier, 1967, 1974; Gautier-Hion, 1971b; Wolfheim and Rowell, 1972).

In the forest monkeys, one notes that the frequency of call occurrence follows the activity rhythm of the animals, increasing with the potential risk of losing contact between congeners, e.g., with decrease in luminosity, increase in speed of movement or density of the environment, or state of insecurity after a disturbance (Itani, 1963; Gautier-Hion, 1970). Other situations, such as the group's coming into the presence of a fruit tree or the sight of a congener, also provoke calls. In most species these calls are given principally by adult females and juveniles. If the vocalizers are male, their vocalizations can easily be differentiated either through structural differences or because of their maturational transformation.

We have seen in the guenons, macaques, langurs, and colobus that type 1 loud calls uttered by males precede, especially in the morning, group movement and punctuate locomotor activity, playing a rallying and coordinating role. A similar system seems to exist in some baboons. Aldrich-Blake et al. (1971) note, for example, that in P. anubis the "two-phase wa hoo bark" in males precedes and coordinates group passage in difficult situations such as the crossing of a road (see also Gautier, 1969). Gartlan (1970) also points out a "mobilizing two-phase grunt" in the drill, similar to that of mandrill (P. Jouventin, pers. comm.). On the other hand, males can retain the same basic call as females and juveniles, but its structure is profoundly modified. Fig. 15 shows the evolution of calls linked with cohesion in a male C. pogonias, the growth of which was followed for seven consecutive years.

Originally, the call was composed of a stable low-pitched unit, followed by a shrill component, modulated in frequency (Fig. 15, CI). Common in young animals, this call becomes rare in adult males; during ontogeny, the shrill component has a tendency to disappear, being replaced by a low-pitched unit of similar duration (Fig. 15, compare CI and C4), while the average pitch of the low structure can go as low as 170 Hz. Note that the curve depicting the decrease in pitch (Fig. 15A) is symmetrical to that showing the increase in weight (Fig. 15B). Both show a marked variation at the beginning of puberty. During the prepuberty period (which lasts five years) the animal gains 2,250 g (an average of 43 g per month) whereas its call decreases by 76 Hz (average of 1.45 Hz per month). On the other hand, during the puberty phase (about nineteen months), corresponding to descent of the testicles and the growth of adult canines, the monkey gains 2,200 g (average of 112 g per month) and the pitch of its call drops by 92 Hz (average of 4.7 Hz per month). Therefore during this period the animal's weight increases as much as in the previous five years and its voice falls 1.2 times as much as it did in those five years (see Table 2). Note also that variability in the pitch of the call is greater when the monkey is young (cf. standard deviation: Fig. 15A). In the female, the weight curve does not have the same variation at the beginning of puberty; likewise, the decrease in the pitch of the call is regular and much smaller than in the male.

Fig. 15. Maturational transformations of the structure of cohesion calls of a male C. pogonias. A: Average pitch of the call's low-pitched component as a function of age (the hatched area corresponds to the standard deviation). B: The animal's weight during the same period. Note the symmetric inflections of the two curves starting at puberty. C: Spectrographic analyses of cohesion calls at different ages. Note the disappearance, between ages 6 (3) and 7 (4), of the high-pitched component, which is progressively replaced by a low-pitched component.

Table 2

Quantitative data for Fig. 15.

The break in the slope of the male weight curve of various guenons (C. nictitans, pogonias, cephus, petaurista, neglectus; Ce. galeritus and albigena: Gautier and Gautier-Hion, in prep.), which seems absent in a Platyrrhine such as the squirrel monkey (Rosenblum and Cooper, 1968) resembles that of humans. It is accompanied by an abrupt transformation in the voice, related to the breaking in the voice in man (Gautier, 1974).

These features are important at the communication level. If, all conditions being equal, each age and sex class possesses different structural characteristics and emission frequencies for the same fundamental vocal type, one can assume that an individual wandering in a dense environment, periodically receiving cohesion calls, could immediately recognize the age and sex of its closest congeners.

In forest guenons cohesion calls also vary according to a more or less graded system as a function of distance between vocalizer and congeners and of the general excitation level. This system, described for the talapoin (Gautier, 1974) is found in a variety of species (Fig. 16) and schematically includes four types of vocalization. The first corresponds to the calls uttered during the usual progression of the group. The second is heard particularly if interindividual distance increases or if the excitation level of the monkeys rises subsequent to a perturbation. The third is typically given by an infant that has lost its mother or a monkey that has lost contact with the group. The fourth variation is uttered by an infant that has reestablished contact with its mother.

The call gradation of this cohesion-distanc-ing-isolation system is total in the talapoin and mona (Fig. 16) but only partial in others such as C. cephus, in which the number of intermediate calls is smaller and the structural diversity greater. The same kind of system seems present in most forest monkeys. In C. aethiops (Struhsaker, 1967b) the "eh eh calls," "progression grunts," and "most rrr calls" are probably comparable.

Fig. 16. Comparison of the vocal systems of "cohesion" in C. cephus (A), C. nictitans (B), C. neglectus (C), and C. pogonias (D). Each column contains calls of comparable emission context and function.

Column 1 : Calls emitted during routine progression. For A, B, C these calls have only a low-pitched unit; for D the low- and high-pitched components are associated (D3; see also Fig. 15C and 42a, b). Column 2: Calls emitted after a slight disturbance, exhibiting a discontinuous transition (A4, B4) or a gradual one (C4, D4) toward calls in Column 3. Column 3: "Isolation" calls, with structures new and pure in C. cephus (A5) or noisy in C. nictitans (B5), whereas they derive from preceding calls in C. neglectus (C5) and C. Pogonias (D5). Note the disappearance of the high-pitched component. Column 4: "Huddling calls" of low intensity, characterized by a vibrating sonority, with structures derived from calls in Column 1 (A2, B2, C2, D2).

Throughout this graded system, the conditions under which one vocal type passes into another, if they generally imply variations in interindividual distance, are sometimes provoked by variations in "psychological" distance, which depend on the excitation level of the animals. Thus, an increase in habitat density, which favors loss of contact, is translated by an evolution of the first type of call into the second. Similarly, a young monkey huddled in its mother's arms might utter an isolation call if its mother refuses to nurse it. Thus we heard isolation calls uttered by most of the members of a mona group an hour after nightfall after a crowned eagle had flown over.

Under such conditions of excitement, mutual vocal enlistment resulting in a chorus can be heard in various species. This is the case in baboons (Hall and DeVore, 1965; Rowell, 1966), mangabeys (Chalmers, 1968; Gautier and Deputte, 1975), the macaques (Rowell and Hinde, 1962; Itani, 1963), and the talapoin (Gautier, 1974).

More or less varied cohesion calls have been noted in macaques, baboons, and mangabeys. In the Japanese macaque, "A-calling sounds" are all used for group cohesion and control of progression. Itani (1963) differentiates them according to their structure, the animals uttering them and the activity in progress: A2 are characteristic of certain females, A9 are emitted when the troop is calm or in slow movement, and A10 are used for departing.

Variations of the same type may exist in other species. Hall and DeVore (1965) mention a great variety of grunts uttered by baboons during routine social behavior and a "doglike bark" emitted by a monkey temporarily separated from the group. The same is true of the mangabeys. Nevertheless, if it seems that all species possess calls used for social cohesion, the mangabeys as savannah monkeys appear freer from environmental constraints, and their cohesion vocalizations have evolved mainly on the basis of more specialized interindividual exchanges in which vocal signals are associated with other sensory modalities.

Signals Associated with Peaceful Interindividual Relations

In A-group sounds of Japanese macaques, Itani (1963) distinguishes "calling sounds" from "muttering." The two have similar structures but the latter are addressed to a particular congener. This type of signal includes all the vocalizations leading to peaceful interindividual close exchanges. In all species for which they have been described, these signals derive, from a structural point of view, from calls linked with cohesion of the group as a whole. Unfortunately the literature offers few data that could permit interspecific comparisons.

In the vervet, Struhsaker (1967b) points out several vocalizations derived from the progression grunt, which are correlated with close interindividual exchanges. Generally speaking, "aar-raugh calls" occur when dominant monkeys and subordinates are at close range: at the approach of a dominant male, a subordinate one gives a "woof-woof," "wa," or "woof-wa" call. A female approached by a dominant female will utter a "wa-waa" call and a juvenile a "rraugh" call.

In the baboons, Hall and DeVore (1965) point out the "high-frequency grunting" characteristic of adult males being approached by an infant. In Ce. albigena and galeritus, adults also emit a particular grunting, derived from the progression grunt, when they come close to an infant. Furthermore, the adult male may utter a slow-rhythm grunting (Fig. 17) (pers. obs.), which does not exist in the female. In the mangabeys in general, a great number of variations based on grunting occur (e.g., in a juvenile when a male approaches, in females preceding mutual sniffing). In the stumptail macaque, Bertrand (1969) also notes a number of variations in these types of calls: "greeting grunts" directed toward infants, "B calls" characteristic of females whose children are out of sight, and "coos" uttered at the sight of a congener or after a separation.

At present the greatest diversity has been noted in the Japanese macaque, apparently due to the quality of the studies rather than to any species-specific peculiarity. Itani (1963) shows evidence for A5 calls uttered between adult males, A6 given by a subordinate male toward a dominant one, and D4 characteristic of receptive subordinate females. Green (1975), in his very detailed study of the coo sounds of this same species, throws new light on the extreme variability of these vocalizations given at close range. He distinguishes seven categories of coos of very similar sonographic structure. One promotes the general progression of the group, and the six others include close-range and "personalized" signals. Thus the "double coo" is characteristic of solitary or "depressed" monkeys (cf. isolation calls of the Cercopithecus) and especially of females who have lost their young, whereas the "dip early high coo," the "dip late high coo," and the "smooth late high coo" are uttered by subordinate individuals in response to dominant ones. These same sounds are also often given by juveniles communicating with their mothers.

In Cercopithecus, infants also give calls with structures close to those used for cohesion but less variable than the coo sounds of the macaques. In some species, however, the young utter shrill calls of a specific structure, which may be trilled (e.g., in C. nictitans, mitis, cephus, ascanius) or not trilled (C. pogonias and neglectus), and which can be associated with cohesion calls in either a discrete or a graded manner (e.g., C. pogonias, Fig. 16).

Their structure is highly variable, especially in intensity and frequency modulation, giving them tones that are sometimes plaintive, sometimes interrogatory and "peremptory," and sometimes violent, according to the vocalizer's excitation level and the context of emission. Four situations may be distinguished: (1) Calls are exchanged between an infant and its mother, rather spontaneously and in the absence of any apparent disturbance. The mother responds to these mother-young contact calls with the same sounds or, more often, with the usual cohesion calls. (2) The calls become more intense when the infant solicits closer contact (carrying or grooming) or suckling. (3) If the mother accepts contact, the call becomes modulated and plaintive, its intensity diminishes, and only a rhythmic and atonal breathing may be uttered. (4) If the mother refuses contact (especially during weaning) the calls become intense, their frequency modulation attenuates, and finally the quavering disappears. These sharp whistlings can become noisy and evolve toward screams (Fig. 18). As in the young of many species, these vocalizations are associated with spasmodic head and tail movements.

Fig. 17. Gruntings of the female (A) and male (B) Cercocebus galeritus,emitted while approaching an infant. Al, 2: binary forms; A3, Bl: unitary forms of call 1 (cf. Fig. 10); B2-B7: grunting in slow rhythm (1.32 units/sec) characteristic of the adult male.

Fig. 18. Trill variations in a young female C.cephus.

Al: "normal" contact calls; A2, 3: calls emitted by a female rejoining a congener after separation; Bl, 2, 3: contact solicitation calls after a slight frustration. Note the separation of the constituent units of the trills (1, 2), which are quite visible on the amplitude modulation spectra (1, 2'), as well as the loss of tonality in call 3. The latter can be emitted by a juvenile reestablishing contact with its mother. C: Calls given after an important frustration. CI: "Quasi-normal" trill with maximum energy concentrated in the second harmonic; C2: "trill-chirp," the last pulse of which is transformed into an alarm call; C3: "scream-trill," opening with a noisy component. Note the reinforcement of harmonics 2, 3, 4 in proportion to the fundamental sound. D: Distress calls. DI: "Trill-scream" with disappearance of quavering in favor of noise; D2: short "scream" without quavering (see 1' and 2’).

The frequency of emission of these calls decreases rapidly in the course of ontogeny, especially in males. The adult female gives them again during contact with infants. Similarly, these vocalizations reappear in juveniles and subadults at the birth of a sibling. This regressive phenomenon occurs frequently in captivity (see Gautier-Hion, 1971b; Gautier, 1974).

All these signals can be classified under a general rubric: lack of, search for, solicitation of, or maintenance of contact. Thus, they incontest-ably play a role in general social cohesion, but they also have a more short-term, immediate significance concerning the emotional state of the uttering monkey. In effect, Green (1975) remarks that the low-pitched coos of the macaques are used in low-level apprehension and agitation situations in vocalizing animals, whereas the high-pitched coos are given much more when the monkey is agitated and probably apprehensive. This same remark, correlating call structure with the vocalizer's emotional state, was made by Kiley (1972) for the ungulates and Gautier (1974) for the talapoin. Thus, as Green points out, signal morphology being a direct reflection of the uttering monkey's internal state, is sufficient to inform the receiver about it.

Green shows that, starting from the same basic sound this mechanism permits a great variety of combinations; the precision of the message received is increased by close-range visual communication and knowledge of the sex, age, and sexual state of the vocalizer. Our observations on the variations in call structures due to ontogeny show that vision is not always necessary for the identification of the vocalizer's age or sex since the signal morphology alone can be sufficient.

The observer must be conscious of this maturational approach to vocalizations, seldom emphasized at the present time in studies on Old World monkeys, before claiming that the calls given by a juvenile and by an adult male under the same stimulation are of different natures. It is often the same call, structural characteristics of which have evolved with age.

Whether the calls are different by nature or because of maturational modifications, the result is the same at the operational level as far as the identification of the message is concerned. However, distinction is fundamental for understanding the evolution of a communication system. Ontogenetic modifications in calls (which differ according to sex) that allow the identification of age and sex classes and modifications caused by the emotional state of the monkeys are two complementary processes that permit the achievement of an extremely varied communication system.

On the basis of these remarks, we can conclude the following: All species (except perhaps the African colobus) have developed calls whose more or less immediate function is maintenance of cohesion of the social unit. This function is particularly obvious in forest guenons, where maintaining contact is a real problem (e.g., for the cryptic talapoin, which lives in a particular dense environment in groups of more than a hundred members). It "blurs," however, in monkeys in an open habitat, where numerous visual exchanges are possible.

In these species, as well as in some forest monkeys like the mangabeys (and doubtless the drills and the mandrills), calls associated with contact and cohesion have become more diversified, interindividual exchanges having become more personalized and sociability having increased. Similarly, the correlation between these calls and the influence of nonbiotic factors, such as density of habitat and luminosity, has become much less evident. The example of the forest and arboreal Ce. albigena seems to show that such a vocal system depends more on the species' degree of evolution than on the direct influence of the environment. We shall see below that exchanges of close-range calls are often associated with visual signals like lip-smacking or presentation, and that they precede or accompany a great number of tactile and olfactory exchanges.

Signals Associated with Agonistic and Sexual Interindividual Relations

An increase in the frequency of interindividual contacts increases the probability of conflicts in which the slight distance separating protagonists permits exchanges of all kinds. Although visual signals play a predominant role in agonistic relations (Marler, 1965), they are frequently accompanied by a great number of vocal and nonvocal sounds. This multimodality consequently increases the structural variability of the signals exchanged. This, taken with the fact that protagonist roles can be reversed rapidly, makes it difficult to separate signals linked with attack from those correlated with flight. Rowell and Hinde (1962) were the first to show that aggression-flight signals taken as a whole constitute an almost perfectly graded system. This statement probably applies to most, if not all, species. Vocal signals that accompany threat behaviors are most generally low-pitched; those linked with submission and flight are shrill. Vocalizations emitted by a monkey conflicting with these two tendencies have a composite structure, blending low-pitched and shrill components (Fig. 9, D, F).

One category of sounds accompanying aggressive behavior consists of brief, low-pitched calls with rolling sonority, which derive from the various grunts acting in cohesion or friendly interindividual relations throughout the group. Such calls are observed in baboons (Hall and DeVore, 1965), macaques (e.g., M mulatta: Rowell and Hinde, 1962; M. fuscata: Itani, 1963; M. nemestrina: Grimm, 1967; M. speciosa: Bertrand, 1969; M. sylvana: Deag, 1974), langurs (P. entellus: Jay, 1965a; Vogel, 1973; P. johnii: Poirier, 1970a), mangabeys (Quris, 1973, and pers. obs.), and the patas ("whoo-wherr growl" of the male: Hall, 1968b).

In various Cercopithecus spp. with a cohesion grunt of the vervet type, an obvious gradation also exists toward the aggressive calls. In certain species (e.g., C. cephus and to a small extent C. nictitans, pers. obs.), these two signals are very close and cannot be distinguished easily without the postural behaviors that acompany them. C. neglectus, curiously enough, which uses no grunt-type call during progression, has an aggressive grunt close to that of C. cephus and nictitans (pers. obs.) (Fig. 19).

When the threat intensifies, the call structure becomes diversified. The calls remain low-pitched but their temporal parameters are modified, probably in proportion to the movements associated with the behavior and with physiological components such as respiratory rhythm. Roars and barks can be distinguished, as well as calls of intermediate structure emitted rhythmically, the last being the commonest in many species. The roars derive from grunts, and Hall and DeVore (1965) term them "loud two-phase grunting" in the baboons. Grunts increase in duration and intensity in guenons also, and such roarings are present in most macaques.

The barks are also generally widespread in the macaques (M irus: Goustard, 1963; M mulatta; M. fuscata; M. nemestrina; M. speciosa ), the baboons ("two-phase barks"), the mangabeys, the langurs ("barking" and "coughing"), the patas, and the guenons. We have seen that different types of loud barking can occur in intergroup relations (cf. type 2 loud calls, Fig. 1) and in alarm situations. Roars and barks are emitted more frequently than grunts by adult males.

Still commoner are the low-pitched rhythmic calls associated with threat, such as the "pant threats" of M. mulatta and M. speciosa, the "chutters" of M. fuscata, the "intention notes" or "staccato growls" of M. nemestrina, and the discontinuous barking of M. irus. The repetition of the "huh-huh sounds" in the patas and the "two-phase uh-uh" in the baboons is another example of the rhythmic emission form. This is also the case in the mangabeys, the langurs, the talapoin, and the guenons ("chutters" of the vervet: Struhsaker, 1967b). Some nonvocal sounds accompany threat behavior: tree shaking, canine grinding (langurs, mangabeys), gnashing (rhesus), or tongue clicking (Colobusguereza), and can for the most part occur in intergroup conflicts as well as in other situations (see below).

Fig. 19. Spectrographic analyses of threat and cohesion calls in Cercopithecus nictitans and C. neglectus. Threat gruntings of the two species (1, 3) and the cohesion grunting of C. nictitans (2) have close structures, characterized by a rolled sonority, quite visible on the amplitude modulation spectra (a, b, c). The cohesion call of C. neglectus (4, d) does not have this characteristic.

Rhythmic calls constitute a link between aggression and flight vocalizations. In the latter there is a distinction between those occurring preferentially in response to alarm situations, emitted singly or in chorus (see above), and those occurring more specifically in interin-dividual agonistic relations. At the start of agonistic encounters, adult females and immature subordinates often give noisy, more or less low-pitched, rhythmic vocalizations. This type of call is emitted by all the Cercopithecus and all the Cercocebus spp. we have studied (C. nictitans, cephus, pogonias, neglectus, ascanius, mona, and Ce. albigena, galeritus, and torquatus). In most of them these vocalizations derive maturationally from the "gecker" of infants and juveniles; like the "yakking" of the Papio spp. (Hall and DeVore, 1965) derives from "chirplike clicking sounds." These calls are present in infants of almost all species; for example, the "gecker" of M mulatta and M. speciosa (Rowell and Hinde, 1962; Bertrand, 1969), the "long cry" of M. nemestrina (Grimm, 1967), or the type 5 call of the talapoin (Gautier, 1974). Their occurrence in agonistic relations in older animals has been noted as the "yak" ("harsh staccato barking": Hall et al., 1965) in the patas, as the B1 call in M. fuscata (Itani, 1963), and in the langurs ("subordinate segmented sound" of P. johnii: Poirier, 1970a).

Fig. 20. Spectrographic analyses of a series of calls exchanged between two young Cercopithecus nictitans females during a conflict. Calls 1-6: High-pitched vocalizations of a threatened animal. Calls 1, 2, 3, 5: high-pitched rhythmic calls; call 4: pure quavered whistling; call 6: pure, then noisy quavered whistling, Calls 7 and 7 bis: Low-pitched rhythmic vocalization of the menacing animal. Call 7: included in the sequence; call 7 bis: detailed analysis.

At a more advanced stage of agonistic relations, these rhythmic vocalizations become shriller and develop into calls of higher frequency. The rhythmic component may either disappear or persist, as in the "chutter squeal" of the vervet (Struhsaker, 1967b). The structure of these vocalizations is either pure ("whistle," "squeal") or somewhat rough ("screech," "scream") (Fig. 20). It would be useless to enumerate the species in which they are present, as they have been noted in practically all. Most authors agree that they are manifested preferentially by females and by the young. Furthermore, it seems difficult to relate their structural diversity as revealed by sonographic analysis to qualitatively different functions. It is generally believed that these vocalizations indicate a high arousal level and function as defensive signals, either in interindividual conflicts or in extra group situations (e.g., the presence of a predator). They possess, even more so than do aggressive signals, a great power to evoke reactions in congeners. Depending on the context, congeners may converge on the emission place and threaten the protagonists or potential predators. These phenomena play a very important role in the defense of infants. In the young, the set of defensive vocal reactions constitute responses to increasingly frustrating situations. Thus, for the infant talapoin (Gautier, 1974), these reactions begin with emissions of the gecker type when mother/young contact is slightly disturbed. If the break in contact is more substantial, the gecker yields to pure, type 6A whistlings (associated or not with type 3 lost calls). If, in the end, the situation becomes serious or if the young animal is threatened, the whistlings are replaced by type 7 screams. As far as species-specific variations are concerned, this chain of infant vocal reactions is common to many species of Old World monkeys.

Fig. 21. Rhythmic call of low pitch emitted by a female Cercocebus torquatus during copulation. The call is a succession of inhaled (atonal) and exhaled (tonal) units associated with cheek movements.

Certain nonvocal sounds express a state of ambivalence and high excitation. Their limited range of action and their association with particular facial expressions cause them to function also as visual signs. Thus the "teeth chattering face" of Macaca speciosa (Bertrand, 1969) may be silent or accompanied by "teeth clicking sounds." This kind of signal, like the widespread lip smacking, will be discussed under visual communication (see below). The fact that they indicate a high level of excitation is revealed by their association with homosexual and heterosexual mounting behavior and sexual behavior in general. They may or may not occur simultaneously with vocalizations related to aggressive calls.

In M. radiata (Sugiyama, 1971), a dominant male soliciting a mount will "grin" and "tongue click." This same sound, associated with "clonic jaw movements," is given by males soliciting copulation with females (Kaufman and Rosenblum, 1966). Males of M. fuscata (Green, 1975) engage in teeth chattering or lip smacking (Tokuda, 1961-62) with females soliciting "consortship." Their homosexual mounting is accompanied by lip smacking, teeth chattering, and vocalizations. In M. sylvana (Deag, 1974), teeth chattering accompanies mounting and precedes copulation in a male looking at a female in estrus. Teeth gnashing is manifested by M. mulatta and M. speciosa males during copulation. In the talapoin (Gautier, 1974), mounting between males is also accompanied by lip smacking and a complex vocalization (type 10) close to that emitted by two partners copulating.

In some species, it is the males that vocalize during copulation. In M mulatta (Southwick et al., 1965), the male utters a "high pitched staccato note"; in M. speciosa, a "vibrato scream" (Bertrand, 1969) or a "rhythmic expiration vocalization" (Chevalier-Skolnikoff, 1974). However, it is more generally the females that vocalize, whether before copulation, during the entire duration of thrusting, or at the end of the mount.

Among calls manifested by receptive females, one must distinguish between signals commonly used in interindividual encounters, the manifestation and structure of which indicate above all the status of the emitting individual (e.g., the gruntings or "soft squealing" of female langurs: Jay, 1965a), and those signals specific to encounters between the two sexes. Thus in the patas (Hall, 1965), M. fuscata ("estrus call": Tokuda, 1961-62), M. nemestrina or radiata (Kaufman and Rosenblum, 1966), M. sylvana (Deag, 1974), and Ce. galeritus, torquatus, and C. neglectus (pers. obs.), receptive females may emit particular calls which are indicative of their receptivity and which potentially play a role in the solicitation of copulation. The same type of call can occur in the course of copulation in all the species mentioned, as well as in other macaques (e.g., M. irus: Goustard, 1963) and in baboons (Hall and DeVore, 1965; Saayman, 1971). In M. radiata and nemestrina, as in the talapoin, both males and females can vocalize. Generally speaking, these calls are strictly linked with respiratory rhythm, and their length and intensity seem to depend on the females' state of excitation (Fig. 21).

If vocalizations preceding copulation play a role in sexual encounter, those appearing during mounting have a less obvious function. However, they draw congener attention to the coupling partners and can provoke harassment from other males or juveniles. In this sense they can contribute to the social regulation of reproduction in certain species.

Among the vocal repertoires of various spedes, vocalizations associated with agonistic behavior seem to be the least specific and the most graded. This is the case in woodland monkeys as well as those of open habitat. The relationship of call structures seems to depend on the context in which the calls occur: when the exchanges take place at close range and are continually sustained or relayed by visual signals, the needs of species specificity are reduced. The variability in calls and the possibility that threat calls may gradually change into those of subordination or flight are also the result of close-range exchanges and rapid reversals of the protagonist roles. Furthermore, elevation of the animal's excitation level is generally indicated in the call structure by an increase in frequency (Kiley, 1972; Gautier, 1974; Green, 1975).

Ontogenetic studies show that various shrill calls appear in frustration situations among infants and occur very early (from the first day of life in the talapoin and mangabeys, pers. obs.). On the other hand, low-pitched threat calls are not uttered until much later (generally at about one year).

VISUAL SIGNALS

Since human vision, like that of the monkeys, is excellent, it is not surprising that visual signals have been described many times and are of particular importance in general works dealing with communication in monkeys (see Andrew, 1963a, 1963b, 1964; Marler, 1965, 1968; Lancaster, 1968; Vine, 1970; Bertrand, 1971).

Despite the difficulty of comparing different studies, it is obvious that the numerous catalogues of visual signals compiled for various species reveal an astonishing similarity. Compare, for example, Altmann (1962) and Hinde and Rowell (1962) for M. mulatta, and Struhsaker (1967a) for C. aethiops. It is quite difficult on this basis to bring out specific differences. Thus any primatologist beginning work on a new species is almost sure to find the quasi-totality of facial displays described in the classic works of Van Hooff (1962; 1967).

In his synthetic essay, Bernstein (1970a) stresses the great fundamental relationship of visual signals in the Cercopithecoidea and tries, with justified precautions, to separate signals that would be "species-specific." Quite often one discovers that the designation "species-specific" is the result of anatomical peculiarities modifying or enriching the appearance of a facial display, or of the rarity of the signal's occurrence, or simply of the lack of studies of certain species.

This resemblance, which goes beyond the order of primates (Bolwig, 1962; Andrew, 1972), should not be surprising since the anatomical bases are relatively comparable in different species and since a considerable part of mammalian facial display and posturing appears to have originated from defense and protection behaviors (Andrew, 1963b). At the functional level, furthermore, this non-species-specificity is easily explained. In visual communication, by definition, animals see each other and are closely spaced. Therefore there is little or no problem of species recognition. This implies a second characteristic: at close range, visual signals can be modulated and extremely refined without the risk that the received message will be incomplete or poorly interpreted (Marier, 1965; Lancaster, 1968).

Starting from a common basis, differentiation is nevertheless carried out through anatomical specializations, e.g., presence of a more or less long and supple tail; more or less striking colorations in facial masking or the ano genital regions; presence or absence of cyclical intumescence of the sexual skin; differences in facial hair covering, development of manes, cranial toupets, or side-whiskers; accentuation of facial wrinkles. Forest monkeys generally possess either brillantly colored faces (Cercopithecus, mandrills), or highly contrasting colors (Co.guereza). In Cercopithecus, these colorations are coupled with well-developed facial hair, which is reduced only around the eyes and the mouth. The rigidity and contrast of these "clownlike" masks do not permit subtle modifications of expression, but do assure immediate species recognition in closed habitats and doubtlessly play a role in reproductive isolation, especially in the numerous species living in association (Gautier-Hion and Gautier, 1974). Among woodland monkeys there are some notable exceptions in coloration: the talapoin, the crested mangabey, and the olive colobus, all of which live near water, are of a rather uniform greenish gray. The mangabeys, macaques, and baboons have the least facial hair. Whereas the often sombre faces of the mangabeys and colobus tend to "obscure" expressions, the dull and often pale faces of monkeys from open habitats permit subtle variations in expression.

Whatever the similarity in basic facial display and posturing of the Old World monkeys, it is clear that the visual communication within a group of forest guenons is fundamentally different from that manifested by a group of baboons. The difference lies partly in the variability and subtlety of the signals displayed (looks, facial expressions, gestures) and partly in the intensity and frequency of exchanges. Even though it may be possible to describe the subtlety of an almost imperceptible eyelid movement, no one seems to have tried to analyze the elements of the look (form, surface, and brilliance of the eye, or dilation of the pupil), which Chance (1967) in Vine (1970) justifiably thinks may constitute "the major stabilizing influence in primate groups." Although a priori it may seem easier to measure the occurrence frequency of behavior patterns, some methodological problems arise. In order to compare baboon communication with that of de Brazza's monkey, should one choose a group in each species of identical size and composition or rely on the fact that the one lives in groups of several tens of individuals while the other lives in social units of from three to six? This choice presupposes two different procedures as far as the causality of the modes of social organization is concerned: in the one, it is hypothesized that the means of communication of a species are directly responsible for its "sociability"; in the other, it is supposed that life in large groups develops and reinforces the probability and nature of exchanges.

In the group, a lot of visual signals act at medium range. This is the case with those that operate passively and are linked to individual morphology and anatomy. In the guenons, the bearing and color of the tail, like the facial coloring, are thus the first indices of species recognition in a woodland habitat. Similarly, all visible signals associated with age and sex can be communicated at a distance. Thus, the ease of recognizing an adult male varies directly with the difference in size between the sexes.

The passive aspect of signals linked to species-specific and individual conformity is enriched by the animals' status or self-confidence. Several types of gait have been described. The confident animal moves in a relaxed manner, with straight back, legs, and arms (e.g., "confident walk" of the vervet: Struhsaker, 1967a; "strutting gait" of the langur: Poirier, 1970a), whereas the subordinate has a hunched back, slightly bent legs and arms, and a low or curved tail. A jumping gait is characteristic of animals at play. Upon stopping, a confident individual will sit down with outstretched legs; a male will spread his legs and exhibit his penis. An individual that is often threatened will hunch its back, hold its head to the side, and gaze all around.

In most species, the one or more dominant males give particular emphasis to their posturing behavior. They sit down with ostentation, and when they stop in a quadrupedal position their legs and arms are stretched out. In woodland monkeys the tail is pulled up over the back in a conspicuous manner. If, as in certain species, the tail is needed for balance, it assumes a signal value in various specific stopping postures: the tail of Ce. galeritus touches its head (Fig. 11); that of Ce. albigena is brought up vertically, the tip curved toward the back; and that of C. cephus forms a backwards question mark. The tail-on-head stopping posture of Ce. galeritus is so frequent that Quris (pers. comm.) thinks that it replaces the function of color markings of Cercopithecus in species recognition.

In monkeys of open habitats, the tail also plays a role in social signaling, even in species with reduced tails, like the stumptail, for which Bertrand (1969) recognizes several positions. "Tail up" is an assertion of dominance, "tail curled up" characterizes a high degree of excitation, whereas "tail curled down" indicates a startled animal. Bertrand remarks that the erected tail is generally manifested by excited and confident animals, whereas the curved tail (like the lowered tail in the dog) is characteristic of threatened individuals. However, in baboons (Hall and DeVore, 1965) and in M. fascicularis (Angst, 1974), the "tail erect" characterizes subordinate animals. Some attitudes or gaits may have in addition more differentiated roles; e.g., the "swinging gait" of the male hamadryas preceding troop departure (Kummer, 1968) or the "drunken gait" of young Cercopithecus and the talapoin, which serves as an invitation to play (Gautier-Hion, 1971b).

Visual signals acting at short range between individuals, bringing them together or separating them, are quite varied (see Marler, 1968). Some are neatly classified in one or the other category, indicating either a friendly or an agonistic tendency; others have more ambivalent significations. The change from the former to the latter depends on the individuals' self-confidence and the variations in excitation level in relation to approach-flight behaviors.

Signals Associated with Peaceful Interindividual Relations

These signals often precede or occur during tactile and olfactory close-range exchanges (mounting, smelling, grooming; see below). The most frequent are lip smacking and teeth chattering, postures of presentation and of invitation to grooming and play, and the facial displays and gestures preceding sexual encounters. These signals are frequently combined; lip smacking and grimacing may be associated with presentation and various tactile exchanges, and they can occur together in peaceful, agonistic, or sexual contexts.

Lip smacking is known in the various baboons, the gelada, the macaques, the African and Asian colobus, the mangabeys, the patas, the guenons, and the talapoin and had been described by van Hooff (1962, 1967) in most of these species before it was observed in natural groups. He describes the different forms that it can assume and distinguishes functional lip smacking, associated in grooming with the ingestion of skin flakes and originating from suckling movements (Anthoney, 1968), from "vacuum lip smacking," in which this lip-tongue movement is not followed by any ingestion. Lip movement and tongue protrusion may vary according to the species, the latter being particularly evident in the langurs (Jay, 1965a) and the gelada (von Spivak, 1971).

Lip smacking is sometimes associated with staring and raising of the eyelids and eyebrows, as in threat. A relationship with threat behavior is particularly obvious when the behavior is intense, as in Ce. albigena, for example, where the upper lip may reveal the teeth and the animal shakes its head vigorously from side to side.

Lip smacking appears during or as a prelude to grooming. Acting as an invitation, it is used especially by individuals whose relations are "strained." It also precedes other types of approach and may be used by a dominated animal as well as by a dominant one. Used by a receptive female going toward the male, it may be followed by copulation; it may precede grooming or sitting in proximity and, in agonistic behavior, it is often associated with presentation in the threatened animal. Dominant males may also lip smack or teeth chatter while approaching subordinate females who are soliciting copulation (e.g., Chacma baboon: Bolwig, 1959; the hamadryas: von Spivak, 1971; the white collared mangabey: pers. obs.; and the Japanese macaque: Green, 1975). Similarly, a dominant female approaching a mother lip smacks before touching the infant. The Barbary macaque also engages in lip smacking and teeth chattering before sniffing an infant and taking it from its mother (Lahiri and South-wick, 1966). In the gelada, the female induces a juvenile to hang from her back by touching it and addressing it with lip smacking.

This behavioral pattern seems therefore to be a positive social signal (see van Hooff, 1962, 1967; Hinde and Rowell, 1962) that may either appease the aggressive behavior of a dominant animal or diminish the flight reaction of a subordinate, thus permitting the fulfillment of subsequent behavior. Its meaning is nevertheless sometimes ambiguous, notably in Cercocebus or Cercopithecus, in which it is often associated with threats. This aspect is especially frequent in agonistic exchanges between a pair of animals of adjacent or poorly established status. The two individuals address each other with head bobbing and lip smacking. In Ce. albigena, intense lip smacking ("snarl-smacking face" of van Hooff, 1967), associated with threats and head shaking, appears to indicate a state of uncertainty in the animal. Hall et al. (1965) also attributes elements of threat and fear to the "gnashing of the teeth" of the patas.

In some species lip smacking appears only in social grooming (as in the mandrills: van Hooff, 1967), but it plays an important social role in interindividual encounter in baboons, macaques, and mangabeys, notably between animals who are poorly acquainted or who have unstable dominance relations. Although present in Cercopithecus (as well as in the patas) during grooming and agonistic manifestations, lip smacking has rarely been observed as a preliminary to encounters between two individuals or as a friendly solicitation.

Most species have several postures of invitation to grooming, indicating a desire either to groom or, more often, to be groomed. Individuals will present preferentially the chest, the back, or the genitals. The ritualization of these postures generally becomes more obvious in direct proportion to the animals' lack of mutual familiarity and the degree to which dominance relations are strained. By contrast, this ritualization does not appear between mother and infant (Gautier-Hion, 1971b).

Genital presentation, which is often associated with lip smacking, occurs in both sexual and various other social contacts. From the qualitative point of view, "normal" presentation, with the animal erect on its paws, is distinguished from crouched presentation, with the individual on bent legs and with a curved back (Fig. 22). The latter is generally found in threatened or strongly dominated animals. It seems to be the rule in female patas and hamadryas (Hall, 1965; Kummer and Kurt, 1965).

"Copulatory" presentation preceding genital sniffing, mounting, or copulation by the male is frequent and obvious in the baboons, macaques, and mangabeys, and also exists in the Colobus spp. It is less distinct in the guenons, in which it does not receive the emphasis that it gets in the baboons. In forest monkeys, presentation is often made with the body arched and the tail curled on the side (C. neglectus) or in the form of a question mark (C. cephus, C. ascanius); the animal looks at its partner with a pout, which may be accompanied by a call.

Fig. 22. "Crouched" presentation in Colobus badius: a female carrying a newborn presents herself to an adult male (Gombe National Park; photo by T. H. Clutton-Brok.)

Nonsexual presentation, although indeed manifested by males, is essentially a female behavior (Hall, 1962). It can precede grooming, passing by or sitting down in the proximity of a congener, or handling of an infant held by its mother (Fig. 23). When displayed by a dominant animal, it indicates friendly intentions and seems to inhibit the flight reaction of the one being approached. Mutual presentations between males can thus be observed. Presentation is also frequent during agonistic behavior in which the pursued animal stops and exhibits its genitals. Most authors consider it as having a role in the cessation of aggressive manifestations, in progress or potential (Carpenter, 1942; Hall, 1962; Altmann, 1962; Poirier, 1970a). Chalmers (1968) has shown with a band of Ce. albigena in the wild that interindividual approaches accompanied by presentation significantly reduced the probability of aggressive behavior.

Fig. 23. A dominant female of a Cercocebus albigena group presents her genitals to a young infant held by its mother before entering in contact with the former. (Paimpont; photo by B. Deputte.)

As Carpenter (1942) noted, presentation is a "greeting gesture." In subordinate monkeys it is a gesture acknowledging the status of a congener, and in dominant animals it is a manifestation of momentary "friendly intentions." This seems obvious, the more so since the presenting animal is quite vulnerable. Hall (1962) stresses that this pattern has a role in status recognition among males in baboon groups, in which the dominant individuals are those to which the most presentations are addressed. In forest guenons presentation rarely occurs as an invitation to interindividual encounters, except occasionally during play or as a prelude to mounting in young males. It is also observed in young males toward an adult male (C. nictitans, C. cephus, C. pogonias, pers. obs.) and can be associated with pouting (which is found in receptive females) and/or trilled calls (Fig. 24).

The grimace can also precede certain peaceful encounters and assume a meaning rather close to lip smacking, with which it can be associated in the same sequence. It appears sometimes in threatened animals (see below) and sometimes in dominant individuals; thus a male gelada going toward a female exhibits a grimace with the upper lip raised, to which he may add lip smacking (von Spivak, 1971) (Fig. 25). Altmann (1962) points out a similar behavior in rhesus males.

Fig. 24. "Arched" presentation, associated with pouting in a young male Cercopithecus pogonias. Note the position of the left rear paw. (Paimpont.)

Various facial expressions, which may or may not be specific variations of the grimace, have been described. A notable case is the mandrill's "eight-smile face," which is associated, like the snarl-smacking face of Ce. albigena, with head shaking. Sometimes considered to be a friendly mode of approach (Bernstein, 1970a), this smile may be an ambivalent approach-flight manifestation, similar to the behavior of Ce. albigena. Note also the "high grin face" of Cynopithecus niger (Bernstein, 1970a), which may correspond to a species-specific exacerbation of the grimace.

Fig. 25. An adult male Theropithecusgelada curls his upper lip during a peaceful contact.(Photo by H. Spivak.)

Head wagging is also present in forest Cercopithecus like C. nictitans or C. cephus and appears in ambivalent situations. In C. neglectus it is associated with closed-mouth chewing movements.

Lip smacking, presentation, various grimaces, and head wagging are all displays indicating social tendencies in which elements of threat are rare or absent. They are followed by an absence of partner reaction or by a reduction of interindividual distance and an increase in the probability of short-range exchanges. Displayed at medium or close range, they are often a prelude to tactile and olfactory exchanges in which the animals, being mutually vulnerable, need previous assurances of the peaceful intentions of the partner. Like the majority of close-range signals, whether vocal, visual, or tactile, these behavioral patterns are increasingly ritualized in direct proportion to the degree to which partner relations are unstable or strained. This may be one of the reasons why lip smacking and grimaces appear to have ambivalent meanings in which approach-flight tendencies are closely associated.

It is notable that visual exchanges that indicate the mood of the partner are essentially present in guenons in their original function (lip smacking and grooming; presentation and copulation), but rarely occur outside of these functional contexts, as though they had not acquired any ritualized social function in these species. The infrequency of these signals parallels the underdevelopment of "personalized"-contact vocal signals. Rowell (1971) justly thinks that this "lack of appeasement and policing are probably the fundamental differences between the behavior of guenons and the baboon-mangabey-macaque genera."

In various species, sexual encounter is accompanied by differentiated visual exchanges. The grimace may appear during copulation or mounting between males. It can be associated with lip smacking or teeth chattering (P. ursinus, P. anubis: Hall, 1962; Hall and Devore, 1965; Saayman, 1970; M. mulatta: Southwick et al., 1965; Lindburgh, 1971; M. fuscata: Itani, 1963; M fascicularis: Angst, 1974; M sinica: C. M. Hladik, pers. comm.; M. talapoin, Ce. albigena, Ce. galeritus: Gautier-Hion, 1971b and pers. obs.). These facial displays, which may be associated with calls (see above), indicate the individual excitation level: the visual signal does not seem very communicative since the partners do not usually perceive it (Fig. 26).

The facial displays and gestures that precede copulation are of a more obvious function, seeming to facilitate sexual encounter. Pouting with protruding lips appears quite frequently in receptive females. This pouting with or without calls exists in M. fuscata (Itani, 1963), P. ursinus (Hall, 1962; Saayman, 1970), Ce. torquatus, Ce. galeritus, Ce. albigena, C. nictitans, C. cephus, C. pogonias (pers. obs.). In the patas, Hall (1965) describes a similar facial display with protruding jaws and swollen cheeks, accompanied by wheezing and chortling sounds. An apparently identical behavior has been observed in C. neglectus (pers. obs.). Finally, the well-known "jaw thrust" (Kaufmann and Rosenblum, 1966) of M. nemestrina and M. radiata seems to be an exacerbation of this same pattern. In M. nemestrina, this display is frequent, especially in males, and appears in varied contexts. In this species, as in the bonnet macaque, the male accompanies it with a lateral head shaking reminiscent of a male Ce. albigena inviting a receptive female to approach.

In Cercopithecus, the receptive female combines this pout with an "arched" presentation, so that the face and posterior are simultaneously directed toward the partner. The same pout, with or without calls, occurs in most species during copulation (Fig. 27).

Finally, there is the play face ("relaxed open mouth face" of van Hooff, 1967), which appears either as an invitation from a distance or during the acting out of the behavior. Andrew (1963a) has commented on its relationship to aggressive faces. As in the latter, the teeth are uncovered but there is an obvious difference in the eyes, which are often "slitted" or partially closed (Fig.28).

Signals Associated with Agonistic Interindividual Relations

A particularly large number of visual exchanges occur in agonistic behaviors, for which they constitute the essential basis of signalization, enriched by a great number of graded vocalizations (see above). The descriptions of these offensive or defensive signals have been attempted (see van Hooff, 1962, 1967; Hinde and Rowell, 1962), but remain unsatisfactory. The problem is that it is necessary to classify the signals into separate patterns, which do not take account of their extreme variability or the behavioral dynamics. In this respect, the methods suggested by Altmann (1965) should permit great progress in understanding behavioral sequence chains.

Fig. 26. Grimace during copulation in Macaca sinica. (Ceylon; photo by C. M. Hladick.)

Fig. 27.Pout associated with inhaled-exhaled call during copulation in an adult female Cercocebus albigena. (Paimpont; photo by A. R. Devez, CNRS.)

Many parts of the body are activated either simultaneously or separately in signals linked with aggression-flight: eyes, eyelids, eyebrows, scalp, ears, lips, tail, legs and arms. Because of this fact, the same open-mouth face, with teeth exhibited, may have different meanings depending on whether the animal's ears are erect or lying down, whether the animal is leaning forward or apparently recoiling, whether its posture is straight or crouched, or whether its tail points up or is bent down.

Fig. 28. "Play face" in a young female Cercopithecus nictitans. (Paimpont.)

An animal engaged in an agonistic action is rarely completely confident. If it is, there is no real agonistic exchange but rather a defined and stable dominance relation in which a simple glance is sufficient to "repress" a partner. In a real agonistic exchange, on the contrary, each animal must at every instant take into account the slightest behavioral variations of the other. Therefore, no matter what species is under consideration, it appears that signals associated with aggression-flight generally include the most graded ones of the species repertoires, dealing as much with vocalizations (see above) as with visual exchanges.

Several general traits can nevertheless be shown: The look can be fixed and intense. The emitting animal stares directly at its partner, its eyes only slightly widened, with the eyelids barely raised and the upper lip perhaps pouting slightly (e.g., M. mulatta: Hinde and Rowell, 1962; and C. nictitans, Fig. 29). This type of look is characteristic of a threatening monkey. An animal never stares at a partner in peaceful group exchanges, which are made with simple glances or vague looks (except lip smacking). On the other hand, an animal that has been stared at or threatened turns away and deliberately looks in the opposite direction from the partner. This looking away can indicate both submission or an attempt at nonparticipation. It can be observed in a dominant animal in response to a fearful glance from a dominated monkey, in which case it indicates nonaggression.

Fig. 29. "Stare" associated with a slight pout in a male sub-adult Cercopithecus nictitans. (Paimpont; photo by A. R. Devez, CNRS.)

Between these two types, numerous other looks are manifested. Altmann (1962) and Bertrand (1969) mention the fearful look characteristic of a potentially threatened animal. In Ce. albigena a female in estrus assumes this fearful look while glancing at the dominant male if another male follows her with his eyes (pers. obs.). Bertrand also notes a look of feigned indifference when a dominated individual pretends not to see the threat or stare of the male, and a look of feigned interest when the threatened monkey intensely busies itself with tail grooming or a random object. These subtle looks can evidently be expressed by all monkeys and appear to be capable of reducing congener aggression.

The stare is intensified by a number of gradual facial movements: raising the eyelids, which is particularly obvious and repeatable in fairly rapid succession in the macaques, baboons, and mangabeys; raising the eyebrows, which reveals the supra-oculary region with perhaps colored eyelids, often of a striking white ( Th. gelada: von Spivak, 1971; M. fascicularis: Angst, 1974; and Fig. 30: Ce. torquatus)', retraction of the scalp, which reinforces the disclosure of the eyelids; and pulling the ears back, which accentuates the stretching of the face.

All these elements are particularly clear in monkeys of an open habitat, as well as in the mangabeys and the talapoin. In the Cercopithecus spp., however, movement of the ears is hidden by the abundant hair surrounding them, and so are raising of the eyelids and retracting of the scalp. These actions are perceptible in C. cephus and C. pogonias and to a slight degree in C. nictitans, but are almost nonexistent in de Brazza's monkeys. On the other hand, in various mangabeys and baboons, scalp movements are accentuated by the presence of toupets or side whiskers that can be turned down or flaunted.

Fig. 30. "Stare," exhibition of white eyelids, "open mouth threat face," associated with grunting, and hair erection in a young male Macaca fascicularis during a chase. (Photo by W. Angst, 1974, in Fortschritte der Verhaltensforschung.)

Various mouth expressions have been described by van Hooff (1962, 1967), who compares their appearance in the different species. The staring open mouth face, or open mouth threat face, appears very generally. It is associated with the stare; the stretching of the eyelids, scalp, and ears toward the back; and a more or less open mouth, frequently in an "O" shape, is particularly obvious in the macaques, but it is just as obvious in a Cercopithecus like C. cephus, for example. In C. diana (van Hooff, 1967), the patas (Hall et al., 1965), and C. neglectus (pers. obs.), the open mouth face appears repeatedly, the mouth opening widely without the teeth being exposed. Poirier (1970a) also notes "air biting" in the langurs, which seems comparable. Sudden openings and closings of the mouth have also been pointed out in the gelada (von Spivak, 1971).

The open mouth threat face appears in most species as an expression of threat, although Struhsaker (1967a), who terms it "gaping," attributes to it a sense of defensive threat, and Deag (pers. comm.) points out that it is rarely followed by attack in the barbary macaque. This face is frequently associated with a lowering of the head (baboons, macaques) or "head bob" (P. hamadryas, macaques, langurs, mangabeys, guenons). In the forest guenons, head bob and forearm jerking, which are both associated with the stare, are so rigid and jerky that the animals look like jacks in the box. Thus the name "ho-cheur," given in French to C. nictitans, could as well be applied to C. cephus.

During a threat, animals can jump in place (baboons, guenons), slap the ground, strike in the direction of a partner (baboons, macaques, langurs, mangabeys, patas, guenons), make sudden forward movements (macaques, patas, guenons). These threats are sometimes followed by real pursuits, with grasping of the scalp and biting, or false pursuits, where the partner is never caught (see Kummer, 1957; Kummer and Kurt, 1965; Bertrand, 1969).

Hair erection appears during agonistic behavior in several baboons (notably in hamadryas, gelada), in M. speciosa, M. fascicularis (Fig. 30), Ce. galeritus, and C. neglectus. It indicates an "emotional" activation of the autonomous system and does not seem to be connected with approach any more than with flight. In the stumptail, Bertrand (1969) considers it to be a "mixture of aggression and fear."

In many species a "bared-teeth threat face" (van HoofF, 1962) associated with the stare prolongs the "O"-shaped mouth (Fig. 31). It can be considered offensive or defensive. In the talapoin, it is the usual threat face. When associated with scalp and ear retraction, it is often followed by attack. It becomes defensive when the scalp and ears come forward (Gautier-Hion, 1971b).

One or more facial displays derived from the grimace are generally manifested by threatened animals. The lips are more or less turned up, revealing the clenched teeth (macaques, baboons, langurs, mangabeys, guenons, patas). These grimaces are either silent or associated with many geckers, screams, and screeches, which, as we have seen, are common to a number of different species. The lifting of the lip is particularly obvious in the gelada (von Spivak, 1971 ; Fedigan, 1972), where the lip can be rolled completely back. This rolling up is also observed in a threat. It is not very apparent in guenons, and especially rare in infants, whose facial displays associated with geckers or screams are mostly characterized by enlargement of the eyes and lifting of the eyelids (Fig. 32).

Fig. 31. "Bared teeth threat face" in an adult male Cercopithecus neglectus. (Paimpont: photo by A. R. Devez, CNRS.)

A threatened animal may also respond by directing a threat face to a third animal. These redirected threats, particularly well described in the hamadryas (Kummer and Kurt, 1965) but also present in many species (e.g., gelada: von Spivak, 1971; mangabeys: pers. obs.; guenons: Gautier-Hion, 1971b; Rowell, 1971), seem particularly frequent in captivity. Under these conditions, chain reactions can involve the entire group of animals (see Rowell, 1971).

Fig. 32. Facial display associated with a "scream" in an infant Cercopithecus nictitans. (Paimpont.)

Special mention should be made of yawning, which so many authors have noted in so many species: the baboons (Bolwig, 1959; Hall and DeVore, 1965; Hall, 1968a; Kummer, 1968; Stoltz et al., 1970), gelada (von Spivak, 1971; Fedigan, 1972), macaques (Hinde and Rowell, 1962; Simonds, 1965; Kaufman and Rosenblum, 1966; Bertrand, 1969; Angst, 1973, 1974), langurs (Poirier, 1970a), Cercocebus spp. (Chalmers, 1968; Bernstein, 1970a; Quris, 1973), Cercopithecus spp. (Gautier, 1971 and pers. obs.), talapoin (Gautier-Hion, 1971b; Wolfheim and Rowell, 1972). In Papio anubis and ursinus, as well as in Ce. albigena (Chalmers, 1968), yawning is considered a threat display. Most authors, however, observing that yawning is often undirected and can even be done with closed eyes, think that it has no more than very low communicative value and constitutes rather an individual expression of an animal, hence its name: "tension yawning" (Fig. 33).

Fig. 33. Nondirected "tension yawning" in a male Macaca fascicularis. (Photo by W. Angst.)

Studies in progress in the cause and function of this behavior on two captive groups of Ce. albigena (Deputte, pers. comm.) show that yawning is quite generally evoked in males by situations exterior to group life, coming either from exchanges between two groups (see also Angst, 1973) or disturbed situations (potential or real predator). They also show that yawning by males elicits no response within the group, even though it may evoke a kind of outbidding between males of the same group when associated with shaking in ritualized sequences, or more rarely between males of neighboring groups. Rather than a threat, so-called tension yawning appears to be a display that expresses status among males.

These generalities about visual signals occurring in agonistic contexts show the close relationship between basic signals in different species. There are, however, profound differences in sequence chains. A Cercopithecus making a threat, stares, opens its mouth in a figure "O," violently wags its head, and jumps up and down on its hind legs. These different elements are repeated in turn, intensely and rigidly, without any gradual blending from one to the other. Under the same conditions and beginning with the same basic elements, a Ce. galeritus will modulate and refine these various patterns. It does not sustain the stare, but raises its eyelids, relaxes its eyes, threatens with open mouth, then makes a defensive face, approaches its partner while lip smacking, and then stops with tail erect before making a false pursuit.

Schematically, one could say that a Cercopithecus attacks or is attacked; a baboon, macaque, or mangabey has more subtle individual relations, which take into account the slightest changes in partner attitude, associated with both threat and appeasement behavior, and they sometimes exaggerate various reactions to the extent of a bluff. A female Cercopithecus pursued by a male flees, lies down, and grimaces and screams when the male reaches her. A female mangabey multiplies defensive expressions, which are mixed with lip smacking and presentations and combined with excessively violent screams, the intensity of which appears to bear little relation to the potential threat. This emphasis is absent in guenons, where aggressive manifestations are rare and of short duration anyway.

In baboons, macaques, and mangabeys, regulation of intragroup relations by visual mechanisms is ceaseless and subtle, linked with frequent looks that yield continuous information on the activity of neighbors. In woodland guenons, the lack of facial expressiveness and the passivity of exchanges causes reactions to be less predictable and subtle, and less susceptible to modulation. These features incontestably indicate a less-developed socialization, correlating with a lesser degree of exchange ritualization. In species with more open habitats, many signals have developed increasing ritualization, liberating them from their original functional context in order to give them an increasingly social significance.

OLFACTORY AND TACTILE SIGNALS

Olfactory communication in Old World monkeys has received relatively little attention, in part because of the relative absence of specialized skin glands in these species and in part because olfactory signals do not appear to be an indispensable means of communication in animals with vision as highly developed as that of the monkeys. This excellent vision has warped human observation; thus all primatologists dealing with genital presentation posture treat it as an essentially visual signal because that is what the observer effectively perceives (see Bertrand, 1971). Nevertheless, Michael and Keverne (1970) have shown in the rhesus, that although the sexual skin of a female is sufficient to attract the attention of a male, it is still ineffective in activating his sexual behavior.

As Moynihan (1967) points out for New World monkeys, the importance of olfactory communication is doubtless greater than the studies would suggest. In these monkeys, as in those of the Old World, any object or individual that is new or has returned after an absence is first sniffed or touched and then intensively sniffed by its congeners. Visual recognition of the new arrival seems to be only a quick means of orienting exploration, which is subsequently made precise and refined by olfaction.

Sniffings are directed to various parts of the body: genitals, abdomen, snout, armpit, or fur. They occur in relatively stereotyped postures, which often imply tactile exchanges probably resulting from the olfactory capacities of the individuals, which do not operate at a distance, as is the case for other mammals. Most observers have therefore retained only the tactile signal. Thus Marler (1965), going back to the list of behavioral features that appear when a stranger congener is introduced into a baboon group (Hall, 1962), emphasizes the wealth of tactile stimuli provoked by the introduction: genital stomach nuzzling, rump nuzzling, back-fur nuzzling, and mouth-head kissing are considered principally contact exchanges.

At present, no experimental proof permits us to assign a particular role to olfaction in these activities, but the fact that they are all accomplished with the nose and directed preferentially to specific parts of the body suggests that the olfactory element plays some role. Thus, we will deal with tactile and olfactory signals simultaneously when behavioral patterns appear to imply both types of signal.

Olfactory or Olfactory and Tactile Signals

Fig. 34. A young male Macaca fascicularis inspects the genitals of a female in presentation. (Photo by W. Angst, 1974, in Fortschritte der Verhaltensforschung.)

Sniffing of genitals is without doubt the most widespread of these signals. It occurs primarily in sexual encounters, provoked either by female presentation (Fig. 34) or by the initiative of a male forcing a female to stand up (M radiata: Nadler and Rosenblum, 1973; Cercopithecus spp.: Booth, 1962; M talapoin: Scruton and Herbert,1970; Gautier-Hion, 1971b; Ce. albigena: pers. obs.). It can also occur temporarily as a check on the sexual state of the female. Thus in M. radiata (Simonds, 1965) or M. sinica (Jay, 1965b) during the course of the day, in a veritable patrol, the males sniff the genitals of all the females in the group.

Sniffing is carried out directly or by means of sniffing a finger that has touched the vaginal orifice. These sniffings are rather infrequent in the guenons, but occur very often in mangabeys and certain macaques (Chalmers, 1973) and are also present in the baboons (Hall and DeVore, 1965) and gelada (von Spivak, 1971). They are rare in langurs, and Poirier (1970a) only observed four in P. johnii during 1,250 hours of observation.

Michael and Keverne (1968) have demonstrated the existence of a pheromone of vaginal origin ("short-chain aliphatic acids": Michael et al., 1971) that acts on the sexual activity of male rhesus through the olfactory pathway. It is probable that similar mechanisms are present in other species and that the function of genital sniffing is to collect information about the state of the females' cycles.

In several species genital sniffing is mutual and assumes a stereotyped form. In C. mitis (Rowell, 1971), C. nictitans, C. pogonias, C. cephus (pers. obs.), a male and a female face in opposite directions and circle while sniffing each other's genitals. In the mangabeys, a number of postures imply mutual sniffing. Bernstein (1970a) describes the side-to-side posture in Ce. atys, where the two congeners mutually sniff their ano-genital parts, with arms and legs passed over the back of the congener. A similar posture is present in Ce. albigena (Fig. 35, c, f), especially among females. Reciprocal ano-genital contacts predominantly between males have also been described in M. radiata (Kaufmann and Rosenblum, 1966).

Fig.35. Various sniffing postures in Cercocebus albigena (see text). (Paimpont.)

Further variations of these sniffings exist in Ce. albigena (pers. obs., Fig. 35, d, e); one individual may sit astride another or lie on it in reversed posture, putting its genitals on the nose of the other while it sniffs the congener's genitals. Fig. 36 shows a female carrying an infant while engaged in such behavior with another female.

Sniffings with or without manipulation of the ano-genital parts is also very widespread with respect to newborns, especially during their first months (baboons: DeVore, 1963; Hall and DeVore, 1965; langurs: Jay, 1963, 1965b; M. radiata: Rosenblum and Kaufman, 1967; M. speciosa: Bertrand, 1969; Cynopithecus niger: Poirier,1970b; M. talapoin: Gautier-Hion, 1971b; M. sylvana: Deag and Crook, 1971; C. aethiops: Struhsaker, 1967a; Ce. albigena, Ce. tor qua tus, C. ascanius: pers. obs.).

In Ce. albigena, M. talapoin, and M. speciosa, the mother and the other females frequently examine an infant's genitals. They lift the juvenile's tail and visually, tactilely, and/or olfactorily inspect its genitals. The role of olfaction is very clear when a mother turns her infant upside down, putting its genitals next to her nose (Fig. 37).

In M. radiata, these examinations are reserved to male infants. In C. aethiops, only females participate in them, whereas in the stumptail, the mangabeys, and the talapoin, sniffings attract the attention of the entire group.

Muzzle contact—an individual touching its nose to the muzzle of a congener—has been described in most species (e.g., "mouth-kissing" in P. ursinus: Hall, 1962; "mouth to mouth" in P. anubis: Hall and DeVore, 1965; "maul beriechen" in Th. gelada: von Spivak, 1971; "sniff at" in M mulatta: Altmann, 1962; "sniffing at face" in M. radiata: Simonds, 1965; "sniffs at" in P. hamadryas: Kummer, 1957, 1968; and Co. guereza: Horwich and Lafrance, 1972; "muzzle-muzzle" in E. patas: Hall, 1965; and C. aethiops: Struhsaker, 1967a; "museau-museau" in talapoin: Gautier-Hion, 1971b; "nose to mouth" in Cercopithecus albogularis: Rowell, 1971).

In the baboons, as in the mangabeys, this behavior is relatively rare and is often associated with alimentary behavior. In the Cercopithecus spp., on the other hand, muzzle-muzzle examination is frequent (Fig. 38), and Struhsaker (1967a) notes that in the vervet it can be associated with grooming, play, and penile displays, and can precede a sniffing of the perineum or a heterosexual mounting as well as follow intense agonistic encounters.

Fig. 36. Female Cercocebus albigena carrying an infant and engaged in reciprocal ano-genital sniffings with another female. (Paimpont; photo by A. R. Devez, CNRS.)

Fig. 37. Sniffing of a young male infant's genital organs by its mother, Cercocebus albigena. (Paimpont; photo by A. R. Devez, CNRS.)

Several other modes of sniffing occur. Sniffing of the ventral part of the abdomen exists in the baboons ("genital nuzzling" of P. ursinus: Hall, 1962), the vervet ("face in inguinal region": Struhsaker, 1967a), the gelada (where the partner examines the "abdominal beads": Bernstein, 1970a), and C. nictitans (pers. obs.).

Fig. 38. A juvenile male Cercopithecus nictitans comes to sniff the muzzle of an adult male. (Paimpont; photo by A. R. Devez, CNRS.)

Other sniffing, mouthing, or chewing, in which a partner's muzzle "digs" in the fur of a congener, occur either in the dorsal fur ("backfur nuzzling" of the chacma baboon: Hall, 1962; sniffing of the back in Colobus guereza: Horwich and Lafrance, 1972) or behind the head or on the side of the neck (M talapoin: Gautier-Hion, 1971b). Subsequently, they are included in mutual embracing behavior along with mouthing and chewing of the neck skin (cf. Fig. 35a).

Kissing is an equally widespread behavior that seems to be more tactile than olfactory. In Miopithecus and Cercopithecus spp., however, kissing often implies sniffing; in these species it appears to derive from the neck-sniffing behavior of a mother toward an infant huddling in her arms (Gautier-Hion, 1971b).

Kissing can be ventro-dorsal (e.g., baboons: Hall and DeVore, 1965; langurs: Jay, 1965b), but ventro-ventral kissing is more generally observed with the partners face to face, holding each other (various macaques, baboons, mangabeys, Cercopithecus spp., Erythrocebus, Miopithecus). It is especially frequent between adult males and can be accompanied by grinning, lip smacking, tongue-clicking (M. radiata, M. nemestrina, talapoin, etc.), or vocalizations (P. johnii, talapoin). In the gelada (von Spivak, 1971), it is accompanied by lifting of the upper lip. In various species, kissing is followed by mouthing, sniffing or chewing of the neck or sometimes the shoulder skin, but it never goes as far as real biting (langurs, macaques, talapoins, baboons).

It must be noted that the guenons possess a characteristic odor in the fold of the neck behind the head. Perhaps it is simply caused by an accumulation of sweat; it seems partially species-specific. In Ce. albigena, a particularly distinct odor of flour is released from the armpit, which is sniffed by females, one lifting her arm at the approach of another (Fig.35b).

Thus, although Old World monkeys are considered to make little use of olfaction, they have developed an important series of signals concerning regions that release particular odors, signals that set in play relatively stereotyped postures that are common throughout several species. It is clear that the distinction between the tactile and olfactory parts of a signal is more or less arbitrary for most of the behavior patterns we have described, and it is quite difficult to know which takes the lead at the level of message transmission.

The function of these olfactory and tactile exchanges is not always obvious. Nevertheless, most authors consider them to be ritualized greeting behavior, of which certain ones are clearly linked to dominance: in M. radiata (Simonds, 1965; Sugiyama, 1971) sniffing of the muzzle can occur between animals of equal rank, but is more often performed by a dominant animal on one of lower rank. In C. albogularis (Rowell, 1971), in 61 percent of all cases this sniffing is directed toward superior individuals in the hierarchy and principally toward adult males. It is the same in C. nictitans, where juvenile males come to sniff the muzzle of an adult male after it has emitted loud calls (pers. obs.). Similarly, Kummer (1968) considers it to be a gesture of "cautious approach" in P. hamadryas.

This sniffing of the muzzle may have originally been a way of exploring what a partner was eating, or more generally whatever it may have been doing (vocal emissions, for example). Hall (1962) rightly thinks that it serves in the acquisition of alimentary habits in young individuals. Depending on the species, it has acquired a more or less important ritualization. It is curious that in forest guenons it is the most frequently used pattern for interindividual encounters, whereas in the baboons, which have developed numerous signals for this purpose, the muzzle-muzzle seems to have maintained its "primitive" function.

Examination of the conditions under which these various olfactory and tactile exchanges occur yields complementary information about their role. These signals are generally activated by the presence of a new individual in the group (newborn or stranger), after any strong disturbance and especially after agonistic behaviors, or during encounters between adult males during a particular excitation and especially in the presence of females in estrus.

Thus, the birth of an infant provokes sniffing from part or all of the group for several weeks or months. This signal, considered by various authors to be a greeting, seems originally to have been a way to recognize and integrate a newcomer. Such signals yield indications about its sex and eventually about its personal odors. Individuals, but principally the mother, can with these sniffings, make an "olfactory identification card for the infant," the odor perhaps playing a role in reinforcing maternal ties. In the talapoins and mangabeys these sniffings are reactivated by any disturbance and are frequent after the child has been carried by another female. Horwich and Lafrance (1972) make the same remark for the back sniffings of the infant Colobus.

The introduction of a new individual into the group provokes a recrudescence of tactile and olfactory exchanges in the same way; this has also been clearly shown by Hall (1962) in the chacma baboon, where the stranger is sniffed; touched on the genitals, the back, and the muzzle; mounted; groomed; and kissed. Identical results were obtained upon introduction of new individuals into a group of talapoins (pers. obs.). Furthermore, an individual that has been temporarily separated from its group is treated in the same way, as though visual recognition were insufficient for its reintegration.

In a stable group, sniffing or kissing occurs during situations of high excitation. Thus male kissing takes place in the presence of females in estrus, after conflict, or when males unexpectedly run into each other. This behavior reduces social tension, making a sort of truce between two congeners. For Kaufman and Rosenblum (1966), kissing reflects a "temporary state of dominance equivalence." In the lutong, kissing occurs in periods of apparent distress. It sometimes becomes a collective behavior, with all the group members precipitating toward each other, kissing and giving piercing calls (Bernstein, 1968).

These exchanges therefore constitute ritualized gestures in a stable group. Originally, and under changing conditions, they probably retain a function in species and individual recognition among group members. Odor may play a role here in the creation and reinforcement of socialties.

The use of odors for individual recognition and integration of group members is a universal trait of insect societies (Wilson, 1968) and is also well known in a number of mammals (Mykytowycz, 1972). Perhaps primates retain primitive traits to varying degrees. It remains to be seen through experimentation at what point the ritualization of exchanges accompanies a decrease in the role played by olfaction.

The recent experiments of Kaplan and Rüssel (1974) with infant squirrel monkeys show that olfaction plays an important role in the motherinfant social attachment and seems to be more active than the visual information furnished by a surrogate. This seems to be an unexplored avenue in the understanding of primate societies.

Tactile Signals

Tactile exchanges are particularly numerous in a group of monkeys in active (e.g., grooming, kissing) or passive situations ("huddling together"). None of these exchanges should be underestimated for the understanding of social regulation because the fact that one individual accepts contact with a congener whereas another refuses it constitutes the key to the social organization of a group and the spatial distribution of its members. Unfortunately, not being able to understand the message received by an individual in contact with a congener, we are reduced to describing the differentiated behavioral patterns (Marler, 1965). In several tactile exchanges, these different patterns do not exist: two individuals simply sit down side by side or back to back. The best measure we have is to note the frequency and duration of these postures.

Marler (1965) distinguishes two broad categories of tactile stimuli on the basis of the behavior they induce: those that produce aggregative tendencies and those that provoke dispersive tendencies. Nevertheless, certain patterns can assume different significations according to the identity of the displaying monkey, and their classification is not simple. Thus the same push with the hand by an adult M. speciosa manifested in order to take the place of a congener and bringing on a distancing between individuals, is used by juveniles as an invitation to play, inducing a reduction in interindividual distance (Bertrand, 1969).

"Negative" tactile exchanges include all noxious signals that occur in agonistic behaviors. They range from hair grasping to slapping and biting and are often associated with visual threats or calls. These various elements are common to all species, but some of them have developed stereotyped behavior in which the gesture is preferentially directed toward a particular area of the body. Thus the male hamadryas "symbolically" bites his females at the base of the neck during his "herding" behavior (Kummer, 1959), whereas in aggressive behavior, female and juvenile vervets preferentially bite their partners' tails (Struhsaker, 1967a). Symbolic biting of the tail is also common in Ce. galeritus and Ce. albigena males. The latter, following olfactory control, may "bite" the sexual skin of a female (Fig. 39).

Fig. 39. An adult male Cercocebus albigena "bites" the sexual skin, after sniffing it, of a female in presentation. (Paimpont; photo by B. Deputte.)

"Neck-biting" or "chewing" is frequent in the baboons (Hall and DeVore, 1965), the bonnet macaque (Simonds, 1965; Sugiyama, 1971), the vervets (Struhsaker, 1967a), and the talapoins (Gautier-Hion, 1971b). It occurs mostly during kissing in the last three species.

Mounting behavior constitutes complex exchanges during which tactile signals occur, frequently associated with characteristic facial displays and vocal or nonvocal sounds. Thus, in various species, male mounting is accompanied by a "grin face" and the emission of complex phrases (e.g., P. ursinus: Hall, 1962; M. fuscata: Itani, 1963; M. talapoin: Gautier-Hion, 1971b; Gautier, 1974). Male mounting is observed especially in moments of tension, for example, in the presence of females in estrus (Hall and DeVore, 1965; Gautier-Hion, 1971b). Heterosexual mounting is the most frequent type (see Bernstein, 1970b); mounting between adult females is rare, but can be observed when one or both females are in heat (e.g., in talapoins and mangabeys: pers. obs.), and a mother will mount a female who presents herself (baboons: Hall and DeVore, 1965).

Mounting frequently occurs before or after grooming, in play, and during agonistic exchanges. It is generally considered an indication of dominance (see Bernstein, 1970b). In some species, its frequency is clearly correlated with group hierarchy, based on aggressive exchanges (e.g., P. anubis). In others the correlation is less obvious, and Simonds (1965) remarks that in M. radiata, inferior individuals can mount dominant ones and sometimes the latter force the former to do so.

Contacts bringing the hand into play are numerous (see negative contacts). "Touching" is described in P. johnii as a "mildly assertive gesture," but it also acts as a gesture of reassurance after a fight. Similarly, in M. radiata, "hand stretching" and 'gentle touching" of one individual by another seems to appease the aggression of the receiver. According to Rowell (1971), such appeasement gestures do not exist in arboreal guenons but are frequent in baboons and macaques.

Touching and manipulating the genitals, a behavior described in numerous baboons and macaques, is addressed most generally to males (Papio ursinus: Hall, 1962; Papio anubis: Hall and DeVore, 1965; M. radiata: Rosenblum and Kaufman, 1967; Sugiyama, 1971; M. Mulatta: Altmann, 1962; M. fuscata: Kawai, 1960). This behavior is also present in the patas (Hall et al., 1965) and C. aethiops (Struhsaker, 1967a), and we have observed it in Ce. galeritus and C. nictitans. In C. nictitans, juvenile males come to touch and sniff the genitals of an adult male notably after hearing loud calls from the latter. Most authors think that this gesture corresponds to a recognition of status, as Kawai (1960) has said.

Grasping hair, pushing, biting the neck or tail, and pulling or holding the tail of a partner are all tactile signals appearing in the course of play, where the list of behavioral patterns involving contacts is endless. A number of these signals serve as invitations to play; characteristically, they are not stereotyped and bear no relation to any sort of dominance status. These contact plays seem to be of capital importance for the normal social development of juveniles (Harlow and Harlow, 1965; Mason, 1965). In the same way, numerous tactile exchanges, either passive ("passive support") or active ("cradling," "starting push") occur between mother and infant—all contacts that act to protect and reassure the young or coordinate its activities (see, e.g., Bobbit et al., 1964). Thus light hand touching exists in most species and serves to invite the infant to hang on its mother.

Social grooming is probably the most important kind of tactile exchange among Old World monkeys, and many authors have discussed its function and distribution throughout age classes (see review by Sparks, 1967). Motor patterns are generally the same for all species, all parts of the body being submitted to grooming. Grooming is broadly distributed through age and sex classes; nevertheless, adult females groom more frequently and longer than do males. In the macaques and baboons, however, adult males are active in social grooming (notably P. hamadryas: Kummer, 1968). In the mangabeys and guenons adult males receive most of the grooming but they groom each other very little.

The correlation of grooming with social rank has given rise to controversies: the results vary according to species and observation conditions (see Bernstein, 1970b). According to Rowell (1971), grooming is particularly directed to the top of the hierarchy in the Cercopithecus spp. (like C. albogularis and aethiops), and to the bottom of the hierarchy in the macaques and baboons. Taking into account species-specific variations, one can say with Sugiyama (1971) that grooming is generally not a "one-way social behavior."

Grooming of an infant by a mother is an important activity in baboons (DeVore, 1963), langurs (Jay, 1963), and macaques (Bertrand, 1969). In the Cercopithecus spp., M. talapoin, and Ce. albigena, on the contrary, grooming of young infants is rare and not intense during the first months of life but develops at a later time (pers. obs.). Frequency of grooming among adult animals may vary according to female cycles. Michael and Herbert (1963) have shown that the quantity of grooming given by rhesus females reaches a minimum at the middle of their cycle whereas that given by males reaches a maximum at that time. In P. ursinus, Saayman (1971) shows that it is females in the deflating phase of the sexual skin (follicular phase of the menstrual cycle) that most frequently groom males. Hall and DeVore (1965) also note the increase in grooming by males of females in estrus. On the contrary, in C. aethiops, Rowell (1971) finds that grooming is most frequent with respect to pregnant females.

All the authors recognize within grooming social activities that go beyond the function of cleaning. It plays a role in the establishment or maintenance of interindividual contact. Thus an individual rejected by another has access to the latter through grooming (M speciosa: Bertrand, 1969). Rhesus females of inferior status groom males when they are in estrus in order to establish contact (Lindburgh, 1971). The frequent increase in grooming by males during periods of female receptivity also seems to facilitate encounters, the avoidance response of females being reduced. Similarly, rhesus females groom other mothers in order to be able to touch their offspring (Rowell, Hinde, and Spencer-Booth, 1964). Grooming also plays a role in appeasement and tension reduction. Poirier (1970b) notes that in P.johnii, 45 percent of all grooming sequences occur after agonistic exchanges and thus help to reduce interindividual tension. Similarly, in a group of talapoins, a female of high rank can interrupt an agonistic sequence by grooming the dominant male when the latter is threatening another individual of the group (Gautier-Hion, 1971b). The appeasement role of grooming also appears clearly during the weaning of an infant. A macaque or talapoin female, harassed by an infant seeking to be nursed, grooms it attentively, thus seeming to calm it and distract its attention.

As Poirier (1970b) notes, the tactile stimuli produced during grooming seem to be "a very pleasurable experience" for the animals. Nevertheless, Bernstein (1970b) citing Falk (1958) remarks that the act of grooming is just as much a social reward as that of being groomed. At any rate, grooming relations are the most likely to be reciprocal. Grooming serves to create, express, and reinforce interindividual social ties through these positive rewards.

Atypical forms of grooming are observed in several species. Kummer (1957) describes the formal grooming with a finger in the hamadryas. In C. mitis and C. neglectus (Booth, 1962), and C. nictitans, Ce. albigena and M. talapoin (Gautier-Hion, 1971b), an unusual form of grooming is observed especially in the male; after having been groomed, he will "pay back" the grooming by rapidly and sometimes brutally hitting his partner's coat without paying any attention to it. Poirier describes a similar pattern in P. johnii, and Rowell (1972) speaks of "aggressive" grooming in the talapoin. No flight reaction is observed in the partner, and it seems that these various kinds of grooming deserve to be termed formal: they are clearly devoid of any function in the cleaning of the coat.

Several more or less active postures are observed in which the animals are in close contact: sitting together, huddling, and tail twining. The "chin on nape" posture described by Bertrand (1969) in various macaques, baboons, and the gelada, also exists in the hamadryas (Kummer, 1957) and in various Cercopithecus spp. and mangabeys (Gautier-Hion, 1971b and Fig. 40). They are used at night or among subgroups during their daytime rests; they clearly indicate particular affinities between individuals. Partners in these subgroups remain the same in a stable social unit, even if through maturation of individuals the evolution of the society transforms other types of relations, such as aggression and sex. A sort of competition may rise in which individuals of low rank try to gain access to these subgroups (pers. obs.). In C. albogularis, Rowell (1971) observes that it is mainly dominant individuals that tend to sit together (82 percent of all cases), whereas others frequently remain alone.

In M. radiata, "huddling" is particularly well developed (Kaufman and Rosenblum, 1966), and Sugiyama (1971) observes groups of up to ten individuals. Baboons and certain macaques like M. nemestrina, however, are not "huddling species" but have developed formal hand contacts and kissing (Rowell, 1972) instead of general and passive body contacts. In the hamadryas, though, members of each "one-male unit" may huddle against each other during the course of the day, the different units being broadly spaced (Kummer, 1968: Fig. 16, p. 34).

Fig. 40. Sleeping group in Cercopithecus pogonias; note the "chin on nape" and "tail twining" postures. (Paimpont.)

In species with long tails, sitting together and huddling are frequently accompanied by tail twining (C. campbelli: Bourlière et al., 1970; M. talapoin, C. nictitans, C. cephus, C. pogonias, C. neglectus, C. petaurista, C. ascanius, Ce. albigena: Gautier-Hion, 1971b and pers. obs.; C. aethiops, C. neglectus: Chalmers, 1973). Although it probably plays a role in the equilibration of these arboreal animals, tail twining in most cases is an active search for contact (Fig. 40). In infants, tail twining seems to depend on the coiling reflexes of the tail. Even in species in which this behavior has become rare among adults (like Ce. albigena), it is a general behavioral component of infants huddled in their mothers' arms.

This survey has tried to bring out the great similarity of basic patterns occurring in various species during close exchanges. Species differentiation should be made afresh on the basis of frequency of appearance, which seems to be correlated with the increasing social function of exchange.

Thus the side-to-side sniffing posture is present in the Cercopithecus spp., in the mangabeys, and at least in M. radiata. But while it is rarely observed in guenons and then only during sexual encounters, it is a very frequent form of social approach among female mangabeys.

Muzzle contact, on the other hand, for which there is little evidence in the baboons and macaques (where it is linked with feeding), is the essential mode of interindividual encounter in the Cercopithecus spp. If one admits that olfaction plays a role in this behavior, its frequency indicates a primitive trait, this pattern being frequent in carnivores especially.

Kissing and social presentation seem especially to characterize baboons, macaques, and mangabeys, in which they occur with numerous other acoustic and visual appeasement signals. In these species, hierarchization within the group is more obvious than in the guenons, and signals that serve to assure status, such as mounting, occur frequently.

Discussion

This chapter is a survey of the most usual signals manifested by Old World monkeys, but it is obvious that the social regulation of populations does not depend solely on these exchanges of "specialized" communicative acts. For Altmann (1967) "social communication is a process by which the behavior of an individual affects the behavior of others." This mode of action is virtually unlimited and does not necessitate individualized signals. As Bertrand (1971) notes, to a congener the sight of a monkey bringing something out of his cheek pouches is a sign that the individual is eating. This behavior can induce the partner to approach and to perform tactile and olfactory exchanges (e.g., muzzle-muzzle) or even some kind of dominance behavior in order to gain access to the food.

This passive communication is not limited to visual signals. An active monkey makes all sorts of noises characteristic of its activities. In forest monkeys, vocal responses are evoked by the noises of movement among the branches in the same way as by cohesion calls. Similarly, the noises of urination and defecation upon awakening are the first indications of reciprocal localization of group members and are followed by vocal contact calls. Some of these nonvocal sounds have become ritualized, e.g., tree shaking or jumping around; on the other hand, some calls must ultimately be considered as passive acts of communication, such as the trills exchanged "spontaneously" between infant and mother without any apparent stimulation and without modification of subsequent behavior.

The production of certain odors undoubtedly also plays a role in passive communication. This is probably the case with the sexual pheromones diffused during the female's period of receptivity, whether she is presenting or eating.

There exists therefore a gradual passage from passive to active communication, correlated with a growing ritualization of signals. Both act simultaneously or in relay, and it is always a little arbitrary to establish a classification separating acts that are communicative, or signals, from those that are not.

It is just as artificial to treat signals of vocal, visual, tactile, or olfactory nature separately, since in most situations these various sensory modalities occur simultaneously (Marler, 1965), especially in close exchanges. Thus in kissing, tactile signals blend with olfactory cues (neck sniffing), sounds (repeated gruntings), and appeasement faces (grimace or lip smacking). At medium distance, visual and auditory signals take turns or work together. This is the case in approach-flight behavior, where sound reinforces gesture by focalizing the partner's attention, as well as in peaceful exchanges where the calls precede contacts.

Visual signals occur alone principally in stereotyped displays like penis exhibition and stopping postures. At a greater distance or when the exchange does not require that the congener be informed of the emitter's identity, sounds act alone, especially in alarm situations or exchanges regulating the spatial distribution of the population.

CHARACTERISTICS OF THE SIGNALS

Throughout this survey, we have noted the great similarity among the visual, olfactory, and tactile signals encountered in all species considered. The more a given species is the object of long-term observation, the more this relationship is confirmed. Thus, after several years of contact with a captive group of C. nictitans, we have just observed for the first time the very characteristic posture of mutual sniffing in the inverted position, which is common in the mangabeys (see Fig. 36). Ultimately it seems conceivable that no truly unique facial display or posture exists (except perhaps stopping postures): those that are species-specific result from morphological structures characteristic of a given species which emphasize the appearance of the displays (see Kummer, 1970); others stem from our own ignorance due to the small number of social exchanges manifested by certain species under observation.

Thus, although Kummer (1970) underlines the difficulties of using frequency as a taxonomic criterion, it seems obvious that the frequency of occurrence of social patterns is one of the first observational features differentiating the baboons, macaques, and mangabeys from the guenons. The structural relationships are less obvious when dealing with vocal signals, for which the parallels that one can establish from species to species are complex. Forest guenons, which include a great variety of species, offer a particularly interesting field of study for this subject, and Struhsaker (1970) has stressed the importance of their vocalizations as a phylogenetic indicator. But this problem is complicated, because on common phylogenetic bases, sympatric species seem to diverge in proportion to the needs of species specificity. We have previously noted that C. neglectus, which is not included in the mona group, nevertheless has boom-type loud calls that are not easily distinguished from those of C. pogonias except on the basis of sequential emission. These two species live in western Africa and have numerous similar calls, but their ecological niches and their different ways of life preclude frequent encounters between them.

Conversely, C. nictitans and C. cephus of western Africa frequently live in association (80 percent of all cases) and have very similar general repertoires, but adult males possess completely different loud calls. The situation is the same for C. mitis and C. ascanius in eastern Africa. Furthermore, as we have already noted, the loud calls of male C. nictitans and male mitis are extremely similar, but curiously enough, the latter has a boom-type call (Rowell, 1971; Marler, 1973). Yet C. mitis does not cohabit with boom emitters. On the contrary, in Gabon, where C. nictitans frequently live with pogonias, booms are reserved to the latter. Recent observations have shown, however, that C. nictitans may occasionally emit them, particularly in captivity (Gautier, 1973); the call appears to be rather like a relic from the ancestral stock.

Thus, starting from a general "pool," close species seem to be able to retain part or all of the vocalizations held in common, or if species specificity necessitates it, to differentiate certain types of calls that then assume highly stereotyped forms. This is the case of loud calls among males of the Cercopithecus spp., which appear to have a role in reproductive isolation. For alarm signals, on the contrary, natural selection has favored the development of very similar sounds for many species, the only imperative seeming to be that the structure of the calls permit rapid maximal diffusion without indicating the position or identity of the uttering monkey. This characteristic is even more obvious for calls linked with approach-flight behavior; infant defensive calls (geckers, screams, screeches, whistles) seem to be especially widespread in Old World monkeys.

The multimodality of exchange is correlated with an increasing variability of signals. In unimodal exchanges, signals are maximally stereotyped, can be perceived clearly despite the distance between emitter and receiver, and imply a species-specific message. At close range, on the other hand, constant shifts through different sensory modalities permit subtle variations. These variations are the result of several phenomena: lack of stereotyped character (with the same basic signal, an animal can modulate individual variations, which are probably due to anatomic peculiarities or to tiny alterations in its excitation level; e.g., trill variations in a juvenile Cercopithecus, Fig. 18); the presence of gradation (structural variations permit passage from one type of signal to another; e.g., graded aggression-flight system in the talapoin, Fig. 9).

The phenomenon of gradation demonstrated by Rowell and Hinde (1962) for the acoustic signals of the rhesus ("graded sounds") is also evident in visual signals (e.g., for approach-flight signals: see also Vine, 1970). This notion is the opposite of that of discrete signals, for which there is no gradual passage from one type to the other (e.g., type 1 loud calls or penile display). In vocal repertoires, the gradation may be total, with all the elements of the system capable of gradually developing into one another: this is probably the case with the baboons, the red Colobus, and (except for loud calls) the mangabeys. The gradation is only partial when there is a structural discontinuity between groups of graded calls in the same repertoire: this is the case for certain macaques and for the talapoin, in which several graded systems coexist (an aggression-flight system, a cohesion system, and a highpitched system: Gautier, 1974). Finally, in the forest Cercopithecus spp., only a few types of calls can develop imperceptibly from one kind to another, notably defensive signals.

The gradation of a communicative system is therefore a question of degree (Marier, 1973). In order for it to be real and functional, the evolution of one structure into another must be rapid and reversible, implying situational and motivational changes. In the opposite case, the analysis of certain structures may show that they are derived from one another, yielding the general characteristic of what one might call the "voice" of a species, without implying a real functional signification in communicative acts (Gautier, 1974).

DETERMINISM AND GENESIS OF THE SIGNALS

A number of authors have emphasized that communicative acts constitute stable behavioral elements within a species (see e.g., Bernstein, 1970a). The works of Kummer and Kurt (1965), for example, have shown that captive hamadryas behave very similarly to wild ones. The manifestation of some particular patterns in each of these environments shows that the nonoccurrence of a behavior does not mean that it is absent from the species repertoire, but rather that it depends on environmental influence, social or nonsocial (cf. the boom of C. nictitans).

Genetic determinism of fundamental call structure seems obvious, although few works make direct reference to it. The recent crossing of two Cercopithecus spp. offers a confirmation. The mother, C. ascanius, can emit two calls during peaceful exchanges—one low-pitched and discontinuous, the other shrill and quavered— both of which retain their own structures when associated in one sequence (Fig. 41,2 and 2 bis). In C. pogonias (the father), however, the frequent association of the two calls is made by transitional structures (Fig. 41, 1 and 1 bis), and the quaver does not exist. At the age of one month, the young hybrid, raised with both parents, emits several kinds of calls: Trilled, shrill calls identical to those of its mother (Fig. 41, compare 3 and 8) and others with a less clear quaver; low-pitched trills in which the structural discontinuity is less apparent than in the mother's (Fig. 41, compare 2 and 2 bis to 4 and 4 bis); and calls resulting from the more or less total association of the two preceding types: the call sometimes possesses just a slight transformation of modulation (Fig. 41, 7); at a subsequent stage, low-pitched and shrill cries are linked by a transitional structure similar to that of the father when it was immature (Fig. 41, compare 1 and 1 bis with 5 and 5 bis). Both maternal and paternal influences appear quite clearly in these signals: passing from a substantial quavering (mother) to a reduced one (father); passing from two distinct calls (mother) to a single pattern through the presence of transitional structures (father).

In the infant, most signals occur as immediate reactions to anything that upsets its contact with its mother, especially with her breast. This is particularly clear for vocalizations. If a talapoin about ten minutes old is removed from its mother and denied any possibility of contact, it gives almost all the basic calls of its species' repertoire, especially the distancing-cohesion-isolation system calls, the flight system calls, and the shrill calls that subsequently develop into alarm vocalizations (Gautier, 1974). Similarly, Winter et al. (1973) have shown that almost all the vocal signals of the squirrel monkey are present at birth.

Threat calls, however, generally occur later than defensive sounds. In the Japanese macaque, they have been observed in the twenty-fourth week (Kawabe, 1965, in Nishimura, 1973) in the nineteenth week (Takeda, 1965, 1966), and in the sixth month (Nishimura, 1973); in the talapoin at more than one year of age (pers. obs.), and in the grey-cheeked mangabey at ten to twelve months (pers. obs.). It is the same for alarm calls or aggressive alarms. These tardy manifestations seem to be due to the particular status of the infants. They are protected by their mothers and turn toward them at the slightest disturbance, and they only begin to individualize their reactions as they develop their independence. One particular case in the development of signals concerns male loud calls. Their manifestation clearly seems to depend on sex hormones, that of type 1 loud calls being strictly correlated with the social status of the vocalizer.

In the course of ontogenesis, calls are submitted to three essential modifications:

1. Their frequency of occurrence increases rapidly during the first months of life (up to six months in the Japanese macaque: Nishimura, 1973), and subsequently diminishes in the course of individual maturation. This decrease in frequency, however, is less obvious in females (pers. obs.).

2. The thresholds of appearance of different types of calls are subject to modifications (Gautier, 1974); this phenomenon is a corollary of variations in emission frequency. In juveniles, very slight alterations in excitation level provoke the emission of a call. In adults, the animal must be submitted to a much more substantial stimulation for the same signal to be uttered.

3. The structure of the calls is subject to transformations. Different parameters are involved (intensity, duration, rhythm, noise), but the most obvious and measurable is drop in pitch. This last phenomenon is accentuated in males of the guenons and mangabeys (and no doubt in some other species) because of the break in voice at sexual maturity.

Fig. 41. Comparison of the calls of a young hybrid with those of its parents.

Parental vocalizations. 1, 1 bis: Father's calls (C. pogonias) before sexual maturity. 2, 2 bis, 3: Mother's calls (C. ascanius) as an adult.

Infant vocalizations. 4, 4 bis: Low-pitched call, 8:high-pitched call, both similar to its mother's. 6, 7: Association. 5: Juxtaposition of low- and high-pitched calls as in the father. ("Bis" indicates analyses done with the help of narrow 45 Hz filters; the other analyses were done with broad 300 Hz filters.)

These developments are not, however, irreversible. An adult monkey, even if it is male, will revert to juvenile calls under conditions in which the stimulations are sufficient to increase its excitation level in an unaccustomed way. Thus, although each age, sex, and status class possesses differentiated vocalizations for a given situation under normal conditions, it appears that under disturbed conditions any adult individual can emit any type of call (Gautier, 1974) except those that are hormonally determined.

The appearance of facial displays and gestures happens more progressively. The first to occur are generally defense or retreat faces, which may or may not be associated with calls. Others observed very early are the play face (fifteen to thirty days for the mangabeys and tala-poins, pers. obs.), yawning (about one month in the same species), as well as a slow form of lip smacking, which is observed from the very first days of life. Only the play face is manifested at an early stage in social exchanges. Lip smacking and presentation are integrated into a social context later (one month for lip smacking and more than four months for presentation in Ce. albigena: pers. obs.). The appearance of presentation seems to be facilitated by genital examinations by the mother and is actively adapted to social exchanges by congeners' influence: a male mangabey forces a passing juvenile to present itself by lifting the young animal's tail.

Facial displays, gestures, and postures generally seem to depend more on learning for their normal integration into social exchanges than do acoustic signals. Thus, although vocal displays suddenly occur in males at the onset of maturity (see Fig. 1), visual displays are present in rough form in infants and require a long period of learning. In Ce. albigena, juveniles engage in yawning from the age of four weeks and do a rough job of tree shaking at about two and a half or three months. But the association of these two kinds of behavior does not occur until eighteen months, and penile display is not added until about three years. The complete sequence of tree shaking, stopping posture, penile display, and yawning is not linked together until the juvenile male reaches sexual maturity, at about five years (pers. obs.). At this point the sub-adult intensely surveys the activities of adult males and performs its displays by imitating them and using the same props.

Winter et al. (1973) find in their ontogenetic study of the vocalizations of the squirrel monkey that there is no difference between the manifestations of calls produced by animals acoustically isolated from birth and those of normally raised monkeys. Before affirming that the manifestation of calls is subject to any sort of learning in monkeys, however, it must be seen experimentally how well the signals given by isolated juveniles are adapted to suitable contexts. Empirical observation shows that calls uttered by monkeys raised in impoverished social environments are not as modulated and variable as those of monkeys raised in social groups, and that the majority of their calls are given without clear discrimination in all frustrating situations.

On the contrary, the experiments of Harlow and his coworkers (see, e.g., Harlow and Harlow, 1965) have shown that social learning is necessary for the normal and adapted manifestation of a great many kinds of postural behavior. Similarly, Mason (1960, 1961a, 1961b), after numerous experiments of social deprivation conducted on the rhesus, notes that "the effective development of the elementary forms of social coordination and communication is dependent upon learning." Conducted according to an extremely rigorous procedure in which monkeys were placed in the presence of photographs or films of congeners, the studies of Miller and his coworkers (see Miller, 1971) have also demonstrated that socially isolated monkeys do not adequately respond to the nonverbal expressions of other monkeys and that these animals seem to be "defective transmitters."

CAUSALITY: TRANSMITTED MESSAGE

According to general opinion, the signals emitted by monkeys essentially indicate the emotional state of the displayers; they rarely if ever convey specific information about the environment. Thus the calls given by a group of monkeys finding a fruit tree are the same as those uttered during their normal progression or manifested by an individual upon the arrival of a congener; only their quantity increases. Similarly, the nature, intensity, and frequency of emission of alarm calls is modified more by the intensity of the stimulation than by the nature of the danger. In a parallel way, displays like shaking, yawning, or penile display appear in situations of high excitation, whether the stimulation is provided by an encounter between two groups or by a non-conspecific potential danger.

Visual signals also convey indications about the emotional state of the emitter. Using methods of interanimal conditioning, Miller and his coworkers (1967, 1971) have shown that the behavior of a "receiver" monkey is modified by very subtle alterations in the face of the displaying monkey. In general, visual, acoustic, and olfactory signals all appear in diverse situations, and they seem to convey no specific indication of the nature of the stimulus, whether it is the presence of a congener, familiar or strange, or an element in the exterior environment.

Green (1975) has classified ten types of fundamental calls of the Japanese macaque's repertoire according to "attributes indicating demeanor and internal state," and has shown that there is a correlation between the excitation level of the animals and the structure of the calls uttered. For Green, arousal is one of the essential components of internal state that determine the form of the signal. Above all, the message is emotional and predisposes the partner to respond from a given behavioral range, the response being modulated according to the context of emission. Green's work, which systematizes what other authors had previously suggested or mentioned (e.g., Rowell and Hinde, 1962; Gautier, 1974), clearly shows that a given type of call does not always occur in a precise context and therefore cannot offer any information peculiar to the situation.

It does not appear, however, that this work provides the "consistent framework" wished for, which would permit comparative studies. The classification of situations according to the demeanor and arousal of emitting individuals remains somewhat subjective insofar as it does not use physiological techniques that would allow, for example, the measurement of variations in arousal before, during, and after vocal emissions. Furthermore, if excitation level partially determines the nature and structure of the emitted signal, one must be conscious of the fact that variations in the arousal do not seem to occur on a comparable scale for all age classes. The thresholds for the appearance of various vocalizations are particularly low in a juvenile, for example; thus, the same stimulation that evokes a scream in an infant will provoke only an alert call in the adult. Group members are implicitly aware of this phenomenon since they take the alarm calls of juveniles "less seriously" than those of adults.

Moreover, in response to a given stimulation, juveniles and adult females will emit social alarm calls, whereas males give barks that can be followed by rallying loud calls uttered by just one individual. We have also seen that the social environment influences the type of reaction evoked in an individual by any sort of stimulation: an isolated animal will react to a disturbing situation by hiding, but one in a group will emit calls. For a given situation, we can conceive on the one hand that alterations of individual internal states will differ according to age, sex, experience, status, and the environment taken as a whole; and on the other hand that other, more specific influences, notably social ones, ultimately determine the form of the vocal response. In fact, it is difficult to establish correlations between signal type and arousal level without dealing separately with the individual classes. In this view, the ontogenetic transformations of the call structures, which give the perceptual bases for identification of the age classes, certainly play a major role in the interpretation of the signals by the congeners.

Mason (1965) has also shown that in juvenile chimpanzees the appearance of some types of social behavior, like play, can be correlated with arousal levels. Such a concept permits an explanation of changes in activity pattern without resorting to independent motivations. Mason points out, however, that some kinds of behavior may overlap in their correlation with arousal level, and that they are differentiated by other factors, especially the surrounding context.

It is generally admitted that the manifestation of signals is involuntary and uncontrolled, and Bertrand (1971), quoting Andrew (1964), points out that monkeys are incapable not only of emitting sounds voluntarily but also of witholding them. Yamaguchi and Myers (1972) also conclude that there is a lack of voluntary control over vocalizations in the rhesus. For Sutton et al. (1973), who have conditioned rhesus to give vocalizations in order to obtain a reward, to select low-pitched sounds, to increase their duration, and to reduce the frequency of calls uttered, emotion is not the only variable capable of determining everything in vocal emissions. On the contrary, these authors think that their experiments, indicating a learning controlled by the discrimination of unfamiliar stimuli, offer an example of voluntary vocal behavior.

The important role played by learning in the adapted manifestation of facial and postural signals can be correlated with a certain control of their expression. Some observations would lead one to believe that, and anyone who has seen a female monkey trying to touch an infant in the arms of its mother has surely been astonished by the subtlety of the behavior. The female grooms the mother with great attention, then surreptitiously slips her hand over the mother's abdomen in order to touch the infant's fur. All the while she pretends to continue grooming with one hand, remaining prepared to return all her attention to the latter activity if the mother intercepts her gesture. All primatologists have observations of this kind in their notebooks, but possessing only a very anthropomorphic vocabulary, they would rather remain silent about them.

Thus, neither the establishment of lists of species-specific signals, nor their correlation with simple variations in arousal, nor even attempts to comprehend their adaptive functions permit us at present to take into account the subtlety of the interindividual exchanges that regulate the life of monkey groups.

CORRELATIONS WITH HABITAT AND MODE OF SOCIAL ORGANIZATION

It is customary to point out that in open habitats visual exchanges predominate over vocal (e.g., Andrew, 1963b, 1964; Marier, 1965; Moynihan, 1967). This is well illustrated by the differences in the nature of intergroup exchanges in woodland and savannah environments. Correlated with the increasing frequency of visual exchanges, an increase in their variability and gradation is to be expected. In a closed habitat, on the contrary, passive visual communication is replaced by vocal emissions punctuating group activity, and active exchanges are more stereotyped and less frequent. Nevertheless, the frequency and the subtlety of visual exchanges also depend on the degree of evolution of the species. A good proof of this is the exam ple of the forest mangabeys, the complexity of whose visual signals approaches that of the baboons, and who also have developed numerous olfactory and tactile exchanges.

Fig. 42. Spectrographs analyses showing the difference in variability for the same type of fundamental call in two Cercopithecus. In C. pogonias, the low and high-pitched structures are associated through transitional elements (a, b); in C. neglectus, on the other hand, they arc separate (a'. b'). Furthermore. in C. pogonias the high-pitched structure pouestes a significant frcqucncy modulation. which u very red need in C. neglectus (compare b and b').

The gradation of vocal systems has also often been linked to the openness of the environment (e.g., Marler, 1965; Moynihan, 1964, 1966). It was thought that discrete signals were necessary in the forest for the transmission of unambiguous messages (see Altmann, 1967). Studying the Colobinae, Marler has subsequently offered evidence that this correlation is not obvious. Of two species of Colobus, both of which live in woodland habitats, one (C. badius: Marler, 1970) possesses a graded vocal repertoire, the other (C. guereza: Marler, 1972) various discrete signals. In the same way, although it lives in very dense forests, the talapoin has an almost fully graded repertoire (Gautier, 1974). Finally, the arboreal mangabeys {Ce. albigena) as much as the semiterrestrial ones (Ce. galeritus), and the drills and mandrills, all have vocal repertoires in which the gradation is probably close to that of baboon calls.

The gradation of a communicative system is more closely related to frequency of contact than to openness of environment and seems to be correlated, as Marier (1970) emphasizes, with a more complex social organization. The latter occurs especially in relatively large groups, since an increase in the number of individuals, which necessarily augments the general activity level (see Gautier-Hion and Gautier, 1974), can favor the development of exchanges. Thus Co. badius forms groups of thirty to fifty individuals, whereas C. guereza groups seldom go beyond about ten animals. Similarly, the talapoin lives in bands that sometimes reach more than a hundred head, whereas those of the Cercopithecus spp. are under twenty.

A supplementary example is offered by two forest species, between which we have already pointed out a relationship in vocal repertoires: C. neglectus, which lives in groups of three to six animals, and C. pogonias, in which groups reach fifteen individuals. In captivity, as in nature, de Brazza's monkey is a discrete, passive animal that can remain immobile for hours. On the other hand, mona groups have a high level of general activity. Although C. neglectus and C. pogonias have a common fundamental call structure, the former emits calls that are not very variable, while the latter's are more modulated (Fig. 42). This example comes close to that of the fox and the wolf (Kortland, 1965, in Vine, 1970). The wolf s repertoire, although basically similar to the fox's, is much larger. Kortland attributes this to differences in social organization, the wolfs methods of hunting in cooperation implying more highly developed means of signalization.

Thus, variability, gradation, and frequency in social exchanges characterize species whose social organization is more complex. These species include essentially monkeys of open habitat: macaques and baboons, which have particularly numerous peaceful or agonistic short-range exchanges. Nevertheless, much more familiarity is required with the forest mangabeys, and even more with the mandrills and drills, before it is possible to judge the subtlety of the messages conveyed by their communicative acts.

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