Effect of oxidation-reduction potential on light-induced cytochrome and bacteriochlorophyll reactions in chromatophores from the photosynthetic green bacterium Chlorobium

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COMMUNICATION BY POSTURES AND FACIAL EXPRESSIONS IN THE RHESUS MONKEY (NACACA MULATTA) BY

R . A. HINDE AND

T . E . ROWELL

Sub-department of Animal Behaviour. Hadingley. Canabridge [Accepted 14th March. 19611

(With 11 figures in the text) The principal postures and facial expressions used by the rhesus monkey in social communication &redescribed

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Introduction Material and method Expressive movements . A Sitting postures ' (i) Upright sitting . (ii) Relaxed sitting . (ci) Hunched sitting (iv) Cat-like sitting (v) Crouching . B AttackandThreat .. (i) Attacking run . . . . (ii) Threat .. .. (iii) Backing threat (iv) Showing hindquarters (v) Branch-shaking (iv) Bouncing . C Fear .. (i) Looking elsewhere . (ii) Frightened grin (iii) Showing neck . (iv) Locomotion in few D Friendly behaviour . . .. (i) Initiation of grooming (ii) Lip-smacking . . .. (iii) Presentation and mounting E Miscellaneous .. (i) Chewing and gnashing (ii) Pacing (iii) Yawning .. Aoknowledgments References . ..

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R. A. HINDE AND T. E . ROWELL

INTRODUCTION

Darwin (1872), in his Expression of the emotions in man und unimuls, described the principal expressive movements and postures in man, some primates, and a number of other mammals. Since that time much interesting data about the behaviour of sub-human primates has been gathered but, with the possible exception of the chimpanzee (Kohts, 1935), there is still no comprehensive description of the expressive movements of any one species. Even the rhesus monkey, which has been widely used as a laboratory animal for several decades, has not yet been studied in any detail in this respect. We have therefore started to describe and analyse the postures, gestures, grimaces and calls of the rhesus monkey. We have concentrated on those movements and calls which are common to all members of the species and are likely to play a role in communication between individuals. This paper describes the principal body postures and facial expressions of the adults : a second paper (Rowell & Hinde, in press is concerned with the principal calls. Since the comparable data for other species are of variable precision we have not attempted a review of related movements or calls in other primates except where it seemed directly relevant to our observations. We hope to present more detailed analyses of aome of the expressive movements in later papers. MATERIAL AND METHODS

The monkeys were obtained from zoos in Great Britain. Their earlier history is unknown : they had all lived with other individuals at the zoos, most were probably imported when young, and some may have lived for a while as household pets. Since they came from diverse sources, common features in their behaviour were unlikely to have been imposed by any particular environment, or by a common tradition. During the fourteen months observation period, we made observations on twenty-three adults-Seven males (about 30 lb.) and sixteen females (9 lb. or over)-for varying lengths of time. They were kept in the four units of a monkey house (Fig. l), each of which consisted of an outside run (8' high and 18' x 8' in plan) connecting by a swing door with an inside compartment (7' 6" high and 6' x 4' 6" in plan). There was also a non-opening plate glass window between the inside compartment and the outside run. Branches were suspended below the roof of the outside run. Heating was provided only in cases of illness, new arrivals, or exceptionally cold weather. Although the runs were not large, we do not believe that the expressive movements were seriously affected by the conditions of captivity, The animals were kept in groups consisting of a male and two to four females : one pen contained only females. Breeding occurred during the period of the study, but no observations on the young are included in this paper. Observations were made of interactions between individuals within each group, of interactions between the groups, and of responses to humans and objects outside the pens. No attempts were made to hide the observer : in practice the animals soon lost interest in a familiar human who kept reasonably still. Our monkeys were not accustomed to handling-males would usually attack and females flee if the pen were entered.

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POSTURES AND FACIAL EXPRESSIONS IN THE RHESUS MONKEY

EXPRESSIVE MOVEMENTS

Even apparently stereotyped movements and postures are variable in some degree, though if they are to be useful in communication this variability must be limited. Description thus involves abstraction of those features which recur with reasonable consistency from one occasion to another. Many of the postures and facial expressions of the rhesus monkey intergrade with each other, or can be combined in various ways : we have not attempted to do more than indicate the general types. To interpret expressive movements it is necessary to relate them to the context in which they occur, and to identify the relevant factors in that context. I n a complex social environment, where there is much going on all the time, this may not be easy. Further, the object at which a movement is directed may not be that which elicited it : thus a female, attacked by a dominant individual, may then turn on one of her own subordinates. Individual variability raises further difficulties : although the form of any particular type of expressive movement is usually fairly constant between individuals, the relation between the extent of the movement and the strength of the causal factors differs. For such reasons, we have given only general descriptions of the situations in which these movements occur.

A. Sitting postures Certain features of the resting posture of a monkey show the state and status of the individual. For example, the sitting postures differ according to whether the animal is dominant or subordinate, relaxed or alert. Some commonly seen types are described below intermediates are of course frequent. (i) Upright sitting The animal sits with its back nearly straight and vertical, its arms resting on its knees. Such a posture is adopted by a dominant male when it is on the look-out and sometimes when it is grooming an inferior. I n the latter case the animal grooms at arm’s length-this is quite different from the close grooming usually seen. (ii) Relaxed sitting Here the back is bent markedly in a smooth curve. The legs and arms are stretched out in front and the neck relaxed so that the head droops between the arms : in this posture, head, neck, back and legs form a U-shape, with the greater curve in the lumbar region. This is the dozing position of a dominant male, and sometimes also of the highest ranking female. (iii) Hunched sitting The back is strongly curved, with the point of maximum curvature slightly more anterior than in relaxed sitting. The legs and arms are tucked close to the body, the forearms resting on the knees, hands hanging in front. The head is low, slightly withdrawn, and often resting between the knees.’ The tail is curled round the side of the body. This is the common resting position of animals of middle rank (Fig. 2a) Small groups of monkeys sit together to sleep in this posture, the chin of one animal resting on the back of its neighbour (Fig. 2b). 1*

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If the animal is alerted, its face is raised : the more subordinate animals tend to keep the head low and look out from under their brows, while the more dominant ones raise the head above the shoulders. The arms may be put to the ground as an intention movement of locomotion. (iv) C'cit-Eike sitting

The lower part of the back is nearly straight, sloping forward, arid there is a marked curve at the shoulders. The neck and head are held upright. The arms are straight, with the hands on the ground just in front of the feet. This is the posture of a low-ranking animal, especially one which has recently been persecuted by others. In the latter case, the lips are tightly shut and the corners of the mouth drawn back a little (Fig. 2c). ( v ) C'roziching -1subordinate monkey which has just been attacked crouches with back liorizontal and beIly near the ground, tail curled down. Its hindquarters are directed towards the animal from which it has been fleeing and its posture soniewhat resembles that of presentation. If it sits, it settles down on its hindquarters. keeping its arms still bent. Often it looks over its shoulder at the attacker and may give the frightened grin. If it runs, the crouched position is maintained.

B. Attack and threat (i) Atfncking run The animal runs towards the object of its attack, mouth slightly open. The lower jaw is often thrust a little forward, showing the lower incisors, but the lips and cheeks are not retracted, so that the upper teeth are exposed only a little. The ears are usually fattened and the hair may be either sleeked or (more often) raised (Fig. 3). The attacking run often starts from a threat posture or from a crouched approach (below), but dominant males may attack directly, without preliminary threat. The run may lead to an actual attack in which the rival is seized and bitten-usually first near the root of the tail and then over the shoulder. Often, however, the attack is not pressed home. Dominant individuals may end the run in an alert posture with arms straight, ears cocked foruard and tail upright. If the attack is not pressed home because of fear, however. the run usually ends in a threat posture (Fig. 4a). Occasionally an attacking run is preceded by a crouched approach-the chest is lowered almost to the fround, the arms being extended forwards for most of the time. The ears are drawn back and the mouth opened somewhat. Forward progress in this position is both slow and quiet, and may permit a surprise attack. (ii) Threat The threat postures are variable but have certain features of the expression wid head inovenients in common. The mouth is held open with the Iower jaw slightly protruding ; the lower teeth are thus partially exposed but the upper ones are mostly covered by the upper lip. The corners of the mouth come

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POSTURES AND FACIAL EXPRESSIONS I N THE RHESUS MONKEY

8 H I

1%. 9. HISDE A#D

Fig. 2 c - 4 l a t -like sitt iiig : This subordinate feriiale has her head raised and pulled back on her shoulders ; her back is straight cxccpt for tho sharp beiid at the shouldrrs, and her hands are on the ground in front of her.

T. E. ROWELL

Fig. 3-An attacking run towards the camera. Note the tail position, and his expression, with mouth slightly open, ears back, and brows lowered.

POSTURES AND FACIAL EXPRESSIONS IN THE RHESUS MONKEY

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forward. The head is jerked towards the object being threatened, then returned to the original position. I n the more vigorous performances the movements of the head towards the object is accompanied by one or more growls or barks. The movement of the head towards the object may be continued into an attacking lunge or run. This is most likely to occur if a number of barks are given. Sometimes, on the other hand, and especially if the movement is made in silence, threat may be followed by turning or moving away from the object. This is often a continuation of a backward jerk of the head. Threat is thus associated with both attacking and fleeing. Usually, however, there is a long period of ambivalence during which the animal jerks head and body at the object without making a decisive move in either direction. These jerks may be made from almost any position, for example (a) from a standing position, with legs and arms braced for immediate locomotion towards the object (Fig. 4a) ; (b) from a sitting position with the hands on the ground ; (c) from a sitting position with the arms held off the ground in front of the chest (Fig. 4b) and (d) from a crouched standing position with legs and arms flexed (Fig. 4c). In the last case the body is usually oriented away from or sideways to the object. The precise nature of the posture depends on the spatial relations between the threatening animal and the object, but the first three positions indicate, in the order mentioned, increasing probability of an attack. The fourth position is more characteristic of a subordinate animal threatening in self defence. In each position the limbs may be flexed or extended in association with the head jerks. A crouched posture, with the back concave, the mouth only slightly open and the body directed towards the object is often a preliminary to an attacking run made without previous threat (see crouched approach). Often the head is held for a second or so at the backward extreme of a jerk. The animal then has a scandalised appearance-the body is usually upright, the neck slightly stretched, the mouth opened, the eyebrows raised and the eyes wide open. Sometimes the eyebrows are moved up and down. A sequence of threatening movements in which this position is conspicuous is unlikely to lead to attack. A similar expression is sometimes, though less frequently, held at the forward extreme of a jerk. (Fig. 4d). Other characteristics of the threat posture are all somewhat variable, and the analysis of their precise significance demands quantitative treatment. The brows are usually lowered and the eyes are opened wide to fixate the object intently. If the head is held momentarily at the end of a forward jerk, the ears may be moved rapidly backwards and forwards. The hair is often raised, this being especially conspicuous where it is longer over the shoulders. Darwin (1872) observed a reddening of the skin in the face of angry rhesus monkeys ; similar observations on other primates have been collected by Goodhart (1960). I n our colony there was considerable individual variation in the redness of the face, and we did not find that increased reddening was a conspicuous feature of aggression. (iii) Backing threat A high-intensity threat posture made by an aggressive animal towards an object of which it is afraid. The posture is closely similar to the crouched

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approach (v. supra) which sometimes precedes an attacking run, but the locomotion is backwards instead of forwards. The ears are flattened and the head slightly raised, with the incisors just visible. (iv) Showing hindqzmrters This occurs in aggressive contexts and is quite likely to be followed by an attacking run. Unlike the threat posture just described, however, the body is turned away from the object threatened. The animal faces three-quarters away from the object, but looks back at it over his shoulder with ears flattened, tail vertical and tip curled over backwards, mouth slightly open. He thereby displays his bright red hindquarters surrounded by a bristle of yellow fur with the black tail tip above. This postureisseen most often in males. It oftenoccurs in intervals of pacing during bouts of threatening between neighbouring groups.

(v) Branch -shaking This involves shaking or vibrating some large object in the pen, making a loud noise. Usually the animal goes through the movements of jumping up and clown on a branch without letting go, so that the branch is shaken up and down several times in a second (Fig. 5a). In especially vigorous performances the animal jumps from point to point, giving several shakes each time he lands. While shaking, the mouth is usually slightly open and the teeth slightly exposed. The ears may be forward or (usually) back, and the tail lowered to the horizontal or below. The tail position may be a matter of balance : as soon as the shaking is finished i t returns to the vertical. Each of our males has a slightly different technique for branch-shaking. One usually makes a series of leaps with four to five shakes in between, as described above. Another gives a longer series of shakes, which often end in his bouncing himself off the branch on to the ground below. A third>while sometimes shaking in the usual way more often stands up on the branch and punches or pulls at the wire netting above his head or at one of the supporting chains (Fig. 5b). Ail three have their favourite positions in the pen for branchshaking, and nil1 walk or run to these positions in order to perform. They will, however, often '' branch-shake .' elsewhere-for instance on the wirenetting of the side walls. Branch-shaking is given most often by males, but is also sometimes shown by females. They do not have such clearly preferred stations for branchshaking as do the males. Branch-shaking occasionally occurs in the absence of any stimulus which can be detected by the observer, but much the most frequent cause in our colony is the noise of jet aircraft-perhaps because the aircraft are always " driven away " by the performance. Branch-shaking is also performed on the approach of strangers, and during bouts oft hreatening between adjacent pens. In such cases it is associated with pacing. When released into the outside run after a period of confinement animals will sometimes branchshake, and one male did so when he was first introduced into the outside run. Branch-shaking is often infectious, one male starting when he hears another. Some components of the movement (month, ear and tail positions), its frequent! association with threat, and the contexts in which it appears all indicate a strong aggressive element in branch-shaking.

POSTURES A N D FACIAL EXPRESSIONS I N THE RHESUS RIOTKEY

Fig. 4a-High iirt,orixit,y threat by a feinttle. The legs arc braced for a n attacking lunge, t,he tail held straight out with the tip curling down. The eyes are wide open, the chili is thrust forward and t’hemouth slight.lyopen. Tho head here is at the upwards end of’ a jerk. The hair over the shoulders is on eiitl.

Pig. 4b-The same animal threatening from a sitting position. The head is being jerked down towards the camera, and the inouth is here open more widely, to show tho lower teeth. The rest of the body has not been moved from its previous sitting position, the toes are clenclied because the ground is cold.

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Pig. 4c-Theateiiing ill self defence. The limbs are braced d to turn away, and the body is bent a ~ ~ already 1)artly turricd from the attacker. The head is pulled back into the shoulders, the tail is low, and the hair is 1)artly raised.

Fig. 4d-Threatening, showing the (‘ scanclttlised ” expression, by a fairly frightened animal. The head is being jerked up and back, eyes very wide open, eyebrows somewhat raised. The chin and mouth corners are thrust forward and t,he mouth is not opened very widely. The hair is on end.

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Fig. Sa-Branch

R. A. H W D E AND T. E. ROWELL

shaking by a dominant male : The feet grip the branch as he throws hiinsolf up and dowii, and the tail is held out horizoutally, perhaps for balance.

Fig, Sb-Another

male ( ‘ branch shakes

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by pulling a t the chains supportiug thc branches.

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Similar behaviour has been recorded by Carpenter (1940) in gibbons and by Nolte (1955) in Macaca radiata and (1958) Cebus upellu. Baboons are said by Darwin (1872) to show their anger by striking the ground repeatedly with one hand, but this appears to be part of a direct threat at a rival (Bolwig, 1959) ; a similar movement sometimes accompanies threat in rhesus monkeys. (vi) Bouncing Like branch-shaking, this is also a variable movement. Usually it consists of a series of jumps on the same spot, the animal taking off from the legs and landing on its hands. The tempo is slower than in branch-shaking-about once or twice a second. The back is usually convex. One male uses a quite different technique-he braces himself across the window aperture with one arm and one leg nearly horizontal and moves his body backwards and forwards by flexing and extending the limbs in turn. Bouncing is less common than branch-shaking, but seems to occur in generally similar situtations. As seen by us it has always taken place on a stable surface, and this may well account for the differences from branchshaking.

C. Fear (i) Looking ebewhre When confronted with an alarming object, a monkey will often sit in a normal posture but deliberately avoiding looking at it-the animal stares attentively in practically every direction except that of the object. The lips are usually tighly compressed and the mouth may be pulled back at the corners. (ii) Frightened grin The characteristic feature here is the retraction of the lips and cheeks so that the teeth are exposed and deep furrows appear on the cheeks. In the initial stages the lips are together, but the corner of the mouth drawn back. Next the lips are parted but the teeth are not separated, the retraction of the lips revealing a rectangle of incisors (Fig. 6a). In its more extreme form the mouth is opened and the lips are retracted even further, the teeth and gums remaining exposed (Fig. 6b). With marked grinning the ears are usually flattened and the head drawn back on the shoulders. The frightened grin appears in situations where there is an inhibited tendency to flee. When one animal is being attacked it will often flee and then crouch and give a frightened grin. Animals who are frightened while isolated from their companions, and animals being offered food but afraid to come for it (through fear either of the offerer or of a dominant monkey in the pen) will grin. A marked frightened grin is often accompanied by squeaks. In the apes, a somewhat similar expression, involving retraction of the lips and drawing up of the cheeks, is apparently indicative of pleasure. It appears in friendly greeting or while the animal is being tickled (e.g. Darwin, 1872 ; Kohler, 1925 ; Foley, 1935 ; Carpenter, 1940 ; Hayes, 1952 ; and others). Apes also have another expression in which the lips and cheeks are retracted, which is given in situations of fear and anger. From the drawings of chimpanzees by Kohts (1935) it would seem that the teeth are exposed much less in the

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pleasure smile than in the fear one. Ambrose (1960) points out that the similarities between them are greater at low intensities, and suggest an evolut,ionary relationship between them. Although Darwin (1.c.) mentions an expression of this type being given in pleasurable situations by Cebus monkeys and by the Barbary ape ( M . sylvana), we have not observed this in the rhesus moilkey. Since the frightened grin is often given on the approach of a dominant animal, it may appear to be (and may perhaps evolve into) an expression of greeting. Greeting, in fact, may usually involve an element of fear. Miller, Nurphy & Mirsky (1959) have shown that a picture of a frightened monkey is sufficient t o induce fear in another animal, as indicated by the number of conditioned avoidance responses (bar pressing) given. They do not give details of all the pictures which they used, but some seem t o have included the frightened grin. (iii) Showing neck The head is turned up and away from the monkey at which the posture is directed, with the neck elongated and exposed towards it. This posture, seen fairly often as an invitation to groom, also occasionally appears during aggressive encounters between females, when it seems to show submission.

(iv) Locomotion in fear \S’hen an alarmed animal is moving about the run, its tail is usually carried below the horizontal and it walks with its legs slightly bent so that its belly is nearer the ground than usual. The ears are back and the lips rather tightly pressed together. As fear increases, the animal crouches lower and may give a frightened grin. This may lead to the position of crouched fear (v. supra). When a subordinate monkey is approaching one of its superiors, it often edges t oaards it sideways on or even backwards, avoiding facing it directly.

D. Friendly behawiour (i) Initiation of grooming In all our groups, much of the time is spent in grooming. Although any nionkey in a group may groom any other, grooming is much more frequent hetween some pairs than between others. In particular, the favourite wife spends much of her time grooming the male, and he sometimes grooms her. The other females groom each other, the subordinate grooming the superior more than vice versa. h i invitation to groom usually entails one animal lying with its back towards the one who will groom it, or sitting in a rather stiff position beside the other, exposing part of its body to be groomed, and with the face turned away. If these methods fail, the animal which is inviting grooming will sometinies mount the other, who then turns and grooms it. (Fig. 7a). The animal which is being groomed is often slapped and pulled about by the grooming animal, but, very rarely objects. It changes position at intervals, hritiging a new part, of its body forward.

POSTURES AND FACIAL EXPRESSlONS I N THE RHESUS MONKEY

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14

Fig. 7tJ-.i

IIIHIC) asks to be grooinetl. Sotc tlitrt the face is again turned away from tlitt gruo~ilur. This chest exposing posturc is accompanied by a spccial growl.

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One of our males often invites grooming from familiar humans, usually by throwing his head up and exposing his chest near the wire (Fig. 7b). Others occasionally do likewise. A female, which had been hand-reared, grooms us rather than inviting grooming. (ii) Lipsmacking When one animal is grooming another, and especially when starting a grooming bout, it sometimes makes kissing movements by rapidly separating its lips and bringing them together again repeatedly. The lips are protruded (Fig. 8a). This lip-smacking usually occurs during active grooming, when the groomer is staring closely at the fur in which its hands are moving. The lip-smacking movements are made in short bursts which are usually unrelated to the transfer of particles into the mouth. Sometimes, however, they are accompanied by eating movements. Lip-smacking occurs in a number of social contexts which do not involve grooming. In such cases the eyebrows are raised, the ears are right back and the eyelids slightly lowered. The head is directed towards or obliquely to the object, and the chin is raised. In most of these features there is considerable variation, the correlates of which have not yet been fully worked out (Fig. Sb). The situations in which lip-smacking occur are diverse, but always involve positive social advances to another individual : this is often combined with slight fear. Here are some examples : lip-smacking by an established male to a newly-introduced female ; an established female to a newly-introduced juvenile ; by a slightly frightened monkey being offered food (to the offerer); by males to females in an adjacent run ; and by females shut out alone in the outside run and confronted with a frightening object, to their group mates which they could see through the window. If the individual or object which is eliciting the fear is also a socially desirable one, then the lip-smacking may be directed towards it, as in the case of an animal being offered food and lip-smacking to the offerer. In many of the examples cited above, however, the lip-smacking is elicited in the presence of a frightening object towards a different and non-frightening but socially desirable object-as with a female, isolated from her pen-mates and confronted with an experimenter in a grotesque mask : this animal lip-smacked to a familiar observer sitting outside the end of the run. Similarly, a mother isolated with her six-week old baby and confronted with the same situation, lip-smacked to the baby. The range of fear over which lip-smacking may appear is considerable. In the case of a male making advances to a newly introduced female, fear must be insignificant, but some of the isolated females lip-smacking to their group companions were very frightened. Since lip-smacking is more often given by an established monkey to a new-comer than vice versa, since it is sometimes associated with threat postures, and since it has been seen to intergrade with chewing (see below), it is possible that it may also involve an element of slight aggression. As a consequence of the wide range of fear which may accompany lip-smacking, it may alternate with a variety of other postures-the

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frightened grin, scandalised expression, looking away, chewing and lowintensity threat. When lip-smacking is given by an established male to a newly introduced female, and also when i t is given at the start of grooming bouts, it seems to have the effect of reducing fear. In the first case the male lip-smacks as he walks away from or laterally to the female, with his head turned back towards her ; or backs away from her, ears flattened, chin up and tail very high (Fig. 8b). Sometimes this is elaborated into a sort of dance in which the male goes a yard or two away from her in this fashion, edges back again, and then repeats the performance. lye had the impression that this caused a reduction in the frightened grinning on the part of the introduced female, and sometimes induced her to follow him. N'hen lip-smacking is given by frightened animals to their superiors, i t seems also to have the effect of reducing aggression. Carpenter ( I 94.2)implies that lip-smacking is characteristic of the " oestrous " period, but we found no evidence for this. Gestures resembling the lip-smacking of the rhesus monkey occur widely in other primates. Darwin (1872) records a similar movement made by an Anubis baboon (Cynocephalw anubis) during a reconciliation with its keeper. In the Chacrna baboon lip-smacking occurs during copulation-as the female solicits she looks over her shoulder and smacks her lips to the male and he does likewise at he approaches and mounts. Tame animals of this species frequently lip-smacked to their keeper, again in association with presenting (Bolwig, 1959). This author also records that he was able to calm an excited Vervet (Cercopitkecus acthiops) by lip-smacking to it. In Howler monkeys (Alouatta palliata) copulation is preceded and accompanied by rhythmic tongue movements (Carpenter, 1934) but the relation between this and lip-smacking is not clear. (iii) Presentation and mounting When presenting to a male the female stands with her hindquarters directed to him, legs fairly extended and arms either extended forwards or slightly bent. The tail position is variable but it is always held so as to expose the vulva. The female's head is often turned round to watch the male. Mounting may be initiated either by the male or by the female. In the former case, the male approaches the female, who then usually presents. If she fails to do so, he may pick up her hindquarters in his hands and then copulate. Occasionally a male will gently bite a female who fails to present, anti she will then do so. The female can prevent the male moiinting by sitting down, or moving away. If the female initiates she does so by edging towards the inale and then turning round and presenting to him. In mounting, the male places his hands on either side of the female's chest or hips and his feet beside her back legs or, more usually, on her heels. The female sometimes makes short rapid contractions and extensions of her arms while being mounted. She may also look up at the male, or reach back along her body with her arm. Nost mountings do not lead to ejaculation. (Fig. 9) (see Carpenter, 1942, for further details). Presentation often occurs without subsequent mounting. For instance, when a female is approaching a male she may edge a little way towards him,

POSTURES AND FACIAL EXPRESSIONS 1N THE ItHESUS MONKEY

Fig. Xa-A €emale lipsmacks as she grooms one of us through the wire of the cage. In this instance the mouth is protruded slightly, but the lips are not much pursed. The eyes are fixed on the working fingers.

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Fig. 8b--4 male lipsmacks to a newly introduced female. The mouth corners are pushed well forward and the lips rather pursed. Note also the raised chin, half-lowered upper lids and very flattened ears. He is " dancing " to the female (see text) and looking a t her face.

Fig. 8c-The same male lip-smacking to a strange female, having walked away and then turiied to face her. The tail posit.ion is atypical because he is turning against the wire, and should be curled up over his back. Note t.he raised chin, rounded lips, and flattened ears.

It. A. HINDE AND T. E. ROWELL

Fig. 9 4 o p u l a t i o n : The female’s position is atypical since she is holding onto the side walls rather than standing foursquare. Her head is turned slightly up towards the male. The position of his tail is characteristic of the dominant male.

Fig. 1 1-Yawning occuis frequently duriiig bouts of threatening betweell males in adjacent cages. I t provitlrs an impressive display of the tusks which may have a secondary intimidating effect.

Fig. 10-Slow pacing. Note the male’s long rather stiff stride, and the tail position typical of the dominant animal.

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present, come a little closer, present again, and so on. If the male takes no action, she may eventually settle down beside him and groom him. Sometimes it is the male who initiates grooming as she sits beside him. Zuckerman (1932) suggested that presenting by baboons in similar contexts represents incipient flight responses, given in situations in which the animal is dominated. Carpenter (1942) also indicated that presentation may have a number of non-sexual functions-it may serve as a greeting gesture, as an expression of affinity, or to deflect the aggressiveness of a dominant animal. Chance (1956) states that it expresses the acceptance of dominant and subordinate status by the two animals, and he also supports the hypothesis that it is an expression of affinity. I n our own colony we have frequently observed that an animal which was being attacked by its companions seemed to be directing its hindquarters towards the attackers, but this was always accompanied by actual fleeing and/or elements of threat, and did not lead to a full presentation posture. We found no evidence that presentation functions to deflect an attack which has already started. Presentation and mounting were, however, associated with aggression in other ways. For instance, mounting was especially likely to occur during threatening bouts between the groups in neighbouring pens. Further, both sexes sometimes threatened other individuals or the observer as a means of inciting the partner to mate. The occurrence of mounting is also related to the dominance relations of the individuals involved ; of the three pairs in which we have seen mounting of a male by a female, in one case the male was sickening and in the other two the females were at the time special favourites of the male. Mountings of female by female are not uncommon and it is usually the dominant female who mounts the subordinate one, but this is not always the case and mountings sometimes occur in both directions in succession. In any group of females, each animal tends to have a preferred partner in mounting (see Carpenter, 1942, for further data). To summarise, presentation and mounting occur in diverse social situations, but there is always a degree of affinity between the animals concerned, with dominance relations playing an important role.

E. Miscellaneous Included here are a number of activities which appear when the animals are excited in some way. They do not appear to be limited to particular situations. (i) Chewing and gnashing These include a variety of ,mouth movements such as chewing (lateral movements of the lower jaw, with grinding of the teeth) and gnashing (sharp opening and closing of the jaws). One male habitually gnashed his teeth during copulation, often in time with the pelvic thrusts. Other males often show chewing and/or gnashing movements during threatening bouts with males in neighbouring pens, and chewing has also been associated with lip-smacking. Similar observations are recorded by Carpenter (1940) for the gibbon (Hylobates lar).

20

R. A. HINDE AND T. E. ROWELL

(ii) Pacing The animal walks up and down the run in long strides, often going up to the netting and glaring over the field, or at a real or supposed enemy. If the pacing is relatively slow, the head position is normal and the tail is usually carried with its base vertical or inclined forward over the back, the tip being curled over backwards (Fig. 10). With faster pacing, the neck may be slightly retracted and the chin raised. The jaws are then slightly separated, and the ears are held back. Sometimes the teeth are ground together. The tail may be lowered to or below the horizontal : in the latter case the tip is curled downwards a little. The gait is tvypical-arms and legs are slightly splayed out, and also flicked forward in long strides. If the pacing is very fast, the animal may suddenly kick at the wire walls of the run, without stopping in his pacing ; the important thing here is probably the noise made by the kick (cf. branch-shaking). Slow pacing may occur without any outside disturbance apparent to the ohserver-though the animal may stop at intervals and glare at a particular spot across the field. Faster pacing, however, is usually a response to some disturbance outside the cage, such as the approach of strangers, or screams from monkeys in nearby runs. It also occurs during bouts of threatening between groups in adjacent runs.

(iii) Yuwning The mouth is opened wide and the head thrown backwards as the yawn reaches its climax (Fig. 11). Yawning often occurs in situations of mild stress, and especially in agressive contexts. This has also been recorded by Darwin (1872) and Zuckerman (1932) in Papio, Macaca and Cercopithecw spp., and by Carpenter (1940) in gibbons. ACKKOWLEDGMENTS

This research was supported by the Medical Research Council and the Mental Health Research Fund. We are grateful to Mr A. R. Jennings and members of the School of Veterinary Clinical Studies, Cambridge University, for help in looking after the health of our animals. REFERENCES

J. A. (1960). The smiling response in early human infancy. Ph.D. Thesis, Idondon. fk>l;wra,N. (1959). A study of the behaviour of the chacina baboon. Be/uwiour 14 : 136-163. ('\RPENTER, C. R. (1934). A field study of the behaviour and social rclations of howling monkeys. C'0,ttp. P ~ y c h o l M0-r. . 10 : (2) 1-168. ('AHPENTER, C. H . (1940). A field study in Siarn of the behaviour and social relations of tho gibbon (Hylobates lar). Cotup. Psychol. Monogr. 16 : ( 5 ) 1-205. VARPEX'TER, C. R. (1942). Sexual behaviour of free-ranging rhesus monkeys (Macaca mdatta). I. Specimens, procedures and behavioural characteristics. 11. Periodicity of oestrus, homosexual, erotic and non.conformist behaviour. J . c o n y . Psycho!. 33 : AhlBROSC,

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