Behaviour

Macaques have a variety of facial expressions which they use to communicate with conspecifics, composed of movements of the ears, brow, eyes and mouth from the neutral state.³ Facial expressions can be used by laboratory staff to infer the attention, intention and internal state of animals. However, the purpose of all macaque facial expressions is not yet fully understood. Expressions may be performed at different intensities in different contexts; there may be individual differences in how expressions appear; and an animal will often perform several expressions and behaviours together, as seen from the videos in this section. About one third of facial expressions are accompanied by vocalisation.⁴

Neutral | Affiliative | Submissive or fearful | Anxious | Agonistic or aggressive

Neutral expression

Resting facial expression, shown in calm social contexts or when resting alone. All other expressions differ from this standard facial display.

Affiliative expressions

Affiliative facial expressions are often performed together with submissive and anxious or fearful expressions, depending on the context.

A cynomolgus macaque showing an affiliative face, with ears and brow drawn back, eyes looking at the interactant and mouth puckered. (Michael Gumert)

During affiliative contact, a cynomolgus macaque lip smacks to maintain peaceful contact; his companion lip smacks in return to confirm affiliation. (Michael Gumert)

In response, the macaque on the left reaffirms his peaceful intent with a bared teeth display. (Michael Gumert)

Components of the affiliative expression

Lip smack

Lip smacking indicates peaceful intentions.⁵ It may be performed between any individuals intent on maintaining a peaceful relationship. Lip smacking is often performed during approach towards another macaque, or even human caregivers. For additional videos of lip smacking, see the RHVIDEO site.

Lip smacking from NC3Rs on Vimeo. In this video, the macaque signals its affiliative intention towards a known human caregiver by lip smacking with ears pulled back and brow raised.

Lip smacking and vigilance from NC3Rs on Vimeo. In this video, the macaque lip smacks to a conspecific whilst also being vigilant and chewing food from its cheek pouches. (Video: MRC Centre for Macaques)

Play face

Play face (Image: Michael Gumert)

Play face (Image: Claire Witham)

The play face stops rough and tumble play getting out of hand. It is seen mostly in younger animals during play. The ears and brow are pulled back, the mouth is open and the top lip is pulled over the teeth.

Submissive or fearful expressions

Grimace/bared teeth

The grimace or bared teeth display signals submission and averts possible attack.⁶ It is performed by low-ranked individuals towards high-ranked individuals; often performed by the subordinate when approached by a dominant animal. The brow is neutral or pulled back with the ears, and the teeth are exposed. The animal performing the grimace, will look towards the interactant or may turn and look away. For additional videos of the grimace, see the RHVIDEO site.

A young cynomolgus macaque performs a bared teeth display (Image: Michael Gumert)

Bared teeth display with tongue protrusion in cynomolgus macaque (Image: Michael Gumert)

A subordinate gives a bared teeth display to an approaching dominant (Image: Gumert)

Female rhesus grimaces as she turns from a dominant male (Image: Alexander Georgiev)

Grin 1 from NC3Rs on Vimeo. In this video, the macaque on the left grins towards a dominant animal approaching from the right.

Fear grin with squeak from NC3Rs on Vimeo. In this video, a female macaque grins at a group member with a squeak vocalisation. (Video: MRC Centre for Macaques)

Anxious expressions

Tense mouth

This expression signals fear and/or alarm. It may be seen in response to aggressive conspecifics, humans, startling stimuli or predators. For videos of tense mouth, see the RHVIDEO site.

Yawn

(Image: Michael Gumert)

Exaggerated yawning with full display of teeth is a threat behaviour or indicative of tension.⁷ Yawning without full display of teeth may simply be an indication of tiredness. Often shown during periods of uncertainty and tension such as unstable hierarchy.

Threat yawn from NC3Rs on Vimeo. In this video, the macaque yawns and stares at the camera operator, indicating tension. (Video: MRC Centre for Macaques)

Yawn from NC3Rs on Vimeo. This yawn is probably a ‘true’ yawn associated with tiredness, since the animal is relaxed and it’s attention is not fixed on any conspecifics. (Video: MRC Centre for Macaques)

Chin up

A macaque sits with chin up, possibly monitoring events from a sideways position (Alexander Georgiev)

Chin up is an avoidant posture that allows covert monitoring of events in the environment while avoiding making eye contact with other animals. It is seen in situations of uncertainty or when an animal has reduced escape options. Males may also approach females with chin up when soliciting for sexual behaviour.

Agonistic or aggressive expressions

During agonistic or aggressive expressions, typically the ears are forward or flapping (indicating intense interest), the brow is lowered or neutral, with eyes open and staring at the interactant, and the mouth is open (the teeth may or may not be exposed). The head may be lowered with both head and body pulled forward.

Open mouth stare

The open mouth stare is used to threaten other individuals. It is seen during tension between group members, and is often performed towards unwelcome humans.

Cynomolgus macaque stare (Image: Michael Gumert)

Open mouth stare (Image: Michael Gumert)

Open mouth stare (Image: Emily Bethell)

Intense open mouth stare (Image: Emily Bethell)

Open mouth threat from NC3Rs on Vimeo. A mother suckling her infant threatens the camera operator with an open mouth stare expression. (Video: MRC Centre for Macaques)

Open mouth grunt from NC3Rs on Vimeo. Examples of two different responses to an intruder. In this video, the macaque on the left lowers its brow, flaps its ears, and moves away – signs of tension or annoyance. The younger, bolder animal on the right comes forward and shows an open mouth stare expression, before also moving away from the camera operator.

Piloerection

Piloerection in a male rhesus macaque (Image: MRC Centre for Macaques)

Piloerection in a cynomolgus macaque (Image: Michael Gumert)

Piloerection during aggressive interaction (Image: Michael Gumert)

Piloerection⁸ is a reflex arousal response in which the macaque’s hair stands up, making it look bigger, triggered by negative situations of extreme fear or anger. Piloerection typically occurs in highly arousing situations, such as the appearance of predators, humans or aggressive conspecifics.

Head-cock

Head-cocking⁹ is thought to help non-human primates observe objects from different angles, allowing them to encode the parameters during learning.¹⁰ It is often observed in youngsters when viewing novel objects.

Crouch

Cynomolgus macaque crouching, with bared teeth (Image: Michael Gumert)

Crouching before an aggressive encounter (Image: Michael Gumert)

Crouch signals a readiness for action. It is seen in situations causing fear, such as the presence of predators or aversive stimuli. Crouching can also be seen before and after aggressive encounters with conspecifics.¹¹ Crouching may be accompanied by pant threats, screams or barks depending on the context (see the Vocalisations tab). For videos of crouching, see the RHVIDEO site.

Freeze

Freezing is a fear response to predators, aversive stimuli or unexpected noise. For videos of freezing, see the RHVIDEO site.

Tail up

Tail up posture in rhesus macaque (Image: Prabal Sarkar)

An erect tail signals alertness and is often seen in animals exerting their dominance over conspecifics. It also accompanies sexual presentations.

Tail wave

Tail wave is seen in affiliative contexts, such as females playing with infants. The tail waves from side to side, with small or large movements.

Postures are also important in the recognition of agonistic/aggressive and affiliative behaviours (see the Expressions and Social behaviour tabs above).

Postures of rhesus macaques (Sade 1973)

A to B – Movement from a high to a low position, indicating threat. An attack by a confident animal may begin with a bobbing of the head accompanied by an open mouth directed towards the victim, grade into a lunging of the shoulders toward the victim, and finally become a charge ending when the dominant individual bites the victim.
C and D – Examples of subordinate posturing. The victim of an attack may attempt to present its hind quarters and grimacing face towards the attacker simultaneously, so that the animal’s body is displayed laterally to the attacker.
E to F – Upward jerking of the head, seen during non-hostile, non-fearful encounters. The upward jerking display may frequently be accompanied by protrusion and smacking of the lips.
G – Neutral sitting posture.
H – One individual of a wrestling pair. Rotation of the head and torso is often seen during wrestling play behaviour.
I to L – Oblique bobbing movements of a querying animal, often directed towards other monkeys, humans or novel objects. The open mouth face of the monkey in figure K indicates an aggressive component.

(Adapted from Sade 1973) 

Macaques have a wide repertoire of vocalisations used in a variety of social contexts.

Rhesus macaques | Cynomolgus macaques

Vocalisations of rhesus macaques

Affiliative vocalisations

These vocalisations signal peaceful intentions and help maintain contact with group members. They are used when approaching higher-ranked animals and infants, approaching to groom another animal, and during group movements.¹² They often accompany lip smacking (see the Expressions tab).

Coo

Around 400 ms in duration, coos are characterised by their harmonic structure. They are relatively quiet calls, with a variation on an OOOH sound.

Spectogram for coo vocalisation

Grunt

Around 200 ms in duration, grunts are characterised by their noisy, time modulated structure.

Spectogram for grunt vocalisation

Girney

Girneys are high-pitched, soft, sing-song vocalisations used by adult female rhesus macaques to establish friendly contact with infants which are not their own offspring.¹³

Threatening vocalisations

These vocalisations are used to signify dominance to lower ranking animals, to enhance visual signals during aggressive, threat displays (see the Expressions tab above), and to scare away potential threats, such as predators.¹⁴

Bark

Often the animal will have its head down and ears back, suggesting a degree of fear within the threatening situation.¹⁵

Pant-threat

Around 300 ms in duration, pant threats are characterised by their noisy and threatening sounding structure. They are often seen with head raised and ears forward, suggesting increased intention to attack. 

Spectogram for pant threat vocalisation

Submissive or alarm vocalisations

These vocalisations may be involuntarily produced as an immediate reaction to surprise, in response to pain or fear, or to appease aggressors. They are given to aggressive or dominant animals, potential threats, and/or alarming or painful stimuli.

Squeak / Alarm call

Often heard in conjunction with grimace (see the Expressions tab), crouch (see the Postures tab) and retreat.¹⁶

Screech, scream and squeal

Loud, high pitched calls, often heard in conjunction with grimace (see the Expressions tab above), crouch (see the Postures tab above) and retreat.

Other vocalisations

Warble, harmonic arch and chirp

Around 500 ms in duration, warbles, harmonic arches and chirps are characterised by their harmonic and contoured frequencies that increase toward the middle or end of the call. They are possible food calls, given when high-quality, rare food items are found. 

Spectogram for harmonic arch vocalisation

Gecker

Geckers area made by infants during weaning, when mothers refuse attempts to nurse.¹⁷

Copulation call

In macaques, both males and females can produce vocalisations during or immediately following the completion of copulation. These are more common in cynomolgus macaques than in rhesus macaques.¹⁸

Vocalisations of cynomolgus macaques

(After Palombit 1992)

Macaques are social primates and interactions with conspecifics are an important part of their daily lives. Social behaviour varies with sex, age, reproductive status and dominance rank.²⁶

Affiliative | Sexual | Agonistic and aggressive | Submissive and fearful

Affiliative behaviours

For affiliative facial displays and vocalisations, see the Expressions and Vocalisations tabs above.

Allo-grooming

One animal picks through the hair of another with hands or teeth, removing skin, dirt or ticks.²⁷ Allo-grooming is used to develop and maintain bonds between individuals. Females form stable life-long attachments, maintained through grooming, touch and close proximity.²⁸ Males groom females more during the mating season.²⁹ Macaques may groom after conflicts to console each other or repair damaged relationships.³⁰ Both giving and receiving grooming releases B-endorphins; after conflict situations, these may reduce pain from injury and relieve stress more quickly.³¹

Female grooms male from NC3Rs on Vimeo. Allogrooming of the male’s back by a female.

Grooming at night from NC3Rs on Vimeo. Female rhesus macaque grooms its group mate whilst resting together at night. (Video: Claire Witham)

Affiliative contact

Rhesus macaques sleeping in close contact (Alexander Georgiev)

Macaques often rest and sleep huddled in family groups; they will also huddle when under threat. In behavioural studies, affiliation is often measured as proximity (e.g. within an arm’s reach of each other), because macaques that are friendly with each other will remain close, to maintain bonds and provide assistance if needed. The neuromodulators oxytocin and serotonin are implicated in development and maintenance of social behaviours such as approach and close contact.³² These contribute to a sense of security from being close to conspecifics and have health benefits, such as maintaining low heart rate.

Present for grooming

An animal will approach or reposition itself in front of another, presenting an area of the body to be groomed. Typically seen during peaceful contexts, or by individuals seeking comfort after a fight.

Present for grooming from NC3Rs on Vimeo. In this video, a macaque presents its tail for grooming by another group member. (Video: MRC Centre for Macaques)

Play

Mostly seen in infants, juveniles and adolescents. Play develops social bonds and motor-coordination skills, allowing younger animals to develop and assess their relative strength to peers. There are sex differences in play: females engage in more play with infants and older females; males engage in more rough-and-tumble play.³³ Adult males may engage older juveniles in play.³⁴

Infants playing 1 from NC3Rs on Vimeo. Two infant rhesus macaques, playing on the forest floor.

Solitary play from NC3Rs on Vimeo. In this video, a young cynomolgus macaque plays by himself.

Infant care and handling

Infant care is performed mainly by nursing mothers during the birthing season. However, other group members are very interested in new infants. Looking after the infants of higher ranking females, either by a low-ranking female or male, will help improve their standing with the mother. The mother-infant bond in macaques is strong, and mediated by oxytocin released during birth and lactation throughout the first year of life.³⁵ It is important that infants are not removed from the mother before natural weaning has occurred, as this will lead to social attachment problems later in life.³⁶

Male taking care of infant from NC3Rs on Vimeo. In this video, a large adult male cynomolgus macaque cradles an infant. (Video: BFC)

Sexual behaviours

Genital present

Male cynomolgus macaque inspects female (Image: Michael Gumert)

When in oestrous and proceptive, a female will present her rump to the male to solicit copulation.³⁷ Outside of mating, both males and females may present their rump as a signal of subordination.³⁸

Mount and copulate

Reproductive behaviours are triggered by seasonal changes in sex hormones (e.g. oestrogen, testosterone). These may be accompanied by reddening of sexual skin on the face, genitals and rump. Mating is highly seasonal in the wild.³⁹ In captivity, mating seasons may be less pronounced.

Rhesus macaque copulation from NC3Rs on Vimeo. (Video: Alexander Georgiev)

Agonistic and aggressive behaviours

See also the Postures tab above.

Displacement

Displacement most often occurs during competition for valued resources such as food, mates, shelter and good resting places. The dominant animal approaches a subordinate, who then moves away to avoid potential conflict. Dominant animals exert their dominance in subtle ways, which helps to conserve energy. In captivity, distributing resources so that they cannot be monopolised by dominant animals reduces stress for subordinates.

Displacement by alpha male from NC3Rs on Vimeo.

Displacement of older animal from NC3Rs on Vimeo. (Video: MRC Centre for Macaques)

Displacement from NC3Rs on Vimeo.

Aggressive approach

Approaching with staring face and an aggressive stance, including lunging with the tail up, are signs of dominance. Aggressive approach is typically performed by a dominant animal towards a subordinate.

Approach from NC3Rs on Vimeo. In this video, a dominant animal approaches a subordinate with high posture and tail up; the subordinate then runs away.

Chase

Dominant animals will chase lower ranked animals away from resources where there is high competition, and use aggression to gain access.

 

Chase into the sea from NC3Rs on Vimeo. Rhesus macaques on Cayo Santiago, showing low ranked animals being chased into the sea.

Slap ground

Threat action, often accompanied by open mouth stare. For videos of slap ground, see the RHVIDEO site.

Lunge

Threat action

Big male foraging from NC3Rs on Vimeo. In this video, the alpha male lunges at members of his group in order to move them away from food he wishes to take for himself. (Video: BFC)

Branch shake

Size and aggression display to drive away potential threats. Most frequently given by males in response to other males, humans or perceived threats. In captivity, macaques will sometimes shake the home cage structure.⁴⁰

Shaking platform from NC3Rs on Vimeo. An adult male rhesus macaque shakes a resting platform is a display of strength. (Video: MRC Centre for Macaques)

Dominant mount

An animal may exert its dominance over another by mounting it. Dominant mounting often occurs during tense situations, as dominant animals seek to re-affirm the hierarchy.

Push, Grab, Fight/Wrestle, Bite, Hit

Physical contact behaviours which can result in injury only occur when aggressive interactions cannot settled by non-contact means.

Push from NC3Rs on Vimeo. In this video, a rhesus macaque female playing with water in a pool repeatedly pushes away a smaller member of the group.

Aggression over food from NC3Rs on Vimeo. The macaque on the left attempts to grab food from the feeding animal on the right. (Video: MRC Centre for Macaques)

Flighting cynomolgus macaque males (Image: Michael Gumert)

Stare

Threat action

Staring from NC3Rs on Vimeo. Rhesus macaques resting together on a raised platform begin to stare at the camera operator. (Video: MRC Centre for Macaques)

Submissive and fearful behaviours

For submissive facial displays and vocalisations, see the Expressions and Vocalisations tabs above.

Avoidance

Subordinates will avoid or move away from dominant or aggressive animals, to avoid physical contact which may result in injury.

Rump present

Rump present indicates submission, performed by subordinates towards dominants.⁴¹ Females may also present their rump to males to solicit copulation.

Lean away

During potentially threatening social situations, macaques may lean away from a conspecific to avoid physical contact which may result in injury. For video of lean away, see the RHVIDEO site.

Look away

Look away from NC3Rs on Vimeo. A macaque turns its back to hide its face from another animal. Dominant mount is also seen in this video.

Flee

Foremost animal flees from an aggressor (Image: Michael Gumert)

Flee is a fear response in which a macaque runs away from a perceived threat. Seen during aggressive encounters, in the presence of predators, and when surprised.⁴²

Freeze

Freeze during an aggressive encounter (Image: Michael Gumert)

Freeze is a response in which a macaque stops all activity and remains still while assessing threat. Seen during aggressive encounters, in the presence of predators, and when surprised.

Foraging/eating

Macaques are highly food motivated. In the wild they spend 20-40% of their day foraging for food, with variance between species and seasons.⁴³ In captivity, macaques will work harder to obtain preferred foods; they also value rewards that are hard to obtain.

Cynomolgus macaque using stone tool to open oyster embedded on rock (Image: Michael Gumert)

Rhesus macaque cracking open coconuts on a concrete jetty (Image: Alexander Georgiev)

Juvenile rhesus macaque foraging in deep litter, with full cheek pouches (Image: MRC Centre for Macaques)

Feeding competition in a large group of rhesus macaques (Image: Alexander Georgiev)

Juvenile rhesus macaque feeding on fresh seaweed (Image: Alexander Georgiev)

Foraging on forest floor from NC3Rs on Vimeo. These cynomolgus macaques foraging on the forest floor on Tinjil Island, Indonesia, call to each other to maintain peaceful contact.

Foraging and vigilance from NC3Rs on Vimeo. These rhesus macaques foraging for small seeds and grains within the wood shavings continually monitor their surroundings. Note their position either side of the wooden visual barrier. (Video: MRC Centre for Macaques)

Locomotion

In the wild, over 20% of the day is spent moving between foraging and resting sites and approaching and avoiding other macaques.⁴⁴ Macaques are opportunists that have adapted to live in a greater range of habitats than any other primate except man. Daily path length varies from 1-3.5 km depending on the habitat.⁴⁵

Self-grooming/scratching

Self-grooming (also called auto-grooming) aids an animal in maintaining its own health, without relying on a conspecific. Excessive self-grooming or scratching is a sign of underlying stress (see Behavioural signs of poor welfare). Grooming removes parasites and dirt or attends to wounds.

Self grooming from NC3Rs on Vimeo.

Inactive/sleeping

Wild macaques rest for around 17-26% of the day, with some seasonal variances.⁴⁶ It is important to allow macaques time to rest, and to not continually stimulate them in captivity. Macaques rest after periods of activity such as foraging and socialising.

Resting contact call from NC3Rs on Vimeo. These cynomolgus macaques are resting in the trees. The macaque on the right makes a coo call in response to a coo from another group member.

Resting from NC3Rs on Vimeo. (Video: MRC Centre for Macaques)

Stand

Being alert in social situations prepares an animal to move away quickly or towards something. It also aids in making them look larger and more threatening, and can allow for a better view of conspecifics, humans, or the surrounding environment.

Foraging and standing alert from NC3Rs on Vimeo. (Video: MRC Centre for Macaques)

Vigilance

Vigilance helps macaques to avoid predators and keep an eye on the activity of conspecifics and other animals. It is often noticeable in foraging and resting animals.

Vigilant while feeding from NC3Rs on Vimeo.

Pay attention from NC3Rs on Vimeo. Watch what happens to one of these macaques whose attention is solely focused on grooming the infant.

Swimming and diving

Swimming and diving have multiple purposes in macaques. They engage in these activities for locomotion, play and access to food across bodies of water, as well as for foraging underwater.⁴⁷ Macaques can swim from birth⁴⁸ and will enjoy playing and swimming in water if provided with the opportunity in captivity (see the Sensory tab under Enrichment).

Dive bomb from NC3Rs on Vimeo.

Object handling, solitary play and tool use

Stone handling may enhance long-term neural and cognitive development in younger macaques, and maintain or repair neural pathways in older macaques.⁴⁹ Cynomolgus macaques have been observed using stone tools to open bivalves, nuts and sea snails⁵⁰, and to wash and rub clean certain foods, including potatoes and roots; they will also peel sweet potatoes.⁵¹ In impoverished captive conditions, a desire to manipulate objects may be manifested in manipulation of the cage fixings.

Stone handling from NC3Rs on Vimeo. (Video: Michael Gumert)

Teeth flossing from NC3Rs on Vimeo. (Video: Michael Gumert)

Abnormal behaviours in macaques can be qualitatively abnormal (those that occur in captivity but not in natural settings, such as stereotypies) or quantitatively abnormal (those that occur more/less often in captivity than in nature, such as excessive grooming, hair plucking or scratching).⁵² It is important to recognize that inactivity (doing nothing) may also be an abnormal behaviour.

Information on using abnormal behaviours to assess welfare, and preventing abnormal behaviour, is given in the Behavioural indicators section.

Hair plucking from NC3Rs on Vimeo. In this video, a cynomolgus macaque can be seen plucking and ingesting its hair.

Macaques diets are highly varied:

• Rhesus macaques eat fruits, young and mature leaves, stems, seeds, flowers, petioles, bark and roots of over 75 different plant species.⁵³
• Cynomolgus macaques are predominantly frugivorous (fruit accounts for 67%-82% of their diet),⁵⁴ but also feed on other plant parts. Foraging is typically conducted below 20 m (65.6 ft); usually around 12 m (39.4 ft) in the lower canopy, understory, and on the ground.⁵⁵ At mangroves they have also been seen to consume bivalves, shrimp and octopus.⁵⁶
• Both species feed opportunistically on grass, clay, mushrooms, invertebrates, eggs, crabs, and small vertebrates such as lizards, frogs, birds and fish.⁵⁷

Non-exhaustive list of plant species and their component parts eaten by rhesus macaques

(Adapted from Zhou et al. 2014)

Diet composition of cynomolgus macaques

(Adapted from Brotcorne 2014)

Examples of food species consumed by Burmese cynomolgus macaques

(Reproduced with permission from Gumert & Malaivijitnond 2012)

A Crown conch (Pugilina cochlidium), B dog conch (Laevistrombus canarium), C polished nerite (Nerita polita), D lined nerite (N. lineata), E miter (Mitra scutulata), F spider conch (Lambis lambis), G nerite snails skating on rocky shore, H Midas ear crassidula (Ellobium aurismidae), I firebrand murex (Chicoreus torrefactus), J ox-palate nerite (N. albicilla), K chameleon nerite (N. chamaeleon), L toothed-lip snail (Mondonta labio), M drill (Thais rufotincta), N drill (T. bitubercularis), O drills on rocky shore feeding on barnacles, P swimming crab (Thalamita sp.), Q sally light-foot (Grapsus albolineatus), R orange mud crab (Scylla olivacea), S thunder crab (Myomenippe hardwickii), T sea almonds (Terminalia catappa) cracked on the rocky shores, U a stone axe hammer left at a rock oyster bed (Saccostrea cucullata), V sea almonds fruiting, W tidal boundary of a rock oyster colony, X pandan fruit carpel (Pandanus tectorius), Y cracked pandan fruit carpel, Z small cluster of rock oysters, AA baby clam (Marcia marmorata), BB forked Venus (Gafrarium divaricatum), CC flavum heart cockle (Vasticardium flavum), DD raywheeled limpet (Cellana radiata), and EE gecko (Hemidactylus sp.).