Macaques have a rich behavioural repertoire. Being able to recognise, interpret and respond appropriately to their communication signals (such as facial expressions, postures and vocalisations) provides a good basis for refining many aspects of their care and use.The advice of a primate behaviour specialist is recommended for helping staff and animals to interact positively within the laboratory environment. For example ethograms and advice on recording behaviour, see the Behavioural indicators of welfare section.
Click here to take our quiz on macaque 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
Components of the affiliative expression
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 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)
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.
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.
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.
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.
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 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.
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.
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.
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-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 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.
Freezing is a fear response to predators, aversive stimuli or unexpected noise. For videos of freezing, see the RHVIDEO site.
An erect tail signals alertness and is often seen in animals exerting their dominance over conspecifics. It also accompanies sexual presentations.
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).
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.
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).
Around 400 ms in duration, coos are characterised by their harmonic structure. They are relatively quiet calls, with a variation on an OOOH sound.
Around 200 ms in duration, grunts are characterised by their noisy, time modulated structure.
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
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
Often the animal will have its head down and ears back, suggesting a degree of fear within the threatening situation.15
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.
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.
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.
Geckers area made by infants during weaning, when mothers refuse attempts to nurse.17
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
(After Palombit 1992)
|Call||Description / acoustic structure||Context|
|Kra19||Extremely common call, occurring in two forms. Kra-(c) comprises three or four more or less discrete sound pulses that appear on sonograms as vertical “columns”. Harsh, rasping quality.20||Appears to act as mild form of threat, but occurs in a wide variety of contexts, including agonistic interactions.|
|Kra-(a) comprises two to four separate sound pulses, similar in duration to kra-(c) but higher in frequency (pitch).||Appears to function as an alert signal, by attracting the attention of nearby monkeys to modifications in the environment. Often accompany alarm calling. Can also occur during agonistic interactions.|
|Alarm||Alarm 1 is a modification of the basic kra-(c) call, comprising three to five sound pulses.||Both types of alarm calls are performed repetitively and quite loudly by noticeably aroused and highly agitated macaques (e.g. in the presence of predators)|
|Alarm 2 sounds more tonal or “chirp-like” to humans than the alarm 1 call, probably because call energy is organized into five to eight narrow, horizontal “bands”.|
|Harr||Moderately loud call composed of five to seven sound pulses, and longer than alarm 1 call. The pulse units of the harr are not delivered plosively, hence it sounds ‘growl-like’ to humans.||Emitted primarily by juvenile macaques. Usually performed when threatened by another monkey during agonistic interactions that may or may not involve physical contact (similar to the “geckering screech” of rhesus macaques)21. Juveniles playing with each other perform harr calls, especially as play becomes rambunctious and grades into aggression.|
|Bark||Kra calls grade into barks, which vary in shrillness depending on the amount of energy in the higher-frequency range.||Associated with agonistic interactions, particularly those involving adult males. Vocal threat via barking sometimes substitutes for aggressive chasing or physical contact. Bark-kras occur in a much wider variety of contexts than barks, including intra-group agonism.|
|Krahoo||Consists of an initial, broadband and characteristically “harsh” segment (the “kra”) followed by a somewhat shorter “trailing off” of call energy in the lower frequencies (the “hoo”). The loudest call in the cynomolgus macaque repertoire. Usually performed in series with pauses in between. Kra component often accompanied by rhythmic, abrupt jerking of the head and upper body.||Performed by adult males only. Possibly functions in inter-group spacing.|
|Wraggh||Comprises both tonal and harsh components, increasing in amplitude.||Performed by both sexes and all ages when agitated. Isolated, solitary macaques perform Wraggh especially frequently, so this call may function in re-establishing social/spatial relations.|
|Scream||Loud, usually plosive vocal discharges whose total energy is distributed over a wide range of frequencies between 1 and 16 kHz. The acoustic structure varies, as with rhesus macaques.22||Performed by both sexes and all ages engaged in agonistic interactions.|
|Khreeet screech||The khreeet screech is a loud, partially tonal scream, increasing then decreasing in frequency, similar to the “arched scream” or “screech” of rhesus macaques.23. Often occurs in long, repetitive series with whimper calls.||Given by distressed and agitated young macaques (juveniles and possibly older infants) in both agonistic and non-agonistic contexts.|
|Squeal||Low-amplitude, high-pitched calls composed of multiple units of often dissimilar form and that characteristically experience marked changes in pitch||Relative rare calls. Performed by young macaques only.|
|Copulation calls||Females give a staccato “ohoh” copulation call. A weak high-pitched bleep” is also performed infrequently by males during copulations.24||Copulation|
|Coo||Relatively quiet, tonal calls.||Given when calm and not agitated.|
|Whimper||A specific, consistently heard patterning of coo call units analogous to the combining of barks to form the “pant threat” of rhesus macaques.25 Contains a distinctive, pronounced upward modulation in frequency that achieves its highest peak in the last two thirds of the call.||Performed by distressed infant or adolescent macaques, such as young juveniles left behind by their mothers. Young monkeys engaged in tantrum behaviour also perform these calls. May be accompanied by screams or khreeet screeches, to which mothers usually respond with retrieval.|
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
For affiliative facial displays and vocalisations, see the Expressions and Vocalisations tabs above.
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
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.
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
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
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.
See also the Postures tab above.
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.
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.
Dominant animals will chase lower ranked animals away from resources where there is high competition, and use aggression to gain access.
Threat action, often accompanied by open mouth stare. For videos of slap ground, see the RHVIDEO site.
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
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.
Submissive and fearful behaviours
For submissive facial displays and vocalisations, see the Expressions and Vocalisations tabs above.
Subordinates will avoid orÂ move awayÂ from dominant or aggressive animals, to avoid physical contact which may result in injury.
Rump present indicates submission, performedÂ by subordinates towards dominants.41 Females may also present their rump to males to solicit copulation.
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.
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 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.
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.
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)
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 (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.
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.
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.
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.
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).
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.
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.
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 ZhouÂ et al. 2014)
Diet composition of cynomolgus macaques
(Adapted from Brotcorne 2014)
|Location||Origin of food (%)||Proportion (%) of food categories in the diet|
|Singapore59||Natural (86) and anthropogenic (14)||44||8||7||–||41|
|Singapore60||Natural (51) and anthropogenic (49)||20.9||21||6.3||–||51.8|
|Natural (74) and anthropogenic (26)||44.8||19.6||9.7||–||28.3|
|Bali – Ubud63||Natural (48) and anthropogenic (52)||32||34||5||29||–|
|Bali – Ubud64||Natural (30) and anthropogenic (70)||25.7||14.7||–||7.5||52.1|
|Bali – TNBB65||Natural (89) and anthropogenic (11)||60||21||–||3||16|
|Bali – Uluwatu66||Natural (52) and anthropogenic (48)||32||19||–||14||35|
|Vietnam67||Natural (75) and anthropogenic (25)||15||20||1||35||29|
|Mauritius68||Natural and anthropogenic||42.2||30.8||7||2.4||17.6|
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.).
Moynihan 1976 ↩
Menzel 1980 ↩
Cantalupo et al. 2002 ↩
Hinde & Rowell 1962 ↩
Raffles 1821 ↩
Rowell 1962 ↩
Augustsson & Hau 1999; Partan 2002; National Research Council 2008 ↩
Hinde & Rowell 1962 ↩
rhesus: Massen & Sterck 2013 ↩
rhesus: Rakhovskaya 2013; cynomolgus: Gumert 2007 ↩
cynomolgus: Cords 1992 Aureli & van Schaik 1991; rhesus: McCowan et al. 2014; Demaria & Thiery, 2001; Call et al. 1999; McCowan et al. 2011 ↩
Russell & Phelps 2013; Dunbar 2010; Shutt et al. 2007 ↩
Simpson et al. 2014; Winslow et al. 2003; Chang et al. 2012; Higham et al. 2011 ↩
Hinde & Spencer-Booth 1967; Brown & Dixson 2000; Hassett et al. 2010 ↩
Wheatley 1999 ↩
Higham et al. 2011 ↩
Prescott et al. 2012 ↩
Estes 1991 ↩
Hinde & Rowell 1962; Wallen et al. 1984 ↩
Rowell, 1963; Dunk, 2013 ↩
Hinde & Rowell 1962 ↩
Maestripieri 1999 ↩
Hinde & Rowell 1962 ↩
Dunbar 1989; Benavides et al. 2007 ↩
Nahallage & Huffman 2008, 2012 ↩
Gumert et al. 2009 ↩
Bruce 1988 ↩
Erwin & Deni 1979 ↩