Other than overt physical clinical signs, ‘behaviour’ is the most readily accessible and commonly used index for assessing an individual animal’s welfare, but perhaps the easiest to misinterpret without contextual and specialist knowledge. In order to use behaviour as an indicator of animal welfare, normal behavioural patterns for the species and the individual need to be defined first as a reference point. Animals can then be monitored for any changes in behaviour.
Relatively few clear behavioural indicators of good (positive) welfare in the laboratory have been evaluated. Generally, macaques with good welfare will appear relaxed, even if there are social tensions related to bids for dominance. They will spend much time grooming, resting in body contact and foraging, and the group as a whole will not appear tense or nervous. See the Behaviour section for more information on normal behaviour for macaques.
Behaviours that may indicate poor welfare in macaques
Behavioural changes that may indicate poor welfare include: a restricted behavioural repertoire; an abnormal time budget; inappropriate social behaviour; and other abnormal behavioural patterns. Examples of behaviours in each category are given below.
|A restricted behavioural repertoire||Failure to make full use of the environment|
|Cessation of foraging or locomotion|
|Little curiosity towards novel objects|
|Little or no vocalization|
|An abnormal time budget||Restlessness or hyperactivity (e.g. circling)|
|Decreased activity (lethargy)|
|General inactivity or unresponsiveness|
|Excessive eating (hyperphagia)|
|Psychogenic excessive water drinkingÂ (polydypsia)|
|Inappropriate social behaviour||Increased aggression to conspecifics|
|Excessive fear towards or withdrawal from conspecifics (e.g. hiding at the back of the enclosure, hiding within or behind enclosure furniture)|
|Over grooming or hair plucking of conspecifics leading to hair loss|
|Failure to mate|
|Killing or neglect of young|
|Change in behaviour towards human handlers (e.g. increased aggression or withdrawal)|
|Change in the behaviour of cage-mates towards the individual animal|
|Other abnormal behavioural patterns||Postural stereotypy* (e.g. saluting/floating limb, head tossing and rocking)|
|Locomotor stereotypy (e.g. excessive pacing, weaving, circling and somersaulting)|
|Self harm behaviours (e.g. biting, eye poking, hair plucking)|
|Consumption of faeces (coprophagy)|
|Teeth clenching or grinding (bruxism)|
Retreat to the back, upper portion of the cage, alarm vocalisations, defensive threatening and aggression, physical resistance to handling, urination and defecation, indicate fear and distress.
Stereotypies and self-harm behaviours
Stereotypies and self-harm behaviours are repetitive and/or harmful behaviours or postures only observed in captivity, often arising in response to an abnormal environment (e.g. a lack of choice, control, and opportunity to express species-specific behaviours1 These behaviours are signs of negative well-being, since they indicate an attempt to cope with chronic stress2 and may be accompanied by physiological changes, particularly an elevation in cortisol (the hormone released by the adrenal gland in response to stress).3
If a captive macaque shows stereotypical or self-harm behaviour, this indicates that the physical and/or social environment is substandard and action needs to be taken to attempt to improve well-being.4 It is important to conduct regular monitoring of animals in order to catch the signs of stereotypies and self-harm behaviours early, since it is more difficult to stop these behaviours once they have become well established. Determining the trigger for performance of abnormal behaviour will aid in its management (see the Preventing abnormal behaviour tab above).
|Specific stereotypic and self-harm behaviours may develop under specific conditions. For example, self-hugging and digit sucking are typically seen in macaques which have been:
Stereotypies and self-harm behaviours may also arise from:
Not all animals experiencing these triggers will develop stereotypies and self-harm behaviours.
Other factors which can affect the development of stereotypies and self-harm behaviour (or learned helplessness) include:
Depressive-like behaviour has been reported in singly- and socially-housed rhesus and cynomolgus macaques, sharing similarities with human depressive symptoms.10 Depression and learned helplessness11 are characterised by a lack of responsiveness to stimuli and may be easily mistaken for ‘resting’ by an untrained member of staff.
|Human major depressive disorder DSM-IV criteria and verbal reports||Macaque depressive-like profile. Daily life home cage observations|
|1. Depressed mood||–|
|2. Decreased interest or pleasure in most activities||
Decreased investigation, maintenance, social behaviours, behavioural diversity
Increased gaze and body orientated toward the wall, location in the back of the cage
|3. Decreased or increased weight/appetite||Decreased feeding|
|4. Insomnia or hypersomnia||Increased inactivity|
|5. Psychomotor agitation or retardation||Decreased locomotion, poorer posture and location diversity|
|6. Fatigue or loss of energy||Increased inactivity while slumped|
|7. Decreased ability to concentrate or indecisiveness||CANTAB testing|
|8. Feelings of worthlessness/inappropriate guilt||–|
|9. Recurrent thoughts of death||–|
Adapted from Camus et al. 2014.
If behavioural abnormalities develop, the underlying cause should be identified immediately by examining housing and husbandry practices, experimental procedures and their outcomes, and all human-macaque and macaque-macaque interactions, and then modifying these as required using the guidance in this website and the scientific literature. Positive reinforcement training techniques have been used successfully to reduce the incidence and severity of abnormal behaviour.12 See Behavioural management on the Habituation & training page under Husbandry.
Strategies for preventing the development of abnormal behaviour:
- Housing animals in socially harmonious groups or pairs and monitoring pair/group stability (see the Social enrichment tab)
- Weaning animals at an appropriate age and level of development (see Life history) and into appropriate social groups
- Providing a varied and stimulating physical environment with good environmental enrichment
- Providing an adequate and varied diet to stimulate natural foraging behaviour (see the Feeding tab)
- Providing animals with appropriate habituation to environmental stimuli and training (see the Habituation & training tab)
- Ensuring sympathetic and positive human-macaque interactions
- Avoiding breeding from animals that show persistent abnormal behaviours
- Monitoring behavioural patterns of individuals carefully so that any adverse changes can be detected early (see the Recording behaviour tab above), and modifying husbandry and care accordingly
- Reviewing records regularly and identifying appropriate action points
The first noticeable response to a stressor in macaques is often a change in behaviour. Staff should therefore be trained to understand the welfare implications of changes in behaviour (see the Signs of poor welfare tab above) and to know the basics of how to record behaviour using a robust, scientific approach. This can help improve staff engagement and job performance.13
Creating and using an ethogram
Creating an ethogram to measure the behaviour of your animals will help you to:
- Learn species-specific behavioural repertoires
- Understand the behaviour of individual animals, and the group dynamics
- Identify animals most suitable for training, breeding and scientific procedures
- Monitor responses to husbandry and scientific procedures
- Detect changes in behaviour quickly (including early warning signs of stress)
You do not need to record ALL behaviours. Only record the behaviours you are interested in looking at changes in:
- Devise a list of the behaviours relevant to your species; this may include those identified in published papers, on this website (see Behaviour), in videos, or those you have personally observed.
- The behaviours in an ethogram are usually defined to be mutually exclusive and objective, avoiding subjectivity and functional inference as to their possible purpose.
- Provide a brief description of these behaviours.
- Beside each listed behaviour, add a symbol or letter which is easily identifiable with that behaviour.
To test that the ethogram is reliable:
- Make sure that everyone who will record behaviour is familiar with the list and agrees with the explanation for each behaviour.
- Conduct group scoring sessions in which staff watch and discuss the behaviours (in real time or from video . Do this until staff are confident in identifying the behaviours in the ethogram.
- Test for inter-observer reliability to ensure that everyone is identifying and measuring behaviour in the same way.
Examples of ethogram / behavioural categories for macaque species
Each of these ethograms has been designed according to species, housing condition, and study purpose:
- Ethogram for general behavioural monitoring – Caralyn Kemp
- Categories for behaviour recording of cynomolgus macaques during toxicology procedures – Tasker (2012), Tables 3.2.8 & 3.2.9b
- Detailed ethogram of free ranging rhesus macaque communication – Partan (2002)
- Ethogram used to measure behavioural changes reflective of underlying affective state in singly housed male rhesus macaques – Bethell (2010), Table 3.6
- Behavioural repertoire and time budgets of singly-housed cynomolgus macaques – Camus et al. (2013), Tables 1 & 2
- Ethogram to allow continuous monitoring of social relations within groups of rhesus macaques and stablish an objective basis for changes in group composition – Augustsson & Hau 2011
How to record behaviour
The following Listen Again presentation (1 hour) covers the fundamentals of recording the behaviour of non-human primates in captivity: