Enrichment

Environmental enrichment is the process of providing a stimulating environment to promote species-typical behaviour, allow a degree of control and choice in behaviour, and to enhance well-being.1 Environmental complexity and predictability of events are as important as having adequate space.2 A good enrichment programme will incorporate enrichment interventions that satisfy a range of needs in the social, locomotory, sensory, cognitive and food-based domains.3 Positive interactions with staff may also be considered as enrichment (see the Habituation and training tab under Husbandry).

Why is Enrichment Important?

Vertical, horizontal and diagonal climbing structures for macaques

An otherwise plain room has been enriched through the addition of windows, wire mesh and multi-levelled climbing structures. (Image: Karolina Westlund)

Through the provision of enrichment, the quality of captive animal care is enhanced, providing the stimuli necessary for optimal psychological and physiological well-being.4 The aims of enrichment include:5

  • to improve or maintain an animal’s physical and psychological health
  • to increase the repertoire of species-specific behaviours exhibited
  • to increase utilisation of the captive environment
  • to prevent or reduce the frequency of abnormal and unwanted behaviours, such as stereotypies
  • to increase the individual’s ability to cope with the challenges of living in captivity

By increasing the complexity of the captive environment, the opportunity for choice also increases. Choice is one way in which captive animals exert control over their environment, their behaviour and their captive situation. Control is an important component of welfare and is linked to predictability, which reduces stress.6 

Environmental enrichment from NC3Rs on Vimeo. These weaned rhesus macaques are provided with a variety of types of environmental enrichment. For example, they are housed in social groups, have access to fixed climbing structures made of wood and suspended tyre swings, and there is food scattered around the enclosure and in the floor substrate to encourage foraging behaviour. (Video: Wolfensohn & Finnemore 2006)

 


Resources

SpiderDesigning and implementing enrichment programmes

Enrichment programmes should be goal-orientated, and ideally developed by an enrichment committee that represents all staff interests (e.g. animal care staff, researchers, facility managers). The S.P.I.D.E.R. Framework, designed by Disney’s Animal Programs, is a simple step-by-step process you can incorporate when designing an enrichment programme.7

Set goals
  • Brainstorm aspects of best practice you want to achieve / current areas for improvement.
  • Enrichment goals may be facility-wide or specific (e.g. targeted to a particular animal or subset of animals)
  • Common goals are to: encourage species typical behaviours; prevent or reduce the occurrence of stereotypical behaviours; increase the amount of choice animals have in their interactions with their environment.
  • The Disney site has a list questions to consider when setting enrichment goals.
  • Consider the behaviour and ecological niche of the species.8
  • Identify intended outcomes of the programme – this will help to determine which measures to use to assess its effectiveness.
  • You should now have agreement on the natural history, individual animal history, research and husbandry constraints, intended outcomes and how to measure them.
Plan
  • Create an enrichment plan that is agreeable to all parties. Changes can be kept small to begin with.
  • Remember that the long-term benefits of enrichment will likely outweigh short-term interruptions to laboratory routines.
  • It is essential at this stage to have good communication between everyone involved.
  • Consider individual needs – different animals may not benefit from each enrichment item in the same way.9 Some animals may require more or less stimulation. Animals which often display signs of stress and stereotypy may need more directed enrichment than other animals.
  • Consider accessibility to items – high ranking animals are more likely to gain access to desirable enrichment items (e.g. feeding items) than low ranking animals, so multiple items may need to be provided, and in different locations, to avoid hoarding.10
  • Make sure you have clarified who will do what and when:
    • Who will make and give the enrichments?
    • Who will monitor enrichment use and outcomes?
    • Who will be responsible for assessing effectiveness of the intervention, or end it if safety concerns arise?
 Implement
  • Provide a variety of enrichment items simultaneously11
  • Organise a roster for the provision of enrichment, so enrichment items are rotated and the animals don’t get bored
  • The Disney site shows a roster in the form of a ‘month at a glance enrichment calendar
  • The roster should be based on the number and type of enrichment items, the number of animals, the needs of the animals, and their interest in the items. For example:
    • Structural enrichment items will be alternated every 2 weeks.
    • Destructible items, such as cardboard boxes, will be removed every 2 days.
    • Food enrichment items will be changed daily.
 Document
  • Documenting which animals use which enrichments, when, where and for how long will help to assess the effectiveness of the enrichment programme and to refine it.12
  • Recording may be done simply and quickly as brief notes on main events as part of daily checks/husbandry, a more systematic ‘tick sheet’ approach, or using traditional behavioural monitoring techniques  (see the Recording behaviour tab under Behavioural indicators) which are more time consuming but provide rich data.
Evaluate
  • Evaluate the effectiveness of the programme by comparing the records for before, during and after provision of the enrichment items.
  • Simple statistical tests can be used to determine whether any changes are significant13
Readjust
  • Note reduced interest in the enrichment items over time. This decline in interaction with enrichment items can occur over a short period (e.g. a single day)14 or longer period (e.g. weeks or month).15
  • Continue to design new enrichment and incorporate this into your programme.

 

A mesh ceiling provides an additional surface from which to hang enrichment and climbing structures. Here chains have been inserted into water hosing to reduce the risk of the monkeys' digits being caught in the links.

A mesh ceiling provides an additional surface from which to hang enrichment and climbing structures. Here chains have been inserted into water hosing to reduce the risk of the monkeys’ digits being caught in the links.

Enrichment safety considerations

The potential dangers of any enrichment item should be carefully considered and assessed before incorporating these stimuli into your enrichment program.16 Safety precautions to consider include the following; also see Enrichment gone wrong!:

  • Choking hazards
  • Strangling hazards
  • Transmission of disease
  • Parts that can be used as weapons
  • The temperament, age, sex or past experience of the animals17
  • Detrimental psychological effects, such as fear18

The Shape of Enrichment website has a searchable ‘Safety Database’, providing information on potentially dangerous enrichment items.

Always observe animals with any new enrichment items to ensure that there are no dangers and to be able to intervene quickly if necessary.

Cardboard boxes from NC3Rs on Vimeo. In this video, destructible items (cardboard boxes) are a source of novelty and provide an element of control in otherwise rigid housing. Packaging from deliveries is a cheap source of enrichment items but should be made safe, for example, by removing large staples. Boxes can be filled with substrate and small food items (e.g. seeds, cereals) to increase interest.

 

Macaques are highly social animals.19 The companionship of other macaques is of vital importance to their welfare in captivity20 Social housing of macaques provides the opportunity for:

  • Performance of species-typical social behaviours, such as allogrooming, huddling and play, which promotes physical and psychological health21
  • Developing and maintaining social bonds, which can reduce the negative effects of stressful events and allow animals to cope better with change (social buffering)22
  • Reducing stereotypical behaviour23
  • Socially housed macaques manipulate enrichment items more often than individually housed animals24
Macaques in social group utiilising climbing structures

Providing multiple climbing structures allows group members to better manage their social interactions

Cynomolgus macaques social group resting on wooden shelves

Ample elevated, wooden shelving allows all group members to rest simultaneously

Providing sufficient quantities of food at feeding times reduces competition and conflict in social groups.

Providing sufficient quantities of food at feeding times reduces competition and conflict

Macaques huddling and grooming

Social housing permits species typical behaviour such as allogrooming and resting in close contact

Pair housing

Pair housing is one option for satisfying social needs where cage space is limited.

 

 

 

 

 

 

 

 

Macaque species naturally live in multi-male, multi-female groups of around 10-50 animals and this structure is ideal for breeding colonies. Grouping a single breeding male with several related females and their offspring (harem) is a common practice, as breeding can be controlled and lineages recorded. Stock groups of 10-20 small (2-3kg) macaques of the same sex are often housed together. Macaques used in experiments can be successfully maintained as groups in toxicology, immunology and neuroscience studies, even those with cranial or other implants.25

Pair housing is not a natural social structure for macaques and will not work in all circumstances, so as a general rule it is always best to aim for larger groups. However, safe pair formation and subsequent pair-housing techniques have been developed for adult male and female rhesus, cynomolgus, stump-tailed and pig-tailed macaques.26 When macaques are housed in pairs rather than larger social groups, widely spaced bars between the compatible pairs can increase perceived group size and social interactions without risking health or competition for food, or making identification and capture of animals more difficult.27

Single housing should no longer be considered acceptable for macaques in the laboratory, with exceptions requiring compelling veterinary or scientific justification.28 If single housing is necessary on the recommendation by a trained primate veterinarian or animal welfare officer, it should be for as short a period of time as possible; the isolated macaque should still be able to hear, see and smell group members.29 Additional resources should be targeted to the care and welfare of such animals to compensate for the absence of social companions.

Socially housed head implanted animals from NC3Rs on Vimeo. Housing in stable compatible groups encourages normal cognitive development and maintains health and psychological well-being, through the ability to express natural behaviours. Even large male macaques with head implants can be housed socially, in enriched enclosures, without damage to the devices. In this video, displacement behaviour can be seen between the three males.


 

Managing social groups

A 2006 survey of US primate facilities revealed that 52% of rhesus macaques and 62% of cynomolgus macaques housed indoors were kept in single cages.30 There is always concern housing non-human primates in groups in case conflicts between animals arise.31 However, these can be managed effectively to allow the welfare benefits of social housing.32 Factors contributing to the successful maintenance of harmonious social groups are summarized below.33

Introductions to conspecifics

Plan introductions carefully:

  • Do not rush introductions – allowing visual, auditory and olfactory contact first, and then tactile contact through a barrier, will allow for better assessment of compatibility
  • The grade/width of mesh panel between animals in adjoining cages can be gradually increased to slowly and safely increase the area of contact
  • Introduce single animals, or small groups of 2-3 of animals, at a time – never large groups
  • Introductions should be started at the beginning of the day and week to allow maximum time for observations and monitoring
  • Ensure that there is an adequate number of staff available, especially when full contact is allowed for the first time; inform the attending veterinarian
  • Always have an ‘interference’ plan in place during introductions, including defining the criteria that will be used to stop an introduction and how to separate aggressive animals
  • Provide distraction objects, such as new enrichment items and scattered food
  • Provide as much space as possible, and ensure there are areas where the animals can retreat from each other but not become trapped without an escape route
  • Monitor the animals over a period of time (short-term and long-term; days and weeks) looking for affiliative behaviours (e.g. grooming, resting in contact, lip-smacking: see the Behaviour section) and evidence of a dominant-subordinate relationship (e.g. mounting)
  • Obtain animals in pre-existing compatible groups or pairs and avoid re-grouping
  • Utilise information from the breeder/supplier about the social history, behaviour, and health of individual animals, previous and current caging, as well as socialization methods
  • Consider temperament testing to determine compatibility
  • Allow individuals the time to resolve minor conflicts and develop bonds

Managing aggression

Where aggression occurs, assess the situation:

  • Is this a long-term situation?
  • Is the aggression occurring between or within groups?
  • Is there a risk of injury, or are conflicts settled without dangerous physical contact?
  • Is the animal at risk of poor health, due to age or scientific procedures?
  • Macaques have hierarchical societies – are conflicts occurring between high and low ranked animals, or are they a result of animals trying to rise up the hierarchy?34
  • Has there been a recent external or internal stressor?
  • Is the aggression linked to particular events (e.g. feeding, weighing), animals or staff?
  • Is the aggression resource related?
  • Acknowledge that social hierarchies fluctuate over time and that aggression is a normal behaviour. Aggressive incidents can occur due to stressors such as stress, illness, puberty, breeding season, husbandry activities and disruptions to the hierarchy
  • Removing members due to conflict can disrupt hierarchies and make it difficult to return these animals to their group
  • Do not house too many animals for the space
  • Provide ample -escape’ routes, refuge and visual barriers
  • For pairs of macaques, house animals of different ages and/or body weights together35
  • Reinforce hierarchies by attending to dominant and confident animals first
  • Keep records of aggressive incidents – when does it occur, who is involved, during what circumstances
  • Minimise arousal at feeding times by feeding without delay (or providing a reliable signal before feeding) and scattering food

Floor as a visual barrier from NC3Rs on Vimeo. Housing design, and the configuration of the internal space, is important for successful social housing of macaques. For example, they should be able to choose to socialize with or avoid, group mates, and to be seen or not seen by neighbours. This can be achieved by provision of visual barriers, such as floor mounted or hanging plastic panels, sacking and wide pipes, or in the case of this breeding centre, the floor of the second tier. (Video: BFC)

Structural enrichment is important to increase 3D complexity and usable space within enclosures for macaques, and to permit species typical behaviours, such as climbing, leaping and resting in an elevated position. Suitable objects include ladders, barrels, tyres, swings, hammocks, platforms, shelves, logs and branches. Such objects need to attached securely within the enclosure, as the monkeys will jump onto them with force. Some studies suggest that adult macaques may prefer fixed structures to moveable ones.36 It is preferable to use wood, where possible, as it is a softer material than metal or plastic, and can be gnawed.

High perch fixed to the enclosure ceiling

Perch fixed to the enclosure ceiling makes use of the 3D space.

Cynomolgus macaque on high perch

Macaque resting on a high perch, where it may feel more secure.

Rhesus macaque in suspended tyres

Suspended tyres provide additional resting areas and places to hide.

Visual barriers

Vertical hanging items act as visual barriers enabling some privacy.

IMG_1403_BSL 1 visual barriers KW

A good amount of structural enrichment (Image: Karolina Westlund)

 

 

 

 

 

 

 

 

Suspended pipe from NC3Rs on Vimeo.

Recipe for suspended pipe 1

Materials Construction
  • 1 strip of fire hose
  • 1 carabiner
  • 1 length of PVC pipe
  • 1 metal ceiling hook/ring
  • Drill a large hole through the piping to thread the fire hose through
  • The length of the fire hose used will determine how low the structure will hang
  • The structure can also be hung off the underside of wooden platforms
  • Plastic balls can also be hung from the end of the pipe
(Image: C Kemp/MRC Centre for Macaques)

(Image 1: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

(Image 2: C Kemp/MRC Centre for Macaques)

 

 

 

 

 

 

 

 

 

Recipe for suspended pipe 2

Materials Construction
  • 1 length of PVC pipe
  • 1 carabiner
  • 1 length of fire hose
  • Bolts/screws
  • Small plastic horse blocks
  • Attach several plastic blocks along the length of the PVC pipe at two points for stability
  • Drill holes into the plastic block to allow water to drain during cleaning
  • The PVC pipe can be hung using rings which can then be attached to fire hose and hung in the housing
  • The plastic blocks can also be attached to other substrates, including wooden poles and the walls to create alternate climbing frames

Fire hose swing from NC3Rs on Vimeo. Swings replicate the flexible branches macaques use in nature and can help to keep the animals physically fit. (Video: MRC Centre for Macaques)

Recipe for fire hose swings / climbing structures

Materials Construction
  • Lengths of fire hose
  • Carabiners
  • Ceiling plate hooks
  • Metal rings
  • Use different lengths of hose to connect different points of the housing and create climbing pathways with different tension
  • Cut holes into the ends of the fire hose with enough room to allow for tearing from general use
  • Several lengths of fire hose can be attached to the same point using carabiners
(Image: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

 

 

 

 

 

 

 

 

 

 

 

Ceiling clamp from NC3Rs on Vimeo. Screw stainless steel rings and clamps into ceilings and solid walls for additional climbing and attachment options. (Video: MRC Centre for Macaques)

Juvenile playing in enriched breeding enclosure from NC3Rs on Vimeo. Moveable objects catch attention and introduce an element of unpredictability. The plastic horse jumps on the floor act as climbing frames and visual barriers. (Video: MRC Centre for Macaques)

Recipe for horse jump climbing structures

Materials Construction
  • Plastic horse jumps
  • Flat wood planks
  • Wooden poles
  • Strips of fire hose
  • Stainless steel pole base plates
  • Long bolts/screws
  • There are a variety of ways in which the plastic horse jumps can be put together
  • Distance between the horse jumps will depend on the length of the wooden planks and poles – be creative by playing with this distance for a range of structures
  • Using fire hose improves the grip of the bolts and reduces the chances the monkeys can pull them out
  • Attaching the wooden pole on the metal base plate increases the height of the structure and provides stability to a round object
  • Drill holes into the horse jumps to allow water to drain after cleaning
  • Using hardwood will ensure that this structure is long lasting, reducing wear from chewing and water rot
  • Plastic balls and blocks can also be attached to these structures for variety
(Image: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

 

 

 

 

 

 

Recipe for toy swings

Materials Construction
  • Length of fire hose
  • Carabiners
  • Hooks and rings
  • Plastic barrels
  • Plastic crates
  • Plastic balls
  • Attach one end of the fire hose to the wall/ceiling/sturdy platform first, then loop it through a barrel or large plastic box and attach the other end
  • Barrels, crates and boxes can also be attached to just one end of the fire hose using a carabiner and allowed to swing freely
  • Drill holes into the bottom of the plastic barrels/boxes/crates/balls to create a drainage point

Willow branches from NC3Rs on Vimeo.

Recipe for suspended tyres

Materials Construction
  • Forklift tyres
  • Fire hose
  • Carabiners
  • Ceiling hooks
  • Metal rings
  • Hardwood planks
  • Chain
  • Tyres can be hung as a swing or anchored upright on the floor
  • Use fire hose or chain with a carabiner to hang the tyre from the ceiling
  • Link tyres together to make a ladder or chain
  • Wood can be bolted onto an upright tyre to maintain its position and create stability

Wooden shelves from NC3Rs on Vimeo. (Video: BFC)

Climbing on rings from NC3Rs on Vimeo. (Video: BFC)

The specific aim of this type of enrichment is to stimulate the macaques’ senses.37 For further information on primate sensory capabilities and their implications for the laboratory environment, see Prescott et al. 2006.

VisionAudition | Olfaction | Touch | Taste


 

Macaque using mirror and avoiding eye contac

Macaque using mirror and avoiding eye contact (Image: Karolina Westlund)

Suspended rings for climbing, in a variety of colours

Suspended rings for climbing, in a variety of colours

 

Vision

Macaques are highly visual animals, with colour vision similar to humans. It is likely that laboratories housing macaques are already providing visual stimulation. You can further enrich the visual experience of captive macaques by providing:

  • A variety of colours within the housing
  • Visual contact with other macaques (e.g. through the use of mirrors, windows, enclosure wiring instead of walls)
  • Televisions, either displaying aired programs, video tapes, static images, or live feed of other monkeys or care staff38
  • Pictures or paintings on the wall
  • Presentation of slides39
  • Mirrors inside or outside the cage

Adjustable mirrors 1 from NC3Rs on Vimeo. Mirrors can improve visibility of activities within the facility, helping to reduce the likelihood of animals being startled by the sudden appearance of care staff. (Video: MRC Centre for Macaques)

Adjustable mirrors 2 from NC3Rs on Vimeo. Mirrors are also a way that macaques can inspect themselves and monitor the activities of members of their social group without making direct eye contact. (Video: MRC Centre for Macaques)

Adjustable mirror mechanism from NC3Rs on Vimeo. The angle of the mirror mounted on the outside of this enclosure can be adjusted via a mechanism linked to the interior, enabling the occupants to gather information about their surroundings and providing an element of control. External mirrors are safe and easily cleaned. (Video: MRC Centre for Macaques)


 

Audition

Macaques have excellent low frequency hearing but can hear sounds up to 40 kHz40; humans only hear up to about 20 kHz. Sounds are a great way to stimulate captive animals and enrich the captive environment beyond everyday noises. These can include:

  • Music41
  • Natural sounds, such as from non-threatening animals, water, wind, etc.
  • Conspecifics from other groups within the facility

Playing music or other sounds can help non-human primates adjust to noise and reduce their startle reflex in response to unexpected or loud sounds.42 However, it is important to carefully monitor the response of the animals for negative effects. Some sounds may be aversive to due to interference with the animals’ hearing range (too high or too low pitch) or because the volume of the sounds make it difficult for the macaques to stay in auditory contact with other groups.43


 

Olfaction

The olfactory ability of primates has been largely over-looked in science44 and thus rarely included in enrichment programs. However, the provision of odours can elicit behaviours from monkeys not otherwise observed.45 Dotted around the enclosure in small quantities at random intervals, odours can elicit investigation, and the animals may even rub themselves against the odour if they find it pleasant or interesting. Olfactory enrichment stimuli can include:

  • Odours of other macaques, such as those found on nesting material or environmental enrichment objects swapped from the enclosure of another group
  • Perfumes
  • Oils
  • Spices and herbs

 

Touch can be stimulated by ensuring that a variety of textures and surfaces are provided within the enclosure (Image: ONPRC)

Grass, earth, rubber straw and cardboard provide tactile stimulation (Image: ONPRC)

Touch

Touch can be stimulated by ensuring that a variety of surfaces are provided within the enclosure. These may include:

  • Wood (ensure that there is no chance of splinters) and gnawing sticks46
  • Smooth plastics
  • Textiles
  • Naturalised floor covering (woodwool, straw, hay, paper shavings, sawdust etc)
  • Waxed cardboard boxes
  • Nylabone rings and tug toys
  • Kong toys (large sized)
  • Rattles and shakers
  • Magazines, telephone directories or other papers
  • Pool for swimming47
Macaque gnawing wooden branch

Wooden branches provide opportunity for gnawing (Image: Karolina Westlund)

Inflatable swimming pool at rhesus macaque breeding centre

Inflatable swimming pool at rhesus macaque breeding centre

Small swimming pool that can be easily transported between enclosures.

Small swimming pool that can be easily transported between enclosures

Rhesus macaque breeding group drinking from outdoor swimming pool

Rhesus macaque breeding group drinking from outdoor swimming pool

Wild rhesus macaque playing with discarded textiles

Wild rhesus macaque playing with discarded textiles (Image: UCD)

 

 

 

 

 

 

 

Nylon rod bulldozer from NC3Rs on Vimeo.

Swimming pools provide effective enrichment for macaques in the laboratory. These animals show high motivation to manipulate the water surface, immerse themselves, dive, swim and play (including underwater), even in the absence of submerged food rewards (e.g. raisins, nuts, banana chips). Advantages of this enrichment technique are that it is based on a natural behavioural inclination, encourages play rather than food-orientated enrichment, provides exercise, keeps both animals and their enclosure clean, and can facilitate thermoregulation in hot weather.

Small indoor swimming pool from NC3Rs on Vimeo. Food can be scattered on the bottom of a swimming pool, to encourage the animals to enter and dive under the water.

Recipe for foraging in water

Ingredients Notes
  • Pool or deep tub
  • Water
  • Waterproof plastic crate with lid
  • Fruit pieces
  • If possible, bolt the crate to the floor of the pool/tub
  • Place the fruit pieces inside the crate and close the lid
  • Ensure that the water is replaced regularly to maintain cleanliness
  • The fruit ice blocks can also be used in water foraging enrichment as the bobbing of the water will increase the challenge level

Large indoor swimming pool from NCRs on Vimeo. Large swimming pools are a good way of encouraging social play in groups of young macaques.

Bubble bath from NC3Rs on Vimeo. Bubble bath has been added to the water in this swimming pool to help keep the skin and hair coat in good condition.

Cynomolgus macaques swimming pools from NC3Rs on Vimeo. Stock and experimental macaques at this laboratory are group-housed and given access to the custom-made polypropylene pools about once per week to maintain some novelty. The macaques can be seen swimming, dive-bombing and wrestling.

Cynomolgus macaques diving into a swimming pool from NC3Rs on Vimeo. Keep your eye on the macaque directly under the camera! (Video: BFC)


 

Taste

If your feeding program includes varied food items presented in interesting ways (see the Food-based tab above), it is likely that you are already covering taste in your sensory enrichment. Some manufacturers add flavourings and vary the colour, texture, size and shape of their pellets to make them more interesting and palatable. Sweet and fruity tastes generally enhance dietary palatability.

Providing a variety of food types can prevent ‘the monotony effect’ (i.e. reduced food intake) that occurs with prolonged feeding of any one food, and can help maintain appetite in sick animals.

The provision of different textured foods can also act as touch-based sensory enrichment; for example, presenting food in ice blocks. Ice-bound food will help to stimulate multiple senses and extend feeding times, as the monkeys must work harder to access the food.

Ice cups from NC3Rs on Vimeo. Paper cups and plastic beakers can be filled with diluted fruit juice and frozen. Obtaining access to the flavoured ice, and eating it, occupies the animals for longer than non-frozen drinks.

Ice cone from NC3Rs on Vimeo.

Recipe for fruit ice blocks

Ingredients Notes
  • Water
  • Bucket
  • Paper cups
  • Fruit pieces
  • Yoghurt
  • Forage mix
  • Peanuts
  • Fire hose
  • Carabiner
  • Ice blocks can be made using paper cups or buckets, with either water (buckets) or yoghurt (paper cups)
  • Mix chopped fruit pieces in with the water/yoghurt in the container
  • When using buckets, suspend a piece of fire hose with a carabiner in the water before freezing
  • Remove the fruit ice blocks once frozen
  • Hang from a suspension hook or place around the housing

 

Two macaques with food puzzle.

Two macaques can work with this food puzzle at the same time

Puzzle feeder

Puzzle feeder

Introducing cognitive challenges into captive environments for macaques is a potential means of enhancing their welfare through the enriching effects of problem solving.48 Opportunities for promoting problem solving skills include puzzles, computer-based cognitive tasks, and training.


Puzzles

Puzzles can integrate rewards, such as food treats.

 

 

Retrieving treats with a pole from NC3Rs on Vimeo. Watch how this macaque obtains the food treats that are initially out of reach.

Shape puzzles 1 from NC3Rs on Vimeo.

Shape puzzles 2 from NC3Rs on Vimeo.

Hiding shapes insides steps from NC3Rs on Vimeo.


Computer-based cognitive tasks

Computer-based cognitive tasks are a way to stimulate higher processing.49

1 CognitiveRew 1 from NC3Rs on Vimeo. This video shows the whole sequence of a macaque on a neuroscience study leaving the home cage, being weighed, working on a cognitive task for food reward, and then being returned to the social group.


 

Training

Positive human-animal interactions can alleviate stress during handling for procedures and help form bonds between animals and care staff.50 Training macaques to understand and perform certain tasks required of them, using positive reinforcement methods, will provide mental stimulation during the process. New skills and tasks should be integrated into the training programme to keep the animal’s interest. See Habituation and training under Husbandry for more information.

High five from NC3Rs on Vimeo. This video illustrates how training simple tasks can be used to develop trust bonds between the macaques and humans.

Macaques will voluntarily work for food, even when it is freely available, which indicates that the act of foraging in itself has intrinsic appeal.51 Feeding macaques should not, therefore, just be seen as satisfying a physical need. Providing food as a single meal on a predictable schedule, or as easy to process food items in one location (e.g pellets in a hopper), ignores the complex behaviour and cognition associated with feeding, and may have adverse consequences for animal welfare. Appropriate nutrition is clearly essential (see the Feeding tab under Husbandry), but providing variety in the content of the diet and in the method of food presentation will enrich the lives of captive macaques.52

  • Create foraging opportunities which increase the time and effort required for retrieval of food. This will help stimulate natural foraging behaviour, as well as cognitive processes, and acts as a reward mechanism.53 Examples include:
    • Scattering food amongst a substrate, such as woodwool or sawdust, either on the floor or inside a paper bag54
    • Feeding a very fine forage mix (e.g. a mixture of peanuts in the shell, sunflower seeds, pumpkin seeds, pine kernels, flaked maize, locust beans, banana chips, dried apricots, raisins, rice grains)
    • Putting food items inside containers, either stoppered with something easy-to-remove (e.g. woodwool) or with a lid that must be peeled or screwed off
    • Utilising puzzle feeders, which require manipulation and the development of fine motor skills for retrieval of food55
    • Suspending food (e.g. browse) within the enclosure; this will make feeding more challenging and introduce unpredictable movement to the process
  • Spread out feeding over a number of times during the day
  • Vary the types of food provided per day and between days
  • Provide whole food items that require manipulation and processing, as well as food cut into smaller portions
  • Smear sticky foods (e.g. honey, apple syrup) on surfaces, such as toys or objects which can be hung from the outside of the enclosure or climbing surfaces. Tennis balls can be rolled in syrup or diluted fruit juices, and then into forage mix
  • Feed live insects. Mealworms are commonly given to captive monkeys, but crickets are also a great source of feeding enrichment as the monkeys must work harder to catch them
  • Freeze liquids, such as fruit juice or diluted yoghurt, into blocks. Kong toys can also be filled with food (e.g. peanuts, fruit, sunflower seeds) and frozen
Cynomolgus macaque foraging in straw substrate

Cynomolgus macaque foraging in straw substrate

Manipulating and eating whole sweetcorn

Rhesus macaque with whole pumpkin

Rhesus macaque with whole pumpkin

Cynomolgus macaque under water - James Anderson

Diving for submerged food (Image: James Anderson)

Mealworms, peanuts and cereals for scatter feeding

Mealworms, peanuts and cereals for scatter feeding

 

 

 

 

 

 

Foraging devices made cheaply from a plastic containers

Foraging puzzle made from a plastic container

Cardboard glove box stuffed with hay and treats

Cardboard glove box stuffed with hay and treats

Packet of forage wrapped in paper

Packet of forage wrapped in paper

Cardboard box filled with hay and food items

Cardboard box filled with hay and forage packet

 

 

 

 

 

 

 

While many novel enrichment items are often presented with food to ease any uncertainty regarding their presentation, it is important to note that not all enrichment items need to be associated with food in order to elicit interest. If an enrichment item is utilised by the macaques without the presence of food, it is recommended that any association with food is avoided if it is suspected that the use of the item would decrease or stop after presentation with food.


 

Fine forage mix from NC3Rs on Vimeo.

Recipe for a low calorie forage mix

Ingredients Notes
  • Millet seeds – 5 cups
  • Hemp seeds – 3 cups
  • Rice – 3 cups
  • Sesame seeds – 2 cups
  • Split peas or similar – 1/2 cup
  • Sunflower or pumpkin seeds – 1/2 cup
  • A low calorie, fine forage mix is useful for promoting calm foraging behaviour in groups of macaques housed indoors, even those whose main diet is controlled for a research purpose or health reasons (e.g. obesity)
  • 10g per animal (approx. 35 calories) can be scattered into floor substrate once or twice per day

Low calorie forage mix 1Fine foraging mix 2Forage mix 3

Recipe for a forage mix

Ingredients Notes
  • Porridge oats
  • Marrowfat peas
  • Red lentils
  • Bran flakes
  • Mustard seeds
  • Safflower seeds
  • Millet
  • Bulgar wheat
  • Barley
  • Desiccated coconut
  • Irradiated wheat
  • Linseed
  • Caraway seeds
  • Coriander
  • Long grain rice
  • Cornflakes
  • Popcorn
  • Sunflower seeds
  • Buckwheat
  • Beans
  • Dun peas
  • Maple peas
  • French maize
  • Yellow peas
  • Dried green peas
  • Cabbage seed
  • Red dari
  • White dari
  • Some of these ingredients can be found pre-mixed in pigeon seed.
  • Mix up different combinations for variety
  • Forage mix can be used as part of the daily diet (thrown into foraging substrate) or can be used in other types of food enrichment (see below)
(Image: C Kemp/MRC Centre for Macaques)

(Image: C Kemp/MRC Centre for Macaques)

Adult male foraging for seeds from NC3Rs on Vimeo.


 

Forage bags 1 from NC3Rs on Vimeo. Paper bags can be filled with small food items (e.g. seeds, cereals, popcorn) to provide low calorie foraging opportunities.

Recipe for forage bags / packets

Ingredients Notes
  • Paper bags (various sizes)
  • Forage mix
  • Straw/shredded paper
  • Ensure that the bags have no staples
  • Stuff the bags with straw/shredded paper and place a handful of forage mix inside
  • Roll the bags up tightly so that the monkeys must work a little to open them
  • Ensure that you have enough bags for the number of monkeys to avoid fights
  • Place the bags around the housing and find hiding places

Forage bags 2 from NC3Rs on Vimeo. Food items can be mixed with hay or wood shavings and placed inside packaging material to encourage exploration and foraging, after which the macaques may spend time destroying the material.


 

Whole oranges from NC3Rs on Vimeo.

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

Foraging on tyre swing from NC3Rs on Vimeo.

Suspended dates from NC3Rs on Vimeo. (Video: BFC)


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  2. Kerl & Rothe 1996; Kitchen & Martin 1996; Jensvold et al. 2001; Bassett & Buchanan-Smith 2007 

  3. Buchanan-Smith 2010 

  4. Shepherdson 1998 

  5. Young 2003; Jennings & Prescott 2009 

  6. Sambrook & Buchanan-Smith 1997; Bassett & Buchanan-Smith 2007 

  7. Colahan & Breder 2003 

  8. Lutz & Novak 2005 

  9. Buchanan-Smith 2011 

  10. Bloomstrand et al. 1986 

  11. Schapiro & Bloomsmith 1995 

  12. Lutz & Novak 2005 

  13. e.g Griffis et al. 2013 

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  16. Young 2003 

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  19. Lindburg 1971 

  20. Jennings & Prescott 2009 

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  27. Crockett et al. 1997 

  28. Carlson 2008; Jennings & Prescott 2009 

  29. Rennie & Buchanan-Smith 2006 

  30. Baker & Bloomsmith 2006 

  31. Visalberghi & Anderson 1993 

  32. Hartner et al. 2001; Wolfensohn 2004 

  33. Jennings & Prescott  2011 

  34. McCowan et al. 2008 

  35. Reinhardt 1994 

  36. Bryant et al. 1988; Kopecky & Reinhardt 1991; Lehman & Lessnau 1992; Dexter & Bayne 1994; Reinhardt & Reinhardt 2008 

  37. Wells 2009 

  38. Butler 1954, 1958, 1961; Platt & Novak 1997; Schapiro & Bloomsmith 1995; Swartz & Rosenblum 1980 

  39. Haude & Detwiler 1976 

  40. Pfingst et al. 1978 

  41. Line et al. 1990; Howell et al. 2003 

  42. Jennings & Prescott 2009 

  43. Ogden et al. 1994; Patterson-Kane & Farnworth 2006 

  44. Laska et al. 2000 

  45. Kemp & Kaplan 2012 

  46. Reinhardt 1990; Line & Morgan 1991 

  47. Anderson et al. 1992, 1994; Parks & Novak 1993; Robin & Waitt 2011 

  48. Whitehouse et al. 2013 

  49. Bloomstrand et al. 1986; Fagot & Paleressompoulle 2009; Clark 2011 

  50. Buchanan-Smith 2011 

  51. Markowitz 1979; Anderson & Chamove 1984; O’Connor & Reinhardt 1994; Reinhardt 1994; Evans et al. 1989 

  52. Jennings & Prescott 2009 

  53. Buchanan-Smith 2011 

  54. Byrne & Suomi 1991; Lutz & Novak 1995 

  55. Bloom & Cook 1989; Heath et al. 1992 

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