training laboratory-housed non-human primates, part 2 ...bowell...training programmes for non-human...

December 2005 Animal Technology and Welfare

Summary Positive reinforcement training is increasingly beingused to refine scientific, veterinary and husbandryprocedures involving laboratory-housed non-humanprimates and to enhance primate care and wellbeing.However, there is a need and demand for greateraccess to resources designed to help laboratorypersonnel develop and implement appropriate trainingprogrammes. This paper includes a tabulated literaturereview of primate training, guidance on developing andimplementing a training programme, and a detailedsample training protocol for training laboratory-housedprimates to enter a transport container on request. Theaim is to facilitate more comprehensive, systematic,humane and efficient use of training to refine primateuse and management.

Introduction Part 1 of this paper presents the results, conclusionsand recommendations of a survey to evaluate theextent to which non-human primates are trained in UKresearch and breeding establishments and to exploretraining knowledge and practice.1 The survey indicatesthat:

� There is considerable scope for refinement ofcommon scientific, veterinary and husbandryprocedures through use of positive reinforcementtraining (PRT)

� Many constraints on training are perceived, ratherthan real, and can be overcome with informationsharing and education

� There is a need and demand for greater access toresources designed to help laboratory personneldevelop and implement appropriate trainingprogrammes.

This paper (Part 2) is designed to help establishmentstake positive action and implement the recommendationsin Part 1 by providing:

1. A tabulated literature review of primate training2. Guidance on developing and implementing a training

programme, including resource and personnelrequirements

3. A detailed sample training protocol for traininglaboratory-housed primates to enter a transportcontainer on request.

It has been produced as part of a set of activitiesinvolving the authors and designed to facilitate morecomprehensive, systematic, humane and efficient useof training:

� A continuing professional development course ontraining primates, coordinated by the University ofStirling ([email protected]) and the UKInstitute of Animal Technology (see Heywood2 for aninformal review of a previous course on marmosetbehaviour and welfare). The aims of the trainingcourse are to:

�� provide information on the costs and benefitsof training the primate species most commonlyused in laboratories

�� describe both the theoretical underpinning oflearning theory and the practical application ofsocialisation, habituation and training oflaboratory primates

�� demonstrate (video and live demonstration)and provide written details of tested protocolsfor training key tasks

�� discuss and provide practical solutions toprimate management problems currentlyexperienced by attendees in laboratories.

� PhD research funded by the Universities Federationfor Animal Welfare Pharmaceutical Housing andHusbandry Steering Committee (UFAW PHHSC),which aims to identify ways to optimise the timeinvestment involved with training, and to providepractical data on how PRT can be used inlaboratories

Training laboratory-housed non-humanprimates, part 2: Resources for developingand implementing training programmesM.J. PRESCOTT,1 V.A. BOWELL2 and H.M. BUCHANAN-SMITH2

1 National Centre for the Replacement, Refinement and Reduction of Animals in Research(NC3Rs), 20 Park Crescent, London, W1B 1AL, UK

2 Department of Psychology, University of Stirling, Stirling, FK9 4LA, UK

Contact for correspondence and request for reprints: [email protected]

Keywords: animal welfare; operant conditioning; positive reinforcement; refinement; socialisation; training

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Training programmes for non-human primates

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� Production of audio-visual aids on interpretingprimate behaviour and training primates for co-operation with common procedures, to be madeavailable by the National Centre for theReplacement, Refinement and Reduction of Animalsin Research (NC3Rs)

� Guidelines for refining food and fluid management inmacaques being developed by a working groupconvened by the NC3Rs.

1. Literature on primate trainingTable 1 shows reports in the scientific literature ofprimate training for co-operation with scientific,veterinary and husbandry procedures. Staff involvedwith primate breeding and use in research and testingshould consult this table to identify opportunities forusing training to refine such procedures (wherepossible, web links are given in the reference list). Staffcan produce better science and reach their goals withbetter animal welfare by training primates to co-operateand investing in good relationships with them, ratherthan using forced restraint and coercion.1,3 The tablealso includes examples of instances where training hasbeen used to enhance animal care and well-being.Although, there is a long history of training primates toperform operant tasks for neuroscience and behaviouralresearch, often using food or water restriction tomotivate the animals, this work is not our focus andhence this literature is not included in Table 1.

2. Guidance on developing andimplementing a training programmeOnce the decision has been made to use training torefine a procedure, the next step is to develop andimplement an appropriate training programme. This willtypically involve:

� Selection of staff� Educating staff about operant conditioning� Developing animal training goals and strategies� Implementing training sessions� Record keeping and follow-up on progress.

With careful planning, adequate staffing and properinstruction, training can be integrated into existingpractices and can be a rewarding endeavour for allinvolved.

Selection of staffThe Biological Council4, Laule5, Colahan and Breder6

and Young and Cipreste7 detail some personnelrequirements for successful animal training. In brief,competent trainers will have empathy with the animalsto be trained, patience, a calm demeanour, beconsistent in their behaviour and be able to analysetheir own behaviour. Participants of the UK survey feltthat a ‘team’ approach to animal training is the bestway to ensure consistency and effectiveness, and that

the team should include animal technicians, scientistsand veterinarians on equal and complementary terms(also see Rice et al.8). In addition, all staff should beaware of, and know the basics of, any trainingprogrammes in place, to ensure that they areinteracting with the animals in a manner that isconsistent with the detailed programme (e.g. notproviding food rewards used during training out-withtraining sessions).

Educating staff about operant conditioningA staff member who is skilled and knowledgeableabout operant conditioning1 and training practices islikely to produce results more quickly than one who isnot. For establishments where staff is unskilled in thisregard, the time needed for educating personnel to usetraining methods effectively and the availability of sucheducation must be considered. There are very few staffeducation courses on operant conditioning and trainingprimates. We are aware of one other for primateshoused in laboratories in addition to the afore-mentioned UK course. Dr. Steven Schapiro at theUniversity of Texas MD Anderson Cancer Center([email protected]) co-ordinates an 8-hour‘Primate Enrichment and Training Workshop’ the maingoals of which are:

� Presentation of the most recent advances in theapplication of environmental enrichment and PRT tothe behavioural management of captive primates

� Provision of an essential complete guide toresources concerning environmental enrichment andtraining for primates

� Presentation of advanced techniques for solvingdifficult behavioural management problems usingenvironmental enrichment and training techniquesas tools.

For staff unable to attend the UK course or USworkshop, a small number of audio-visual resources onanimal training are available on international loan fromthe Shape of Enrichment ‘Enrichment and TrainingVideo Library’ (www.enrichment.org/collection.html).Although primarily for use with zoo animals, thesevideos can be used for individual study or formaleducation.

There is also a growing body of literature available onhow to train captive animals. Biological Council4,Laule5, Young and Cipreste7 and Pyror9 define anddiscuss training methods and related learningprocesses (e.g. operant conditioning, positive

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1 The principle behind operant conditioning is that the consequenceof a specific behaviour shapes the likelihood that the behaviour willhappen again and hence the frequency with which it will occur.Positive reinforcement refers to a schedule of behaviour modificationwithin the paradigm of operant conditioning whereby the frequency ofa specific (required) behaviour is increased because somethingdesirable is obtained on its performance (e.g. a favoured food).


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Table 1Reports in the scientific literature of training of primates (often including habituation and desensitisation) for co-operation with scientific, veterinary and husbandry procedures and for enhancement of care and well-being

––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––Procedure Species Reference Notes––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––

Capture from the Rhesus, Bonnet and 25 Using a transport container, singly-housed, juvenile females,group/home cage Long-tailed macaques combination of PRT and NRT, species differences were found in

training effectiveness and corticosteroid response to confinement in the container after training

Rhesus macaque 43,44 (video) Using a transport container, young and adult males and femalesin a breeding group, combination of PRT and NRT, includes a training protocol

Rhesus macaque 45 Using a transport container, adult males and females, singly- and pair-housed, combination of PRT and NRT

Rhesus macaque 38 Using a transport container and chute, young and adult males and females, combination of PRT and NRT, includes analysis of time investment

Rhesus macaque 46 File one at a time through a tunnel on cue, group-housed, combination of PRT and NRT, includes a training protocol

Rhesus macaque 47 Using a modified transport container which is also used to restrain animals for behavioural testing, combination of PRT andNRT

Stump-tailed macaque 48 Using a transport container, males and femalesLong-tailed macaque 49 Using a transport container, males and femalesBonnet macaque 50 Using a transport container, includes a training protocol, young

females, singly-housedLong-tailed macaque 36 Using a transport container, young females, singly-housed,

combination of PRT and NRTRhesus macaque, 51 Using a pole and collar system, adult males and femalesBaboonDrill 52 Diabetic adult maleChimpanzee 53 Using a transport containerSquirrel monkey 54 Using a transport container

Transfer to a Japanese macaque 55holding area Chimpanzee 56 Indoors from outside, PRT, includes a training protocol and

analysis of time investment

Handling Primates 22 A review containing a table similar to this

Blood collection Rhesus macaque 57 Using a restraint apparatus, adult females, group-housed, combination of PRT and NRT, includes a training protocol

Rhesus macaque 58 Adult females, combination of PRT and NRT, includes a trainingprotocol

Rhesus macaque 59 Evidence of reduced cortisol response for trained animalsRhesus macaque 26 Adult males, pair- and singly-housed, combination of PRT and

NRT, includes a training protocolRhesus macaque 21 Young females, pair-housed, includes a training protocolRhesus macaque 60 Adult females and male, combination of PRT and NRT, includes

a training protocol, also faecal samplingRhesus macaque 12 Combination of PRT and NRT, includes a training protocol,

analysis of time investment and evidence of reduced cortisol response for trained animals

Rhesus macaque 61 Adult males, pair-housed, via vascular access portsLong-tailed macaque 62 Diabetic animal trained to present a hand for finger punctureStump-tailed macaque 63 Adult females, pair-housed, includes a training protocolStump-tailed macaque 64 Males and femalesVervet monkey 65 Adult females, singly-housedDrill 66 Adult male, clicker training, includes a training protocolChimpanzee 20 Infant female, includes a training protocolChimpanzee 67 Young female, includes a training protocolOrang-utan 68Brown capuchin 69 Adult females, combination of PRT and NRT using restraint

apparatus, includes a training protocolPrimates 15 PRT, avoids use of squeeze-back, includes a training protocol,

summarises techniques for training

Blood and bile collection Rhesus macaque 70 Males and females, animals are trained with PRT for wearing of jackets, to present subcutaneous access ports to the front of the cage, and to remain stationary


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Blood pressure Rhesus macaque 71 Males and femalesmeasurement Savannah baboon 72 Reduced cortisol response for trained animals

Savannah baboon 73 Adult males, singly-housed, PRT, includes a training protocolInjection Rhesus macaque 10 Stand for intramuscular injection, combination of PRT and NRT,

includes a training protocolRhesus macaque 74 Adult femalesRhesus macaque 75 Increased cortisol for non-trained animalsLong-tailed macaque 62 Diabetic animalLion-tailed macaque 76Savannah baboon 77 Adult male, intramuscular injection in the arm, PRT, includes a

training protocolDrill 52 Adult male, insulin injection, combination of PRT and NRT,

includes a training protocolChimpanzee 78 Subcutaneous injection into the abdomen, PRTChimpanzee 79 Anaesthetic injection into the leg, PRT, trained animals showed

lower mean values of total white blood cells, segmented neutrophils, glucose, cholesterol, and systolic and diastolic blood pressure, and higher hematocrit levels

Chimpanzee 80 Anaesthetic injection, adult makes and females, PRT, includes atraining protocol and analysis of time investment

Chimpanzee 81 Subcutaneous injection into the abdomen, PRTIntramuscular injection into the thigh, PRT or a combination of PRT and NRT

Western lowland gorilla 82 Anaesthetic injectionGibbons and Siamang 17 Includes a training protocolApes 83 Includes a training protocol

Urine collection Vervet monkey 84 Adult males, group-housed, PRT, includes a training protocolChimpanzee 85 Adult females, single- and group-housed, PRTChimpanzee 20 Infant female, PRTChimpanzee 86 Adult females, PRTGorilla 87 For collection on request, adult females, singly-housed, PRT,

includes a training protocolWestern lowland gorilla 88 Adult females, group-housed, PRT, includes a training protocolCommon marmoset 89 For collection of first void, young and adult males and females,

involves single-housing, includes a training protocolCommon marmoset 11 For collection on request, includes a training protocol and

analysis of time investment and effectiveness, PRT, does not involve single-housing

Geoffroy’s marmoset 90 Quantitative data for collection on request, PRTEmperor tamarinGolden lion tamarinCotton-top tamarin 91Pale-faced saki monkey 92

Scent-mark Common marmoset 93 Includes a training protocol

Saliva collection Rhesus macaque 94 Adult males, using a pole or a screen methodWestern lowland gorilla 95 (video)Western lowland gorilla 96Common squirrel 97 Chewing on a dental rope attached to a polemonkeyCommon marmoset 98 Chewing on a cotton bud and allowing staff to retrieve the bud

Topical drug Stump-tailed macaque 99 Present heads through a Plexiglas plate, adult males and application females, pair-housed

Western lowland gorilla 100 Adult female, clicker training

Oral drug Long-tailed macaque 48application Pig-tailed macaque 101 Training to take juice from a syringe

Savannah baboon 102

Semen collection Chimpanzee 103 Adult male, using an artificial vaginaChimpanzee 81 Adult males, using an artificial vagina, PRTWestern lowland gorilla 104 Adult maleBonobo 105 Adult maleBonobo 106 Adult maleOrang-utan 107 Adult male, using an artificial vagina

Insemination Drill 108 Adult females, hindquarter presentationBonobo 105 Adult femaleBonobo 106 Adult female


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Vaginal swabbing Stump-tailed macaque 64 Adult females, group-housed, hindquarter presentationBlack-handed spider monkey 109

Pinworm Chimpanzee 81 Presentation of the perineum for a tape test, PRTassessment

Restraint Common marmoset, 110 Tube restraint deviceOwl monkey

Eye tracking Rhesus macaque 111 Using a primate chair, head restraint and eye coilRhesus macaque 47 Where neurophysiological recordings are not necessary, using

an infra-red camera, transport container and face mask

Position emission Rhesus macque 112 Using a head restraint device and primate chairtomography

In home-cage Rhesus macaque, 113 Cognitive tests from the CANTAB, includes a training protocolbehavioural Common marmosettesting Rhesus macaque, 47

Common marmoset

In home-cage Common marmoset 11 PRT, includes a training protocol and analysis of time investment weighing and effectiveness

Stay at a Rhesus macaque 13 PRT, includes an analysis of time investment and effectivenessparticular location

Basic husbandry Western lowland gorilla 114 (video)and veterinary Bonobo 115 Multi-task medical behavioursexamination Primates 6 Describes in detail development of a programme of animal

management based on trainingNew World primates 18 Describes in detail development of training programme for 17

species, evidence of species’ differences in response to training

Cardiac Bonobo 116 Physical evaluation, venepuncture and transthoracic evaluation echocardiography

Physical therapy Gorilla 117 Adult femalefor arthritis

Reduce aggression Chimpanzee 23 Adult male, PRTduring feeding Laboratory animals 5 Includes a training protocol, summarises techniques for training

Improve Rhesus macaque 118socialisation Drill 108

Management for Drill, Western lowland 119 Reviews a range of PRT activities and benefits which could havereproduction gorilla application to captive breeding programs

Infant care Western lowland gorilla 120Western lowland gorilla 121Western lowland gorilla 122White-cheeked gibbon 17Orang-utan 123Primates 6 Lists training goals for pregnant females and infants

Reduce abnormal Drill 14and/or stereotypic Drill 124 Juvenile male, reduction in fence nibbling, self-biting, and behaviour examining and eating faeces and increase in positive social

interactionRhesus macaque 125 Adult females, PRT, 4/6 animals trained to touch a target

showed a reduction in stereotypic behaviourOlive hybrid baboons 126 Juvenile males, reduction in whole-body stereoypes, cage- and

self-directed behaviours, increase in activity levelsChimpanzee 127 Regurgitation and reingestionOrang-utan 128 Female of a mated pair, PRT, reduction in stereotypic behaviour

Enhance Captive animals 129 Reviews use of PRT as an enrichment strategy to enhanceenrichment psychological well-beingprogrammes

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reinforcement, negative reinforcement, shaping orsuccessive approximation, desensitisation, stationing,targeting, time out, regression). These resources serveas good introductions to the basic principles for traininganimals. Additionally, Pryor9 and Young and Cipreste7

give advice on choosing reinforcers, timing and size ofreinforcers, schedules of reinforcement, shaping,establishing a cue, use of stimulus control, methods ofusing reinforcement to decrease unwanted behaviour,and clicker training. A number of further considerationsfor training may be obtained from the website of theAnimal Behavior Management Committee of theAmerican Association of Zoo Keepers: (www.aazk.org/aazknew/committees/comm_animalbehavior.asp).

Briefly, the most important principles for implementingpositive reinforcement successfully are to:

� Ensure that staff is well educated in the principles oftraining and appreciate that if training is notimplemented correctly it may have a negative impacton animal behaviour (e.g. providing a primate withfood after he/she has been aggressive will onlyserve to increase this undesirable behaviour)

� Choose an appropriate (i.e. biologically relevant andrewarding) form of positive reinforcement

� Establish clear rules to be followed for training (i.e.a clear and specific description of the behaviour thatis to be reinforced)

� Ensure that access to the positive reinforcementthat is to be used for training is restricted at othertimes (e.g. do not feed in the daily diet the food typeused as a reward)

� Ensure that reinforcement occurs at the right timeand place for the desired end result

� Initially arrange the situation to minimise the risk offailure (e.g. choose a location with minimaldisturbance, but note that an isolated stressedanimal is less likely to learn).

Another important step towards developing a trainingprogramme is to teach staff to be aware of theiractions and how these affect primate behaviour.10 It isalso important that staff appreciate at the outset thatthe time investment they make in training animals islikely to be recouped later.11,12,13

Developing animal training goals andstrategiesAn astute training programme will take into account theskill level of personnel, the research objectives, thenatural history (behavioural ecology) of the species tobe trained, and the temperament of individual animals.Failure to successfully train primates, or use ofinappropriate techniques, may lead to frustration onthe part of the animal (and staff) and a decrease inhis/her well-being.14 Therefore, it is recommended thata specialist in the field of behaviour modification beinvolved in the development of any training programme.

For a list of specialists willing to assist establishmentsin the development and implementation of behaviouralmodification programmes contact Dr. Mark Prescott([email protected]).

The electronic discussion forum ‘Laboratory AnimalRefinement and Enrichment Forum (LAREF)’ co-ordinated by Dr. Viktor Reinhardt at the Animal WelfareInstitute (www.awionline.org/Lab_animals/) is anothersource of advice and contains regular correspondenceon animal training, as does the Animal Training ListServe of the American Association of Zoos andAquariums (contact [email protected]). It mayalso be possible to contact the authors of the paperslisted in Table 1 to take account of their experiences inimplementing training and addressing any problems.For example, Laule et al.15 and Wolfensohn andHoness10 give advice for laboratories that are movingtoward an animal management system based ontraining with positive reinforcement, and Whittaker etal.16 describe development of a behavioural manage-ment programme for chimpanzees at the MD AndersonCancer Center Science Park.

Many North American zoos have extensive trainingprogrammes for veterinary management and breedingof their primates and, as such, can be valuable sourcesof advice for research and breeding establishments.Colahan and Breder6 describe the philosophy andframework for a training programme at Disney’s AnimalKingdom (DAK), emphasising setting goals, planning,implementing, documenting, evaluating and re-adjusting. Further information on the cues and criteriaused for husbandry training of gibbons and siamangsat DAK is given in Richards et al.17 and Savastano etal.18 who describe the development of a trainingprogramme for seventeen species of New Worldmonkeys at the Bronx Zoo involving a wide range ofbasic and advanced behaviours (e.g. syringe feeding,targeting, scale and crate training, and transponderreading). The authors include details of the cues used,criteria for successful learning, time scales forlearning, logistical and animal challenges andsolutions.

Before any training programme is started it is essentialto put in place some key elements which will facilitatethe smooth running of the programme and produce thehighest success rate. Time should be allocated forstaff involved in the programme to meet to plan exactlyhow the programme should be run, who hasresponsibility for what, which behaviours will bereinforced, and which cues and rewards will be used.

It is useful if one person has overall responsibility forthe training programme to ensure a consistentapproach, although a number of people can be involvedwith the training. Consistency of technique betweentrainers is important; otherwise, for example, the


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wrong behaviours can be accidentally reinforced andtraining disrupted. Therefore, the method andsequence of training should be agreed by all involved atthe outset and written protocols should be establishedwhich clarify approved and, where appropriate, non-approved, training methods. Laule5 includes a sampleprotocol for training for co-operative feeding, and adetailed sample protocol for training laboratory-housedprimates to enter a transport container on request isincluded below (see also Table 1).

Station (approach a specific location) and target (toucha specific object) are useful behaviours to train in theearly stages of a training programme because they canbe used in a number of circumstances. For example, aprimate that learns to follow a target can be requestedto sit on a weighing scale in the home cage, therebyavoiding capture, restraint and removal from the cage.11

These behaviours are especially helpful for managingprimates that are not easily handled, displayaggressive behaviours, or live in large enclosures orgroups.

Training is easiest with animals that are well socialisedto humans11,19,20 and it is recommended that, as a firststep, all animals are habituated to accept food fromthe hands of staff. This can be achieved initially byplacing food in front of the animals’ enclosure withinreach of the animals and stepping back from theenclosure front, gradually decreasing the distancebetween human and animals over time until food isaccepted from the hand. (Eye contact should begradually increased for marmosets, but not withmacaques, who should not be looked at directly).Alternatively, food can be provided on the end of a polethat can be used to control the distance betweenanimal and human (see sample training protocolbelow).

In order to successfully train primates it is essentialthat all animals involved can be individually and easilyrecognised. If individuals are not naturallydistinguishable, this can be achieved, for example, byusing collars and tags, site-specific hair clipping (e.g.from the tail) or subtle coloured dye marks on the fur.All individuals should be named, preferably not withnames which reflect less amenable aspects of theirpersonality (e.g. Grumpy or Biter) but with those thatare distinctive and easily spoken (e.g. Angus or Erin).

It is important to recognise that not all animals may beable to be trained.13,21,22,23,24 Primates have distinctpersonalities and aptitudes and, as such, individualsare bound to vary in both their willingness and ability tolearn. There may also be sex, species and groupdynamic dif ferences that affect behaviour andtrainability.6,18,24,25,26,27,28,29 Trainers, therefore, arerequired to be knowledgeable about these aspects andplan their protocols accordingly.6

Avoid separating primates for training as this maycause stress and the animals will learn less well.Having said that, it is important to understand andwork with the dominance hierarchy, training the mostdominant animal first. Be aware that if a dominantanimal is nearby, watching a subordinate being trained,the subordinate can become unsettled, unfocussedand may be reluctant to accept the reward (K. Morris,pers. comm. to H.M. Buchanan-Smith).

Implementing training sessionsFor some facilities the principle cost of training is thetime investment involved in implementing thebehavioural modification process.1 In order to facilitateefficient use of time, facilities can keep trainingsessions short (e.g. 2-10 minutes). Training sessionsshould be short anyway, so as to maintain the animal’sinterest, but the optimum length varies betweenspecies and individuals.18 Although more trainingsessions in a given time enables training goals to beachieved faster, training can still be achieved with threeto four sessions per week. Once the desired behaviourhas been well established, reinforcement forperforming the behaviour can be even less frequent(e.g. once every two weeks), but it is important that thebehaviour does continue to be reinforced or else theanimal will stop performing the desired response andwill require re-training.

Establishments can take small steps towards aproactive behavioural management programme byincorporating training into the daily routine (e.g.whenever primates are being fed). Sessions can berelatively passive depending on the desired behaviour.For example, training primates to initially go into atransport container may be as simple as placing theirfood closer to the transport container over a period ofdays, and eventually inside it. Facilities with younganimals can begin by exposing those animals tounfamiliar objects that they may encounter later in life(e.g. stethoscope, syringe, primate chair). Curiositytowards novel objects in young primates has beennoted by many authors, whereas adults, in comparison,may be considered conservative due to theaccumulation of experience.30,31,32,33,34,35 Associatingunfamiliar objects with feeding times can helpdesensitise the animals to these objects.

Although training can be easily incorporated into thedaily routine, the time invested to develop andimplement a structured programme can havetremendous benefits. Eventually, procedures can beperformed quickly, efficiently and calmly, saving time inthe long run.11,12,22,36,37,38,39 Therefore, instead of viewingtraining as an additional luxury to include in dailyoperations, managers should consider training asessential to the successful operation of an animalfacility and plan and budget accordingly. Forestablishments with large numbers of animals, it may


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help to prioritise and focus on key studies, animals,behaviours or procedures, (e.g. those that cause mostsuffering, for which training protocols exist, or for whichco-operation can be achieved most quickly).

Training methods should be based on positivereinforcement since this is considered to be the mosthumane method of training.5,9,15 Negative reinforcementshould only be used when positive alternatives havebeen exhausted. If negative reinforcement must beused (e.g. for training aversive procedures), it shouldbe used in combination with positive reinforcement.40

Record keeping and follow-up on progressRecords of training performance should be kept foreach session and regularly reviewed (e.g. weekly) foreach animal, noting their achievements and anyabnormal, unpredictable or otherwise significantbehavioural irregularities at each training session.Such records can be used to identify when to begin totrain the next behaviour/task in a programme ofsuccessive approximation, to help monitor success orotherwise of the training programme, and to justify tomanagement the time investment involved.41 Knowingwhen to train the next step of successiveapproximation in the programme is important; theprimate must be allowed to succeed and be reinforcedbut, in order to maintain interest in the task and toensure progress to the final desired behaviour, newgoals must be introduced. If the primate has notsucceeded to obtain many rewards during the session,reverting to earlier learned behaviours at the end of thesession is important so that the session ends on apositive note.

3. Sample training protocol: Traininglaboratory-housed primates to enter atransport container on requestUse of a transport container (box) enables primates tobe confined and moved from one cage or enclosure toanother without chemical restraint or anaesthesia. Thisis useful for:

� Veterinary management (e.g. health examination,collecting physiological samples, administeringtopical or injectable medications)

� Breeding management (e.g. setting up temporarypairings)

� Husbandry (e.g. relocating animals during cagecleaning or maintenance, weighing)

� Enrichment (e.g. relocating animals to remote play orexercise areas)

� Research purposes (e.g. temporary move to ametabolism cage for collection of faecal samples orto a testing site for cognitive studies).

A protocol for training laboratory-housed primates toenter a transport container on request is given below.The protocol was developed for common marmosets at

the MRC Human Reproductive Sciences Unit inEdinburgh, where it has been used successfully. Theprotocol can be modified for use with other species;some suggestions for macaques are given here. Analternative for moving marmosets between cages is theuse of plastic tubing (Figure 1).

Goal: The goal is to train laboratory-housed primatesusing PRT to enter a transport container (box) onrequest, and to remain relaxed whilst they are shut inand transported to another location.

Select a training reward: A ‘training reward’ should beagreed upon which is a favoured food that will only beused during training sessions and will not be part of theregular diet (e.g. raisins, cornflakes, dates ormarshmallow for marmosets. Although high sugar/highfat foods should be avoided, marmosets work morereliably for marshmallow than for other rewards).Rewards should be prepared prior to the start of eachsession, so there is no delay in producing a rewardonce training has begun. Each reward should be small;no more than one mouthful (i.e. 1/2 raisin or 1/12th

small marshmallow for marmosets). Problems ofaggression can occur if the reward is too highlyfavoured. Such problems can be overcome by using aslightly less favoured food with occasional ‘jackpots’ ofthe most favoured food and by giving an individual areward only in his/her ‘reward zone’ (see below).

Select bridges and cue words: Selection of secondaryreinforcers (bridges) and cue words should beestablished when setting up a training programme. Thebridge is a sound or word which is used to mark thedesired behaviour (a sound is usually more consistent ifmany trainers will be working with the animals). It is

Figure 1. Marmosets will readily travel through air ventilationducting, which is cheap, flexible and easily attached toenclosures. It can be used to move marmosets betweenlocations, obviating the need for capture, and marmosets willreadily travel long distances (> 10m) once they are familiarwith the ducting. If long vertical stretches are included, it isrecommended that some strips of matting are inserted intothe ducting (as seen in this photograph) to allow themarmoset to grip.


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used to say to the animal ‘what you are doing right nowis the thing you are getting a reward for’. The bridgeenables the trainer to reward the animal for doingsomething when he/she is physically distant from thetrainer (i.e. not at the front of the cage). Commerciallyavailable clickers can be used for macaques, but theseare often too loud for more timid primate species (e.g.marmosets), so a vocal tongue click can be used or theclick of a retractable pen. Advice on establishing thebridge is provided below. Cue words are used to providethe trainer with control over which animal performs whatbehaviour when; similar to when we ask a dog to sit. Inthis protocol it may be decided to use the primate’sname followed by the word ‘box’ to request that he/shegoes into the box (e.g. ‘Angus, box!’). A calm but upbeatvoice should be used to encourage a response. If thebehaviour is performed readily (e.g. target), then thecue word can be introduced early. For complexbehaviours that require to be shaped (training to urinateon request), it is best to increase the frequency of thebehaviour first, before introducing the cue word.

Define staff responsibilities: Whilst a number of peoplecan be involved in training the animals it is best if eachperson has responsibility for a particular group orroom, and that they remain the sole trainer of thatgroup/room until the behaviour is established. Thisensures the approach is consistent throughout theearly stages of establishing a behaviour. However itmay be useful to have two or more people working withlarger groups of animals to prevent squabbles overaccess to the food, and to facilitate cover over holidaysand sick days. If there are multiple trainers, eachperson should take responsibility for certain animalsand only reward those animals. Each trainer shouldignore animals that they are not responsible fortraining. The primates will soon learn who theirdedicated trainer is and ignore the other trainer.

Establish hand feeding: The first behaviour it isessential to establish is hand feeding, whereby theanimals will come forward and take a food reward fromthe trainer. Even at this early stage it is useful toestablish ‘reward zones’ whereby each individualanimal in the group only gets a food reward whilst in aparticular location (e.g. top, left-hand side of the cage).If each individual has his/her own location, this willhelp to prevent squabbling and food stealing. Nervousor hesitant individuals who are reluctant to come andtake food from the trainer can be offered food on a poleinside the cage. The distance between the trainer andthe food reward can then be decreased gradually untilthe animal will take the food directly from the trainer.The distance should only be reduced once the animalis reliably taking the reward at the longer distance (i.e.takes the reward nine times out of ten). If the animalfails to take the reward at the shorter distance for threeconsecutive occasions, the distance should beincreased to one where he/she is performing reliably

before being shor tened again. Any undesirablebehaviour (e.g. aggression between conspecifics,threats or aggression towards the trainer, abnormalbehaviours such as fur-plucking) should be ignored anda time-out introduced. The time-out must occurimmediately after the undesirable behaviour starts andinvolves the trainer turning round so they have theirback to the cage, and food rewards are out of sight.Training can resume only once the animals are calmand relaxed again. It is essential that the animal isnever rewarded for per forming an undesirablebehaviour and the trainer must be particularly aware oftheir own behaviour in regards to this. It is particularlyeasy to train primates to grab and scratch the trainerwhen giving them their food reward. However, it isimportant not to withhold the reward from snatchers ifthey have preformed the desired behaviour. Rather givea double reward when they take the reward calmly.Hand feeding can be performed two to three times perday in short sessions (~2 minutes) until all animals inthe group will eat in this way.

Establish the bridge: Once all animals in the group canbe hand-fed in a relatively calm manner (someexcitement is acceptable, as enthusiasm for gettingtheir rewards will encourage the animals to work andmaintain interest during training sessions) the bridgecan be established. To do this the click (or whateverbridge has been decided upon) should be paired withthe arrival of the food reward, so the trainer shouldclick immediately before (i.e. <1 second) the food isdelivered to the animal’s mouth. The animal may beslightly startled at first but careful repetition will soonenable him/her to associate the click with the food.The trainer should then click just before the foodreward is delivered and if the animal has made theconnection between the click and the food rewardhe/she will look for the food reward. If this does nothappen the training has been too fast and the trainershould go back a stage to allow the animal to make thisconnection. It is vital that this stage is not rushed (e.g.minimum of three to four sessions) as a strong bridgeis essential for all the later stages of training. The aimof this part of the training is to establish a responsewhereby the animal will wait attentively for his/her foodreward for 2-3 seconds following the click. Again, shortsessions are preferable (e.g. maximum of 8 minutes)or until the animal earns eight rewards (but this mayvary depending upon the size of group). If time allows,there can be multiple sessions each day, and trainingwill be quicker but, if time does not permit, transportbox training can also be achieved with three to foursessions per week.

Begin target training: It is then useful to train theanimals to hold a ‘target’. Target training enables thetrainer to keep stationary one or more animals whilstworking with another, and also enables the trainer toguide the target animal into the transport box once it is


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introduced. The target should be an easily replaced,easily cleaned object which the animals do not see outof training sessions (a pen would not be suitable). Eachanimal in the group should have its own target which isidentifiable by colour2. A suitable target for marmosetsis a plastic teaspoon; black and white are the bestcolour combination for pairs. In the individual’s rewardzone the trainer should hold a food reward behind thetarget and click the animal as he/she touches thetarget whilst reaching for the reward. This should berepeated until the animal deliberately touches thetarget on five consecutive occasions it is offered. Nextthe animal should be clicked and rewarded only ifhe/she actually holds the target, however briefly (theclick must come whilst the animal is holding thetarget). Once the animal will hold the target on fivesuccessive occasions the duration of hold should beincreased, first 1 second for five consecutiveoccasions, then increasing to 3 seconds, 5 secondsand 10 seconds, each for five successive occasions.(Actually, with marmosets, holding is achieved relativelyquickly and successive steps may not be needed for allindividuals). Longer durations can be introduced ifrequired. This is done by clicking only after the desiredduration of hold has passed. If, at any point, the animalfails to hold the target for the required duration on twoconsecutive occasions, or three out of tenpresentations, the trainer should go back to the laststage and re-establish that. It is also often useful tostart a session at a slightly lower level than previouslyachieved as this allows the animal to have easysuccess and helps maintain their interest andenthusiasm. For this reason it is also important tofinish every session with a short run of successes,even if this means working at a lower level. Sometimesthe primates will become a little overenthusiastic andtry to hold their cage-mate’s target. This behaviourshould be ignored, and not rewarded either by food ora vocal response.

Move the target: The target should now be movedaround the cage and the animal rewarded for holding itwherever it is presented. The target should gradually bemoved away from the reward zone, again going back astep if the response becomes unreliable. If desired, averbal cue can now be introduced with the requiredbehaviour. As the target is presented, the trainershould use the cue word (e.g. ‘Angus, hold!’). The cueword should be used on every occasion the target ispresented.

Introduce the transport box: To introduce the transportbox, it should be carefully and securely placed on thefront of the cage with the box door open and the

animals given access to it (Figure 2). They should beallowed a few minutes to explore the box if they wishto. At first, for social reassurance, several animals canbe target trained in the box simultaneously. However, ifthere is a requirement to separate just one individual,the trainer should then ensure all but one of theanimals in the group is holding their targets away fromthe box (in groups of more than two primates it may beuseful to have a second trainer to target the otherprimates, whilst the original trainer works on boxtraining). The trainer should then place the target of theanimal he/she is working with at the end of thetransport box. The animal may then enter the box. Ifthere is hesitancy the target can be placed near the boxdoor as a guide for the required behaviour, and theanimal rewarded for holding it. The target can then begradually placed further inside the box, each timeclicking and rewarding the animal for holding it untilhe/she will come into the box in a relaxed manner(Figure 3). The duration of wait in the box should thenbe increased as described for target training until theanimal will remain in the box for 10-20 seconds.

Habituate the animal to the box door opening andclosing: Next, the door needs to be shut. This createsnoise and some movement in the box, which maycause the animal to become unsettled. This can bereduced by ensuring the door is running freely prior totraining, but, providing the target response has beenwell established, the animal should remain holding thetarget (Figure 4). The trainer can click the continuedhold at first, providing he/she does so only if theanimal remains relatively calm. The animal should berequested to hold the target and the door closed andimmediately opened. The animal should remain in thebox once the door has reopened for at least 2 seconds,then clicked and rewarded; this is to ensure thathe/she does not learn to rush out of the box as soonas it opens. The animal should then be asked to leavethe box using their target. This process can berepeated until the animal becomes habituated to thedoor opening and closing (i.e. no longer takes anynotice of it).

Increase the duration of time the animal spends in thebox: The duration of time the animal spends in the boxcan then be increased by leaving the door closed for 2seconds, then 5 seconds, working up in smallincrements until the box remains shut for 5 minutes.The animal does not need to hold his/her target for thisentire time, but he/she should always be recalled tohold before the door is reopened to control his/her exit.The animal should be clicked and rewarded for calmbehaviour in the box during these waits. Bear in mindthat some primates, especially younger animals, maybecome bored during these waits. The trainer can askfor intermittent target holds during this time to preventundesirable behaviours occurring due to boredom. Theduration of wait in the box should be varied from no wait

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2 Note that most diurnal New World primates have polymorphic colourvision – only heterozygous females can be trichromatic (similar tomost humans), whereas homozygous females and all males aredichromatic (colloquially colour blind).42


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to the maximum being trained at that time to keep theanimal’s concentration and interest. Cue words can nowbe introduced as described above, so that the behaviourcan be requested verbally. Given that the same task ofholding the target is required, no new cue words needto be introduced (i.e. use ‘Angus, hold!’ as before).

Habituate the animal to transport in the box: The boxcan now be carefully detached from the home cage andplaced a short distance away, ensuring visual, olfactoryand auditory communication with conspecifics ismaintained. The animal should be held in the box for 1minute, clicked and rewarded for remaining calm,before the box is returned to the home cage and theanimal released (following a target hold whilst the dooris opened). This should be repeated and providing theresponse remains reliable (i.e. nine out of tenrequests) the distance between the home cage and thebox increased until the box is out of visual contact,then out of auditory and olfactory contact. Once this isreliably established longer duration waits can beintroduced, and releases at different environments(e.g. play areas).

Providing the routine is kept varied, and desirablebehaviours continue to be reinforced, the trainedprimates should now be easy to catch and move to newlocations. The bridge can be used in other situations toreinforce desired behaviours and target training can beused, for example, to select animals for visualinspections or applying topical medications whilst theanimal remains in his/her home cage.

AcknowledgementsSpecial thanks to Keith Morris and staff at the MRCHuman Reproductive Sciences Unit for their continuedsupport and encouragement. We appreciate discussionswith Jean McKinley and staff at Dstl Porton Down ontraining protocols. MJP is employed by the NC3Rs.HMB-S was supported by a grant from the EuropeanCommission (QLRT-2001-00028). VAB was supportedby the UFAW PHHSC.

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Figure 3. Marmoset calmly holding the target in the transportbox.

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