Refinement of the use of non-human primates in...

215

copy 2006 Universities Federation for Animal WelfareThe Old School Brewhouse Hill WheathampsteadHertfordshire AL4 8AN UK

Animal Welfare 2006 15 215-238ISSN 0962-7286

Refinement of the use of non-human primates in scientific researchPart II housing husbandry and acquisition

AE Rennie and HM Buchanan-Smith

Department of Psychology University of Stirling Stirling FK9 4LA Scotland UK Contact for correspondence and requests for reprints hmbuchanan-smithstiracuk

Abstract

In order to safeguard the welfare of laboratory-housed non-human primates refinement techniques should be applied to every aspectof the life of animals used in the laboratory from birth to death with the aim of both minimising harm and maximising well-beingIn this second part of a three-part review we summarise published information on housing and husbandry practices and describeways to minimise contingent inhumanity associated with the use of primates in laboratories and their breeding and supply (whereinhumanity is defined as the infliction of distress) We also discuss methods by which the welfare of these animals can be maximisedon a day-to-day basis The principles of enrichment aspects of the housing environment social and physical enrichment and acquisi-tion are discussed Refinement of the influence of humans and experimental procedures are discussed in Parts I and III of this reviewrespectively

Keywords animal welfare environmental and social enrichment housing husbandry refinement transportation

IntroductionWith the aim of harmonisation the essence of Russell andBurchrsquos (1992) original concept of refinement and the mostprogressive recent concepts of refinement since have beenincorporated into the following definition of refinementproposed by Buchanan-Smith et al (2005)

ldquoAny approach which avoids or minimises the actual orpotential pain distress and other adverse effects experi-enced at any time during the life of the animalsinvolved and which enhances their well-beingrdquo(Buchanan-Smith et al 2005)

Refinement techniques that can be used to minimise harmand maximise the well-being of animals during proceduresare discussed in part III of this review However in order tosatisfy the ethical and scientific need to reduce contingentharm arising indirectly as a result of the use of animals inscience and to maximise well-being on a day-to-day basisrefinement must also be applied to routine housinghusbandry and care practices and during the process ofacquisition and transportation Such practices are consid-ered likely to have a particular impact on the welfare of non-human primates (henceforth primates) destined for orcurrently in use in laboratories because of their capacity forsuffering in inadequate environments the manner in whichthey may legally be acquired and the relatively largedistances over which they are often transportedAlthough many of the refinements discussed in this reviewhave been discussed previously in the literature informa-tion regarding the use of refinement in primates can be

difficult to find as data on primate species are published ina diverse selection of journals This second part of a three-part review summarises published literature on housing andhusbandry and provides a sample of the types of refine-ments that could be incorporated into normal practice inlaboratories With a focus on Europe it also includes adescription of current practices still in common use globally(eg single housing) and summarises the scientific evidenceas to why these should not be continued With careful usebased upon knowledge of species-specific needs theserefinements have the potential to greatly improve thewelfare of laboratory-housed primates whilst reducingcontingent harm in accordance with the definition of refine-ment proposed by Buchanan-Smith et al (2005)

Primate housing and husbandry and the useof enrichmentThe environment in which primates are kept has a signifi-cant effect on their well-being The concept of environ-mental enrichment has been applied to the laboratoryenvironment in an effort to promote well-being In the USAthe legal requirement to consider the psychological well-being of laboratory-housed primates has resulted in a signif-icant change in attitude to housing and husbandry ofprimates in the laboratory and provided momentum for theuse and development of enrichment strategiesEnvironmental enrichment was defined by Shepherdson(1998) as ldquoan animal husbandry principle that seeks toenhance the quality of captive animal care by identifyingand providing the environmental stimuli necessary for

Universities Federation for Animal Welfare Science in the Service of Animal Welfare

216 Rennie and Buchanan-Smith

optimal psychological and physiological well-beingrdquo(Shepherdson 1998 p 1)Thus environmental enrichment is a refinement whichmaximises the well-being of laboratory-housed primatesThe scale of enrichment techniques varies widely from thecomplete redesign of housing to the introduction of smalltoys but according to Shepherdsonrsquos definition all areconsidered enrichments if they can be shown to positivelyaffect the well-being of laboratory-housed primates(Shepherdson 1998) Evidence shows that the proper use ofenrichment can improve the psychological well-being oflaboratory-housed primates (Snowdon 1991) indicated byincreases in the animalsrsquo ability to cope with challengesreduction in aberrant behaviours increased frequency ofspecies-typical behaviour (Pyle et al 1996 Wright 1995)and improvements in health and reproductive success(Erwin 1986 Wallis 2002) Despite the potential positiveeffects of enrichment misguided attempts at enrichmenthave the potential to cause harm for example by causinginjury (see review by Bayne 2005 Nelson amp Mandrell2005) causing aggression (Honess amp Marin 2006) or whenenrichment opportunities are provided but then removed(Bryant et al 1988) Other enrichment strategies may beimpractical for use in the laboratory environment forexample those which take up too much staff time or whichhave the potential to affect the outcome of experiments(Newberry 1995 Bayne 2005) Thus all enrichment strate-gies must be tested to ensure that their introduction affectswelfare positively and that they are practicable in the labo-ratory An understanding of species-typical behaviour andphysiology is essential for proper assessment of enrichmentsuccess and imagination innovation motivation and someresources are a requirement during design (Markowitz ampLine 1990) The literature on environmental enrichment isvast and cannot be comprehensively covered within thescope of this paper (see Lutz amp Novak 2005 for a recentreview) However the range of enrichment strategies andevidence of their effects will be considered and sources ofconflict and difficulties that may be encountered during thedevelopment of proposed enrichments will be discussed

Psychological well-beingThe ability to express species-typical behaviour and to fulfilbehavioural needs has been considered important to thepsychological well-being of laboratory-housed primates(Snowdon amp Savage 1989 Eaton et al 1994 Newberry1995) The capacity for control and the degree ofcomplexity and predictability of the enrichment are alsothought to be important (OrsquoNeill 1989 Sambrook ampBuchanan-Smith 1997 Vick et al 2000 Bassett ampBuchanan-Smith in press) The view of the relative impor-tance of these concepts has changed since the earliest use ofenvironmental enrichment and it is well accepted that thesuccess of enrichment strategies is very much dependentupon the individual and species concerned (Markowitz ampLine 1989)

Behavioural needsAs the aim of enrichment is to increase an animalrsquos behav-ioural opportunities and to prevent or reduce the expressionof abnormal behaviours (including stereotypies) discus-sions of the concept of behavioural or ethological needs areinevitably and correctly included in the analysis of enrich-ment strategies Indeed the lsquoneedsrsquo concept has been incor-porated into the European Directive (86609EEC) whichstates that ldquoany restriction on the extent to which an exper-imental animal can satisfy its physiological and ethologicalneeds shall be limited to an absolute minimumrdquo (EuropeanUnion [EU] 1986 Article 5 paragraph b)Thus European law supports the use of enrichment forlaboratory animals The concept of behavioural or etholog-ical needs was first introduced by Brambell (1965) in areport on the welfare of farm animals in intensivehusbandry systems In this report it was considered thatprevention of the expression of behaviours which theanimal is highly motivated to perform could result in frus-tration and that the degree of frustration experienced woulddictate welfare The performance of such behaviours couldtherefore be considered an ethological need Later Dawkins(1983) attempted to pinpoint exactly what was meant by theconcept of behavioural or ethological needs defining etho-logical needs as the effect of high levels of causal factors toperform a particular behaviour pattern Dawkins (1983)argued that true needs (as opposed to lsquoluxuriesrsquo) could beidentified using the principles of consumer demand theoryapplied to operant and preference tests Using this principleonly those behaviours that the animal would work hard orovercome aversive stimuli to perform could be consideredneeds The frustration of behavioural needs is considered tobe one of the main causes of stereotypical behaviours incaptive animals where animals are motivated to perform apattern of behaviour that they cannot perform normally orcompletely (Mason 1991b) Abnormal and stereotypicalbehaviours are also likely to occur when the animal issubject to experiences over which it has no control andcannot therefore respond appropriately (Mason 1991b)Thus the presence of abnormal and stereotypical behav-iours has been used as an indicator of poor welfare and inad-equate housing and care (Mason 1991a) Abnormalbehaviours including stereotypic circling and pacing eyeprodding self-sucking depilation self-mutilationcoprophagy and regurgitation have been observed in labora-tory-housed chimpanzees Old World monkeys andcallitrichids (Baskerville 1999 Fritz et al 1999 Poole et al1999) The occurrence of abnormal and stereotypical behav-iours can be reduced (Watson et al 1993 Eaton et al 1994Crockett 1998 Lutz et al 2003 Novak 2003 Bourgeois ampBrent 2005) or prevented (Lutz amp Novak 2005) by the useof carefully considered enrichment strategies supportingthe hypothesis that these behaviours occur as the result ofthe thwarting of behaviours that the animal is highlymotivated to perform (Marriner amp Drickamer 1994)

copy 2006 Universities Federation for Animal Welfare

Refining primate housing husbandry and acquisition 217

Performance of natural behavioursThe term behavioural need is commonly misused often inconjunction with the assumption that captive animals mustshow a full repertoire of species-specific behaviours foroptimal welfare (Chamove amp Anderson 1989 Veasey et al1996) This proposal falls short if we consider the welfare ofanimals foraging without success during periods of foodshortage or animals showing species-typical predatoravoidance behaviour Veasey et al (1996) discussed thismisrepresentation of the term behavioural need in thecontext of wild versus captive behaviour and concluded thatthe expression of wild-type behaviours may be correlatedwith good welfare rather than being the cause of goodwelfare as is often assumed Thus the performance of thefull range of species-typical behaviour is not necessary initself but the ability to respond in a species-typical mannerto stimuli encountered in the captive environment is criticalThis idea is developed in analyses of enrichment strategiesin terms of control complexity and predictability

Control complexity and predictabilityThe concepts of control complexity and predictability arealso considered to be important facets of enrichment strate-gies However despite general acceptance that these factorshave some bearing on the efficacy of enrichment attemptsfew studies have studied their importance in detail Thepurported importance of control was stressed by Snowdonand Savage (1989) who stated that ldquoanimals cannotpassively receive environmental events they must be ableto act on the environment and consequences must resultfrom their actionsrdquo (Snowdon amp Savage 1989 p 81)The idea that control was necessary for well-being wasestablished in studies using aversive stimuli in whichanimals learned that performance of a selected behaviourcaused the aversive stimulus to cease (see Overmier et al1980 for a review) In primates Hanson et al (1976) usedhigh intensity noise to test the effects of control of astressful stimulus in rhesus macaques (Macaca mulatta)They found that those animals which could influence theduration of exposure to the noise by pushing a switch toturn it off had a plasma cortisol concentration similar tothat of animals which were not exposed to the noise Incontrast those animals which were exposed to the unpre-dictable noise but could not influence the duration ofexposure showed significantly higher plasma cortisolconcentrations A lack of control over aversive events canresult in lsquolearned helplessnessrsquo or depressive behaviour inwhich the animal ceases to attempt to respond to its envi-ronment and shows reduced learning capacity (Bloomsmithet al 2001)Despite the availability of evidence indicating that thecontrol of stressful events is critical for well-being there arefew such studies in which the need for control of positiveevents has been examined However those studies which doconsider control over positive events indicate that thiscontrol can have far-reaching positive effects on well-beingand development For example Mineka et al (1986) studied

the long-term effects of a rearing environment in whichinfant rhesus macaques had control of the schedule offeeding water availability and provision of treats incomparison with yoked individuals which had no control ofthe schedule In subsequent behavioural tests individualswhich had had control of their feeding schedule showed lessfear in the presence of novel objects and in novel environ-ments and showed more exploratory behaviour than yokedsubjects Also individuals which had had control were moreactive in their attempts to regain social contact in a separa-tion test than yoked conspecifics The responses of yokedcontrols were similar to those observed in infants reared instandard laboratory cages with variation in access to rein-forcers indicating that the ability to control had positivelyaffected the behaviour of the young macaques However inthe laboratory environment where the provision of enrich-ment is dependent upon the availability and motivation ofstaff it is also important to consider further the results of thestudy by Hanson et al (1976) Despite evidence of positiveeffects of control of the noisy stimulus Hanson et al (1976)also found that if control was taken away from the individ-uals which had previously had control over the noise theconcentration of cortisol in plasma increased to levelssimilar to the individuals that had never had control Thisincrease in cortisol was associated with the expression ofaggressive behaviours that were not observed in yokedanimals suggesting that loss of control is more stressfulthan never having had control in the first placeSambrook and Buchanan-Smith (1997) agreed that animalsneed to have a degree of control over events that affectthem but argued that having complete control over allevents is also sub-optimal They proposed that the conceptsof novelty and control are linked and that the novelty of anobject could be defined in terms of the degree to which theanimal has control over it Thus it is the process of learningto control and overcome the novelty of the stimulus that isrewarding Once an animal has gained control its expecta-tions of control rise to meet its ability to control and thusloss of control is stressful whilst the ability to controleverything in its environment results in predictability andregression into boredom Sambrook and Buchanan-Smith(1997) suggested that a balance between total control andlack of control is optimal and that by providing objects andenvironments that suggest controllability but that resistcontrol responsiveness can therefore be maintained In1996 Sambrook and Buchanan-Smith investigated therelative importance of control and complexity to fourspecies of guenons in a novel object study The results ofthis study supported the idea that control is important andthat an object whose responsiveness is contingent upon theanimalrsquos behaviour towards it becomes the target of moreattention than an object that is identical in appearance butdoes not respond However this study also suggested thatthe complexity of an object per se is not importantHowever it could be argued that if the complexity of theobject or environment increases its resistance to controlthen complexity contributes to enrichment Sambrook andBuchanan-Smith (1997) also argued that there is an

Animal Welfare 2006 15 215-238


optimum degree of predictability of events totalpredictability may result in behavioural frustration andboredom whereas complete unpredictability results instress This view is supported by the work of Markowitz andLine (1989) who found that an apparatus that rhesusmacaques can control but that is also responsive to manip-ulation was used by more individuals and for longer thanone that is unresponsive Older animals which have beenhoused singly for a long period of time do not respondgreatly to passive forms of enrichment but when given evena limited amount of control they show sustained use ofresponsive equipment and recover more quickly fromstressful encounters (Markowitz amp Aday 1998) Chamove(1989) also found that objects that responded to manipula-tion by captive chimpanzees were favoured over inanimateobjects and that objects that responded unpredictably werealso favoured This is consistent with the theory that avariable schedule of reward is more reinforcing than a fixedschedule of reward and is likely to reflect the animalsrsquoability to adapt to dynamic natural environments in whichanimals must learn to respond in effective ways in order tosurvive (Markowitz amp Aday 1998)

Housing conditions and enrichmentIn accordance with the European Directive (86609EEC)ldquoall experimental animals must be provided with housingan environment at least some freedom of movement foodwater and care which are appropriate to their health andwell-beingrdquo (EU 1986 Article 5 paragraph a)Details of how these provisions should be met are given inAppendix A to the European Convention (ETS 123) whichlists acceptable ranges and minimum standards of provisionfor most aspects of the housing environment including cagesize ventilation temperature humidity lighting noisealarm systems health monitoring feeding watering theprovision of bedding cleaning and the provision of exercise(European Commission [EC] 1986) These recommenda-tions are currently being revised but their present statusdictates the minimum standard of housing conditions forlaboratory-housed primates in Europe In practice theselection of housing and husbandry practices is dependentupon many factors including the use of the animal at thetime and the related need for human contact age researchneeds personnel safety animal safety staff experienceeconomic considerations climate and the degree of urbani-sation For example breeding and stock animals are usuallyheld in different accommodation from that in which animalson experiment are held (Baskerville 1999) The cages usedfor experiments are commonly the most restrictive ananimal will experience (Baskerville 1999) Implicit withinthe European guidelines are the practicalities associatedwith laboratory use of primates Whilst providing a bareminimum of protection for primates housed in laboratoriesthey promote the needs of the institute scientist and careworker It must be accepted that the needs of staff involvedin the use of primates in laboratories are important espe-cially in terms of safety but it is also critical in the revisionof the guidelines to find a better balance between the needs

of staff and those of the animals Laboratory housing musttake into account costs practicality and experimentalrequirements as well as the needs of the laboratory-housedanimals

Environmental parameters

Temperature and humidity

Appendix A to the European Convention (ETS 123)includes recommendations on the rate of ventilation ofanimal rooms and acceptable temperature and humidityranges A ventilation rate of 15ndash20 air changes per day isconsidered adequate for all species in this guide It is alsostated that relative humidity should be maintained at55 plusmn 10 and that humidities below 40 and above 70should be avoided These very general recommendations donot take into account the very different ecology of the rangeof primate species kept in laboratories For example NewWorld species typically inhabit warm but very humidhabitats in the rainforest whereas baboons may live incomparatively arid climates However control of the rangeof humidity within the suggested bounds is likely to bemore easily maintained than more extreme states ofhumidity Similarly the current Appendix A recommendsthat the temperature of primate housing should be main-tained at 20ndash28degC for New World species whereas OldWorld primates should be housed in rooms kept at 20ndash24degC(EC 1986) Although maintenance of the environment atthis temperature is unlikely to adversely affect welfare thisrecommendation does not take into account the range oftemperatures at which primates would live in the wild Themaintenance of temperature and humidity within thecurrently required ranges is practical in that they ensure thatthe working environment is not uncomfortable for the staffIt is noted in the current Appendix A that the temperatureand humidity range suitable for very young primates issmaller than that for adults a difference that must be takeninto account (EC 1986) The species-specific differences inenvironmental requirements are recognised in the ongoingrevisions of Appendix A It is noted that fluctuations inhumidity are less well tolerated by marmosets (Callithrixspp) and tamarins (Saguinus spp) and that these speciesshould not be exposed to humidity of less than 30 as respi-ratory disorders may result Poole et al (1999) noted that therelative humidity should be in the range 40ndash60 In therevised Appendix A species-specific variations in tempera-ture requirements are also recognised A temperature rangeof 23ndash28ordmC is recommended for housing marmosets andtamarins and similar temperatures are considered appro-priate for squirrel monkeys (24ndash26ordmC) A wider range oftemperatures is considered appropriate for the majority ofmacaque species used in laboratories and for baboons(16ndash25ordmC) However it is noted that a temperature range of21ndash28ordmC is more appropriate for the long-tailed macaque

Lighting

Although recommendations regarding the appropriatetemperature and humidity for housing primates in laborato-ries are given in the current Appendix A to the European



Convention (ETS 123) little consideration is given to lightintensity in primate housing (Reinhardt 1997a) InsteadAppendix A states that there is a need to satisfy the biolog-ical needs of the animals and to provide a safe workingenvironment Evidence shows that lighting levels can affectboth the breeding success of laboratory-housed primatesand their behaviour For example in common marmosetsbright conditions have been shown to increase breedingsuccess and activity whereas dim conditions inhibitbreeding and result in reduced activity (Heger et al 1986)In contrast however Schapiro et al (2000) found no statis-tically significant differences in behaviour in long-tailedmacaques (Macaca fascicularis) housed in cages that variedin illumination In natural conditions light intensity variesfrom 100 000ndash150 000 lux in bright sunlight to 5ndash10 lux indim moonlight (Clough 1999) Recommendations for thelight intensity of animal rooms range from 150 to 400 lux inthe centre of the room (Clough 1999) However lightinglevels in animal rooms are not constant and those housed inlower tier cages may experience light of a much lowerintensity than those in the top tier (Reinhardt amp Reinhardt2000a) Consideration should also be given to the wave-length of light as different types of bulb emit light ofdifferent wavelengths (fluorescent lights emit moregreenndashyellow light [500ndash650 nm] whereas incandescentlamps emit light at the red end of the spectrum[600ndash700 nm]) (Clough 1999) The range of colours thatprimates can see should thus be taken into account whenselecting the lighting system (Strasser 1970 cited in Clough1999) It has been shown that exposure to natural light canreduce the occurrence of abnormal behaviours in youngrhesus monkeys (OrsquoNeill 1989) and it has been suggestedthat choices of the intensity and potentially the wavelengthof light should be provided matching the choices made byprimates in the wild between sunlight and shade (Buchanan-Smith 1997) If it is not possible to provide natural light inthe laboratory (for physical or scientific reasons) it hasbeen recommended that artificial light that provides a widerange of wavelengths in a natural way (without introducingharsh contrasts) should be used (Clough 1999) Howevercare should be taken when selecting an appropriate lightingregime for primates Lights that simulate sunlight areavailable commercially but it has been found that the use ofthese lights has both positive and negative effects on thebehaviour of primates with comparison to artificial fluores-cent lighting Novak and Drewsen (1989) compared thebehaviour of laboratory-housed rhesus macaques before andafter exposure to a lamp designed to simulate natural lightThey found that monkeys exposed to both the light andradiation from the lamp showed an increase in affiliativebehaviour which persisted when the animals were returnedto normal artificial light In contrast monkeys which wereexposed to the light from the lamp but were protected fromthe ultra-violet (UV) radiation showed an increase in affil-iative behaviour which declined again when the animalswere returned to fluorescent lighting Monkeys exposed toUV radiation also showed more aggressive and sexualbehaviour and showed greater urinary cortisol responses to

stress than those exposed only to the light from the lampThus it appears that in rhesus monkeys exposure to a lightsource which simulates natural light can result in changes inbehaviour that are likely to be indicative of increasedpsychological well-being but exposure to UV radiationfrom these light sources may not be so beneficial Incontrast marmosets and tamarins benefit from exposure toUVB radiation which reduces the incidence of metabolicbone disease and improves immunity (Hampton et al 1966Lopez et al 2001) However no empirical data on the effectof UVB radiation on the behaviour and psychological well-being of marmosets and tamarins have been foundIt has been recommended that light should be faded in andout at the start and end of each day to simulate dusk anddawn so that the animals are not plunged into darkness orlight (Buchanan-Smith 1997) As most primate speciesnaturally inhabit regions close to the equator a 12-hourlightdark cycle is considered to be most appropriate butlow intensity light should be provided at night to allowanimals to readjust their position without dangerAdjustment of day length can also be made to simulatenatural seasonal changes which may also aid breeding(Buchanan-Smith 1997) The need to control lighting withinthe laboratory has been acknowledged in the revision ofAppendix A to the European Convention (ETS 123)Noise

Ventilation heating systems automated washing machinesalarms and general human and animal activity all createnoise The use of easily cleaned stainless steel caging andhard surfacing on walls and floors makes the job of the careworker easier but it also increases the noise levels in theenvironment It should be noted that the ability of humansto perceive sound is very much less developed than that ofmost other animals and the level of sound that we perceivein the laboratory is likely to be very much less than thatwhich primates perceive (Clough 1999) This is particularlytrue of New World species which communicate using high-pitched frequencies and are known to be able to hear ultra-sonic frequencies (Sales et al 1999) Sudden loud noises cancause fear and continuous exposure to loud uncontrollablenoise has been found to be stressful to primates (Hanson etal 1976) The current European recommendations do notinclude specification of acceptable noise levels (EC 1986)but UK guidelines recommend that background noise in thelaboratory should not exceed 50 dB (Home Office 1989)and in the draft revision of Appendix A of the EuropeanConvention (ETS 123) it is recommended that backgroundnoise in the laboratory should not exceed 65 dB for morethan short periods of time The limits on noise recom-mended in the UK guidelines are supported by Clough(1999) who considered that if background noise is main-tained below 50 dB adverse effects on biology should beprevented The use of bedding floor substrate and woodenfurniture can dampen noise to some extent but sources ofultrasound for example from dripping taps and computermonitors should be identified and shielded or removedwhere possible (Clough 1999) The provision of low-level



background noise like soft music or the radio has beeninvestigated as a means of masking sudden loud andorunfamiliar noises and as a form of enrichment For examplein a recent study Howell et al (2003) found that exposure tomusic loud enough that the lyrics and melody could beheard resulted in a decrease in aggressive or agitatedbehaviours and in active and exploratory behaviours and inan increase in affiliative inactive behaviours like groomingin chimpanzees (Pan troglodytes) Howell et al (2003)noted that the reduction in aggressive or agitated behaviourwas most pronounced in the morning when routinehusbandry procedures were carried out and that theincrease in affiliative behaviour was most pronounced ingroups composed entirely of females An increase in affilia-tive behaviour was also recorded in rhesus monkeys duringexposure to jazz music and occurred irrespective of whetherthe monkeys could or could not control their duration ofexposure to the music within a 2-hour period (Novak ampDrewsen 1989) OrsquoNeill (1989) noted that abnormal behav-iours associated with confinement in winter housingincluding stereotypical behaviours and self-mouthing werereduced when young rhesus macaques were exposed toclassical musicAlthough music and masking sounds have apparentlypositive effects in some studies not all attempts to enrichthe lives of captive primates with music and other soundshave produced clear results For example after exposure torainforest sounds adult lowland gorillas (Gorilla gorilla)showed more frequent locomotion thought to be indicativeof agitation whereas infants spent less time clingingsuggesting that the sound successfully masked the noisesproduced by caretakers ventilation systems and otheranimals It was concluded that the rainforest sounds wereenriching for the infant gorillas but increased agitation inthe adults (Ogden et al 1994) It is possible that the maskingof routine husbandry noises induces stress because theanimals are no longer able to monitor the position andactivity of staff It should also be noted that such maskingnoises must be selected to suit the species concerned Muchof the sound produced by a radio is of a frequency that isthought to be imperceptible to rats (Clough 1999) and mayalso be imperceptible to New World primates (McDermottamp Hauser 2004) It has also been suggested that the soundsintended to mask aversive noises in the laboratory mayinadvertently mask communications between conspecifics(Newberry 1995) the effects of which are likely to bedependent on the nature of the communications that aremasked

Cage sizeAccording to Appendix A of the European Convention (ETS123) the vertical height of cages provided for primatesshould be the greatest dimension and is considered to be justas important as the floor area although this is emphasisedonly for simian primates and apes The guidelines also statethat it is important that the animal can stand fully erect andthat those species that brachiate can extend their bodiesfully without their feet touching the floor Recommended

sizes range from that for primates weighing less than 1 kg(callitrichid species) for whom the minimum required cagesize is 025 m2 with a height of 060 m to that for primatesweighing 15ndash25 kg for whom a floor area of at least 15 m2

and a cage height of 125 m are recommended According tothe guidelines these cages can hold either one or twoanimalsThe minimum standards are considered by many to be inad-equate because they are based upon the weight of the animaland do not consider the animalsrsquo linear dimensions This isproblematic for certain species for example the minimumrequired cage height for the relatively light long-tailedmacaque is actually less than the head-to-tail length of theanimal This means that long-tailed macaques housed in acage of minimum size cannot perch in the cage without theirtails touching the ground (Buchanan-Smith et al 2004) Thecurrent minimum cage size also does not allow for adequateexercise species-specific differences in behaviour or theincorporation of adequate environmental enrichment (Pooleet al 1994 Baskerville 1999)The assumption in Appendix A of the European Convention(ETS 123) that lighter animals require less space than heavyanimals is also refuted when we consider that the weight ofan animal is closely associated with its age and thatyounger lighter animals are generally more active than olderadults (Poole et al 1994) In response to these criticisms ofthe 1986 guidelines experts at the 1993 Berlin Workshop onthe Accommodation of Laboratory Animals in Accordancewith Animal Welfare Requirements developed new recom-mendations for cage size allowing for proper extension ofbody parts in all species and the incorporation of cagefurniture that would allow for the expression of morespecies-typical behaviour (Poole et al 1994) For marmosetsa minimum of 10 m2 of floor space was recommended forone to two adults and 025 m2 extra space was required foreach additional animal A recommended cage height of15 m was proposed In larger species 3 m2 of floor spacewas recommended for adult cercopithecoids of more than5 kg with a cage height of 15 m (Poole et al 1994) Thusthe importance of vertical height in the cage was empha-sised for the small and naturally arboreal species but notprioritised to such an extent for Old World primates manyof which live semi-arboreal lives in the wild In practice itis important that a distinction is made between differentspecies of Old World monkeys as the extent to which thevertical dimension of the cage is used varies between eventhe most commonly used species of macaque Rhesusmacaques are naturally the most terrestrial of the macaqueswhereas long-tailed macaques are a mainly arboreal species(Baskerville 1999) The importance of cage height tocommon marmosets was demonstrated by Ely et al (1998)who found that they used the upper part of the cage in pref-erence to the lower half Although the provision of verticalspace appears to be important the positive effects ofincreased cage height can be negated if a tiered cagingsystem is used Cage height is thought to be important toaccommodate primatesrsquo need for a vertical escape response



It is also likely that animals in the lower tier are inspectedless thoroughly because they are not as easy to see bothbecause of limited lighting and because the carer must bendto see clearly (Reinhardt amp Reinhardt 2000a) Poole et al(1999) and Baskerville (1999) stated that marmosetstamarins and Old World monkeys show a preference to lookdown on handlers From this vantage point they canproperly assess the magnitude of danger The restriction ofthe vertical flight response in lower tier caging may be asource of stress as the individual is unable to respond in aspecies-appropriate manner to perceived dangers forexample the sudden appearance of a handler (Baskerville1999 Poole et al 1999) Ely et al (1998) examined this pref-erence in habituated common marmosets and found that thepreference for height in the cage was associated with theheight of the handlerrsquos face suggesting a desire to interactwith the handler rather to retreat beyond their reach Theseresults demonstrate that if a positive working relationship isdeveloped (Rennie amp Buchanan-Smith 2006) vertical flightshould not occur in response to caretakers entering a roombut that in fact the presence of handlers in the room can beenriching (Ely et al 1998)In an investigation to determine the effects of cage size onbehaviour appetite and urinary cortisol in pig-tail macaques(Macaca nemestrina) Crockett et al (2000) found thatappetite and urinary cortisol were unaffected by housing incages ranging from 22 to 148 of the recommended size(USA recommendations) The study also found thatbehaviour was unaffected in all but the smallest of thecages which was so small that it effectively prevented anylocomotion at all However it was noted in this study thatno cage furniture (for example perches) was includedBayne and McCully (1989) found that housing rhesusmacaques in the next available cage size (USA standards) achange in cage size that might practically be offered in factincreased the occurrence of self-directed abnormal behav-iours This demonstrates that increased cage size alone doesnot constitute an enrichment if no further enrichment isprovided to enable the animal to respond appropriately tochallenges associated with life in the laboratory In contrastDraper and Bernstein (1963) found that in rhesusmacaques large increases in cage size had a significanteffect on behaviour and greatly reduced the occurrence ofstereotypical behaviours The cages used in this study weremuch larger (091 times 091 times 091 m 12 times 091 times 244 m and732 times 1463 times 244 m [length times width times height] for smallmedium and large cages respectively) than those studied byCrockett et al (2000) and Bayne and McCully (1989) butperhaps more importantly were constructed from wire onwhich the monkeys could climb and hang Thus whenhoused in the larger cages the monkeys were able to makeuse of the whole space in a species-typical mannerBuchanan-Smith et al (2004) argued that a suite of charac-teristics (including morphometric physiological ecolog-ical locomotor social reproductive and behaviouralcharacteristics) should be used to determine minimumcage size

Cage furnitureIn order to ensure that primates use their allotted space tothe fullest extent the furnishing of the cage must be consid-ered carefully It is also essential that the furniture does notunduly interfere with cleaning feeding capture and impor-tantly in the laboratory easy inspection of the occupants Inthe smallest cages the opportunities for enrichment areobviously fewer but small changes can have a dispropor-tionately positive effect on welfare The principles ofenrichment of cage design and structure are the sameregardless of the size of the cageThe provision of perches adds a vertical dimension to abarren cage and gives the occupant a vantage point and inrhesus macaques (Reinhardt 1994b) and New Worldmonkeys (Buchanan-Smith 1997) offers space to groomWhere space will allow the provision of multiple perches ofdifferent diameters has been recommended (Roder ampTimmermans 2002) and introduces variety that canstimulate very different behaviours For example Caine andOrsquoBoyle (1992) found that red-bellied tamarins (Saguinuslabiatus) tended to show more wrestling play on flat hori-zontal perches and more chasing play on thinner branch-likestructures In New World monkeys the provision of swingsslings ladders and ropes which move in response tomovement by the cage occupant adds an element ofcontrollable unpredictability to a very simple enrichment(Buchanan-Smith 1997) Such structures can be made of avariety of materials including PVC (Reinhardt 1997b)rubber wood (Buchanan-Smith 1997) or metal (Kelley ampHall 1995) In the case of marmosets the provision ofwooden branches allows the performance of species-typicalgnawing and scent-marking and in macaques the provisionof wooden perches or blocks has been recommendedbecause it increases species-typical manipulation andgnawing a possible element of dental care (Reinhardt1997c) The use of wooden furniture is important for allcallitrichid species as they have claw-like rather than flatnails on all digits except for the thumb and therefore havedifficulty gripping smooth metallic and plastic surfacesAlthough wooden structures will need to be replaced morefrequently than the highly resistant PVC and metal alterna-tives they are cheap (Baskerville 1999) and can still becleaned in standard cage-cleaning machines or by hand(HM Buchanan-Smith personal observation 2006) Theyalso provide a higher degree of responsivity and texture aswell as dampening noise (Baskerville 1999 Poole et al1999 Eckert et al 2000) It is commonly supposed that theanimals prefer wood to metal and plastic substrates(Baskerville 1999 Eckert et al 2000) but no publishedempirical data on such a preference could be foundAlthough studies have shown that Old World primates canbenefit from the provision of structural enrichment theirresponse varies depending on the enrichment offered Forexample Dexter and Bayne (1994) reported no change inthe occurrence of abnormal behaviour in adult rhesusmacaques which were provided with different types ofswing The authors concluded that swings do not constitute



an enrichment for singly-housed adult rhesus macaques Incontrast Kopecky and Reinhardt (1991) compared the useof swings with that of perches as means of enriching cagesof paired adult female rhesus macaques They found thatperches were used eight times more often than swings andthat swings distracted the animals for a negligible timeperiod The authors proposed that this preference arosebecause perches allowed the macaques to sit in a species-typical relaxed posture near the front of the cage fromwhere they could view the environment outside the cagemore easily This demonstrates the need to consider species-typical behaviour when selecting appropriate enrichmentsfor primates of different speciesWild marmosets and tamarins seek security by climbinghigh into trees and hiding in dense vegetation Cagedcallitrichids benefit from the provision of similar refuges bythe inclusion of wooden nest boxes high in the cage (Pooleet al 1999) Thus callitrichids typically retreat into nestboxes to rest for the night a habit which is beneficial forhuman carers as the animals remain active during the dayand thus the nest box does not normally prevent easyinspection of the cage occupants Similarly families of owlmonkeys (Aotus spp) naturally seek the shelter of a hollowin a tree trunk or in dense foliage in which to sleep duringdaylight hours and benefit from the provision of a nest boxin which the whole family can rest (Erkert 1999) Howeverbecause owl monkeys are only active at night it is beneficialto maintain their 12-hour lightdark cycle so that at leastsome of the animalsrsquo waking hours occur during workinghours (Erkert 1999) Low lighting must be provided toallow inspection of the animals Wood is preferable forconstruction of nest boxes because unless well ventilatedbreath condensate can collect on the inside of metal andplastic boxes and on the fur making the animals wet and ithas been suggested that wet fur falls out more easily (Pooleet al 1999) Screens can also provide refuge particularlyfrom aggressive encounters (Chamove 1984) and resultedin increased affiliative behaviour in groups of marmosetsand tamarins (McKenzie et al 1986) The beneficial effectsof screens were found to be less in stable social groups(McKenzie et al 1986) Care must be taken that screens donot interfere with inspection of the animals Indeed retreatto a refuge for long periods of time and avoidance ofcompanions can often be a sign of a health andor welfareproblem (Wolfensohn amp Honess 2005)A further means of enrichment which has been used mainlywith the common marmoset (Callithrix jacchus) is theaddition of a small veranda to the front of the cage Thisprovides additional space in the cage but also provides avantage point from which individuals can see the activitiesof conspecifics in other cages and of staff more clearlyStudies have shown that verandas are the most highlypreferred area in the cage (Ely et al 1998) However theirplacement must be carefully considered as they bring indi-viduals into closer proximity This has the potential to leadto arousal and redirected aggression towards cagemates(HM Buchanan-Smith personal observation 2006)

The selection of a good floor substrate can encourage theanimals to use the floor space even in arboreal species likethe common marmoset that are naturally less inclined to doso (McKenzie et al 1986) This effectively increases theamount of usable space in the cage (Chamove and Anderson1989) Many authors recommend a solid floor and suggestthat it should be covered with wood shavings straw or asimilar substrate (McKenzie et al 1986 Buchanan-Smith1997 Poole et al 1999 Roder amp Timmermans 2002) Foodcan be scattered amongst such substrates to provideforaging enrichment (McKenzie et al 1986 Newberry1995)Enrichment can be provided for animals housed in smallcages by allowing them access to a separate large play roomor cage on a rotational basis In studies in rhesus macaquesJapanese macaques (Macaca fuscata) and capuchins (Cebusapella) (Bryant et al 1988 Tustin et al 1996 Wolff ampRuppert 1991) such cages were used to provide enrichmentfor singly housed animals Although this system of rota-tional enrichment resulted in an increase in active behav-iours in both the play cage and the home cage (Tustin et al1996) and could be managed safely for the majority ofsingly caged animals (Wolff amp Ruppert 1991) the positiveeffects appear to be less for older animals which had beensingly caged for a long period of time before visits to theplay cage were introduced These individuals sat in oneplace for the entire exercise periodIt should be noted that although the use of such cages hasthe potential to be beneficial the removal of a primate fromhis or her home cage can be stressful (Reinhardt et al 1990)especially if the animal is unused to the procedure Careshould be taken to ensure that the animals get used tomoving to the play room or cage on a regular basis and thattransfer is achieved using the least stressful possible meansIt is proposed that although the rotational use of a play cagemay appear beneficial whilst in use it is possible that theloss of enrichment on return to the home cage is morestressful than the lack of such enrichment in the first placein accordance with evidence showing that loss of control isstressful (Hanson et al 1976) This theory is supported byBryant et al (1988) who concluded after examination ofseveral enrichment strategies that rotational group use of aplay area was less beneficial not only than continuousaccess to a pair-mate within the home cage but also than theintroduction of enrichment to the home cage However thisshould not be taken to imply that animals destined for singlehousing should not be socially housed whenever possiblePrimates will be better socially adjusted and better able tocope with the challenges that they face in laboratory exper-imentation if they have a secure social environment Thework of Novak (2003) and Lutz and Novak (2005) showsthat the age at which rhesus macaques are put into singlehousing impacts on whether they will develop abnormal(stereotypical and self-injurious) behaviours Thereforemaintaining primates in species-appropriate social condi-tions for as long as possible is advisable



Cage space can be increased in standard caging systems bylinking more than one cage together with tubing This hasbeen achieved with both New and Old World monkeys(Baskerville 1999 Poole et al 1999) Such tubing moveswhen the monkeys move through it creating a responsivesubstrate and a degree of unpredictability It has been foundthat monkeys spend a large proportion of their time in cagelinks which can be used as a vantage point from which moreof the colony room and other animals in the colony can beseen (Scott 1991)

Novel objects and feeding enrichmentToys and other enrichment devices have also been intro-duced to cage environments to increase species-typicalbehaviour Their provision is dependent upon cost and themotivation and time of staff and therefore must be cheap (orfree) and easy to deliver It is imperative that such toys arerelatively safe even on destruction so that attemptedenrichment does not result in harm Examples of enrichmenttoys and devices include interactive computer gamesactivated by a joystick (Bloomsmith et al 2001) movingand standing water (Parks amp Novak 1993) pools for diving(Anderson et al 1992) mirrors both hand-held and attachedto the wall (Brinkman 1996) Nylaballsreg and other itemssuitable for chewing (Tustin et al 1996) phonebooks(Brinkman 1996) cardboard or plastic tubes and containers(Buchanan-Smith 1997) In a study of a wide range of toysprovided for single-housed male long-tailed macaquesBrinkman (1996) found that those toys that were manipu-lable and could be carried around were used mostfrequently Species-specific differences in the use of suchobjects should be considered if maximum enrichment is tobe gained from their use For example interactive toysgiven to the common marmoset must be small and lightenough for the animal to move or carry around (Buchanan-Smith 1997) Rotation of toys can help to maintain novelty(Brinkman 1996 Buchanan-Smith 1997)Primates are adapted to spend most of their waking hoursforaging and feeding (Anderson amp Chamove 1984) Forexample long-tailed macaques spend more than 50 oftheir time either foraging or feeding (Wheatley 1980 ascited by Baskerville 1999) In the laboratory food is oftenprovided in an easily accessible form and much of the timethat should naturally be spent feeding remains unusedFurthermore when primates are housed in social groups itis common for the more dominant individuals to monopo-lise easily accessible food sources (Tardif amp Richter 1981Michels 1998) Thus extending the time spent feeding hasbeen one of the main targets of enrichment strategies for allcaptive and laboratory-housed primates (eg Snowdon ampSavage 1989) All or a proportion of the daily allowance offood can be presented in enriched feeding systems Caremust be taken that all animals are still able to obtain suffi-cient food This can be achieved by feeding specificallydesigned complete foods in the morning with enrichedfeeding provided later in the day as it is important to ensurethat the animals continue to obtain balanced nutrition(Wolfensohn amp Honess 2005) The provision of a foraging

substrate in which small items of feed (eg grain orsunflower seeds) can be scattered and then foraged for hasbeen found to increase species-typical foraging and toreduce aggression (Chamove et al 1982 Anderson ampChamove 1984) Similar foraging opportunities can beprovided by means of foraging trays which may be easierto remove and keep clean (Spector et al 1994) Food canalso be buried in straw or placed in puzzle feeders fromwhich the primate can obtain a desired food item simply bypersistent manipulation or by learning the lsquotrickrsquo to solve thepuzzle (eg Murchison amp Nolte 1992 Box amp Smith 1995Murchison 1995 Pyle et al 1996 Buchanan-Smith 1997Glick-Bauer 1997) More simply food can be given in aform that requires manipulation and processing beforeeating for example by feeding nuts in their shells and fruitthat has not been peeled (Buchanan-Smith 1997) or byfreezing juice (Schapiro et al 1996) or small items of foodwithin ice cubes Spreading feeds over a wider area andensuring that items take longer to eat also makes it moredifficult for dominant animals to monopolise the feedFrozen items may also aid cooling if primates are exposedto warm climatic conditions These feeding enrichments notonly increase the time taken to feed but also increase theanimalsrsquo choice about when to feed and what to feed onSpecies-specific feeding enrichments have been designedand used with great success For example McGrew et al(1986) developed a wooden gum-feeding device forcommon marmosets in which the marmosets could gougethrough the wood in a naturalistic manner to obtain gumarabic Anecdotal evidence in the white handed-gibbon(Hylobates lar) and quantitative evidence from preferencestudies in stump-tailed and rhesus macaques and in chim-panzees indicate that primates may prefer to work to obtaintheir food rather than obtain it more quickly for free(contrafreeloading) (Markowitz 1982 Anderson ampChamove 1984 Menzel 1991 Reinhardt 1994a) Studieshave shown that the predictability of feeding has a signifi-cant effect on the psychological well-being of laboratory-housed primates It has been shown that highly predictableschedules of feeding can be associated with food anticipa-tory activity characterised by increases in arousal andactivity and the occurrence of stereotypical behaviours(Mistlberger 1994 Bloomsmith amp Lambeth 1995) Bassett(2003) found that common marmosets showed more signsof arousal and anxiety prior to feeding when they were fedon an unreliable temporal schedule and with unreliablesignals than control animals This feeding schedule isanalogous with schedules commonly seen in laboratoryhusbandry systems where noises associated with foodpreparation and delivery may be associated with thedelivery of food with the food being delivered to otheranimals or being delayed In contrast those marmosets thatwere fed on an unreliable temporal schedule but were givena reliable signal informing that feeding would occur showedno change in behaviour with respect to controls Bassett(2003) suggested that the provision of a reliable signalgiven just prior to feeding could therefore be used to reducestress associated with food anticipation and frustration of



feeding motivation Bassett and Buchanan-Smith (in press)provided a thorough review of the behavioural and physio-logical effects of the predictability of aversive and appeti-tive stimuli and the application of experimental findings toanimal husbandry in practice

Section summary and conclusionsThe introduction of enrichments has been found to reducestress and frustration increase primatesrsquo ability to cope withstressful experiences and improve their health and repro-duction To be most effective enrichments must be appro-priate for the species concerned but also should not hinderlaboratory practice unduly The complexity andpredictability of enrichments are important as these charac-teristics affect the rate at which the animal can learn to exertcontrol over the enrichmentThe temperature and humidity must be appropriate to thespecies and age of primates Natural wavelengths of lightare most appropriate although the effects of exposure toUVB radiation vary with species The provision of choicebetween light and shade and an artificial dawn and dusk arethought to be beneficial Background noise should be keptto a minimum and ultrasonic noise should be eliminatedwhere possible Music can be beneficial to mask suddennoises but may reduce ease of communication and predic-tion of significant eventsThe animalrsquos size age and natural propensity for activityand arboreality should be taken into account in determiningcage dimensions Cage height is considered to be importantto highly arboreal New World primates although relation-ships between staff and animals should be such that care-takers do not cause a vertical flight response Cage furnitureshould maximise useable space and facilitate expression ofa range of species-typical postures and behaviours Objectenrichments must be appropriate to the species but withthought and motivation can easily be delivered on a routinebasis with little cost Feeding enrichment should be used toincrease foraging time and food manipulation and reducethe possibility of food monopolisation

Social enrichment and husbandry of primatesNo method of enrichment for laboratory-housed primateshas been found to be as effective as the presence ofconspecifics (Hennessy 1984 Reinhardt 1990 Schapiroet al 1996) especially those favoured by the individual(Smith et al 1998) and an inherent need for social compan-ionship has been recognised in most primate species (egHarlow amp Harlow 1962) However it has been noted thatalthough all infant primates require social contact species-specific differences exist in the optimal social grouping(Novak amp Suomi 1991) For these reasons guidance on theideal grouping and social dynamics for laboratory-housedprimates should be taken from natural populations(Buchanan-Smith 1997) matching their social environmentas closely as possible with that to which they are adaptedthrough evolution

Single housingSingle caging of primates has traditionally been the housingmethod favoured by researchers in an attempt to minimiseexperimental variation (Hartner et al 2001) Single cagingalso allows relatively easy and safe access to the animalsfacilitates monitoring and reduces the risk of injury anddisease transmission associated with social housing(Kessler et al 1985 Line 1987 Hartner et al 2001) thusfurther reducing experimental variation (Baskerville 1999Hartner et al 2001) It is now widely recognised that singlehousing of primates is detrimental to psychological well-being in the majority of primate species preventing socialinteraction and because single cages are typically small andbarren reducing scope for enrichment and the expression ofspecies-typical behaviours (Hartner et al 2001) Theevidence of psychological distress as a result of socialisolation is extensive and dates back to the early 1960swhen the effects of social isolation on primates were thesubject of considerable interest in relation to human devel-opment (eg Harlow amp Harlow 1962) Harlow and Harlow(1971) described several abnormal behaviour patterns insocially deprived rhesus macaques of all ages includingself-sucking and biting rocking abnormally passivebehaviour and stereotypical behaviours Similarly studiesby Gluck and Sackett (1974) showed that the occurrence ofself-aggression was more common in socially isolated indi-viduals of both sexes Single caging can result in loss ofcondition nervous behaviour and an increased incidence ofinjury disease and mortality in both New and Old Worldprimate species (Reinhardt 1990 Poole et al 1999) Sucheffects are likely to increase experimental variation ratherthan reduce it (Garner 2005) For example Gwinn (1996)found that singly housed squirrel monkeys lost more weightafter the application of a test substance than those that werehoused in pairs Detrimental effects of poor psychologicalwell-being on the immune system have also been indicated(Laudenslager et al 1982 1990 Coe 1993 Clarke et al1996 Gust et al 1996 Johnson et al 1996a) For exampleindividuals experiencing social stress have been found to bemore susceptible to disease whereas those receiving affilia-tive behaviour showed more rapid immune system recovery(Gust et al 1996) Contrary to the belief that single housingreduces injury and disease transmission Reinhardt (1990)found that during one year only 10 of socially housedrhesus monkeys required non-experimental veterinarytreatment In contrast more than 25 of singly housedrhesus macaques required such veterinary treatment(Reinhardt 1990) Serious wounding occurred in only 08of socially housed animals in 36 months Further Schapiroet al (2000) found that socially housed rhesus macaquesshowed enhanced immune responsiveness in comparisonwith singly housed individuals following challenge withgastrointestinal pathogens and Staphylococcus aureus Theytherefore argued that immunological studies carried out onsingly housed animals may be more difficult to interpretand that in order to study the effects of ecologicallyrelevant immune challenge primates must be housed in anecologically relevant environment for example a stable



species-typical social structure and management systemthat minimises stressOld World monkeys continue to be housed in single cagesmore frequently than the smaller callitrichid species mainlybecause of their size and the comparatively higher risk asso-ciated with handling them However the traditional viewthat primates particularly macaques are dangerous andaggressive is changing (Reinhardt 2002) and more of thoseinvolved in primate care accept that aggression directedtowards handlers is most likely to occur when the animalfeels threatened or insecure (Hartner et al 2001)Breeding in single cages

Although single caging is most commonly used for animalson experiments some establishments continue to houseprimates in single cages full-time Baskerville (1999)described how timed breeding of Old World monkeys canbe carried out in a single caging system by introducing thefemale to the malersquos cage for mating and removing heragain when mating has taken place This system allows theproduction of infants to suit demand and ensures that thepregnant female can be easily monitored For competentmothers the birth of an infant probably improves well-being as the infant provides social contact and a naturalfocus for her maternal behaviour However for thesemothers the return to single housing when the infant istaken away at weaning has considerable adverse effects(Seay et al 1962 Coe et al 1983) In contrast for newandor incompetent mothers continuous exposure to theinfant may represent a source of stress (Capitanio et al1985) Therefore this system not only has significant detri-mental effects on the adults involved but also results inabnormal physical behavioural and psychological develop-ment in infants as normal social interaction with numerousconspecifics of varying ages is prevented (Harlow ampHarlow 1962) Satisfactory (or normal) socialisationincluding experience of normal maternal care and play(Fagen 1993) has been shown to be critical for the mainte-nance of health and growth (Green 1990) and to prevent thedevelopment of abnormal and stereotypical behaviours(Harlow amp Harlow 1971) Abnormal or inappropriate socialbehaviour incompetent or absent sexual behaviour as anadult and reduced maternal aptitude occur in individualswhich are not raised maternally (Harlow amp Harlow 1962Mitchell et al 1966 Suomi 1978 Capitanio 1986Ljungberg amp Westlund 2000) Ruppenthal (1992) showedthat the offspring of singly caged mothers are more likely tobe subordinate when socially housedTimed breeding has not proven to be a successful produc-tion strategy in squirrel monkeys (Mendoza 1999) or inmarmosets and tamarins (Poole et al 1999) Meanwhile innocturnal lemurs males and females naturally meet only tobreed and thus timed matings may be the most appropriatemeans of breeding these animals in the laboratory (Bearderamp Pitts 1999)

Social enrichment in single cages

It is noted that some experimental protocols may stillrequire single housing and that it is not always possible to

house primates in alternative systems if a suitable partner(s)cannot be found (Line et al 1991 Watson 2002) In thesecircumstances refinements to reduce the detrimental effectsof isolation must be used Numerous potential methods ofinanimate enrichment are described above but in addition itis vital to provide some social enrichment in single housingsystems and complete social isolation should never occurThe ability to observe other singly housed conspecifics canbe beneficial and physical contacts (eg holding hands orgrooming) between individuals in adjacent cages arecommonly observed (Wolff amp Ruppert 1991 Brinkman1996 Crockett et al 1997) Anderson and Chamove (1986)found that the provision of a mirror to isolated infant stump-tailed macaques partially compensated for the lack of socialinteraction with conspecifics although these individualswere still less responsive than individuals raised with a peer(Anderson amp Chamove 1984) Interaction with humans canbe seen as a form of social enrichment and animals whichdevelop a bond with their regular carers may actively seeksuch interactions (Waitt amp Buchanan-Smith 2002) Thismay explain why animals take part in positive reinforce-ment training sessions voluntarily as it provides an oppor-tunity for social interaction as well as an opportunity tolearn and to gain rewards

Isosexual pairingAs an alternative to single housing primates in laboratoriescan be housed in isosexual pairs Such pairing is consideredto be a useful means of keeping stock animals (Baskerville1999 Poole et al 1999) Although this grouping is unnaturalfor the species most commonly used in laboratoriesevidence shows that such pairing can improve well-beingIsosexually pair-housed rhesus macaques spend more than20 of their time grooming one another (Reinhardt ampCowley 1990 Reinhardt 1991) a behaviour used tomaintain social cohesion and known to reduce heart rate andtension within groups of primates (Nieuwenhuijsen amp deWaal 1982 Schino et al 1988 Boccia et al 1989)Grooming has also been shown to result in the release of β-endorphin indicating a physiological basis for reward inboth groomer and groomee (Keverne et al 1989) The tran-sition from single housing to pair-housing has also beenreported to stop the occurrence of self-biting behaviour inrhesus macaques that had been observed self-biting over aperiod of 4 years (Reinhardt 1999) and to reduce otherabnormal behaviours including abnormal postures stereo-typic actions stereotypic locomotion and self-abuse (Lineet al 1990) Further Schapiro and Bushong (1994) showedthat isosexually pair-housed rhesus macaques had diarrhoealess frequently than singly housed individuals Hennessy(1984) found that isosexually pair-housed squirrel monkeysshowed reduced responsiveness to stressful stimuli in thepresence of a newly introduced pair-mate than they didwhen exposed to the stressor in isolation even if they hadexperienced little social contact prior to pairing Thusduring any stressful experience associated with laboratoryuse including routine husbandry and procedures thepresence of a companion may increase the ability of indi-vidual primates to cope



Factors influencing isosexual pair formation

Studies by Erwin (1986) indicated that bonds betweenfemale macaques and baboons can endure despite separa-tion for up to 25 years This work also demonstrated thatrelations between familiar males tended to be moreamicable than those between unfamiliar males Severalfactors influence the ease with which pairs may be formedincluding the species concerned and the age sex andprevious experience of the individualIn rhesus macaques the social experience of individuals cansignificantly affect their compatibility during pairing orgrouping as socially inexperienced individuals show lessappropriate social behaviour than those reared naturally(Mitchell et al 1966) Species differences in the ease withwhich primates will accept unfamiliar individuals must beconsidered For example in callitrichid species it has beensuggested that marmosets are likely to be more difficult tomix than tamarins because young tamarins tend to migrateto new groups whilst marmosets remain in their natal group(Poole et al 1999) Aggression tends to occur morefrequently and to be more serious between sexually matureprimates (Goosen et al 1984 Lynch 1998 Majolo et al2003b) In macaque species aggression tends to be moresevere between sexually mature males (Crockett et al 1994Watson 2002) although females are also aggressive to unfa-miliar females In marmosets and tamarins females have atendency to be more aggressive to female conspecifics thanto males and males are less aggressively reactive overallthan females (French amp Inglett 1989 Rothe amp Darms1993) Owl monkeys of the same sex should not be housedtogether as aggression is common resulting in severe injury(Erkert 1999) These differences are the result of speciesdifferences in social dynamics and behavioural ecologyAs an alternative to pairing adult primates several studieshave shown that mature animals can be successfully pairedwith sexually immature but socially experienced animalsof the same sex (Reinhardt et al 1987 Majolo et al 2003b)As play behaviour is most often observed between infantsor between an adult and an infant (Voland 1977 Fagen1981) this cross age pairing may result in the added benefitof increasing play and socially directed activity in the olderindividual (Majolo et al 2003b) Alternatively immatureanimals can be paired with conspecifics of the same age andsex In marmosets the simplest and least disturbing meansof pairing is to take the oldest same sex pair of twins froma family group and to house them together (Poole et al1999 Majolo et al 2003b) Sub-adult long-tailed pig-tailand rhesus macaques of the same sex have also been intro-duced and paired without serious aggression (Reinhardt1995 Cardinal amp Kent 1998 Watson 2002) It has thereforebeen recommended that where isosexual pairing of primatesis the only alternative for social enrichment the pairing ofsocially experienced but sexually immature individuals witheither a peer or with an adult should be preferred(Baskerville 1999 Poole et al 1999) However althoughadults do show more aggression (Majolo et al 2003b) thesupposition that all previously isolated adult primates of

limited social experience are impossible to pair isunfounded (Harlow amp Harlow 1962) although compati-bility varies with species age and sex (Crockett et al 2001)Studies have shown that in a period of non-contact famil-iarisation in socially neutral surroundings (ie not within thehome cageroom of either individual) respectivedominance statuses can be established through behaviouraldisplays whilst contact aggression is prevented Gwinn(1996) also found that previously singly housed squirrelmonkeys could be paired after gradual introduction using apole and collar to control aggressive interactions initiallyand with careful observation to identify compatible pairsRhesus stump-tailed long-tailed and pig-tail macaques andfemale common marmosets have all been successfullypaired in the laboratory environment (Line et al 1990Reinhardt 1994c Reinhardt et al 1995 Byrum amp St Claire1998 Cardinal amp Kent 1998 Lynch 1998 Watson 2002Majolo et al 2003b) Using these techniques it has beenconcluded that compatible social partners showing clearand stable dominantsubordinate relationships can be foundfor most individuals (Reinhardt 1994b Marks et al 2000Hartner et al 2001)Despite the evidence that compatible pairs can be formedbetween primates of the same sex care must be taken thatthe pairing is beneficial for both partners Lack of aggres-sion depression or injury and the occurrence of foodsharing can be used to monitor the continued compatibilityof the paired rhesus macaques (Hartner et al 2001) andaggression arising between pairs can be reduced by theprovision of enrichment (Majolo et al 2003a) although caremust be taken that sufficient enrichments are provided sothat they are not monopolised by the dominant individualAlthough overt aggression may not be apparent questionsabout compatibility must constantly be asked and the pairmonitored on a regular basis This is particularly true insame-sex marmoset pairs and malendashmale macaque pairingswhich deviate significantly from the natural tendency ofthese species (Crockett et al 1994 Majolo et al 2003b)Ideally compatible group mates should affiliate (eg groomhuddle) with each other

Heterosexual pairingHeterosexual pairing is most frequently used for commonmarmosets and other callitrichid species (Poole et al 1999)owl monkeys (Erkert 1999) and galagos lorises andtarsiers (Bearder amp Pitts 1999) It is not generally used forOld World species in the laboratory (Baskerville 1999) Incommon marmosets heterosexual pairing represents amuch more natural grouping than isosexual pairing and thisis reflected in the comparative ease with which such pairscan be formed and maintained Even without a pre-pairingfamiliarisation period sexually mature malendashfemale pairsof marmosets have been formed simply by the introductionof two animals to a home cage (Johnson et al 1996b)During the first weeks of pairing sexual and affiliativebehaviours predominate in common marmosets althoughthe frequency of sexual behaviour declines over time(Woodcock 1982 Johnson et al 1996b) However it should



be noted that previously heterosexually paired marmosetsmay take longer to pair up with new partners if a partner islost through naturally occurring or experimentally inducedillness or death as a stable monogamous pair-bonddevelops between long-term partners (Smith et al 1998Gerber et al 2002) Introduction to potential new partnerscan be associated with aggression as well as sexualbehaviour (Gerber et al 2002) It is likely that the formationof heterosexual pairs of marmosets would also benefit fromsome pre-pairing familiarisation if not to ease pair-formation directly then at least to ensure that individualsthat show particularly high aggression towards one anotherare not placed together Owl monkeys are also monogamousand heterosexual pairs can also be housed together success-fully (Erkert 1999) Tamarins including the saddle-backtamarin (Saguinus fuscicollis) and the cotton-top tamarin(Saguinus oedipus) breed best in monogamous pairs (Priceamp McGrew 1990) but can also be successfully housed instable sexually active compatible triads comprising onefemale and two males (Caine 1993) Galagos (Galago spp)lorises (Loridae) and tarsiers (Tarsius spp) are not naturallymonogamous species In the wild males and females live intheir own (sometimes overlapping) territories Howeverbecause these species show some social behaviour and mayplay and sleep together it has been recommended that theseprimates also be kept in heterosexual pairs (Bearder amp Pitts1999) Further empirical studies examining the most appro-priate and practical method of housing prosimian species inthe laboratory would be of benefit

Families and harem groupsHeterosexual pairs of callitrichids and their offspring can bekept together in a family group of 8ndash10 individuals withjuveniles from previous litters remaining in the group tohelp rear the most recent infants (Poole et al 1999) Thissystem is close although not identical to the socialdynamics of callitrichids in the wild (Stevenson amp Rylands1988) and is the most appropriate system for housingcallitrichids used in laboratories (Price amp McGrew 1990Rothe amp Darms 1993) Similar small family groups havebeen recommended for housing owl monkeys (Erkert 1999)and for galagos lorises and tarsiers (Bearder amp Pitts 1999)Harem grouping of one male with several females is themost natural housing system for macaques in laboratories(Baskerville 1999) This system provides the most appro-priate housing system for breeding and rearing infantsallowing a full range of appropriate social interactions to aidproper development of social sexual and parentalbehaviour (Harlow amp Harlow 1962 Mitchell et al 1966Suomi 1978 Capitanio 1986) If there are many females inthe harem group juvenile males can be introduced ensuringthat when older males are removed from the group disrup-tion is minimised (Baskerville 1999) Harems can becontained within large pens with indoor and outdoor areaslarge cages and within rooms Very large corral enclosurescontaining harems tend to be used by source-countrybreeders (Baskerville 1999) In the laboratory animals canbe housed in such group-housing systems during some

experiments particularly if a single caging or handlingfacility is attached In this way individuals can be isolatedfor short procedures before being returned to the group(Baskerville 1999)Population control in harems and family groups

In breeding colonies conception normally occurs soonerafter the birth of offspring than in wild populations becauseof the ready availability of nutrients In this situationcontraception may be used to increase the inter-birthinterval ensuring that females regain condition betweenbirths and that infants are born in accordance with demandThe condition prior to pregnancy is particularly important incallitrichid species where twins or triplets are the norm andlactation is therefore particularly energetically costly Therelative welfare benefits and risks associated withvasectomy contraceptive implants prostaglandin injec-tions intrauterine devices and immuno-contraception asmethods of population control in primate species werereviewed by Sainsbury (1997) and Glatston (1998) Thesuitability of different methods of contraception will varyon a case-by-case basis depending primarily upon the useof the animal at the time and upon the health and reproduc-tive status of each individual It is unclear which of thecontraceptives mentioned might be considered to have theleast impact on well-being as all appear to have significantdisadvantages Extension of inter-birth intervals is a refine-ment from the perspective of the individual but if moreanimals are then needed in breeding establishments in orderto cope with demand a conflict between refinement andreduction becomes apparent

WeaningIn contrast in commercial breeding groups it is oftenconsidered necessary to reduce inter-birth intervals in orderto maximise production (Goo amp Fulgate 1984) One of themethods by which this is achieved is by the early weaningof infants In the wild weaning refers to the point when theinfant stops suckling but usually refers to the time that theinfant is removed from the mother in captive situations(Wolfensohn amp Honess 2005) In the wild weaning usuallyoccurs at around 14 months in cynomolgus macaques butyoungsters remain with their mothers until the next baby isborn which can be for up to 2 years (inter-birth intervalsbeing between 12 and 24 months for both rhesus andcynomolgus macaques) (Smith amp Boyd 2002) In OldWorld monkeys artificial weaning may be as low as 90 days(Welshman 1999) and guidelines vary considerably(Wolfensohn amp Honess 2005) Social contact is particularlyimportant for development when the motor sensory andemotional systems of youngsters begin to mature andbecome fully integrated and they become extremelyinvolved in exploratory behaviours and social learning(Wallis amp Valentine 2001) Such early weaning is stressfulresulting in overt behavioural and physiological manifesta-tion of distress in rhesus and long-tailed macaquesincluding 66 weight loss a transient rise in cortisoldepression-related behaviour lasting at least 7 daysincreased locomotion (a behaviour associated with arousal



and agitation) and close contact with peers (Seay et al 1962Koyama amp Terao 1986) These changes were alleviated tosome extent by the presence of a nurse female althoughsome effects were still apparent in these nursed juveniles(Koyama amp Terao 1986) Therefore the welfare costs ofearly weaning outweigh the potential benefit of increasedproduction as a commercial practice and natural weaningshould be promoted Further whereas in macaques earlyweaning has been reported to result in the earlier onset offertility in females (Goo amp Fulgate 1984) studies inbaboons have shown that the earlier the infant wasseparated from the mother the longer the interval beforepostpartum oestrus and the later the next infant was born(Wallis amp Valentine 2001) The shortest inter-birth intervalwas found when the infant remained in the natal group untilmaturity and weaning occurred naturally (Wallis ampValentine 2001) It is possible that this difference was asso-ciated with distress in the mother as a result of separationfrom her infant and shows that early weaning may notalways improve production Careful investigation is neededto ensure that early weaning is necessary to reduce inter-birth intervals in other primate species and is not theproduct of misapplication of theory from species to species

Hand-rearingSome motherndashinfant separation may be used routinely in thelaboratory for welfare reasons In common marmosets thefemale may often produce more infants than she is able tofeed and assistance or hand-rearing may become necessaryThis may be done either by rearing one individual entirelyartificially or by providing the mother with assistance bygiving infants supplementary feeding on a rotational basisStudies have shown that separation even for the short timerequired to feed the infant can result in significant stressand significant behavioural abnormalities and in long-termdifferences in the ability of the individuals to cope with laterpsychosocial stress (Dettling et al 2002a b) This increasesthe variability in animals used and hence in the experi-mental results Further investigation is needed to evaluatethe relative welfare costs and benefits of this practice butcurrently the practice of selective euthanasia of the weakestindividuals in triplet and quadruplet marmoset litters mayprove to be a more humane and more scientifically soundoption than rotational hand-rearing This is alreadypractised in some laboratories in the UK It has been shownthat in some circumstances adult marmosets will acceptinfants that are not their own (Watson amp Petto 1988) Suchfostering might provide an alternative to rotational hand-rearing and euthanasia of some infants from large litters orfor orphaned individuals Further data on the feasibility offostering on a larger scale and of the comparative behav-ioural physiological and psychosocial effects of fosteringand rotational hand-rearing would be of use to fullyevaluate the costs and benefits of each It may also bepossible to use positive reinforcement to train marmosets tostation while their infants are given supplementary feedingwhile still on the carrierrsquos back

Gang housingWeaning may also be required when family groupings oflaboratory-housed primates become too big Weanedjuvenile primates could be housed in pairs but it is alsocommon practice to house sexually immature primates inlarge same-sex lsquogangsrsquo of unrelated individuals In the caseof common marmosets these social groupings may also bemade up of the oldest offspring removed from social groupsthat have become too large (Poole et al 1999) Thisgrouping is also unnatural and aggression escalating toserious fighting is common resulting in severe stress in themajority of individuals Johnson et al (1996b) studied theeffects of such social grouping on the adrenocorticotropichormone cortisol and behaviour of common marmosets andfound that cortisol was elevated with respect to that seen instable paired marmosets Social relationships are mostcritical during development and deprived or defectivesocial contact during development can have serious conse-quences for psychological well-being and the ability to copewith stress in later life (Johnson et al 1991 1996a) Incontrast in squirrel monkeys large groups of same andmixed sex individuals that are all of a similar age occurnaturally (Mendoza 1999) In these groups aggressionoccurs only rarely and is more common (although lesssevere) between females Conception and infant viabilityhave been reported to increase in this system of housing(Schiml et al 1996) However it should be noted thatnaturally occurring groups have essentially unrestrictedspace in which aggression can be avoided In the restrictedspace of the laboratory setting agonistic encounters mayoccur more frequently and must still be monitored It hasbeen reported that agonistic encounters usually occur attimes of excitement and Mendoza (1999) recommended thatthe individual that initiates arousal should be removed fromthe group when aggression occurs frequently rather thanremoving the most aggressive individual as group stabilitycan usually be regainedWestergaard et al (2000) reported that reproductiveperformance was better in multi-male multi-female groupsthan in harem-housed groups of rhesus macaques Howeverthere were many factors other than group composition thatcould have influenced infant survival in this study Theseincluded the number of animals in each group which washigher in the harem system and the degree of enrichmentwhich was less in the harem grouping The success of peergroup housing is therefore dependent upon the needs of thespecies but enrichment and group size also have aninfluence on the potential success of this housing system

Need for monitoring and management of socialhousingThe benefits of housing primates socially are clear andanimals housed in appropriate social combinations can ifsuccessfully managed be free from injury high rates ofdisease transmission social distress and under-nourishment(Reinhardt 1990) Maintenance of social colonies isdependent upon careful observation for changes in social



compatibility It should be noted that negative interactionsare part of social relationships and aggression can result inboth injury and mortality Subordinate individuals can showsigns of chronic social stress including depressive behav-iours (Shively et al 1997) Care must be taken that suchnegative interactions do not get out of hand in the laboratoryenvironment Any destabilising influences including birthof an infant movement of the group and rehousing removalor introduction of an individual may result in an increase inaggression in the group (Erwin 1979 Hambright amp Gust2003) Dominant animals can monopolise food andpreferred resources (Tardif amp Richter 1981 Brennan ampAnderson 1988 Deutsch amp Lee 1991) and care must betaken to ensure that the introduction of an enrichmentdevice does not therefore adversely affect welfare of subor-dinate individuals Extra resources must be provided so thatsubordinate animals can go to another resource if they aremoved on by a dominant animal Sufficient social spacemust be provided so that subordinate animals can showappropriate subordinate behaviour towards dominant indi-viduals moving away to an appropriate distance when chal-lenged (Reinhardt amp Reinhardt 2000b) The importance ofthe ability to control social interactions was shown instudies by Bloomsmith et al (2001) who examined theeffects of control of enrichment devices in chimpanzees Inthis study chimpanzees which had control over the appear-ance of a video of conspecifics showed more solitary playthan yoked conspecifics At the same time more scratching(considered a sign of anxiety in primates [Maestripieri et al1992 Cilia amp Piper 1997]) was observed in individualswhich could not control the appearance of the video ofconspecifics The inclusion of visual barriers within thecage can allow subordinate individuals to retreat in responseto movement or threatening gestures from the dominantpartner thus increasing the relative social space (Reinhardtamp Reinhardt 2000b) Although the value of such cageenrichments is generally accepted it cannot be assumed thatsuch visual barriers will prevent outright aggressionentirely as any significantly destabilising event is likely toresult in transient increases in aggression (Baskerville1999) Further McCormack and Megna (2001) found thatthe provision of barriers resulted in a reduction in non-contact aggression including threats vocalisations andchases but no change in the frequency of contact aggressionincluding biting and grabbing Such barriers may alsoreduce the visibility of the primates to technicians makingroutine welfare checks more arduous It is imperative thatall individuals in the group are frequently observed toensure that none are subject to stress-inducing levels ofaggression particularly during transitions in socialgroupings Caution should be exercised when animals areremoved and then reintroduced to groups after proceduresespecially if the animal is compromised in any way asabnormal behaviour may result in aggression from othermembers of the group and the dominance hierarchy withinthe group may be disturbed (Hambright amp Gust 2003)Reintroduction is possible even after long-term absencesbut staff must be on hand to observe and separate animals

which are agonistic if necessary (Kessler et al 1985)Individuals particularly adult males which experiencefrequent agonistic responses from the group have beenshown to experience significant stress in terms of bothhypothalamo-pituitary-adrenal (HPA) activation andimmune cell measures (Gust et al 1993) It should also benoted that for scientific reasons long periods (up to a year)of acclimatisation to new social systems should be allowedwhere possible because the effects of changes in socialenvironment can take time to become apparent (Schapiroet al 2000) Overcrowding in social groups has the potentialto increase agonistic encounters but studies have shown thatsocial dynamics are more important to the nature of socialinteractions in the group than group size (McIntyre amp Petto1993) Indeed rhesus macaques have been shown to be ableto adapt their behaviour to avoid conflict during short-termcrowding (Judge amp de Waal 1993) Despite potentialproblems evidence shows that if well managed withconsideration of species sex age group and experience onan individual basis appropriate social enrichment can beprovided for all species of laboratory-housed primatestudied (Reinhardt 1990) With appropriate husbandry andmanagement social enrichment can improve psychologicalwell-being and reduce the stress associated with experi-ments thus increasing their validity

Outdoor housingAccess to outdoor enclosures is generally considered to bebeneficial for laboratory-housed primates (but seeWolfensohn amp Honess 2005) mainly because of theincreased scope for enrichment in this environment Thespace provided for each individual is increased because allof the animals in the enclosure must be able to access anenvironmentally controlled portion of the enclosure at alltimes This area must fulfil the space requirements appli-cable to entirely indoor facilities Within this largerenclosure there is space to provide more structural enrich-ment allowing the primates to express more species-typicallocomotive behaviours There can also be more opportunityfor feeding enrichments like scatter feeding The environ-ment itself is more enriched with the primates beingexposed to a much wider range of sensations includingnatural light (including radiation) different backgroundnoise smells insects birds and weather The controllabilityof all environmental parameters is dramatically reducedwhen laboratory-housed primates are allowed access to theoutdoors particularly in temperate climates All primatesshould have access to shelter from both sun and inclementweather This and the ability to return inside to an environ-mentally controlled draught-free enclosure ensures that theanimals benefit from a choice of environment Contact withwild animals (including contact with faecal material) shouldbe prevented to ensure that the health and well-being oflaboratory-housed primates is not compromised by diseasestransmitted from such contact Access to outdoor enclosuresmay not be a feasible option for specific pathogen-freeanimals (Wolfensohn amp Honess 2005)



The benefits of outdoor housing have been demonstrated ina range of species (eg chimpanzees Clark et al 1982 rhesusmacaques OrsquoNeill 1989 common marmosets Pines et al2002) For example OrsquoNeill (1989) showed that the occur-rence of abnormal behaviour was greatly reduced in youngrhesus macaques which had been reared without mothersand with 5 hours of contact with peers each week whenhoused outdoors However OrsquoNeill also found thatreturning the juveniles to indoor enclosures resulted in anincrease in self-mouthing and the expression of stereotyp-ical behaviours such that the expression of these behavioursoccurred more frequently than had been recorded prior tooutdoor housing These results are in agreement with theproposal that loss of control (in this case access to theenriched environment) may be more stressful to laboratory-housed primates than never having had control in the firstplace (ie never receiving access to the outdoors) Thisconclusion supports the work of Bryant et al (1988) whofound that home cage enrichment was more beneficialoverall than the provision of rotational access to an enrichedplayroom Further evaluation of the use of outdoor facilitiesin temperate climates including the security implicationswould be valuable

Section summary and conclusionsSocial enrichment is the most effective form of enrichmentbut must be managed in an appropriate manner for thespecies concerned with reference to natural populationsSingle housing is used mainly to facilitate research but isrecognised to be detrimental to physical and psychologicalwell-being reducing the range of species-typical behaviourresulting in inhibition of the immune system and a higherfrequency of expression of abnormal behaviour Singlehousing systems are used more commonly for Old Worldprimates because of the perceived danger associated withhandling them Timed breeding in single cages is consideredinappropriate for most primate species because social spaceis limited both for the mother and her infant the opportu-nity for social development is greatly reduced and themother must be returned to isolation when the infant is arti-ficially weaned If unavoidable singly housed primatesmust be socially enriched by housing them in closeproximity allowing visual auditory olfactory and physicalcontact Isosexual housing is also relatively unnatural but ispreferable to single housing as the presence of a compatibleconspecific has been shown to reduce stress and increasethe ability to cope Compatibility of individuals isdependent on species age sex and social experience Non-contact familiarisationsocialisation can be used to assesscompatibility and allow dominantsubordinate relationshipsto be established without aggression Heterosexual pairingis more natural for callitrichid species and is recommendedfor owl monkeys and for some prosimian species In thesecases if the pairs breed they can be kept with offspring infamily groups Harem housing is the most natural systemfor housing Old World monkeys It is particularly appro-priate during breeding and for the development of infants

Contraception is important in group housing systems toensure that the supply of infants matches demand and toallow females to maintain condition Early weaning toincrease interbreeding intervals should be avoided wherepossible to allow juveniles to develop socially especially ifthey are to be used for breeding themselves Separation forhand-rearing is stressful and can influence development andthe ability of the animal to cope with challenges in later lifeAs an alternative to rotational rearing of marmoset tripletssupplementary feeding of all infants on the carrierrsquos backeuthanasia of the smallest infant or fostering could beattemptedGang-housing is more stressful than pair or family grouphousing in marmosets but is a naturally occurring groupingin squirrel monkeys Reproductive success in macaques canalso be higher in this system than in harems Outdoorhousing provides greater environmental variability and mayprovide greater scope for enrichment but must be carefullymanaged particularly in temperate climates All sociallyhoused primates should be observed frequently to ensurethat social stability is maintained and that no individualreceives excessive social stress

Acquisition and transportationThe process of the acquisition of primates and their trans-portation to the research facility is another aspect of the lifeof a laboratory-housed primate that could be significantlyrefined (Wolfensohn amp Honess 2005) Many factors havethe potential to affect the welfare of the primates duringacquisition and transportation First the individual iscaptured in many cases isolated and confined and access tofood or water may be restricted During transportation theprimate may be exposed to a range of environmentalstressors including fluctuations and extremes in temperatureand humidity excessive noise and novel movementsHusbandry is carried out by unknown handlers which maybe particularly important if stopovers are required (Malagaet al 1991) Finally on arrival at the destination the indi-vidual will be exposed to a novel environment unknownhandlers and in some cases to unknown conspecificsHowever the magnitude of the effect of exposure to suchstressors on the welfare of primates is not yet fully under-stood The stress associated with transportation can result ininhibition of the immune system and as a result clinicalsigns of disease may develop in previously apparentlyhealthy animals (LABALASA 1993) and thus pre-trans-portation health checks must be thorough and stress must beminimised This is particularly important in wild-caughtanimals which are likely to be harbouring sub-clinical infec-tions and for whom the novel process of capture confine-ment transportation and subsequent captivity is likely to bemore stressful Studies of transportation in calves haveshown that health monitoring must be continued for severalweeks as clinical signs of disease may develop some timeafter the transport event (Knowles 1995)By law in Europe wild-caught primates may only be usedin science in exceptional circumstances (EU 1986) Thetransportation of animals for use in research must be carried



out within the provisions of the European Directive(91628) on the Protection of Animals during Transportwhich is currently under revision the European Convention(ETS 123) and according to the Resolution on theAcquisition and Transport of Laboratory Animals adoptedby the Multilateral Consultation in May 1997 (Council ofEurope 1997) These are general provisions applying to allanimals and include the requirement that the travel shouldbe carefully planned and carried out without avoidabledelay that all animals should be fit to travel handledcarefully and that they must be protected from inadequateventilation extremes of temperature lack of feed and waterand should be transported in suitable containers If theanimals are to be transported by air the International AirTransport Association (IATA) Live Animal Regulationsmust be followed (International Air Transport Association[IATA] 2003) These regulations include husbandrystandards for animals being transported and provide specifi-cations for containers that should be used Enforcement ofthese regulations in India resulted in a considerablereduction in transport-related deaths in macaques (Cullum1966)The common marmoset breeds well in captivity (Poole et al1999) and is more commonly bred lsquoin-housersquo than otherprimate species (Rennie amp Buchanan-Smith 2005)although breeding of other primate species is carried outacross Europe Provided that the housing and husbandryused are appropriate for the species concerned lsquoin-housebreedingrsquo is an important refinement of laboratory practiceas the need for long distance transportation is eliminated(although animals are still likely to be relocated from timeto time) and exposure to the majority of the stressors asso-ciated with transportation is avoided Furthermore by main-taining standardised husbandry routines across the researchestablishment (as far as possible) and using positive rein-forcement to socialise and habituate the young primates tostaff other animals and procedures from an early age thestress associated with relocation of in-house-bred primatescould be greatly reduced (Prescott amp Buchanan-Smith2003)In contrast a much greater proportion of the Old Worldmonkeys that are used in research are imported from sourcecountries (Owen et al 1997 Rennie amp Buchanan-Smith2005) New World monkeys are also imported to a greateror lesser extent depending on the country concerned(Rennie amp Buchanan-Smith 2005) All imported primatesmust be transported by air and road to the user establish-ment in journeys that can last several days (Malaga et al1991) These animals are more likely to experience stress asa result of transportation than those relocated within estab-lishments as the degree of change and the duration ofexposure to stressors are greater However by careful use ofspecies-appropriate refinements the degree of stress experi-enced can be reduced Details of general measures that canbe used to reduce the stress experienced by primates duringtransportation are provided in the LABALASA guidelinesfor the care of laboratory animals in transit (LABALASA

1993) and in the IATA Live Animals Regulations Moredetailed species-specific recommendations are made in TheUFAW Handbook on the Care and Management ofLaboratory Animals (Baskerville 1999 Erkert 1999 Pooleet al 1999) and by Wolfensohn and Honess (2005)In the revision of European regulations relating to the trans-portation of animals it has been recognised that animals areexposed to the most stress during confinement and loadingand unloading These regulations refer mostly to primatesbeing transported for agricultural and domestic purposes butdata from laboratory-based studies indicate that loading andunloading are likely to be the most stressful components ofthe transportation process applied to primate species It hasbeen shown that capture confinement in a transport cageand relocation to another room even within the same estab-lishment can result in activation of the HPA axis diarrhoeaand injury (Line et al 1987 Luttrell et al 1994) Althoughthe severity of these problems can be reduced with the useof positive reinforcement training (Klein amp Murray 1995Reinhardt 1992 Scott et al 2003) elevated cortisol has beenrecorded in trained macaques confined in a transport cagefor as little as 5 minutes (Line et al 1987) Although it isgenerally considered that the degree to which individualprimates are affected by transportation is dependent uponthe distance travelled duration of the journey degree ofsocial contact permitted degree of protection afforded bythe transport container (Swallow 1999) and competence ofthe staff involved one quantitative study of 450 wild-caughtowl monkeys suggested that the duration of the journey maynot be as important as the age of the animals (Malaga et al1991) On arrival younger owl monkeys (juveniles and sub-adults) had lost more weight than adults regardless of thetime spent in transit (3ndash4 6ndash7 or 9ndash14 days) Howeverwhen the animals were weighed again after 30 days in theirnew laboratory environment the younger animals appearedto have adapted better showing a gain in weight withrespect to their pre-transit weight In contrast adults did notregain the weight they had lost during transit Youngeranimals may be more reactive to novelty because they haveless experience of the changes which may have contributedto the greater magnitude of weight loss in these animalsduring transportation It was supposed that adult animals didnot regain the weight lost during transportation as a result ofsocial stress as they were unable to establish appropriateboundaries by scent-marking because of the close proximityof the other animals Honess et al (2004) compared thebehaviour of cynomolgus macaques in an overseas breedingfacility and following transportation by air to a newlocation The transport and relocation caused significantchanges indicative of stress with no return after 1 month tobehavioural patterns observed at the breeding centre Thesestudies illustrate the need to determine the most appropriateage for transportation and the need to ensure that animalsare fully acclimatised to their new environment before theyare included in scientific studiesIt has been shown that the presence of a favoured conspe-cific can reduce stress associated with confinement novelty



and procedures in both New and Old World primates(Crockett et al 1993 Smith et al 1998) Wolfensohn andHoness (2005) suggested that transporting affiliating pairstogether allows for mutual support They argued thatkeeping affiliating primates together should extend beyondthe transport phase to the destination housing This is a clearrefinement of previous recommendations Baskerville(1999) and the LABALASA guidelines for the care of labo-ratory animals in transit recommended that Old Worldprimates should be transported in individual containers tominimise the risk of injury as a result of fear-related aggres-sion Both sets of guidelines recommended that unweanedinfants should be carried with their mothers but that theyshould be checked on a regular basis to ensure that theinfant is not being harmed (LABALASA 1993 Baskerville1999) Under IATA regulation pregnant females and thosewith suckling young are not accepted for transportConversely it has been recommended that marmosets andowl monkeys be transported in compatible pairs or familygroups (Erkert 1999 Poole et al 1999) thus eliminatingstress associated with separation from favouredconspecifics and exposure to unknown conspecifics onarrival at their destinationThe value of positive interactions with care staff for thewell-being of laboratory-housed primates has beendiscussed at length above The benefit of positivehumanndashanimal interaction and the presence of a knownhandler during transportation of primates was stressed anec-dotally in a report of the translocation of a group of 10gorillas from the Netherlands to Australia in which knownhandlers accompanied the gorillas throughout the journey(Kartzoff 1997) Although it is noted that such carefulinvolvement of known handlers during each phase of trans-portation is rarely feasible in the commercial transportationof primates the importance of the competence of anyhandler encountered during the transportation process isillustrated by Kartzoffrsquos report Handler training is alsocritical for the safety of the handlers themselves In fear-inducing circumstances primates can become particularlydangerous (Reinhardt 2002) and there are many diseasescarried by primates which are transmissible to humans(Weber et al 1997) Where possible habituation or desensi-tisation to transport cages prior to the day of transit is alsolikely to be beneficial (Laule 1999) and transportationshould be avoided where possible

Section summary and conclusionsTransportation results in the exposure of primates to a widerange of stressors from capture isolation environmentalextremes and novelty The effects of transportation arelikely to be more severe in wild-caught animals The effectsof relocation of primates bred lsquoin-housersquo can be reduced bystandardising husbandry and management and by social-ising young animals to both humans and conspecificsSocial contact can reduce stress during transportation Thepresence of known handlers and habituation to the transportcontainer may also be of benefit

Conclusions and animal welfare implicationsRefinement techniques must be applied to all aspects of thelife of non-human primates in the laboratory from birth todeath to fulfil our ethical and scientific responsibility tominimise harm and maximise well-being Thus refinementof housing husbandry and care is of great importanceBasic guidance on appropriate housing and husbandrypractices is outlined in Appendix A to the EuropeanConvention (EC 1986) which is currently being revisedHowever these guidelines do not take into account differ-ences in species-specific needs Many refinements couldfeasibly be introduced to improve on basic husbandrypractices but all must be introduced with the specific needsof the species and where possible the individuals in mindThis simple principle applies to the housing environmentand caging facilities object feeding and social enrichmentsas well as to breeding practices and the transportationprocessAlthough many of the refinements discussed in this revieware not novel the best available practices with respect toprimates are less well known In this review we haveprovided an overview of current thinking on refinement ofpractice applicable to the housing husbandry and care oflaboratory-housed primates Used appropriately and incombination with refinement of the procedures in whichprimates are used and of the impact of humans both duringhusbandry and in procedures the refinements discussed inthis review have the potential to both minimise harmimposed upon the primates used in laboratories and tomaximise their well-being

AcknowledgementsWe thank Mark Prescott and David Morton for theirvaluable comments on a draft of this paper Anna Robertsfor all her help and two anonymous referees whosecomments substantially improved the manuscript AER andHMB-S were supported by a grant from the EuropeanCommission (number QLRT-2001-00028)

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Capitanio JP Weissberg M and Reite M 1985 Biology ofmaternal behavior Recent findings In Reite M and Field T (eds)The Psychobiology of Attachment and Separation pp 51-85 AcademicPress London UKCardinal BR and Kent SJ 1998 Behavioural effects of simplemanipulable environmental enrichment on pair housed juvenilemacaques (Macaca nemestrina) Laboratory Primate Newsletter 371-4Chamove AS 1984 Role of vision in social development in mon-keys Child Development 55 1394-1411Chamove AS 1989 Enrichment in chimpanzees unpredictableropes and tools Journal of the Association of British Wild AnimalKeepers 16 139-141Chamove AS and Anderson JR 1989 Examining environmen-tal enrichment In Segal EF (ed) Housing Care and PsychologicalWell-Being of Captive and Laboratory Primates pp 183-202 NoyesPublications New Jersey USAChamove AS Anderson JR Morgan-Jones SC and JonesSP 1982 Deep woodchip litter hygiene feeding and behavioralenhancement in eight primate species International Journal for theStudy of Animal Problems 3 308-318Cilia J and Piper DC 1997 Marmoset conspecific confrontationan ethologically-based model of anxiety Pharmacology Biochemistryand Behavior 58 85-91Clarke AS Juno CJ and Maple TL 1982 Behavioral effects ofa change in the physical environment A pilot study of captivechimpanzees Zoo Biology 1 371-380Clarke MR Harrison RM and Didier ES 1996 Behavioralimmunological and hormonal responses associated with socialchange in rhesus monkeys (Macaca mulatta) American Journal ofPrimatology 39 223-233Clough G 1999 The animals house design equipment and envi-ronmental control In Poole T (ed) The UFAW Handbook on theCare and Management of Laboratory Animals pp 94-134 BlackwellScience Oxford UKCoe CL Wiener SG and Levine S 1983 Psychoendocrineresponses of mother and infant to disturbance and separation InRosenblum LA and Moltz H (eds) Symbiosis in Parent-OffspringInteractions pp 189-214 Plenum Press London UKCoe CL 1993 Psychosocial factors and immunity in non-humanprimates A review Psychosomatic Medicine 55 298-308Council of Europe 1997 httpwwwcoeinttelegal_affairs_coop-erationbiological_safety_use_of_animalslaboratory_animalsRes20acquisition20transportasp (accessed June 2006)Crockett CM 1998 Psychological well-being of captive non-human primates In Sheperdson DH Mellen JD and Hutchins M(eds) Second Nature Environmental Enrichment for Captive Animalspp 129-152 Smithsonian Institute Press Washington DC USACrockett CM Bellanca RU Bowers CL and Bowden DM1997 Grooming-contact bars provide social contact for individu-ally caged laboratory macaques Contemporary Topics in LaboratoryAnimal Science 36 53-60Crockett CM Bowers CL Bowden DM and Sackett GP1994 Sex differences in compatibility of pair-housed adult long-tailed macaques American Journal of Primatology 32 73-94Crockett CM Bowers CL Sackett GP and Bowden DM1993 Urinary cortisol responses of longtailed macaques to fivecage sizes tethering sedation and room change American Journalof Primatology 30 55-74



Crockett CM Koberstein D and Heffernan KS 2001Compatibility of laboratory monkeys housed in grooming-contactcages varies by species and sex American Journal of Primatology 54(Suppl 1) 51-52Crockett CM Shimoji M and Bowden DM 2000 Behaviorappetite and urinary cortisol responses by adult female pigtailedmacaques to cage size cage level room change and ketaminesedation American Journal of Primatology 52 63-80Cullum LE 1966 Air transport of monkeys from India Journal ofthe American Veterinary Medical Association 149 909-911Dawkins MS 1983 Battery hens name their price consumerdemand theory and the measurement of ethological lsquoneedsrsquoAnimal Behaviour 31 1195-1205Dettling AC Feldon J and Pryce CR 2002a Early deprivationand behavioral and physiological responses to socialseparationnovelty in the marmoset Pharmacology Biochemistry andBehavior 73 259-269Dettling AC Feldon J and Pryce CR 2002b Repeatedparental deprivation in the infant common marmoset (Callithrixjacchus) and analysis of its effects on early development BiologicalPsychiatry 52 1037-1046Deutsch JC and Lee PC 1991 Dominance and feeding compe-tition in captive rhesus monkeys International Journal of Primatology12 615-628Dexter S and Bayne K 1994 Results of providing swings toindividually housed rhesus monkeys Laboratory Primate Newsletter33 9-12Draper WA and Bernstein IS 1963 Stereotyped behavior andcage size Perceptual and Motor Skills 16 231-234Eaton GG Kelley ST Axthelm MK Iliff-Sizemore SA andShigi SM 1994 Psychological well-being in paired adult femalerhesus (Macaca mulatta) American Journal of Primatology 33 89-99Eckert K Niemeyer C Rogers RW Seier J Ingersoll BBarklay L Brinkman C Oliver S Buckmaster C KnowlesL Pyle C and Reinhardt V 2000 Wooden objects for enrich-ment A discussion Laboratory Primate Newsletter 39 1-5Ely A Freer A Windle C and Ridley RM 1998 Assessmentof cage use by laboratory-bred common marmosets (Callithrix jac-chus) Laboratory Animals 32 427-433Erkert HG 1999 Owl monkeys In Poole T (ed) The UFAWHandbook on the Care and Management of Laboratory Animalspp 574-590 Blackwell Science Oxford UKErwin J 1979 Aggression in Captive Macaques Interaction ofSocial and Spatial Factors In Erwin J Maple TL and Mitchell G(eds) Captivity and Behavior Primates in Breeding ColoniesLaboratories and Zoos pp 139-171 Van Nostrand Co New YorkUSAErwin J 1986 Environments for the captive propagation of pri-mates interaction of social and physical factors In Benirschke K(ed) Primates The Road to Self-Sustaining Populations pp 397-305Springer Verlag New York USAEuropean Commission (EC) 1986 European Convention forthe protection of vertebrate animals used for experimental andother scientific purposes ETS 123 Strasbourg FranceEuropean Union (EU) 1986 Council Directive 86609EECParis FranceFagen R 1981 Animal Play Behaviour Oxford University PressOxford UKFagen R 1993 Primate juveniles and primate play In Pereira MEand Fairbanks LA (eds) Juvenile Primates Life History Developmentand Behaviour pp 182-196 Oxford University Press Oxford UK

French JA and Inglett BJ 1989 Female-female aggression andmale indifference in response to unfamiliar intruders in liontamarins Animal Behaviour 37 487-497Fritz J Wolfle TL and Howell S 1999 Chimpanzees In PooleT (ed) The UFAW Handbook on the Care and Management ofLaboratory Animals pp 643-658 Blackwell Science Oxford UKGarner JP 2005 Stereotypies and other abnormal repetitivebehaviors Potential impact on validity reliability and replicabilityof scientific outcomes ILAR Journal 46 106-117Gerber P Schnell CR and Anzenberger G 2002Comparison of a beholderrsquos response to confrontations involvingits pairmate or two unfamiliar conspecifics in common marmosets(Callithrix jacchus) Evolutionary Anthropology 11 117-121Glatston AR 1998 The control of zoo populations with specialreference to primates Animal Welfare 7 269-281Glick-Bauer M 1997 Behavioral enrichment for captive cotton-top tamarins (Saguinus oedipus) through novel presentation ofdiet Laboratory Primate Newsletter 36 1-3Gluck JP and Sackett GP 1974 Frustration and self-aggressionin social isolate rhesus monkeys Journal of Abnormal Psychology 83331-334Goo GP and Fulgate JK 1984 Effects of weaning age on mater-nal reproduction and offspring health in rhesus monkeys (Macacamulatta) Laboratory Animal Science 34 66-69Goosen C Vandergulden W Rozemond H Balner HBertens A Boot R Brinkert J Dienske Janssen GLammers A and Timmermans P 1984 Recommendations forthe housing of macaque monkeys Laboratory Animals 18 99-102Green WH 1990 A theoretical model for classical psychosocialdwarfism (psychologically determined short stature) In HolmesCS (ed) Psychoneuroendocrinology Brain Behaviour and HormonalInteractions pp 92-112 Springer-Verlag Publishers London UKGust DA Gordon TP Hambright MK and Wilson ME1993 Relationship social-factors and pituitary-adrenocorticalactivity in female rhesus monkeys (Macaca mulatta) Hormones andBehavior 27 318-331Gust DA Gordon TP Wilson ME Brodie ARAhmedansari A and McClure HM 1996 Group formation offemale pigtail macaques (Macaca nemestrina) American Journal ofPrimatology 39 263-273Gwinn LA 1996 A method for using a pole housing apparatus toestablish compatible pairs among squirrel monkeys ContemporaryTopics in Laboratory Animal Science 35 61 (Abstract)Hambright MK and Gust DA 2003 A descriptive analysis of aspontaneous dominance overthrow in a breeding colony of rhe-sus macaques (Macaca mulatta) Laboratory Primate Newsletter 428-11Hampton JK Hampton SH and Landwehr BT 1966Observations on a successful breeding colony of the marmoset(Oedipomidas oedipus) Folia Primatologica 4 265-287Hanson JD Larson ME and Snowdon CT 1976 The effectsof control over high intensity noise on plasma cortisol levels inrhesus monkeys Behavioural Biology 16 333-340Harlow HF and Harlow MK 1962 Social deprivation in mon-keys Scientific American 207 136-146Harlow HF and Harlow MK 1971 Psychopathology in mon-keys In Kimmel HD (ed) Experimental Psychopathology RecentResearch and Theory pp 203-339 Academic Press London UKHartner M Hall J Penderhest J and Clark L 2001 Group-housing subadult cynomolgus macaques in a pharmaceutical envi-ronment Laboratory Animals 30 53-57



Heger W Merker HJ and Neubert D 1986 Low light inten-sity decreases the fertility of Callithrix jacchus Primate Report 14260 (Abstract)Hennessy MB 1984 Presence of companion moderates arousalof monkeys with restricted social experience Physiology andBehaviour 33 693-698Home Office 1989 Code of Practice for the Housing and Care ofAnimals used in Scientific Procedures HMSO Cambridge UKHoness PE Johnson PJ and Wolfensohn SE 2004 A study ofbehavioural responses of non-human primates to air transportand re-housing Laboratory Animals 38 119-132Honess PE and Marin CM 2006 Enrichment and aggression inprimates Neuroscience and Biobehavioral Reviews 30 413-436Howell S Schwandt M Fritz J Roeder E and Nelson C2003 A stereo music system as environmental enrichment forcaptive chimpanzees Laboratory Animal 32 31-36International Air Transport Association (IATA) 2003 LiveAnimal Regulations IATA Montreal CanadaJohnson EO Kamilaris TC Carter S Gold PW andChrousos GP 1991 Environmental stress and reproductive suc-cess in the common marmoset (Callithrix jacchus jacchus) AmericanJournal of Primatology 25 191-201Johnson EO Kamilaris TC Calogero AE Gold PW andChrousos GP 1996a Effects of early parenting on growth anddevelopment in a small primate Pediatric Research 39 999-1005Johnson EO Kamilaris TC Carter CS Calogero AEGold PW and Chrousos GP 1996b The biobehavioral conse-quences of psychogenic stress in a small social primate (Callithrixjacchus jacchus) Biological Psychiatry 40 317-337Judge PG and de Waal FBM 1993 Conflict avoidance amongrhesus monkeys mdash coping with short-term crowding AnimalBehaviour 46 221-232Kartzoff L 1997 The successful transportation of ten Westernlowland gorillas (Gorilla gorilla gorilla) from Apenheul Primate Parkthe Netherlands to Taronga Zoo Australia Gorilla Gazette 11 26-35Kelley ST and Hall AS 1995 Housing In Bennett BT Abee CRand Henrickson R (eds) Non-Human Primates in BiomedicalResearch pp 193-209 Academic Press Inc San Diego USAKessler MJ London WT Rawlins RG Gonzalez JMartinez HS and Sanchez J 1985 Management of a harembreeding colony of rhesus monkeys to reduce trauma-relatedmorbidity and mortality Journal of Medical Primatology 14 91-98Keverne EB Martensz ND and Tuite B 1989 Beta-endor-phin concentrations in cerebrospinal-fluid of monkeys are influ-enced by grooming relationships Psychoneuroendocrinology 14155-161Klein HJ and Murray KA 1995 Restraint In Bennett BT (ed)Non-Human Primates in Biomedical Research pp 286-297 AcademicPress San Diego USAKnowles TG 1995 A review of post transport mortality amongyounger calves The Veterinary Record 137 406-407Kopecky J and Reinhardt V 1991 Comparing the effectivenessof PVC swings versus PVC perches as environmental enrichmentobjects for caged female rhesus macaques (Macaca mulatta)Laboratory Primate Newsletter 30 5-6Koyama T and Terao K 1986 Psychological stress of maternal sep-aration in cynomolgus monkeys the effect of housing with a nursefemale In Else JG and Lee PC (eds) Primate Ecology and Conservationpp 101-113 Cambridge University Press Cambridge UK

LABALASA 1993 Guidelines for the care of laboratory animalsin transit Laboratory Animals 27 93-107Laudenslager ML Held PE Boccia ML Reite ML andCohen JJ 1990 Behavioral and immunological consequences ofbrief mother-infant separation a species comparisonDevelopmental Psychobiology 23 247-264Laudenslager ML Reite M and Harbeck RJ 1982 Suppressedimmune-response in infant monkeys associated with maternalseparation Behavioral and Neural Biology 36 40-48Laule G 1999 Training laboratory animals In Poole T (ed) TheUFAW Handbook on the Care and Management of Laboratory Animalspp 21-27 Blackwell Science Oxford UKLine SW 1987 Environmental enrichment for laboratory pri-mates Journal of the American Veterinary Medical Association 190854-859Line SW Clarke AS and Markowitz H 1987 Plasma cortisolof female rhesus monkeys in response to acute restraintLaboratory Primate Newsletter 26 1-4Line SW Morgan KN Markowitz H Roberts JA andRiddell M 1990 Behavioral responses of female long-tailedmacaques (Macaca fascicularis) to pair formation LaboratoryPrimate Newsletter 24 1-9Line SW Markowitz H Morgan KN and Strong S 1991Effects of cage size and environmental enrichment on behaviour-al and physiological responses of rhesus macaques to the stress ofdaily events In Novak MA and Petto AJ (eds) Through the LookingGlass Issues of Psychological Well-being in Captive Non-humanPrimates pp 160-179 American Psychological AssociationWashington DC USALjungberg T and Westlund K 2000 Impaired reconciliation inrhesus macaques with a history of early weaning and disturbedsocialization Primates 41 79-88Lopez J Wormell D and Rodriguez A 2001 Preliminary eval-uation of the efficacy and safety of a UVB lamp used to preventmetabolic bone disease in pied tamarins (Saguinus bicolor) at JerseyZoo Dodo 37 41-49Luttrell L Acker L Urben M and Reinhardt V 1994Training a large troop of rhesus macaques to cooperate duringcatching analysis of the time investment Animal Welfare 3 135-140Lutz C Well A and Novak M 2003 Stereotypic and self-inju-rious behavior in rhesus macaques A survey and retrospectiveanalysis of environment and early experience American Journal ofPrimatology 60 1-15Lutz CK and Novak M 2005 Environmental enrichment fornon-human primates Theory and application ILAR Journal 46 178-191Lynch RL 1998 Successful pair-housing of male macaques(Macaca fascicularis) Laboratory Primate Newsletter 37 4-6Maestripieri D Schino G Aureli F and Troisi A 1992 Amodest proposal mdash displacement activities as an indicator ofemotions in primates Animal Behaviour 44 967-979Majolo B Buchanan-Smith HM and Bell J 2003a Responseto novel objects and foraging tasks by common marmoset(Callithrix jacchus) female pairs Laboratory Animal Europe 3 25-33Majolo B Buchanan-Smith HM and Morris K 2003b Factorsaffecting the successful pairing of unfamiliar common marmoset(Callithrix jacchus) females Preliminary results Animal Welfare 12327-337



Malaga CA Weller RE Montoya E Moro J andBuschbom RL 1991 Mortality and body weight changes in Aotusnancymai shipped from Iquitos Peru to Richland WashingtonJournal of Medical Primatology 20 6-11Markowitz H 1982 Behavioral Enrichment in the Zoo VanNostrand Reinhold Company Inc New York USAMarkowitz H and Aday C 1998 Power for captive animals InSheperdson DH Mellen JD and Hutchins M (eds) Second NatureEnvironmental Enrichment for Captive Animals pp 47-58 SmithsonianInstitute Press Washington DC USAMarkowitz H and Line S 1990 The need for responsive envi-ronments In Rollin B and Kesel ML (eds) The Experimental Animalin Biomedical Research pp 153-170 CRC Press Boca RatonFlorida USAMarkowitz H and Line S 1989 Primate research models andenvironmental enrichment In Segal EF (ed) Housing Care andPsychological Well-being of Captive and Laboratory Primates pp 203-212 Noyes Publications Inc New Jersey USAMarks D Kelly J Rice T Ames S Marr R Westfall JLloyd J and Torres C 2000 Utilizing restraint chair training toprepare primates for social housing Laboratory Primate Newsletter39 9-10Marriner LM and Drickamer LC 1994 Factors influencingstereotyped behavior of primates in a zoo Zoo Biology 13 267-275Mason G 1991a Stereotypies A critical review Animal Behaviour41 1015-1037Mason GJ 1991b Stereotypies and suffering Behavioural Processes25 103-115McCormack K and Megna NL 2001 The effects of privacywalls on aggression in a captive group of rhesus macaques(Macaca mulatta) American Journal of Primatology 54 (Suppl 1) 50-51 (Abstract)McDermott J and Hauser M 2004 Are consonant intervalsmusic to their ears Spontaneous acoustic preferences in a non-human primate Cognition 94 B11-B21McGrew WC Brennan JA and Russell J 1986 An artificialgum-tree for marmosets (Callithrix j jacchus) Zoo Biology 5 45-50McIntyre DT and Petto AJ 1993 Effect of group size on behav-ior of group-housed female rhesus macaques Laboratory PrimateNewsletter 32 1-5McKenzie SM Chamove AS and Feistner ATC 1986 Floor-coverings and hanging screens alter arboreal monkey behaviorZoo Biology 5 339-348Mendoza SP 1999 Squirrel monkeys In Poole T (ed) The UFAWHandbook on the Care and Management of Laboratory Animalspp 591-600 Blackwell Science Oxford UKMenzel EW Jr 1991 Chimpanzees (Pan troglodytes) problemseeking versus the bird in hand least effort strategy Primates 32497-508Michels AM 1998 Sex differences in food acquisition and aggres-sion in captive common marmosets (Callithrix jacchus) Primates 39549-556Mineka S Gunnar M and Champoux M 1986 Control andearly socioemotional development infant rhesus monkeys rearedin controllable versus uncontrollable environments ChildDevelopment 57 1241-1256Mistlberger RE 1994 Circadian food-anticipatory activity mdash for-mal models and physiological-mechanisms Neuroscience andBiobehavioral Reviews 18 171-195Mitchell GD Raymond EJ Ruppenthal GC and HarlowHF 1966 Long-term effects of total isolation in behaviour of rhe-sus monkeys Psychological Reports 18 567-580

Murchison M 1995 Forage feeder box for single animal cagesLaboratory Primate Newsletter 34 1-3Murchison MA and Nolte RE 1992 Food puzzle for singlycaged primates American Journal of Primatology 27 285-292Nelson RJ and Mandrell TD 2005 Enrichment and nonhumanprimates ldquoFirst do no harmrdquo ILAR Journal 46 171-177Newberry RC 1995 Environmental enrichment mdash increasingthe biological relevance of captive environments Applied AnimalBehaviour Science 44 229-243Nieuwenhuijsen K and de Waal FBM 1982 Effects of spatialcrowding on social behavior in a chimpanzee colony Zoo Biology1 5-28Novak MA 2003 Self-injurious behaviour in rhesus monkeysnew insights into its etiology physiology and treatment AmericanJournal of Primatology 59 3-19Novak MA and Drewsen KH 1989 Enriching the lives of cap-tive primates issues and problems In Segal EF (ed) Housing Careand Psychological Well-being of Captive and Laboratory Primatespp 161-182 Noyes Publication Inc New Jersey USANovak MA and Suomi SJ 1991 Social-interaction in nonhu-man-primates mdash an underlying theme for primate researchLaboratory Animal Science 41 308-314Ogden JJ Lindburg DG and Maple TL 1994 A preliminarystudy of the effects of ecologically relevant sounds on the behav-ior of captive lowland gorillas Applied Animal Behaviour Science 39163-176OrsquoNeill P 1989 A room with a view for captive primates issuesgoals related research and strategies In Segal EF (ed) HousingCare and Psychological Well-Being of Captive and Laboratory Primatespp 135-160 Noyes Publications Inc New Jersey USAOvermier JB Patterson J and Wielkiewicz RM 1980Environmental contingencies as sources of stress in animals InLevine S and Ursin H (eds) Coping and Health pp 1-38 PlenumPress New York USAOwen S Thomas C West P Wolfensohn S and Wood M1997 Report on primate supply for biomedical scientific work inthe UK Laboratory Animals 31 289-297Parks KA and Novak MA 1993 Observations of increasedactivity and tool use in captive rhesus monkeys exposed totroughs of water American Journal of Primatology 29 13-25Poole T Hubrecht R and Kirkwood JK 1999 Marmosets andtamarins In Poole T (ed) The UFAW Handbook on the Care andManagement of Laboratory Animals pp 559-574 Blackwell ScienceOxford UKPines MK Kaplan G and Rogers LJ 2002 Comparison ofbehavior changes and cortisol levels of common marmosets(Callithrix jacchus jacchus) to indoor and outdoor cages Caring forPrimates Abstracts of the XIXth Congress The InternationalPrimatological Society Beijing Mammalogical Society of China267Poole TB Costa P Netto WJ Schwarz K Wechsler Band Whittaker D 1994 Non-human primates In OrsquoDonoghuePN (ed) The Accommodation of Laboratory Animals in Accordancewith Animal Welfare Requirements Bundesministerium furErnahrung Landwirtschaft und Forsten Bonn GermanyPrescott MJ and Buchanan-Smith HM 2003 Training nonhu-man primates using positive reinforcement techniques Guest edi-torsrsquo introduction Journal of Applied Animal Welfare Science 6 157-161Price EC and McGrew WC 1990 Cotton-top tamarins(Saguinus o oedipus) in a semi-naturalistic captive colony AmericanJournal of Primatology 20 1-12



Pyle DA Bennett AL Zarcone TJ Turkkan JS Adams RJand Heinz RD 1996 Use of two food foraging devices by singlyhoused baboons Laboratory Primate Newsletter 35 10-15Reinhardt V 1990 Social enrichment for laboratory primates acritical review Laboratory Primate Newsletter 29 7-12Reinhardt V 1991 Serum cortisol concentrations of single-housed and isosexually pair-housed adult rhesus macaques Journalof Experimental Animal Science 34 73-76Reinhardt V 1992 Improved handling of experimental rhesusmonkeys In Davis H and Balfour AD (eds) The Inevitable BondExamining Scientist-Animal Interactions pp 171-177 CambridgeUniversity Press Cambridge UKReinhardt V 1994a Caged rhesus macaques voluntarily work forordinary food Primates 35 95-98Reinhardt V 1994b Effective environmental enrichment forcaged rhesus macaques In Touch 1 1-5Reinhardt V 1994c Pair-housing rather than single-housing forlaboratory rhesus macaques Journal of Medical Primatology 23426-431Reinhardt V 1995 Arguments for single-caging or rhesusmacaques are they justified Animal Welfare Information CentreNewsletter 6 7-8Reinhardt V 1997b Species-adequate housing and handling con-ditions for Old World primates kept in research institutions InReinhardt V (ed) Comfortable Quarters for Laboratory Animals pp 84-93 Animal Welfare Institute Washington DC USA Reinhardt V 1997a Lighting conditions for laboratory monkeysare they adequate Animal Welfare Information Centre Newsletter 83-6Reinhardt V 1999 Pair-housing overcomes self-biting behavior inmacaques Laboratory Primate Newsletter 38 4Reinhardt V 2002 The myth of the aggressive monkey Journal ofApplied Animal Welfare Science 5 321-330Reinhardt V and Cowley D 1990 Training stumptailed mon-keys (Macaca arctoides) to cooperate during in-homecage treat-ment Laboratory Primate Newsletter 29 9-10Reinhardt V Cowley D Scheffler J Vertein R andWegner F 1990 Cortisol response of female rhesus-monkeys tovenipuncture in homecage versus venipuncture in restraint appa-ratus Journal of Medical Primatology 19 601-606Reinhardt V Liss C and Stevens C 1995 Restraint methodsof laboratory non-human primates a critical review AnimalWelfare 4 221-238Reinhardt V and Reinhardt A 2000a The lower row monkeycage an overlooked variable in biomedical research Journal ofApplied Animal Welfare Science 3 141-149Reinhardt V and Reinhardt A 2000b Meeting the lsquosocial spacersquorequirements of pair-housed primates Laboratory PrimateNewsletter 39 7Reinhardt V Reinhardt A Eisele S Houser D and Wolf J1987 Control of excessive aggressive disturbance in a heteroge-neous troop of rhesus monkeys Applied Animal Behaviour Science18 371-377Rennie AE and Buchanan-Smith HM 2005 Report on theextent and character of primate use in scientific proceduresacross Europe in 2001 Laboratory Primate Newsletter 44 6-12Rennie AE and Buchanan-Smith HM 2006 Refinement of theuse of non-human primates in scientific research Part I the influ-ence of humans Animal Welfare 15 203-213Roder EL and Timmermans PJA 2002 Housing and care ofmonkeys and apes in laboratories adaptations allowing essentialspecies-specific behaviour Laboratory Animals 36 221-242

Rothe H and Darms K 1993 The social organization of mar-mosets a critical evaluation of recent concepts In Rylands AB(ed) Marmosets and Tamarins Systematics Behaviour and Ecologypp 176-199 Oxford University Press Oxford UKRuppenthal GC 1992 Effects of rearing conditions on behav-ioural development indices of stress XIVth Congress of theInternational Primatological Society pp 236 (Abstract) IPSStrasbourg FranceRussell WMS and Burch RL 1992 The Principles of HumaneExperimental Technique Universities Federation for AnimalWelfare Wheathampstead Herts UKSainsbury AW 1997 The humane control of captive marmosetand tamarin populations Animal Welfare 6 231-242Sales GD Milligan SR and Khirnykh K 1999 Sources ofsound in the laboratory animal environment a survey of thesounds produced by procedures and equipment Animal Welfare 897-115Sambrook TD and Buchanan-Smith HM 1996 What makesnovel objects enriching A comparison of the qualities of controland complexity Laboratory Primate Newsletter 35 1-4Sambrook TD and Buchanan-Smith HM 1997 Control andcomplexity in novel object enrichment Animal Welfare 6 207-216Schapiro SJ and Bushong D 1994 Effects of enrichment onveterinary treatment of laboratory rhesus macaques (Macacamulatta) Animal Welfare 3 25-36Schapiro SJ Bloomsmith MA Porter LM and Suarez SA1996 Enrichment effects on rhesus monkeys successively housedsingly in pairs and in groups Applied Animal Behaviour Science 48159-171Schapiro SJ Stavisky R and Hook M 2000 The lower-rankcage may be dark but behavior does not seem to be affectedLaboratory Primate Newsletter 39 4-6Schiml PA Mendoza SP Saltzman W Lyons DM andMason WA 1996 Seasonality in squirrel monkeys (Saimiri sci-ureus) social facilitation by females Physiology and Behavior 601105-1113Schino G Scucchi S Maestripieri D and Turillazzi PG1988 Allogrooming as a tension-reduction mechanism a behav-ioral approach American Journal of Primatology 16 43-50Scott L 1991 Environmental enrichment for single housed com-mon marmosets In Box HO (ed) Primate Responses toEnvironmental Change pp 265-274 Chapman and Hall London UKScott L Pearce P Fairhall S Muggleton N and Smith J2003 Training nonhuman primates to co-operate with scientificprocedures in applied biomedical research Journal of AppliedAnimal Welfare Science 6 199-208Seay B Hansen E and Harlow HF 1962 Mother-infant separationin monkeys Journal of Child Psychology and Psychiatry 3 123-132Shepherdson DJ 1998 Tracing the path of environmentalenrichment In Sheperdson DH Mellen JD and Hutchins M (eds)Second Nature Environmental Enrichment for Captive Animals pp 1-12 Smithsonian Institute Press Washington DC USAShively CA Laberlaird K and Anton RF 1997 Behavior andphysiology of social stress and depression in female cynomolgusmonkeys Biological Psychiatry 41 871-882Smith JA and Boyd KM 2002 (eds) The Use of Non-HumanPrimates in Research and Testing The British Psychological SocietyLeicester UKSmith TE McGreer-Whitworth B and French JA 1998Close proximity of the heterosexual partner reduces the physio-logical and behavioral consequences of novel-cage housing inblack tufted-ear marmosets (Callithrix kuhli) Hormones andBehavior 34 211-222



Snowdon CT 1991 Naturalistic environments and psychologicalwell-being In Novak MA and Petto AJ (eds) Through the LookingGlass Issues of Psychological Well-Being in Captive Non-HumanPrimates pp 103-115 Washington DC American PsychologicalAssociation USASnowdon CT and Savage A 1989 Psychological well-being ofcaptive primates general considerations and examples for cal-litrichids In Segal EF (ed) Housing Care and Psychological Well-being of Captive and Laboratory Primates pp 75-89 NoyesPublications Inc New Jersey USASpector MR Kowalczyk MA Fortman JD and Bennett BT1994 Design and implementation of a primate foraging trayContemporary Topics in Laboratory Animal Science 33 54-55Stevenson MF and Rylands AB 1988 The marmosets genusCallithrix In Mittermeier RA Rylands AB Coimbra-Filho AF andFonseca GAB (eds) Ecology and Behavior of Neotropical PrimatesVol II pp 131-222 World Wildlife Fund Washington DC USASuomi SJ 1978 Maternal behavior by socially incompetent mon-keys Neglect and abuse of offspring Journal of Pediatric Psychology3 28-34Swallow JJ 1999 Transporting animals In Poole T (ed) TheUFAW Handbook on the Care and Management of Laboratory Animalspp 171-187 Blackwell Science Oxford UKTardif SD and Richter CB 1981 Competition for a desiredfood in family groups of the common marmoset (Callithrix jacchus)and the cotton-top tamarin (Saguinus oedipus) Laboratory AnimalScience 31 52-55Tustin GW Williams LE and Brady AG 1996 Rotational useof a recreational cage for the environmental enrichment ofJapanese macaques (Macaca fuscata) Laboratory Primate Newsletter35 5-7Veasey JS Waran NK and Young RJ 1996 On comparing thebehaviour of zoo housed animals with wild conspecifics as a wel-fare indicator Animal Welfare 5 13-24Vick SJ Anderson JR and Young R 2000 Maracas for maca-ca Evaluation of three potential enrichment objects in twospecies of zoo-housed macaques Zoo Biology 19 181-191Voland E 1977 Social play behavior of the common marmoset(Callithrix jacchus) in captivity Primates 18 883-901

Waitt C and Buchanan-Smith HM 2002 The effects of care-taker-primate relationships on primates in the laboratory Journalof Applied Animal Welfare Science 5 309-319Wallis J 2002 Reproduction in baboons The influence of envi-ronmental enhancement American Journal of Primatology 57 85(Abstract)Wallis J and Valentine B 2001 Early vs natural weaning in cap-tive baboons the effect on timing of postpartum estrus and nextconception Laboratory Primate Newsletter 40 10-13Watson LM 2002 A successful program for same- and cross-agepair-housing adult and subadult male Macaca fascicularis LaboratoryPrimate Newsletter 41 6-9Watson L Cosby R and Lee-Parritz D 1993 Behavioraleffects of enrichment devices on laboratory primates with stereo-typic and self-directed behavior American Journal of Primatology 30355-356Watson LM and Petto AJ 1988 Infant adoption and reintro-duction in common marmosets (Callithrix jacchus) LaboratoryPrimate Newsletter 27 1-4Weber H Berge E Finch J Heidt P Hunsmann GPerretta G and Verschuere B 1997 Sanitary aspects of han-dling non-human primates during transport Laboratory Animals 31298-302Welshman M 1999 Breeding macaques in source countries InPoole T (ed) The UFAW Handbook on the Care and Management ofLaboratory Animals pp 636-642 Blackwell Science Oxford UKWestergaard GC Izard MK and Drake JH 2000Reproductive performance of rhesus macaques (Macaca mulatta)in two outdoor housing conditions American Journal of Primatology50 87-93Wolfensohn S and Honess P 2005 Handbook of PrimateHusbandry and Welfare Blackwell Science Oxford UKWolff A and Ruppert G 1991 A practical assessment of a non-human primate exercise program Laboratory Animals 20 36-39Woodcock AJ 1982 The first weeks of cohabitation of newly-formed heterosexual pairs of common marmosets (Callithrix jac-chus) Folia Primatologica 37 228-254Wright BW 1995 A novel item enrichment program reduceslethargy in orangutans Folia Primatologica 65 214-218



optimal psychological and physiological well-beingrdquo(Shepherdson 1998 p 1)Thus environmental enrichment is a refinement whichmaximises the well-being of laboratory-housed primatesThe scale of enrichment techniques varies widely from thecomplete redesign of housing to the introduction of smalltoys but according to Shepherdsonrsquos definition all areconsidered enrichments if they can be shown to positivelyaffect the well-being of laboratory-housed primates(Shepherdson 1998) Evidence shows that the proper use ofenrichment can improve the psychological well-being oflaboratory-housed primates (Snowdon 1991) indicated byincreases in the animalsrsquo ability to cope with challengesreduction in aberrant behaviours increased frequency ofspecies-typical behaviour (Pyle et al 1996 Wright 1995)and improvements in health and reproductive success(Erwin 1986 Wallis 2002) Despite the potential positiveeffects of enrichment misguided attempts at enrichmenthave the potential to cause harm for example by causinginjury (see review by Bayne 2005 Nelson amp Mandrell2005) causing aggression (Honess amp Marin 2006) or whenenrichment opportunities are provided but then removed(Bryant et al 1988) Other enrichment strategies may beimpractical for use in the laboratory environment forexample those which take up too much staff time or whichhave the potential to affect the outcome of experiments(Newberry 1995 Bayne 2005) Thus all enrichment strate-gies must be tested to ensure that their introduction affectswelfare positively and that they are practicable in the labo-ratory An understanding of species-typical behaviour andphysiology is essential for proper assessment of enrichmentsuccess and imagination innovation motivation and someresources are a requirement during design (Markowitz ampLine 1990) The literature on environmental enrichment isvast and cannot be comprehensively covered within thescope of this paper (see Lutz amp Novak 2005 for a recentreview) However the range of enrichment strategies andevidence of their effects will be considered and sources ofconflict and difficulties that may be encountered during thedevelopment of proposed enrichments will be discussed

Psychological well-beingThe ability to express species-typical behaviour and to fulfilbehavioural needs has been considered important to thepsychological well-being of laboratory-housed primates(Snowdon amp Savage 1989 Eaton et al 1994 Newberry1995) The capacity for control and the degree ofcomplexity and predictability of the enrichment are alsothought to be important (OrsquoNeill 1989 Sambrook ampBuchanan-Smith 1997 Vick et al 2000 Bassett ampBuchanan-Smith in press) The view of the relative impor-tance of these concepts has changed since the earliest use ofenvironmental enrichment and it is well accepted that thesuccess of enrichment strategies is very much dependentupon the individual and species concerned (Markowitz ampLine 1989)

Behavioural needsAs the aim of enrichment is to increase an animalrsquos behav-ioural opportunities and to prevent or reduce the expressionof abnormal behaviours (including stereotypies) discus-sions of the concept of behavioural or ethological needs areinevitably and correctly included in the analysis of enrich-ment strategies Indeed the lsquoneedsrsquo concept has been incor-porated into the European Directive (86609EEC) whichstates that ldquoany restriction on the extent to which an exper-imental animal can satisfy its physiological and ethologicalneeds shall be limited to an absolute minimumrdquo (EuropeanUnion [EU] 1986 Article 5 paragraph b)Thus European law supports the use of enrichment forlaboratory animals The concept of behavioural or etholog-ical needs was first introduced by Brambell (1965) in areport on the welfare of farm animals in intensivehusbandry systems In this report it was considered thatprevention of the expression of behaviours which theanimal is highly motivated to perform could result in frus-tration and that the degree of frustration experienced woulddictate welfare The performance of such behaviours couldtherefore be considered an ethological need Later Dawkins(1983) attempted to pinpoint exactly what was meant by theconcept of behavioural or ethological needs defining etho-logical needs as the effect of high levels of causal factors toperform a particular behaviour pattern Dawkins (1983)argued that true needs (as opposed to lsquoluxuriesrsquo) could beidentified using the principles of consumer demand theoryapplied to operant and preference tests Using this principleonly those behaviours that the animal would work hard orovercome aversive stimuli to perform could be consideredneeds The frustration of behavioural needs is considered tobe one of the main causes of stereotypical behaviours incaptive animals where animals are motivated to perform apattern of behaviour that they cannot perform normally orcompletely (Mason 1991b) Abnormal and stereotypicalbehaviours are also likely to occur when the animal issubject to experiences over which it has no control andcannot therefore respond appropriately (Mason 1991b)Thus the presence of abnormal and stereotypical behav-iours has been used as an indicator of poor welfare and inad-equate housing and care (Mason 1991a) Abnormalbehaviours including stereotypic circling and pacing eyeprodding self-sucking depilation self-mutilationcoprophagy and regurgitation have been observed in labora-tory-housed chimpanzees Old World monkeys andcallitrichids (Baskerville 1999 Fritz et al 1999 Poole et al1999) The occurrence of abnormal and stereotypical behav-iours can be reduced (Watson et al 1993 Eaton et al 1994Crockett 1998 Lutz et al 2003 Novak 2003 Bourgeois ampBrent 2005) or prevented (Lutz amp Novak 2005) by the useof carefully considered enrichment strategies supportingthe hypothesis that these behaviours occur as the result ofthe thwarting of behaviours that the animal is highlymotivated to perform (Marriner amp Drickamer 1994)














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