Bibliographyon Refinement and Environmental Enrichment for Primates. Refinement
(2,b) Structured Space
(2,c) Playpen, OutdoorHousing, Exercise Cage
(5) Animate Enrichment
(7) Workingwith Cooperative Animals
(8) Treatmentof Trained Animals in their Home Enclosure
(9) Cage Arrangement
Refinement is the attempt to enhance animal welfare andcontrol extraneous variables that may increase research data variability.
Bayne K, McCully C 1989. The effectof cage size on the behavior of individually housed rhesus monkeys.Lab Animal 18(1), 25-28
A moderate increase of unstructured cage space does not affectstereotypical behaviors in individually caged rhesus macaques
Boot R, Leussink AB, Vlug RF 1985.Influence of housing conditions on pregnancy outcome in cynomolgusmonkeys (Macaca fascicularis). Laboratory Animal Science19, 42-47
More successful pregnancies were recorded for females housedindividually in large cages than for females housed in small cages.
Brent L 1992. The effects of cagesize and pair housing on the behavior of captive chimpanzees.American Journal of Primatology 27, 20
"Environmental manipulation was higher and inactivitylower in the [furnished] large single cage than in the [furnished]small single cage. The mean abnormal behaviors decreased in thelarger cages but the difference was not significant."
Crockett CM, Shimoji M, Bowden DM2000. Behavior, appetite, and urinary cortisol responses by adultfemale pigtailed macaques to cage size, cage level, room change,and ketamine sedation. American Journal of Primatology 52, 63-80
A moderate increase of unstructured cage space does not affectabnormal behaviors in individually caged pig-tailed macaques.
Daschbach NJ, Schein MW, Haines DE1983. Cage-size effect on locomotor, grooming and agonistic behaviorsof the slow loris (Nycticebus coucang). Applied AnimalEthology 9, 317-330
"Results of the experiments in this study indicate thatslow lorises kept in larger [furnished] cages will be more activethan those housed in [furnished] cages approaching recommendationsfor size proposed by the U.S. National Research Council."
Kitchen AM, Martin AA 1996. The effectsof cage size and complexity on the behaviour of captive commonmarmosets, Callithrix jacchus jacchus. Laboratory Animals30, 317-326
"Stereotyped behaviours, which occurred in the small [furnished]cages, were never exhibited in the large [furnished] cages. Weconclude that the welfare of captive marmosets is enhanced bythe provision of larger and more complex cages."
Line SW, Morgan KN, Markowitz H, StrongS 1990. Increased cage size does not alter heart rate or behaviorin female rhesus monkeys. American Journal of Primatology20, 107-113
A moderate increase of the dimensions of standard cages that lackany structures for climbing, perching, swinging or other activitiesdid not affect the behavior of individually caged rhesus macaques.
Mallapur A, Waran N, Sinha A 2005.Use of enclosure space by captive lion-tailed macaques (Macacasilenus) housed in Indian zoos. Journal of Applied AnimalWelfare Science 8, 175-185
"Captive lion-tailed macaques used the edge zone the spaceclosest to the visitor areas when their ... environments weredeficient in appropriate environmental stimuli."
Paulk HH, Dienske H, Ribbens LG 1977.Abnormal behavior in relation to cage size in rhesus monkeys.Journal of Abnormal Psychology 86, 87-92
"Observations were made of 24 monkeys that were introducedsingly into a [barren] small and a [barren] large test cage. Ina large cage, more normal but less stereotyped locomotion wasshown than in a small cage."
Williams LE, Steadman A, Kyser B 2000.Increased cage size affects Aotus time budgets and partnerdistances. American Journal of Primatology 51(Supplement1), 98
"Aotes spp. housed in typical, small, laboratory cagesappear to be sedentary animals that spend large amounts of timesitting alone or in physical contact with social partners. ...The Aotus, housed as pairs or family groups, were moved from cagesmeasuring 0.63m x 1.5m x 0.76m to larger housing measuring 1.5mx 3m x 2m. Perches and nest boxes were provided in both housingconditions. ... Results indicate that Aotus will disperse anduse the cage area provided. Changes in time budgeting are indicativeof more relaxed animals, spending less time huddled with familymembers or in their nest box [alone], and spending more time eatingand drinking."
Erwin J 1977. Factors influencingaggressive behavior and risk of trauma in the pigtail macaque(Macaca nemestrina). Laboratory Animal Science 27,541-547
"Provision of cover ... reduced aggression among membersof stable groups."
Günther MM 1998. Influence ofhabitat structure on jumping behaviour in Galago moholi.Folia Primatologica 69(Supplement 1), 410
"These results suggest that support material [perches],as well as height, influences the behaviour of G. maholi and theseshould be taken into consideration in behavioural and biomedicalstudies as well as in the construction of cage facilities. Studieswhich do not take these factors into account are to some extentvitiated."
Maninger N, Kim JH, Ruppenthal GC1998. The presence of visual barriers decreases agonism in grouphoused pigtail macaques (Macaca nemestrina). AmericanJournal of Primatology 45, 193-194
"Instances of bite, grab and chase were found to be significantlygreater [among members of harem groups of 23 pig-tailed macaques]when visual barriers were absent compared to when they were present."
McCormack K, Megna NL 2001.
"Preliminary results suggest that non-contact aggression(vocalizations, fear grimaces, chases, and threats) is significantlyreduced after the introduction of the privacy walls (p<.05)."
Miller-Schroeder P, Paterson JD 1989.Environmental influences on reproduction and maternal behaviorin captive gorillas: Results of a survey. In Housing, Careand Psychological Wellbeing of Captive and Laboratory PrimatesSegal EF (ed), 389-415. Noyes Publications, Park Ridge
Females reproduced more successfully if their enclosures containedvarious structures, especially privacy refuges like sight barriersand cages.
Nakamichi M, Asanuma K 1998. Behavioraleffects of perches on group-housed adult female Japanese monkeys.Perceptual and Motor Skills 87, 707-714
"When [4 adult female] monkeys were housed in a cage whichcontained eight wooden perches to increase usable space, the rateof agonistic interactions ... decreased in comparison with thoseevident when they were housed in a cage [identical dimension]without such perches."
National Research Council 1998. ThePsychological Well-Being of Nonhuman Primates NAP, Washington
"Optimal use of available cage space might well dependmore on the placement of perches, platforms, moving and stationarysupports, and refuges than on cage size itself."
Neveu H, Deputte BL 1996. Influenceof availability of perches on the behavioral well-being of captive,group-living mangabeys. American Journal of Primatology38, 175-185
"A total deprivation of perches yielded an increase inaggressive behaviors and locomotion, and a decrease in cohesiveness.Placing perches progressively in the experimental cage restoredthe level of all the variables to levels found in the controlcage [with five perches]."
Reinhardt V 1989. Evaluationof the long-term effectiveness of two environmental enrichmentobjects for singly caged rhesus macaques. Lab Animal18(6), 31-33
"While perching, the monkeys sat in front of the cagefor 95% of the time, in the middle or rear of the cage for 5%of the time. ... The proportion of time spent with the pipes wasthree times greater for animals living in lower-row cages thanfor animals living in upper-row cages. ... In the elevated position,the light exposure was increased, a fact that made the pipes ofparticular value for the lower-row cages animals."
Reinhardt V 1990. Aperch for caged macaques. Humane Innovations and Alternativesin Animal Experimentation 4, 134-135
Perches are "particularly attractive for animals duringthe daily cleaning of their cages because they offer a dry, comfortableplace to sit while the floors of their cages are sprayed withwater."
Ricker RB, Williams LE, Brady AG,Gibson SV, Abee CR 1995. Environmental enhancement for laboratory-housedsquirrel monkeys: Fifteen-year retrospective analysis of procedures.Contemporary Topics in Laboratory Animal Science 34(4),55
"Cut pieces of PVC pipe (12 in diameter) were hung ineach run as a hide box, allowing eye contact to be broken betweendisputing animals. This decreased fight wounds by 60%."
Shimoji M, Bowers CL, Crockett CM1993. Initial response to introduction of a PVCperch by singly caged Macaca fascicularis. Laboratory Primate Newsletter 32(4),8-11
Single-housed "monkeys spent significantly more time clingingto the cage wall ("suspended") in the absence of theperch. ... There was less stereotypy when the perch was present."
Spencer H 2005. A tale of two cynos.Tech Talk 10(3), 4 & 6
"After implementing the vertical tunnels, both [pair-housedmale cynos] primates stopped exhibiting stereotypical and self-injuriousbehaviors." The two animals "were free of stereotypicalbehavior for a little over two years."
Westergaard GC, Izard MK, Drake JD,Suomi SJ, Higley JD 1999. Rhesus macaque (Macaca mulatta)group formation and housing: Wounding and reproduction in a specificpathogen free (SPF) colony. American Journal of Primatology49, 339-347
"When forming new rhesus macaque breeding groups, dividedcorrals that provide for social and visual separation of individualslead to lower rates of traumatic wounding than do undivided corrals."
Wolff A 1989. Polyvinylchloride piping as perch material for squirrel monkeys. LaboratoryPrimate Newsletter 28(1), 7
"An additional unexpected benefit of the PVC piping hasbeen a decrease in dorsal tail-head abrasions, frequently seenin squirrel monkeys that sit on the stainless steel flooring ofstandard primate cages."
Baker KC, Ross SK 1998. Outdoor access:The behavioral benefits to chimpanzees. American Journal ofPrimatology 45, 166
"When compared to the results of ameliorative environmentalenrichment techniques furnished to the indoor-housed subjects,the small outdoor groups of [two or three] chimpanzees showedbroader and more dramatic improvements in well-being." Animalswith outdoor access showed significantly less abnormal behavior(e.g., coprophagy, regurgitation/reingestion), less yawning, andmore self-grooming.
Bayne K, Dexter S, Suomi S 1992. Apreliminary survey of the incidence of abnormal behavior in rhesusmonkeys (Macaca mulatta) relative to housing condition.Lab Animal 21(5), 38-46
"The greatest frequency of overall abnormal behavior andstereotypic exploratory behavior was in the SC [single cage] condition,and the lowest frequency of occurrence in the CC [corn crib] condition... in IO [indoor/outdoor] runs, the animals showed no self-directedbehavior."
Brent L, Lee DR, Eichberg JW 1991.Evaluationof a chimpanzee enrichment enclosure. Journal of MedicalPrimatology 20, 29-34
Chimpanzees were given access to a complex new outdoor playground."Activity and environmental manipulation increased whileabnormal and self directed behaviors decreased."
Bryant CE, Rupniak NMJ, Iversen SD1988. Effectsof different environmental enrichment devices on cage stereotypiesand autoaggression in captive cynomolgus monkeys. Journalof Medical Primatology 17, 257-269
"Stereotypy and autoaggression were markedly reduced inthe playpen, but reappeared on return to the home cage."
Clarke AS, Juno CJ, Maple TL 1982.Behavioral effects of a change in the physical environment: apilot study of captive chimpanzees. Zoo Biology 1, 371-380
A group of chimpanzees was translocated from a laboratory environmentto a naturalistic man-made island. Stereotyped and self-directedbehaviors were dramatically reduced on the island.
Fontenot MB, Wilkes MN, Lynch CS 2006. Effects of outdoor housingon self-injurious and stereotypic behavior in adult male rhesusmacaques (Macaca mulatta). Journal of the American Associationfor Laboratory Animal Science [Contemporary Topics in LaboratoryAnimal Science] 45(5), 35-43
"Our findings suggest that self-biting and self-directedstereotypic behavior in rhesus macaques with a history of self-injuriousbehavior is significantly reduced by outdoor housing" incorncribs equipped with perches and toys. The outdoor housingprovided a 114% increase in floor area for single-housed animalsand a 364% to 837% increase in floor area for group-housed animals.
Fried J, Whitehouse M 1992. A pre-postoccupancy comparison of activity budgets and habitat utilizationin a group of captive mandrills (Mandrillus sphinx). AmericanJournal of Primatology 27, 28
"For the group as a whole, feeding, traveling and objectoriented behaviors increased, and stereotypic behaviors decreased"in the naturalistic environment.
Goerke B, Fleming L, Creel M 1987.Behavioral changes of a juvenile gorilla after a transfer to amore naturalistic environment. Zoo Biology 6, 283-295
"Coprophagy and regurgitation/reingestion were reducedin the juvenile [group-housed] gorilla in the larger and morenatural environment."
Honess PE, Marin C, Brown AP, WolfensohnSE 2005. Assessment of stress in non-human primates: applicationof the neutrophil activation test. Animal Welfare 14, 291-295
"All macaques were group-housed indoors in either a traditionalcaging system of three linked modules of typical reinforced stainlesssteel two-tier laboratory cages, or in open-rooms containing eitherthese cages with the fronts removed or no caging at all. ... Animalshoused in a traditional caging system produced a significantlylower leukocyte response than animals housed in open-rooms, indicatingthat there was a higher level of stress associated with cagedhousing than open-room housing."
Jensvold MLJ, Fouts RS, Fouts DH 1999.Behavioral changes in captive chimpanzees. ChimpanZoo ConferenceProceedings, 66
"Overall, after the move to the larger [structurally enriched]facility, there was an increase in activity, a decrease in stereotypicalbehaviour, and an increase in threat behavior."
Kessel AL, Brent L 1995. An activitycage for baboons, Part I. Contemporary Topics in LaboratoryAnimal Science 34(6), 74-79
Single-housed "baboons provided with a large enrichedactivity cage [during two days each month] display dramatic changesin behavior typically considered to represent positive psychologicalwell-being. ... The home cages and the activity cage were locatedin the same room, and provided visual, olfactory, and auditoryaccess to other baboons." .
Kessel AL, Brent L 1997. Behaviouraleffects of transferring singly housed baboons to outdoor socialgroups. In Proceedings on the 2nd International Conferenceon Environmental Enrichment Holst B (ed), 142-147. CopenhagenZoo, Frederiksberg
"Moving singly housed baboons to an enriched outdoor enclosurehad significant effects on all behaviors analyzed. Abnormal behavior,cage directed activities, and self-directed activities all decreasedin the corn cribs. Inactivity, locomotion, and normal behavior,as well as enrichment directed activities and social behaviorall increased in the corn cribs."
Leu M, Crockett CM, Bowers CL, BowdenDM 1993. Changes in activity levels of singly housed longtailedmacaques when given the opportunity to exercise in a larger cage.American Journal of Primatology 30, 327
"Over a period of 36 days, each [single-housed] animalhad 15 min per day access to a multicompartmental [large] exercisecage." Locomotion increased while stereotypical behaviordecreased when the animals were in the exercise cage.
Maple TL, Finlay TW 1987. Post-occupancyevaluation in the zoo. Applied Animal Behaviour Science18, 5-18
"We investigated the effects of translocating great apesfrom barren cages to innovative naturalistic habitats. ... Forboth gorillas and orangutans, the new environment had the effectof reducing the variety and frequency of aggressive interactions.... Some behaviors, such a play-biting, were recorded for thefirst time in the new enclosure. Both gorillas were prone to regurgitationand re-ingestion in their former cages. However, in the naturalisticenvironments these abnormal behaviors were never observed."
Marriott BM, Marriott RW, Norris J,Lee D 1993. Asemi-natural habitat for housing small, nonhuman primates.Journal of Medical Primatology 22, 348-354
A semi-natural habitat was designed to house a group of squirrelmonkeys. Animals maintained in this environment were "healthy,and none of the animals exhibited locomotor stereotypies."
McGuffey LH, McCully CL, Bernacky BJ, Blaney SM 2002. Incorporationof an enrichment program into a study protocol involving long-termrestraint in macaques. Lab Animal 31(10), 37-39
"In our experience, the provision of periodic intervalsof unrestricted activity directly correlated with an increasedtolerance during relatively more extended periods of [chair] restraint."
O'Neill PL 1989. Short-term and long-termbenefits of environmental enrichment on laboratory rhesus monkeys(Macaca mulatta) . American Zoo and Aquarium Association(AZA) Regional Conference Proceedings, 616-625
The animals were transferred from their barren group cage toa more spacious playroom equipped with climbing /perching structuresand swings for one hour per day, five days a week: The animalsshowed a decline in the frequency of three [out of four] behavioraldisorders in the playpen. This therapeutic effect was nullifiedback in the barren homecage."
*Pines MK, KaplanG, Rogers LJ 2007. A note on indoor and outdoor housing preferencesof common marmosets (Callithrix jacchus). Applied Animal BehaviourScience 108(3-4), 348-353
"When given free access to move between their home cageand outdoors, the marmosets spent 70% of their day in the outdoorcage."
Seier JV, Loza J, Benjamin L 2004.Housing and stereotyped behaviour: Some observations from an indoorcolony of vervet monkeys (Chlorocebus aethiops). FoliaPrimatologica 75(Supplement 1), 332
Adult females displaying stereotypies in single cages were exposedsequentially to a foraging log and an exercise cage, as well ascages of varying complexity and dimensions. The animals "spentmost time in stereotypies when in unenriched single cages. Thiswas significantly reduced by the provision of either an exercisecage or a foraging log. No stereotyped behaviour was observedin the largest most enriched cages."
Storey PL, Turner PV, Tremblay JL2000. Environmental enrichment for rhesus macaques: A cost-effectiveexercise cage. Contemporary Topics in Laboratory Animal Science39(1), 14-16
"Increased visual attentiveness by other animals, decreasedself-directed biting and hair picking, and improved food consumptionwas observed when rhesus macaques were permitted access to anexercise cage for several hours daily."
Tustin GW, Williams LE, Brady AG 1996.Rotational use of a recreational cage forthe environmental enrichment of Japanese macaques (Macaca fuscata). Laboratory Primate Newsletter 35(1),5-7
The rotational use of a "recreation cage" resultedin increased use of enrichment devices and a decrease in stereotypicalbehaviors.
Wilkes MN, Lynch CS, Fontenot MB 2006. Outdoor housing decreasesself-injurious and stereotypic behavior in adult male rhesus macaques( Macaca mulatta). American Journal of Primatology68(Supplement ), 106 (Abstract)
Access to an outdoor area decreased self-injurious and stereotypicalbehaviors in adult male rhesus who had been single-caged or group-housedindoors.
Baker KC 1997. Straw and forage materialameliorate abnormal behaviors in adult chimpanzees. Zoo Biology16, 225-236
"In an [successful] effort to reduce abnormal behaviors,especially regurgitation and reingestion, and promote higher activitylevels [locomoting and playing], straw and scattered forage materialwere added to the enclosures of 13 indoor-housed chimpanzees livingin pairs and trios."
Baker KC, Springer DA 2006. Frequencyof feeding enrichment and response of laboratory nonhuman primatesto unfamiliar people. Journal of the American Association forLaboratory Animal Science [Contemporary Topics in Laboratory AnimalScience] 45(1), 69-73
"The data presented support the hypothesis that levelsof treat feeding influence monkeys' receptivity to unfamiliarpeople."
Bayne K, Dexter SL, Mainzer H, McCullyC, Campbell G, Yamada F 1992. The use of artificial turf as a foraging substratefor individually housed rhesus monkeys (Macaca mulatta). Animal Welfare 1, 39-53
"An increasing trend in time spent foraging with a concomitantdecline in aberrant behaviour over a time period of six monthswas particularly noteworthy [in the single-housed subjects]."
Bayne K, Dexter S, Suomi S 1992. Apreliminary survey of the incidence of abnormal behavior in rhesusmonkeys (Macaca mulatta) relative to housing condition.Lab Animal 21(5), 38-46
"The greatest frequency of overall abnormal behavior andstereotypic exploratory behavior was in the SC [single cage] condition,and the lowest frequency of occurrence in the CC [corn crib] condition... in IO [indoor/outdoor] runs, the animals showed no self-directedbehavior."
Bayne K, Mainzer H, Dexter SL, CampbellG, Yamada F, Suomi SJ 1991. The reduction of abnormal behaviorsin individually housed rhesus monkeys (Macaca mulatta) witha foraging/grooming board. American Journal of Primatology23, 23-35
All of the single-housed "animals foraged from the boardto the point that a significant reduction in the level of abnormalbehavior was noted."
Bennett BT, Spector MR 1989. The useof naturally occurring manipulanda to improve the psychologicalwell-being of singly housed baboons. Journal of the AmericanVeterinary Medical Association 194, 1782
The single-housed animals demonstrated a marked reduction ofstereotypy when they had corn-on-the-cob.
Bloomsmith MA, Alford PL, Maple TL1988. Successful feeding enrichment for captive chimpanzees. AmericanJournal of Primatology 16, 155-164
Four feeding techniques were simultaneously implemented. "Agonistic,abnormal, and grooming behaviors were significantly reduced."
Boccia ML 1989. Long-termeffects of a natural foraging task on aggression and stereotypiesin socially housed pigtail macaques. Laboratory PrimateNewsletter 28(2), 18-19
"Two months following the introduction of the foragingtask stereotypies remained depressed, and hairpulling remainedrare. In addition, bedding exploration and other types of explorationremained elevated, and agonistic behaviors remained low."
Boccia ML, Hijazi AS 1998. Aforaging task reduces agonistic and stereotypic behaviors in pigtailmacaque social groups. Laboratory Primate Newsletter37(3), 1-5
"The monkeys increased the time they spent engaged inenvironmentally directed [foraging] behaviors, and this correlatedwith a decrease in time spent in agonistic (for one group) andabnormal behaviors (for both groups). ... Both groups also evidenceddeclines in hairpulling. ... Stereotypies (such as pacing) alsosignificantly decreased in both groups."
Boinski S, Gross TS, Davis JK 1999.Terrestrial predator alarm vocalizations are a valid monitor ofstress in captive brown capuchins (Cebus apella). ZooBiology 18, 295-312
"Our results are consistent with the interpretation thatin conditions of low environmental enrichment the study subjectswere more stressed, and therefore more reactive to the presenceof a threatening terrestrial stimulus (human observer), than whenin more enriched conditions."
Brent L, Eichberg JW 1991. Woodchipbedding as enrichment for captive chimpanzees. American Journalof Primatology 24, 91-92
"Abnormal behavior and environmental manipulation weresignificantly lower during the woodchip [not mixed with food]condition."
Brent L, Long KE 1995. The behavioralresponse of individually caged baboons to feeding enrichment andthe standard diet: A preliminary report. Contemporary Topicsin Lab Animal Science 34(2), 65-69
"Increasing foraging opportunities in this study reducedabnormal behaviors from 16.4% of the data points in the baselinecondition to 4.9% and 5.7% in the chow [normal feeding condition]and feeder condition, respectively."
Brent L, Belik M 1997. The responseof group-housed baboons to three enrichment toys. LaboratoryAnimals 31, 81-85
"Abnormal, cage-directed, inactive and self-directed behavioursall significantly decreased after the [simultaneous] provisionof the toys."
Brown DL, Gold KC 1997. Effects ofstraw bedding on non-social and abnormal behavior of captive lowlandgorillas (Gorilla gorilla gorilla). In Proceedings onthe 2nd International Conference on Environmental EnrichmentHolst B (ed), 27-35. Copenhagen Zoo, Frederiksberg
"Two individuals were frequently observed to hold theirears or head while the exhibit was in an unbedded condition. Thisbehavior virtually disappeared in the enriched condition. ...Of the eight individuals found to engage in coprophagy, five individualswere observed to exhibit this behavior in solely the unbeddedcondition." Individuals who engaged in regurgitation-reingestiondemonstrated lower levels of this behavior in the bedded condition.
Chamove AS, Anderson JR, Nash VJ 1984.Social and environmental influences on self-aggression in monkeys.Primates 25, 319-325
"It is clear that enriched environmental conditions reducedSA [self-aggression]. Allowing monkeys to forage through cleanwoodchips, even when there is no obvious incentive, substantiallyreduced the level of this abnormal behavior."
Crockett CM, Bellanca RU, HeffernanKS, Ronan DA, Bonn WF 2001. PuzzleBall foraging device for laboratory monkeys. LaboratoryPrimate Newsletter 40(1), 4-7
"We were please that the empty Puzzle Balls were associatedwith a reduction [approximately 60%] in abnormal behavior."
Eaton GG, Kelley ST, Iliff-SizemoreSA 1993. Rawhide 'chew-bones' reduce abnormal behavior in individuallyhoused adult rhesus macaques. American Journal of Primatology30, 308
"Self-clasp showed a significant decline when the rawhidebones were present. We conclude that rawhide chew-bones are aneffective, and relatively inexpensive method of enriching theenvironment of individually housed rhesus macaques."
Honess PE, Marin CM 2006. Enrichmentand aggression in primates. Neuroscience and BiobehavioralReviews 30, 413-346
"There is considerable evidence that primates housed underimpoverished conditions develop behavioural abnormalities, including,in the most extreme example, self-harming behaviour. This hasimplications for all contexts in which primates are maintainedin captivity from laboratories to zoos since by compromising theanimals' psychological well-being and allowing them to developbehavioural abnormalities their value as appropriate educationaland research models is diminished. This review examines the extensivebody of literature documenting attempts to improve living conditionswith a view to correcting behavioural abnormalities and housingprimates in such a way that they are encouraged to exhibit a morenatural range and proportion of behaviours, including less self-directedand social aggression. The results of housing, feeding, physical,sensory and social enrichment efforts are examined with specificfocus on their effect on aggressive behaviour and variation intheir use and efficacy. It is concluded that while inappropriateor poorly distributed enrichment may encourage aggressive competition,enrichment that is species, sex, age and background appropriatecan dramatically reduce aggression, can eliminate abnormal behaviourand substantially improve the welfare of primates maintained incaptivity."
Kessel AL, Brent L 1998. Cage toysreduce abnormal behavior in individually housed pigtail macaques.Journal of Applied Animal Welfare Science 1, 227-234
"Providing multiple manipulable toys as enrichment for[single-caged] pigtail macaques was effective in reducing abnormalbehavior" during 30- min observation session.
Lam K, Rupniak NMJ, Iversen SD 1991.Useof a grooming and foraging substrate to reduce cage stereotypiesin macaques. Journal of Medical Primatology 20, 104-109
"Stereotyped behaviours were reduced by up to 73% by useof the fleece pad both alone and with foraging crumbles."
Maki S, Alford PL, Bloomsmith MA,Franklin J 1989. Food puzzle device simulating termite fishingfor captive chimpanzees (Pan troglodytes). AmericanJournal of Primatology 19(Supplement 1), 71-78
"Significant reductions of abnormal behavior and significantincreases in activity occurred with the pipe feeder's availability."
Meunier LD, Dukting JT, Landi MS 1989.Modification of stereotypic behavior in rhesus monkeys using videotapes,puzzlefeeders, and foraging boxes. Laboratory Animal Science39, 479
"Results of this study demonstrate that foraging boxesand puzzle feeders can reduce stereotypic behavior significantly[in single-housed subjects]."
Murphy DE 1976. Enrichmentand occupational devices for orang utans and chimpanzees.International Zoo News 137(23.5), 24-26
Subjects were provided with an artificial termite mount. "Themost encouraging result was a reduction in the female's stereotypedpacing. The environmental enrichment of the chimp exhibit hasresulted in a decrease in observable coprophagy, a diversificationof the activities, and a probable improvement in the physicaland psychological condition of the animals."
Nadler RD, Herndon JG, Metz B, FerrerAC, Erwin J 1992. Environmental enrichment by varied feeding strategiesfor individually caged young chimpanzees. In Chimpanzee Conservationand Public Health: Environments for the Future Erwin J, LandonJC (eds), 137-145. Diagnon/Bioqual, Rockville
"Providing an ear of unhusked corn on alternate days,in addition to laboratory chow, resulted in more time spent contactingfood [primarily the corn] an hour after feeding than feeding laboratorychow alone. Seven of eight [single-housed] animals exhibited lessstereotypy on the days they received the ear of corn. Stereotypicalbehavior, which occurs at relatively low frequencies under naturalconditions, was reduced somewhat when the animals were fed three[rather than one] meals."
Neu K, Lambeth S, Toback E, SchapiroS 2001. Haycan be used to decrease feces smearing in groups of captive chimpanzees.American Journal of Primatology 54(Supplement 1), 78
Feces smearing on the walls decreased significantly when haywas present compared to when no hay was available.
Poffe A, Melotto S, Gerrard PA 1995.Comparison of four environmental enrichment strategies in captivecommon marmosets (Callithrix jacchus). Primate Report42, 24-25
"Access to the puzzles was accompanied by increase insocial interaction and activity and decrease in stereotypic behaviour.This behavioural profile was also observed, to a lesser extent,in animals exposed to the 'gum tree'. ... Novel objects alone[toys] failed to significantly alter behaviour."
Preilowski B, Reger M, Engele H 1988.Combining scientific experimentation with conventional housing:A pilot study with rhesus monkeys. American Journal of Primatology14, 223-234
Manipulatory activity required by the apparatus reduced motorstereotypies but not self-biting in single-housed subjects.
Pyle DA, Bennett AL, Zarcone TJ, Turkkan.J. S., Adams RJ, Hienz RD 1996. Useof two food foraging devices by singly housed baboons. LaboratoryPrimate Newsletter 35(2), 10-15
"Stereotypical behaviors are reduced [in single-housedsubjects] when the devices are present. In addition, the foragingdevices elicited species-typical behaviors such as foraging andgrooming, even after food appeared to be absent from the devices."
Roberts RL, Roytburd LA, Newman JD1999. Puzzle feeders and gum feeders as environmental enrichmentfor common marmosets. Contemporary Topics in Laboratory AnimalScience 38(5), 27-31
"Gum feeders and Puzzle-Feeders loaded with waxmoth larvaeare useful for reducing the rates of pacing and inactivity"in single-housed and in pair-housed marmosets.
Steen Z 1995. Effectsof enriched food acquisition on activity budgets of two tamarinspecies at Adelaide Zoo. International Zoo News 42,284-298
Simple bamboo pipe feeder is described and tested in group-housedanimals. "The aim of the study was to [successfully] increaseforaging time with an increasing number of feeding devices [brawnbowl, bamboo pipe]. ... Prior to the study large amounts of furwere found in the nesting box of the golden tamarins. The zoovet suspected that this was a result of overgrooming. During andafter the study the overgrooming apparently ceased because theanimals had something else to do."
Taylor TD 2002. Feedingenrichment for red-handed tamarins. The Shape of Enrichment11(2), 1-3
Access to a 'feeding basket' [stuffed with straw mixed withtheir normal feed and hung from a perch] and suspended stickssmeared with acacia gum increased feeding activities while reducingthe incidence of stereotypy [primarily somersaulting], hyperactivity,coprophagy and excessive grooming and scent marking in a 3-adult-membergroup.
Watson L 1992. Effectof an enrichment device on stereotypic and self-aggressive behaviorsin singly-caged macaques: A pilot study. Laboratory PrimateNewsletter 31(3), 8-10
"A [temporary] reduction in some behavior pathology wasnoted, possibly due to replacing the stereotypic behaviors withactivities directed toward the feeder."
Weld K, Erwin J 1990. Provision ofmanipulable objects to cynomolgus macaques promotes species-typicalbehavior. American Journal of Primatology 20, 243
"A different pet toy was provided to each [single-caged]monkey" during six weeks. "Self-directed abnormal behaviorwas reduced or eliminated in all subjects in the presence of objectsbut increased after removal of the toys."
Wiard J 1992. Reduction of regurgitationand reingestion (R&R) in lowland gorillas at the OklahomaCity Zoo. Gorilla Gazette 6(3), 6-7
"The addition of browse or hay to the diet of captivegorilla reduces the occurrence of R&R [regurgitation-reingestion].Novelty items tend to reduce R&R [only] for short periodsof time."
Brent L, Weaver D 1996. Thephysiological and behavioral effects of radio music on singlyhoused baboons. Journal of Medical Primatology 25,370-374
Vocalization [of the single-housed subjects] was twice as highwhen the radio was off. Blood pressure did not vary with radiocondition, but the heart rate was significantly lower when theradio was playing.
Howell S, Roeder E, Nelson C, FritzJ, Schwandt M 2002. The effect of music on the behavior of captivechimpanzees (Pan troglodytes).American Journal of Primatology 57, 83-84
"Results suggest music has a significant effect on behaviorof captive chimpanzees. It resulted in decreased aggression andactive exploratory behavior and increased inactive resting andsocial behavior (principally social grooming). .. We suggest musicmay have a calming effect on behavior and good potential as therapeuticenvironmental enrichment."
*McDermott J,Hauser MD 2007. Nonhuman primates prefer slow tempos but dislikemusic overall. Cognition 104, 654-668
Both tamarins and marmosets preferred slow tempo to fast tempmusic, and when allowed to choose between slow tempo musical stimuliand silence they preferred silence.
Videan EN, Fritz F, Howell H, Murphy J 2007. Effects of two typesand two genre of music on social behavior in captive chimpanzees(Pan troglodytes). Journal of the American Association forLaboratory Animal Science [Contemporary Topics in Laboratory AnimalScience] 46(1)
"The purpose of this study was to test the effects of2 different types (vocal versus instrumental) and 2 genres (classicalvocal versus 'easy-listening' vocal) of music on social behaviorin 31 female and 26 male chimpanzees (Pan troglodytes). Resultsindicated that instrumental music was more effective at increasingaffiliative behavior in both male and female chimpanzees, whereasvocal music was more effective at decreasing agonistic behavior.A comparison of 2 genre of vocal music indicated that easy-listening(slower tempo) vocal music was more effective at decreasing agonisticbehavior in male chimpanzees than classical (faster tempo) vocalmusic. Agonistic behavior in females remained low (<0.5%) throughoutthe study and was unaffected by music. These results indicatethat, like humans, captive chimpanzees react differently to varioustypes and genres of music. The reactions varied depending on boththe sex of the subject and the type of social behavior examined."
Wells DL, Coleman D, Challis MG 2006. A note on the effectof auditory stimulation on the behaviour and welfare of zoo-housedgorillas. Applied Animal Behaviour Science 100(3-4), 327-332
Six gorillas housed in Belfast Zoo "were exposed to threeconditions of auditory stimulation: a control (no auditory stimulation),an ecologically relevant condition (rainforest sounds) and anecologically non-relevant condition (classical music). The gorillas'behaviour was recorded in each condition using a scan-samplingtechnique. There was no significant effect of the auditory environmenton the gorillas' behaviour, although animals tended to show morebehaviours suggestive of relaxation (i.e. resting, sitting) andfewer behaviours typically associated with stress (i.e. aggression,abnormal behaviour) during the ecologically relevant, and, inparticular, the non-relevant, conditions than the control. Overall,findings suggest that certain types of auditory stimulation mayhold some merit as a method of enrichment for zoo-housed gorillas."
Alexander S, Fontenot MB 2003. Isosexualsocial group formation for environmental enrichment in adult maleMacaca mulatta. AALAS [American Association for LaboratoryAnimal Science] 54th National Meeting Official Program, 141
Isosexual groups [averag group size: 4.2 animals] of 80, previouslysingle-caged 4-10 years old male rhesus macaques were formed [groupformation protocol is not outlined]. "Thirty-one [38.8%]of these animal had at least one prior incidence of SIB [self-injuriousbiting]. .. During the year prior to group formation, the clinicalhistory of the subjects included a 20% of diarrhea, 1.0% incidenceof wound infection and 12.5% incidence of severeSIB requiringpharmacological intervention and wound care. Animals with severeSIB were treated pharmacologically for 2-11 months prior to groupformation. All of these cases were removed from treatment priorto group formation. Over the 4-month period post formations <5.0%of the animals were removed for treatment of minor fight wounds.Less than 2.0% of the animals were removed for clinical purposed(e.g., diarrhea, dehydration). No occurrence of sever SIB wasnoted. We concluded that the formation of isosexual social groupsis a suitable alternative to individual housing of adult malerhesus monkeys and may decrease the occurrence of SIB in a susceptibepopulation."
Baker KC 1996. Chimpanzees in singlecages and small social groups: Effects of housing on behavior.Contemporary Topics in Laboratory Animal Science 35(3),71-74
Chimpanzees housed in pairs or trios showed fewer signs oftension, anxiety and aggressiveness than those housed singly.
Baker KC 1997. Human interaction asenrichment for captive chimpanzees: A preliminary report. AmericanJournal of Primatology 42, 92
"These results suggest that simple, unstructured affiliationbetween humans and chimpanzees has a powerful impact on well-being,promoting activity and relaxed conspecific interactions and amelioratingundesirable behaviors [e.g., abnormal behaviors]."
Bayne K, Dexter SL, Suomi SJ 1991.Social housing ameliorates behavioral pathologyin Cebus apella. LaboratoryPrimate Newsletter 30(2), 9-12
Change from single- to group-housing "effectively reducedstereotypic behaviors; however, it also was associated with morepassive behaviors being exhibited by the subjects. The concurrentshifts in these components of the behavioral repertoire suggeststhat the animals were in a calmer state when housed socially."
Bayne K, Dexter SL, Strange GM 1993.The effects of food treat provisioning and human interaction onthe behavioral well-being of rhesus monkeys (Macaca mulatta).Contemporary Topics in Laboratory Animal Science 32(2),6-9
"The effects of human interaction and food supplementationappear to be protracted, resulting in a reduction of pathology[behavioral disorders] even after the enrichment is removed."
Bloomsmith MA, Baker KC, Ross SK,Lambeth SP 1998. Enlarging chimpanzee social groups: The behavioralcourse of introductions. American Journal of Primatology45, 171
Stereotyped rocking declined in newly integrated individuals.
Boccia ML, Reite M, Laudenslager ML1989. On the physiology of grooming in a pigtail macaque. Physiologyand Behavior 45, 667-670
When the subject received grooming from others, heart ratewas significantly lower than during self grooming, as well asduring other behaviors.
Bourgeois SR, Brent L 2005. Modifyingthe behaviour of singly caged baboons: evaluating the effectivenessof four enrichment techniques. Animal Welfare 14, 71-81
Seven singly caged adolescent [mean age: 4.2 years] male baboonswere studied. "Analysis of baseline behaviour verified substantialdurations of abnormal behaviour [9.8/30- min observations (33%of time)]. We tested the effectiveness of ... positive reinforcementtraining (PRT), food enrichment [fruits, frozen fruit/juice, foragingdevices], non-food enrichment [toys], and social enrichment (pair/trio)....The social enrichment condition resulted in the most positivebehavioural changes, including ... near elimination of abnormalbehaviours [0.7/30-min observation (2% of time)]. Significantreduction in total abnormal behaviour levels were also found forother types of enrichment, but only social enrichment and PRTwere effective in reducing whole-body stereotypies. ... Animateenrichment (human or conspecific stimulation), as opposed to inanimateenrichment, provides optimal means of behaviour modification forsingly caged baboons."
Bushong D, Schapiro SJ, BloomsmithMA 1992. Self-aggression in nonhuman primates: A review of itsdevelopment/possible causes, methods of therapeutic treatment,and its relevance to the zoo situation. American Zoo and AquariumAssociation (AZA) Regional Conference Proceedings, 723-728
"Social enrichment appears to be the most effective methodof reducing the development or frequency of abnormal behaviors."... After the animals "were moved from single- to pair-housing,preliminary analyses of individual behavior indicated that therewas a decrease in time spent in self-aggressive behaviors."
Choi GC 1993. Humans enrich the livesof lab baboons. WARDS (Working for Animals Used in Research,Drugs and Surgery) Newsletter 4, 3-7 & 13
"The reduction in cage painting and banging was dramaticand remarkable" after the single-housed animals receivedmore attention from the attending personnel.
Coe CL, Franklin D, Smith ER, LevineS 1982. Hormonal responses accompanying fear and agitation inthe squirrel monkey. Physiology and Behavior 29, 1051-1057
"The presence of a social partner reduced signs of behavioraldisturbance."
Coelho AM, Carey KD, Shade RE 1991.Assessing the effects of social environment on blood pressureand heart rates of baboon. American Journal of Primatology23, 257-267
In the social companion condition, a subject was able to havevisual, tactile, and auditory interactions with his companionthrough the wire mesh walls of the specially designed cages. "Whenanimals were housed with social companions their blood pressureswere consistently lower than when they were either housed individuallyor with social strangers. ... Measurements of cardiovascular physiologyobtained under social housing may more closely model normal physiologythan ... individual housing."
Eaton GG, Kelley ST, Axthelm MK, Iliff-SizemoreSA, Shiigi SM 1994. Psychological well-being in paired adult femalerhesus (Macaca mulatta). American Journal of Primatology33, 89-99
Paired females show strong preference to spend time in closeproximity; agonistic behaviors are very infrequent. Health measures,body weight gains, reproduction and immune responses do not differbetween dominant, subordinate, and single-housed females. Pairedfemales spend less time engaged in abnormal behavior than single-housedfemales."
Fritz P, Fritz J 1979. Resocializationof chimpanzees. Journal of Medical Primatology 8, 202-221
"With the exception of Tim, stereotyped behaviors in otherindividuals decreased almost immediately upon introduction ofa compatible cage mate and continued to decrease as socializationproceeded."
Gonzalez CA, Coe CL, Levine S 1982.Cortisol responses under different housing conditions in femalesquirrel monkeys. Psychoneuroendocrinology 7, 209-216
Plasma levels of cortisol "were significantly lower inpair-housed females than in those living in a social group orindividually. The increment in cortisol levels after stress (handlingand ether anesthesia) also was smaller in females housed in pairs."Dominant and subordinate partners of female pairs did not differin their plasma cortisol levels.
Goodwin J 1997. The application, use,and effects of training and enrichment variables with Japanesesnow macaques (Macaca fuscata) at the Central Park WildlifeCenter. American Zoo and Aquarium Association (AZA) RegionalConference Proceedings, 510-515
A training protocol is briefly described which allows the keepersthrough vocal and visual cues to herd the animals to a holdingarea. Training sessions were "deterring stereotypic and abnormalbehaviour - such as excessive grooming and fur-pulling."
Goosen C 1988. Studies of disturbedbehaviour in macaques. In Biomedical Research in Primates.Proceedings of the TNO Symposium Jonker M (ed), 67-74
Stereotyped locomotion amounted to about 20% of the time whenthe subjects were housed solitary. The amount of time spent inthis behaviour was reduced to about 4% when the subjects had oneor more social partners.
*Gunnar MR, GonzalezCA, Levine S 1980. The role of peers in modifying behavioral distressand pituitary-adrenal response to a novel environment in year-oldrhesus monkeys. Physiology and Behavior 25, 795-798
Infant rhesus macaques were captured from their social groupand placed in an unfamiliar environment for 24 hours either (a)alone or (b) with another infant from the same group. When testedalone, the animals exhibited significantly more signs of distress- agitation, distress vocalization - than when they were testedwith a companion, indicating that the companion had a stress-bufferingeffect.
Gust DA, Gordon TP, Brodie AR, McClureHM 1994. Effect of a preferred companion in modulating stressin adult female rhesus monkeys. Physiology and Behavior55, 681-684
"Adult female rhesus monkeys exhibited a profound stressresponse when removed from their social group to a novel environment.Recovery time [of T cell subsets] was significantly enhanced bythe presence of a preferred companion."
Gwinn LA 1996. A method for usinga pole housing apparatus to establish compatible pairs among squirrelmonkeys. Contemporary Topics in Laboratory Animal Science35(4), 61
Pair formation protocol in a pole-and-collar housing systemis described. "Pair housing the animals has not interferedwith research. During nine treatments with an identical test compound,singly housed animals lost significantly more weight on averagethan did pair housed animals."
Hartner MK, Hall J, Penderghest J,White E, Watson S, Clark L 2000. A novel approach to group-housingmale cynomolgus macaques in a pharmaceutical environment. ContemporaryTopics in Laboratory Animal Science 39(4), 67
"Twenty percent of our primates are maintained in a single-housedenvironment. Of those single-housed animals, 40% exhibited moderateto marked degrees of self-directed activity; i. e., hairpulling.By contrast, none of the pair or group-housed animals exhibitedthese behaviors. ... These primates are now more receptive tohandling and training, and will therefore be better animal models,as noted by a marked decrease in vocalization and self-directedbehavior during pole/collar capture and chair restraint procedures."
*Hennessy MB1984. Presence of companion moderates arousal of monkeys withrestricted social experience. Physiology and Behavior 33,393-398
When placed in a novel environment for 30 minutes, juvenilesquirrel monkeys emitted significantly more high-pitched vocalizationswhen tested alone than when tested in the presence of the companion.A significant elevation of plasma cortisol was observed only whenanimals were exposed to the novel environment alone.
Kessel AL, Brent L 1997. Rehabilitatinga rheboon (Macaca mulatta x Papio hamadryas cynocephalus),from single housing to social housing: A case study. AmericanJournal of Primatology 42, 121
Abnormal behavior was reduced from 46% of observation timein the single-housed condition to 4% after introduction to anenclosure with ten other rhesus females.
Kessel A, Brent L 2001. The rehabilitationof captive baboons. Journal of Medical Primatology 30,71-80
"Eleven baboons who had been singly housed indoors foran average of 5 years were moved to outdoor social groups in anattempt to provide a more species-typical environment and reducehigh levels of abnormal behavior. ... Abnormal behavior decreasedsignificantly from an average of 14% of the observation time inthe single cages to 3% in the sixth month of social housing. Cagemanipulation and self-directed behaviors also significantly decreased."
Line SW, Morgan KN, Markowitz H, RobertsJ, Riddell M 1990. Behavioral responses of female long-tailedmacaques (Macaca fascicularis) to pair formation. Laboratory Primate Newsletter 29(4),1-5
"Self-abusive behaviors were recorded for five of theten subjects when singly housed, but were completely absent afterpair formation."
Lutz CK, Novak M 2005. Environmentalenrichment for nonhuman primates: Theory and application.ILAR [Institute for Laboratory Animal Research] Journal46(2), 178-191
"Only social contact satisfies the goal of promotinga wide variety of species-typical activities while at the sametime reducing or preventing the development of abnormal behavior... A number of toys should be provided initially and rotated ona regular basis to maintain interest. .. At present, the mosteffective form of enrichment for captive primates is social housing."
Mahoney CJ 1992. Some thoughts onpsychological enrichment. Lab Animal 21(5), 27,29,32-37
"Isolation 'wards' for ill animals and infectious studychambers can have windows or transparent plastic panels betweencages, providing visual communication without interfering withindependent or filtered air-flow."
Mason WA 1960. Socially mediated reductionin emotional responses of young rhesus monkeys. Journal ofAbnormal and Social Psychology 60, 100-110
"Previous observations that social stimuli may functionas a source of security and a means of mitigating emotional distressin young primates are fully supported by the present results."
Miller LC, Bard KA, Juno CJ, NadlerRD 1986. Behavioral responsiveness of young chimpanzees (Pantroglodytes) to a novel environment. Folia Primatologica47, 128-142
"Extreme distress reported previously for chimpanzeesand human children when tested alone in a novel situation wasrarely observed in these tests when an attachment figure [humancaretaker] was present."