Re finem for Annot ment a Prima tated nd En ates K Biblio vironm ...

Table of ContentsSpecies-typical Behavior .................................................................................................... 1Behavioral Pathologies (Abnormal Behavior) ................................................................. 2Extraneous Variables .......................................................................................................... 2-28(1) Definition ......................................................................................................................... 2(2) Scientific Principles ........................................................................................................ 2-6(3) Insufficient/Inadequate Space ....................................................................................... 6-8(4) Barren environment ....................................................................................................... 8-9(5) Single-caging ................................................................................................................... 9-13(6) Premature Weaning ....................................................................................................... 13(7) Enforced Restraint ......................................................................................................... 14-19(8) Queue Effect, Sequential Treatment ............................................................................ 19(9) Unfamiliar Environment ............................................................................................... 19-21(10) Double-tier Cage Arrangement .................................................................................. 21-25(11) Neighbor Effect ............................................................................................................ 25-26(12) Observer Effect, Presence of Personnel ..................................................................... 26-28(13) Noise .............................................................................................................................. 28Refinement ........................................................................................................................... 29-57(1) Definition ......................................................................................................................... 29(2,a) Unstructured Space ..................................................................................................... 29-30(2,b) Structured Space ......................................................................................................... 30-32(2,c) Playpen, Outdoor Housing, Exercise Cage ............................................................... 33-36(3) Inanimate and Feeding Enrichment ............................................................................. 36-41(4) Acoustical Enrichment .................................................................................................. 41-42(5) Animate Enrichment ...................................................................................................... 42-50(6) Natural Weaning ............................................................................................................ 50-51(7) Working with Cooperative Animals ............................................................................. 52-56(8) Treatment of Trained Animals in their Home Enclosure .......................................... 56-57(9) Cage Arrangement ......................................................................................................... 57Environmental Enrichment ............................................................................................... 58-134(1) Definition ......................................................................................................................... 58(2) Promoting Social Behavior ............................................................................................ 58-88(2,1,a) Group-housing: Practical Issues ................................................................................. 59-63(2,1,b) Group-housing: Group Formation/Introduction/Integration ...................................... 64-70(2,2,a) Pair-housing: Practical Issues, Time Budget .............................................................. 71-78(2,2,b) Pair-housing: Pair formation ...................................................................................... 78-83(2,3) Grooming-Contact Caging ............................................................................................ 83(2,4) Positive Interaction with Humans ................................................................................. 83-88(3) Promoting Intelligent Behavior (positive reinforcement training) ............................ 88-99(3,1) Basic Recommendations ............................................................................................... 88-90(3,2) Species-specific Recommendations .............................................................................. 90-99(4) Promoting Foraging and Food Processing Behavior .................................................. 99-115(4,1) Foraging Devices .......................................................................................................... 99-107

Species-typical Behavior1The following reports provide excellent overviews of the species-typical behavior of wildprimates.Caldecott JO 1986. An Ecological and Behavioral Study of the Pig-tailed macaque. Karger,Basel, SwitzerlandChopra PK, Seth PK, Seth S 1992. Behavioural profile of free-ranging rhesus monkeys. PrimateReport 32, 75-105Hall KR 1968. Behaviour and ecology of the wild patas monkey, Erythrocebus patas, in Uganda.In Primates - Studies in Adaptation and Variability Jay PC (ed), 32-119. Holt, Rinehart andWinston, New York, NYHall KRL, DeVore I 1965. Baboon social behavior. In Primate Behavior - Field Studies ofMonkeys and Apes DeVore I (ed), 53-110. Holt, Rinehart and Winston, New York, NYLindburg DG 1971. The rhesus monkey in North India: an ecological and behavioral study. InPrimate Behavior: Developments in Field and Laboratory Research, Volume 2 Rosenblum LA(ed), 1-106. Academic Press, New York, NYPoirier FE 1970. The Nilgiri langur (Presbytis johnii) of South India. In Primate Behavior:Developments in Field and Laboratory Research, Volume 1 Rosenblum LA (ed), 251-383.Academic Press, New York, NYRoonwal ML,Mohnot SM 1977. Primates of South Asia - Ecology, Sociobiology, and Behavior.Harvard University Press, Cambridge, MASchaller GB 1965. The behavior of the Mountain Gorilla. In Primate Behavior - Field Studies ofMonkeys and Apes DeVore I (ed), 324-367. Holt, Rinehart and Winston, New York, NYSimonds PE 1965. The bonnet macaque in South India. In Primate Behavior - Field Studies ofMonkeys and Apes DeVore I (ed), 175-196. Holt, Rinehart and Winston, New York, NYSouthwick CH, Beg MA, Siddiqi MR 1965. Rhesus monkeys in North India . In PrimateBehavior - Field Studies of Monkeys and Apes DeVore I (ed), 111-159. Holt, Rinehart andWinston, New York, NYTeas J, Richie T, Taylor H, Southwick C 1980. Population patterns and behavioral ecology ofrhesus monkeys (Macaca mulatta) in Nepal. In The Macaques: Studies in Ecology, Behavior andEvolutionLindburgh DG (ed), 247-262. Van Nostrand Reinhold, New York, NYVan Lawick-Goodall J 1968. A preliminary report on expressive movements and communicationin the Gombe Stream chimpanzee. In Primates - Studies in Adaptation and Variability Jay PC(ed), 313-374. Holt, Rinehart and Winston, New York, NYWheatley BP 1999. The Sacred Monkeys of Bali. Waveland Press, Prospect Heights, IL

2Behavioral Pathologies (Abnormal Behavior)The following articles describe abnormal behavior patterns commonly shown by captiveprimates.Erwin J, Deni R 1979. Strangers in a strange land: Abnormal behavior or abnormalenvironments? In Captivity and Behavior Erwin J, Maple T, Mitchell G (eds), 1-28. VanNostrand Reinhold, New York, NYFittinghoff NA, Lindburg DG, Gomber J, Mitchell G 1974. Consistency and variability in thebehavior of mature, isolation-reared, male rhesus macaques. Primates 15, 111-139Walsh S, Bramblett CA, Alford PL 1982. A vocabulary of abnormal behaviors in restrictivelyreared chimpanzees. American Journal of Primatology 3, 315-319Extraneous Variables(1) DefinitionAn extraneous variable is a factor that is not the object of investigation yet bears the potentialof changing the research data in uncontrolled ways.(2) Scientific PrinciplesAmerican Medical Association 1992. Use of Animals in Biomedical Research - An AmericanMedical Association White Paper. AMA Group on Science and Technology, Chicago, IL"Biomedical experiments are conducted in accordance with the principles of the scientificmethod developed by the French physiologist, Claude Bernard, in 1865. This method establishedtwo requirements for the conduct of a valid experiment: (1) control of all variables so that onlyone factor or set of factors is changed at a time, and (2) the replication of results by otherlaboratories. Unless these requirements are met, an experiment is not considered valid. ...Stressed animals do not make good research subjects."American Society of Primatologists 2000. American Society of Primatologists guidelines for theethical treatment of nonhuman primates. ASP Bulletin 24(4), 4"We should make use of information on a species natural history to improve management andenrich environments, because physical and psychological well-being are essential not only to thehealth of the animals but also to the validity of the research results."Animal Welfare Institute 1979. Comfortable Quarters for Laboratory Animals, 7th Ed. AnimalWelfare Institute, Washington, DC"Whenever possible, primate conspecifics should be housed together in social groups because oftheir social needs, and these needs should not take second place to housing systems designedprimarily for the convenience of animal care technicians. Independent of ethical considerations,to deprive a gregarious animal of its basic behavioral, emotional, and social needs is no lessdetrimental to the validity of many scientific investigations than deprivation of light, fresh air,food and water."

3Bayne K 2005. Environmental enrichment: Potential for unintended consequences and researchresults. ILAR [Institute for Laboratory Animal Research] Journal 46(2), 129-139http://dels.nas.edu/ilar_n/ilarjournal/46_2/html/v4602bayne.shtml"Although it is unlikely that every possible variable can be controlled ... more detailed disclosurein journals ... of the living environment of the subject animals .. will allow for a bettercomparison of the findings, and contribute to the broader knowledge base of the effects ofenrichment.“Brockway BP, Hassler CR, Hicks N 1993. Minimizing stress during physiological monitoring.In Refinement and Reduction in Animal Testing Niemi SM, Willson JE (eds), 56-69. ScientistsCenter for Animal Welfare, Greenbelt, MD"Elimination of sources of variability (stress for example) may allow the use of fewer animalsgiving equally valid results."Chance MR, Russell WMS 1997. The benefits of giving experimental animals the best possibletreatment. In Comfortable Quarters for Laboratory Animals, 8th Ed. Reinhardt V (ed), 12-14.Animal Welfare Institute, Washington, DC"If we use ethological sophistication to provide laboratory animals with the very best physicaland social environment conditions for their well-being, we need to use fewer of them in researchexperiments or routine tests, and our results will be accurate and reliable."Davis DE, Bennett CL, Berkson G, Lang CM, Snyder RL, Pick JR 1973. Recommendations for astandar-dized minimum description of animal treatment. ILAR News 16(4), 3-4"It is clear [from this survey] that many investigators do not realize the influence of ...environmental variables [e.g., housing, handling, temperature, light] on experimental results orat least do not adequately describe the environmental history of the animals used forexperimentation."Fuchs E 1997. Requirements of biomedical research in terms of housing and husbandry:Neuroscience. Primate Report 49, 43-46"Housing conditions are among the parameters which are important contributors to the nature,quality, and reproducibility of research obtained in laboratory animal investigations. ... It isabsolutely important that the animals are able to display as many aspects of their naturalbehavioural repertoire and confounding factors such as abnormal behavior, injuries, diseases,and stress are excluded."Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housingand Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London, UKhttp://scienceandresearch.homeoffice.gov.uk/animalresearch/legislation/codesofpractice/housingcare"Experimental results may be influenced by environmental conditions. ... To demonstrate anyexperimental response against such a variable background generates a requirement for greateranimal usage if the result is to be statistically valid."Lang CM, Vesell ES 1976. Environmental and genetic factors affecting laboratory animals:impact on biomedical research. Federation Proceedings 35, 1123-1124The survey "suggests that many investigators do not fully recognize the influence ofenvironmental and genetic variables on experimental results.... Failure to give an adequatedescription of these variables makes it difficult, if not impossible, to duplicate an experiment inother laboratories."

Meyerson BJ 1986. Ethology in animal quarters. Acta Physiologica Scandinavica 554 (S), 24-31The requirements for 'carefully controlled conditions' counteracts its fundamental purpose if itresults in housing conditions where the animals have difficulties in adapting(psychoneuroendocrine changes which may disturb the experimental results).National Research Council 1996.Guide for the Care and Use of Laboratory Animals. NationalAcademy Press, Washington, DChttp://www.nap.edu/books/0309053773/html/"A good management program provides the environment, housing, and care that ... minimizesvariations that can affect research. ... Animals should be housed with the goal of maximizingspecies-specific behaviors and minimizing stress-induced behaviors."Novak MA, Bayne K 1991. Monkey behavior and laboratory issues. Laboratory Animal Science41(4), 306-307"Monkeys are socially complex creatures. When this aspect of their nature is accommodated inresearch settings, the benefit to science is a less stressed animal that provides meaningfulscientific data."Öbrink KJ, Rehbinder C 1999. Animal definition: a necessity for the validity of animalexperiments? Laboratory Animals 22, 121-130"'Material and Methods' section mostly reveals an obvious or almost total lack of informationabout the animals. ... The animal definition should not only include species, sex and age but also... the environmental conditions to which the animals are exposed. ... The prerequisites for theuse of fewer animals per project, while still retaining a sufficiently high degree of accuracy arehigh levels of reproducibility and precision in the experimental results. Factors that may affectthese will be discussed in this paper. If a researcher, through carelessness or ignorance, shoulduse more animals for a project than is necessary, it must be considered unethical. ...Withouthesitation, it is a scientific demand that all factors that have not proven to be insignificant shouldbe checked, controlled or kept constant."Public Health Service (PHS), U.S. Department of Health and Human Services 1994. Theimportance of animals in biomedical and behavioral research. Laboratory Primate Newsletter33(4), 12http://www.brown.edu/Research/Primate/lpn33-4.html#state"Like most people, scientists are concerned about animal well-being. ... Institutions receivingsupport from the Public Health Service are obliged to adhere to the highest possible standardsfor the humane care and responsible use of laboratory animals. And scientists themselves haveadopted the principle: 'Good Animal Care and Good Science Go Hand in Hand'."Reinhardt V 1991. Impact of venipuncture on physiological research conducted in consciousmacaques. Journal of Experimental Animal Science 34, 212-217http://www.awionline.org/Lab_animals/biblio/es34-2~1.htm"Despite the fact that venipuncture often is a stressful event for research animals, 81% of the[58] studies [assessing stress-sensitive physiological data] did not account for this circumstanceby providing no information as to how the subjects were caught and how they were immobilizedduring venipuncture. ... It was concluded that the description of the experimental animal'shandling prior to and during venipuncture is a methodological issue that needs to be clarified inorder to account for a dependent possibly data-biasing variable.”4

5Reinhardt V, Reinhardt A 2000. Blood collection procedure of laboratory primates: A neglectedvariable in biomedical research. Journal of Applied Animal Welfare Science 3, 321-333http://www.awionline.org/Lab_animals/biblio/jaaws2.html"A survey of 75 biomedical articles dealing with stress-dependent blood parameters in cagedprimates revealed that the conditions under which blood collection occurred were in most cases[72%] described either not at all or so haphazardly that it would be impossible to determine ifhumane handling procedures were used and basic principles of scientific methodology applied.These findings were unexpected because not only is there ample scientific evidence that stresssensitiveresearch data are influenced by traditional blood sampling procedures, but also thatthose data-biasing effects can be avoided. If dependent variables of the blood collectionprocedure are not controlled, data variability will increase thereby automatically alsoincreasing the number of animals needed for statistical analysis. For ethical and scientificreasons, it was recommended that editors of biomedical journals should require that authorsprovide sufficient information of the blood collection - and when applicable also of the sedativeinjection - procedure to assure that the experiment was done with the smallest number ofanimals possible to achieve statistical significance, and that the investigation can be replicatedreliably in another laboratory and the research data interpreted with reasonable accuracy."Reinhardt V, Reinhardt A 2000. The lower row monkey cage: An overlooked variable inbiomedical research. Journal of Applied Animal Welfare Science 3, 141-149http://www.awionline.org/Lab_animals/biblio/jaaws1.htm"A survey of 96 primatological articles revealed that cage location of research monkeys isusually not mentioned (98%), in spite of the fact that the environment of upper- and lower-rowhoused animals markedly differs in terms of light quality, light intensity and living dimension.Not accounting for these uncontrolled variables may increase variability of data and,consequently, the number of experimental animals needed to obtain statistically acceptableresults.”Russell WMS 1997. Shooting the clock: Timeless lessons of the past still guide today'srefinement initiatives. WARDS Newsletter 8(3), 1-2"Scientifically, we must ensure the validity of research results and a stressed animal is not aproper specimen for science."Russell WMS, Burch RL 1959. The Principles of Humane Experimental Technique Methuen,London, UKhttp://altweb.jhsph.edu/publications/humane_exp/het-toc.htm"The wages of inhumanity" are "paid in ambiguous or otherwise unsatisfactory experimentalresults. .. If we can ... remove any unwanted source of variance, we reap our reward at once insmaller residual variance, greater precision, and hence fewer experimental animals."Schwindaman D 1991. The 1985 animal welfare act amendments. In Through the Looking GlassNovak MA, Petto AJ (eds), 26-32. American Psychological Association, Washington, DC"It is only common sense, for instance, that an animal will not respond normally if it is stressedor undernourished. ... Because the validity of research results is so dependent on the health ofresearch animals, the future of science depends on the integrity of scientific methods and thetreatment of animals used in research.”T-W-Fiennes RN 1972. Primates - General. In The UFAW Handbook on the Care andManagement of Laboratory Animals Fourth Edition Universities Federation for Animal Welfare(ed), 374-375. Churchill Livingstone, London, UK

6"An animal treated unsympathetically is liable to become aggressive and uncooperative;furthermore, unless care is taken over its comfort and needs, it is liable to become stressed andthe results of the experiment may be vitiated for this reason."Veira Y, Brent L 2000. Behavioral intervention program: Enriching the lives of captivenonhuman primates. American Journal of Primatology 51(Supplement), 97“The most common behaviors reported were hair pulling, pacing, rocking and self-aggression."It was suggested "that baboons with abnormal behaviors do not cope well with theirenvironment, are not good candidates for research or breeding purposes, and many [are]eventually euthanized. ... Abnormal and stress-related behaviors in nonhuman primates have ameasurable negative impact on research and breeding program effectiveness."Warwick C 1990. Important ethological and other considerations of the study and maintenanceof reptiles in captivity. Applied Animal Behaviour Science 27, 363-366"The majority of scientists seem to make great efforts to avoid being associated with 'animalwelfarist' or to become open to allegations of being somehow 'scientifically soft'. However,awareness of actual and potential stress and distress among animals in whatever situationshould not be regarded as subjective but as a sound scientific base for the study of animals.Whether an observer maintains a high personal respect of the well-being of the individualanimal or holds classic concepts of animals as being experimental 'models', it should be morewidely recognized that there is typically a scientific necessity to have animals at ease with theirenvironments if studies are to remain objective."Wolfle TL 1996. How different species affect the relationship. In The Human/Research AnimalRelationship Krulisch L, Mayer S, Simmonds RC (eds), 85-91. SCAW, Greenbelt, MD“The right technician instills qualities in the animals that make them better and more reliableresearch subjects. Stress, on the other hand, leads to profound physiological and behavioralchanges that increase the variability of the data and decrease the reliability of the results."(3) Insufficient/Inadequate SpaceBoot R, Leussink AB, Vlug RF 1985. Influence of housing conditions on pregnancy outcome incynomolgus monkeys (Macaca fascicularis). Laboratory Animal Science 19, 42-47More successful pregnancies were recorded for females housed individually in large cages thanfor females housed in small cages.Boyce WT, O'Neill-Wagner PL, Price CS, Haines MC, Suomi SJ 1998. Crowding stress andviolent injuries among behaviorally inhibited rhesus macaques. Health Psychology 17, 285-289A rhesus group of 36 animals was kept during 6 'warm' months in a large outdoor enclosure,during 6 'cold' months confined in a building. "During the 6-month period of confinement stress,a fivefold acceleration in [medically-attended] injury incidence was found."Draper WA, Bernstein IS 1963. Stereotyped behavior and cage size. Perceptual and Motor Skill16, 231-234"It was concluded that spatial restriction which does not permit 'normal' locomotor behavior,e.g., running, climbing, etc., results in substitute motor expression which frequently takes theform of repetitive stereoptyped movement."Faucheux B, Bertrand M, Bourliere F 1978. Some effects of living conditions upon the pattern ofgrowth in stumptail macaque (Macaca arctoides). Folia Primatologica 30, 220-236

7"Confinement and prolonged lack of physical exercise are very probably responsible for thereduced weight and size of our monkeys bred in laboratory conditions. ... This is apparently dueto the impaired development and resulting athrophy of the muscles, particularly those of the hindquarters. This athrophy was especially noticeable in lab-bred group II monkeys which have beenkept in small individual cages for years. ... The ways in which most primates are bred and kept inmany research laboratories are obviously far from ideal. Many 'normal' control subjects mightwell be in fact abnormal both somatically and behaviorally."Kerl J, Rothe H 1996. Influence of cage size and cage equipment on physiology and behavior ofcommon marmosets (Callithrix jacchus). Laboratory Primate Newsletter 35(3), 10-13http://www.brown.edu/Research/Primate/lpn35-3.html#kerl"The mean daytime heart rate increased with increasing cage size for the standard cages. Thiswas expected because of the increased options for locomotor behavior."Kitchen AM, Martin AA 1996. The effects of cage size and complexity on the behaviour ofcaptive common marmosets, Callithrix jacchus jacchus. Laboratory Animals 30, 317-326"Stereotyped behaviours, which occurred in the small cages, were never exhibited in the largecages."Mendoza SP 1999. Squirrel Monkeys. In The UFAW [Universities Federation for AnimalWelfare] Handbook on the Care and Management of Laboratory Animals Seventh Edition. PooleT, English P (eds), 591-600. Blackwell Science, Oxford, UK"The most common form of stereotypic behavior in squirrel monkeys is an exaggerated headtwirling, usually associated with pacing. ... The incidence of the behaviour seems to be morefrequent in small cages, and frequent occurrence of this behaviour may indicate that more spaceis required."National Research Council 1996. Guide for the Care and Use of Laboratory Animals. NationalAcademy Press, Washington, DChttp://www.nap.edu/books/0309053773/html/“For arboreal animals that normally flee upward and spend much of their locomotor timeclimbing, floor area might be secondary to vertical space in providing for postural andlocomotor expression. The volume of space available, rather than floor area, might be criticalfor nonhuman primates.”Paulk HH, Dienske H, Ribbens LG 1977. Abnormal behavior in relation to cage size in rhesusmonkeys. Journal of Abnormal Psychology 86, 87-92"Observations were made of 24 monkeys that were introduced singly into a [barren] small and a[barren] large test cage. In a large cage, more normal but less stereotyped locomotion wasshown than in a small cage."Turnquist J 1985. Passive joint mobility in patas monkeys: Rehabilitation of caged animals afterrelease into a free-ranging environment. American Journal of Physical Anthropology 67, 1-6Housing in small cages had detrimental effects on joint mobility, which could be reversed byreleasing the animals into a free-ranging environment.van Wagenen G 1950. The monkeys. In The Care and Breeding of Laboratory Animals Farris EJ(ed), 1-42. John Wiley, New York, NY

8"If sufficient room is not provided, some males will soon show depression, sitting quietly in thepart of the cage which affords the best view. For a while this may be interpreted as anadaptation. ... Too often, however, this persistent posture apparently results in a pressureatrophy, bringing on a lower-limb palsy, the so-called 'cage paralysis'."Westergaard GC, Izard MK, Drake JH 2000. Reproductive performance of rhesus macaques(Macaca mulatta) in two outdoor housing conditions. American Journal of Primatology 50, 87-93"We conclude that, for rhesus macaques, outdoor corral housing leads to better reproductiveperformance than does semi-sheltered gang housing, probably as a result of increased individualspace and relaxation of intense social stressors."(4) Barren EnvironmentBayne K, Dexter SL, Mainzer H, McCully C, Campbell G, Yamada F 1992. The use of artificialturf as a foraging substrate for individually housed rhesus monkeys (Macaca mulatta). AnimalWelfare 1, 39-53http://www.awionline.org/Lab_animals/biblio/aw1-39.htmWhen their cages were not enriched, eight single-caged subjects exhibited "abnormal behaviors"approximately 37% of the time.Bayne K, Dexter SL, Suomi SJ 1991. Social housing ameliorates behavioral pathology in Cebusapella. Laboratory Primate Newsletter 30(2), 9-12http://www.brown.edu/Research/Primate/lpn30-2.html#bayne"No specific enrichment devices were included in the [single-] cages." The seven subjects' meanpercentage of occurrence of "stereotypic behaviors" was 13%.Bayne K, Mainzer H, Dexter SL, Campbell G, Yamada F, Suomi SJ 1991. The reduction ofabnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with aforaging/grooming board. American Journal of Primatology 23, 23-35Prior to enrichment, individuals spent on average 25% of their time engrossed in abnormalbehaviors.Bayne K, Mainzer H, Dexter SL, Campbell G, Yamada F, Suomi SJ 1991. The reduction ofabnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with aforaging/grooming board. American Journal of Primatology 23, 23-35Prior to enrichment, individuals spent on average 25% of their time engrossed in abnormalbehaviors.Garner J 2002. Why every scientist should care about animal welfare: Abnormal repetitivebehavior and brain function in captive animals. Fourth World Congress on Alternatives andAnimal Use in the Life Sciences, 95 (Abstract)”Barren laboratory housing also induces abnormal behaviors in many species, particularlystereotypies, fur and feather plucking, and self-mutilation. Similar behaviors in human mentaldisorder are correlated with dysfunction in brain areas that control the selection and sequencingof behavior. Experiments in several captive species will be reviewed, showing the samebehaviors correlate with dysfunction in the same brain areas. For instance, in laboratory mice:like stereotypy in autism and schizophrenia, stereotypy correlates with impairments of basalganglia function; and like hair pulling in trichotillomania and autism, barbering (hair plucking)correlates with impairments of prefrontal cortex function. Therefore, far from standardizing

9laboratory animals, barren environments may induce severe brain abnormalities. Theseabnormalities call the validity of a wide range of experiments into question. Limits of currentknowledge and pressing research directions will be identified. In particular, enrichments thatprevent these behaviors may reduce variability between animals and produce animals that arebetter models of normal function. Thus, enrichment may actually improve the standardization ofresearch animals and refine current animal models. In short, 'good welfare is good science'.“Kessel AL, Brent L 1996. The effectiveness of cage toys in reducing abnormal behavior inindividually housed pigtail macaques. XIXth Conference of the American Society ofPrimatologists, Abstract No. 519Prior to the provision of environmental gadgets subjects exhibited "abnormal behavior" 24% ofthe time.Lam K, Rupniak NMJ, Iversen SD 1991. Use of a grooming and foraging substrate to reducecage stereotypies in macaques. Journal of Medical Primatology 20, 104-109http://www.awionline.org/Lab_animals/biblio/jmp20-1.htm"Animals exhibited idiosyncratic repertoires of stereotyped behaviour, including repetitivepacing, swaying circling, bouncing, cage charging, and rocking. These activities occupied onaverage 11% of baseline observation periods" prior to the introduction of the enrichmentgadget.Reinhardt V 1997. Refining the traditional housing and handling of laboratory rhesus macaquesimproves scientific methodology. Primate Report 49, 93-112http://www.awionline.org/Lab_animals/biblio/pr-refi.htm"A monkey housed in an empty cage is literally a behavioral cripple because s/he is chronicallydeprived of appropriate stimuli for the expression of species-typical behavior patterns. It isdifficult to know objectively if a monkey experiences boredom when being kept in anunderstimulating environment. However, many such animals show signs of depression and/orengage in gross behavioral disorders."5) Single-cagingAlexander S, Fontenot MB 2003. Isosexual social group formation for environmental enrichmentin adult male Macaca mulatta. AALAS 54th National Meeting Official Program, 141Thirty-one [38.8%] of a colony of 80, previously single-caged 4-10 years old male rhesusmacaques had at least one incidence of self-injurious biting.. During the year prior to groupformation, the clinical history of the subjects included a 12.5% incidence of severe self bitingrequiring pharmacological intervention and wound care. These animals were treatedpharmacologically for 2-11 months prior to group formation. All of these cases were removedfrom treatment prior to group formation. No self biting was noted during a follow-up period offour months after the animals had been transferred to group-housing.Bellanca RU, Crockett CM 2002. Factors predicting increased incidence of abnormal behavior inmale pigtailed macaques. American Journal of Primatology 58, 57-69"Abnormal behavior was unrelated to the subject's housing location (biocontainment vs. otherfacility) or invasiveness of research. Nursery-reared subjects displayed more abnormal behaviorthan mother-reared subjects. Across and within rearing categories, the proportion of the first 48months of life spent singly housed was positively related to the amount of abnormal behavior atmaturity. … Locomotor stereotypy, by far the most frequent form of abnormal behavior, waspositively related to time in single housing but was unrelated to rearing.”

Canadian Council on Animal Care 1984. Non-human primates. In Guide to the Care and Use ofExperimental Animals, Volume 2, 163-173. Canadian Council on Animal Care, Ottawa, ON"Any primate housed alone will probably suffer from social deprivation, the stress from whichmay distort processes, both physiological and behavioural."Chase WK, Marinus LM, Novak MA 2000. A behavioral comparison of male rhesus macaques(Macaca mulatta) in four different housing conditions. American Journal of Primatology51(Supplement), 51 (Abstract)Animals in socially restricted housing paced significantly more, locomoted significantly less andwere more aggressive than subjects housed in groups.Coelho AM, Carey KD, Shade RE 1991. Assessing the effects of social environment on bloodpressure and heart rates of baboon. American Journal of Primatology 23, 257-267In the social companion condition, a subject was able to have visual, tactile, and auditoryinteractions with his companion through the wire mesh walls of the specially designed cages."When animals were housed with social companions their blood pressures were consistentlylower than when they were either housed individually or with social strangers. ... Measurementsof cardiovascular physiology obtained under social housing may more closely model normalphysiology than ... individual housing."de Waal FBM 1991. The social nature of primates. In Through the Looking Glass. Issues ofPsychological Well-being in Captive Nonhuman Primates Novak MA, Petto AJ (eds), 67-77.American Psychological Association, Washington, DC"Physiological, immunological, and neurological measures collected on isolation-reared (andhence psychologically deviant) nonhuman primates might not be representative, and thereforemight be suboptimal for the development of models applied to the human species. Social housingwould avoid that possibility. ... Social deprivation should not be considered any more normalthan, say, water or food deprivation."Gwinn LA 1996. A method for using a pole housing apparatus to establish compatible pairsamong squirrel monkeys. Contemporary Topics in Laboratory Animal Science 35(4), 61"During nine treatments with an identical test compound, singly housed animals lostsignificantly more weight on average than did pair housed animals."Jorgensen MJ, Kinsey JH, Novak MA 1998. Risk factors for self-injurious behavior in captiverhesus monkeys (Macaca mulatta). American Journal of Primatology 45, 187"Research has shown that approximately 10% of captive, individually housed monkeys have hadsome veterinary record of self-injurious behavior within their life-time." The incidence of selfbitingwas 14% [!] in a test colony of 188 male individually housed rhesus macaques. Self-bitinganimals had spent more time - starting at an earlier age - in single-cages than controls.Lilly AA, Mehlman PT, Higley J 1999. Trait-like immunological and hematological measures infemale rhesus across varied environmental conditions. American Journal of Primatology 48, 197-223"Single housing can produce significant, long-term features of immunosuppression. ... Longperiods of single caging produced significant increases in plasma prolactin concentrations,indicative of stress-induced anxiety. ... The observation that NE [norepinephrine] wassignificantly decreased during the latter portions of Single Cage Housing may be further,tentative physiological evidence for the occurrence of depression in these animals. .... As single10

11caging continued, an increasing percentage of the animals showed withdrawal and depressionas witnessed by crouching, huddling, and overall inactivity, clearly indicative of an 'inactive' or'despair' phase commonly described."Line SW, Shively CA, Heise ER, Rabin BS, Cohen S 1993. Influence of single caging oncellular immune function in female cynomolgus macaques (Macaca fascicularis). AmericanJournal of Primatology 31, 328Immune responses are affected by housing condition. "These findings suggest that single cagingmodulates several aspects of cellular immune function in female cynomolgus monkeys."Luck CP, Keeble SA 1967. African Monkeys. In The UFAW Handbook on the Care andManagement of Laboratory Animals Third Edition Universities Federation for Animal Welfare(ed), 734-742. Churchill Livingstone, London, UK"If housed in a small cage by itself the vervet may become listless and apathic, although it willsurvive."Lutz C, Well A, Novak M 2003. Stereotypic and self-injurious behavior in rhesus macaques: Asurvey and retrospective analysis of environment and early experience. American Journal ofPrimatology 60, 1-15“Behavioral assessments of 362 individually housed rhesus monkeys were collected at the NewEngland Regional Primate Research Center .. and combined with colony records. Of the 362animals surveyed, 321 [sic] exhibited at least one abnormal behavior (mean: 2.3, range: 1-8).”National Research Council 1998. The Psychological Well-Being of Nonhuman PrimatesNational Academy Press, Washington, DChttp://books.nap.edu/books/0309052335/html/index.html“Social interactions are considered to be one of the most important factors influencing thepsychological well-being of most nonhuman primates. ... The common practice of housing rhesusmonkeys singly calls for special attention. ... Although the causes of self-directed biting arepoorly understood, prolonged individual housing is probably an influential contributing factor.”Novak MA, Kinsey JH, Jorgensen MJ, Hazen TJ 1998. Effects of puzzle feeders on pathologicalbehavior in individually housed rhesus monkeys. American Journal of Primatology 46, 213-227"Self-injurious behavior (SIB) occurs in about 10% of individually housed monkeys. Monkeyswith SIB bite their own bodies frequently, occasionally inflicting wounds as a result. ... Of greatconcern is the development of a severe form of abnormal behavior in which a small [sic]percentage of monkeys (about 5-12%) engage in self-inflicted wounding.Novak MA 2003. Self-injurious behavior in rhesus monkeys: New insights into its etiology,physiology, and treatment. American Journal of Primatology 59, 3-19“In our study population, 14% of individually housed monkeys (the vast majority of which aremales) have a veterinary record for self-inflicted wounding. Wounding is rare, but self-directedbiting is common. SIB can be elicited during aggressive altercations and may be associated withhusbandry events. Some monkeys appear to be more vulnerable to acquiring SIB. This increasedvulnerability is associated with certain social experiences in the first 2 years of life and withexposure to a larger number of moderately stressful events as compared to controls.”

12Platt DM, Kinsey JH, Jorgenson MJ, Novak MA 1996. Factors affecting the expression of selfinjuriousbehavior in rhesus monkeys (Macaca mulatta). XVIth Congress of the InternationalPrimatological Society/XIXth Conference of the American Society of Primatologists, AbstractNo. 768"Approximately 10% of laboratory housed rhesus monkeys spontaneously develop self-injuriousbehavior (SIB) such as biting their own bodies with sufficient force to produce tissue damage. ...Monkeys with SIB tended to spend a somewhat greater proportion of their lives in individualcages than controls."Rosenberg DP, Kesel ML 1994. Old-World monkeys. In The Experimental Animal in BiomedicalResearch. Volume II Rollin BE, Kesel ML (eds), 457-483. CPR Press, Boca Raton, FL"Single or individual caging systems are the basic or staple housing used for primates. ... Almostall 'hard' scientific data .. have been acquired from singly caged primates."Russell C, Russell WMS 1985. Conflict activities in monkeys. Social Biology and HumanAffairs 50, 26-48Isolated monkeys redirect violence against themselves. They "pinch the same patch of their ownskin repeatedly until it is raw or even bite and tear themselves."Schapiro SJ, Nehete PN, Perlman JE, Sastry KJ 2000. A comparison of cell-mediated immuneresponses in rhesus macaques housed singly, in pairs, or in groups . Applied Animal BehaviourScience 68, 67-84“Since rhesus monkeys live socially in nature, and the immune responses of singly housedanimals differed from those housed socially, there is considerable .. justification for suggestingthat the use of singly housed rhesus macaques may complicate interpretations of normalimmunological responses.”Shively CA, Clarkson TB, Kaplan JR 1989. Social deprivation and coronary arteryatherosclerosis in female cynomolgus monkeys. Atherosclerosis 77, 69-76"We conclude that these findings indicate that single cage housing promotes coronary arteryatherogenesis in these monkeys."Sokol KA 1993. Commentary: Thinking like a monkey - "primatomorphizing" an environmentalenrichment program. Lab Animal 22(5), 40-45"Solitary confinement is a severe punishment even for monkeys."Stoinski TS, Czekala N, Lukas KE, Maple TL 2002. Urinary androgen and corticoid levels incaptive, male Western lowland gorillas (Gorilla g. gorilla): Age- and social group-relateddifferences. American Journal of Primatology 56, 73-87"Animals housed socially .. had similar corticoid levels, whereas solitary males showed greatercorticoid levels than their socially-housed counterparts. The increased levels of corticoids insolitary-housed males suggest this management strategy might not be optimal.“Tiefenbacher S, Fahey MA, Rowlett JK, Meyer JS, Pouliot AL, Jones BM, Novak MA 2005.The efficacy of diazepam treatment for the management of acute wounding episodes in captiverhesus macaques. Comparative Medicine 55, 387-392”This study examined the effects of diazepam (Valium) on self-wounding and other abnormalbehaviors in eight individually housed male rhesus monkeys (Macaca mulatta). Each monkey'sresponse to an anxiolytic dose of diazepam (1 mg/kg or greater orally) was compared with theanimal's behavior during drug-free periods. When examined across all animals, treatment with

13diazepam did not significantly alter wounding frequency or rates of self-directed biting withoutwounding. However, closer examination of the data revealed that four of the animals showedsignificant decreases in self-biting and wounding frequency (positive responders, PR group),whereas the remaining monkeys showed a trend towards increased wounding frequency(negative responders, NR group). Subsequent examination of colony and veterinary recordsdemonstrated that compared with NR monkeys, PR monkeys had spent significantly more yearsin individual cage housing and had experienced a greater number of minor veterinaryprocedures."Yaroshevsky F 1975. Self-mutilation in Soviet prisons. Canadian Psychiatric Association J 20,443-446“Isolation “'cages' are so terrible that many prisoners prefer to maim themselves rather thanstay there."(6) Premature WeaningGoosen C 1988. Influence of age of weaning on the behaviour of rhesus monkeys. Primate Eye34, 16-17"The rather early age of weaning of infants as practised in the course of the breeding procedurewas an important factor in the induction of stereotyped locomotion and of self-directed infantilebehaviour. Both these classes of abnormal behaviour persist into adulthood."Reinhardt V 2002. Artificial weaning of Old World monkeys: Benefits and costs. Journal ofApplied Animal Welfare Science 5, 149-154http://www.awionline.org/Lab_animals/biblio/jaaws6.html”The perceived benefits of permanent, pre-weaning mother-infant separation are not supportedby scientific findings. ... As long as there is an excessive number of monkeys and insufficient cagespace, there is no ethically legitimate reason for attempting to enhance the animals’reproductive output, especially when such measures are not proven to be effective but causeunequivocal psychological distress. ... It is conceivable that maternal-infant separation for thepurpose of artificial weaning flaws primate husbandry to the extent of increasing - rather thandecreasing - the total number of monkeys needed for research. Thus, artificial weaning is notonly an avoidable source of distress but it may also be an economically unsound managementpractice.“Warniment A, Brent L 1997. Abnormal behavior in a captive chimpanzee colony. The Newsletter8(3), 1-3http://www.animalwelfare.com/Lab_animals/biblio/jo-9.htm"The purpose of this study was to link abnormal behaviors often expressed by chimpanzees livingin captive environments to factors related to their care and housing." Individuals who had spentmore time with their mothers had less abnormal behavior.

14(7) Enforced RestraintAdams MR, Kaplan JR, Manuck SB, Uberseder B, Larkin KT 1988. Persistent sympatheticnervous system arousal associated with tethering in cynomolgus macaques. Laboratory AnimalScience 38, 279-282"Persistent elevation in heart rate associated with tethering appears to be the result of apersistent influence of the sympathetic nervous system on cardiac function. ... Other organs andsystems, e.g., pituitary-gonadal system, also may be affected."Albrecht ED, Nightingale MS, Townsley JD 1978. Stress-induced decrease in the serumconcentration of progesterone in the pregnant baboon. Journal of Endocrinology 77, 425-426Ketamine infusion did not prevent the reduction in the concentration of progesterone resultingfrom enforced restraint for blood collection.Berendt R, Williams TD 1971. The effect of restraint and position upon selected respiratoryparameters of two species of Macaca. Laboratory Animal Science 21, 502-509"Restraint significantly affected the tidal volume and respiration rate."Bouyer JJ, Dedet L, Debray O, Rougenl A 1978. Restraint in primate chair may cause unusualbehavior in baboons: Electrocorticographic correlates and corrective effects of diazepam.Electroencephalic Clinical Neurophysiology 44, 562-567"The prolonged drowsy-like ECoG [electrocorticogram] and behaviour may therefore underlinea reaction to the 'stress' conditions brought on by restraint" in primate chair.Brockway BP, Hassler CR, Hicks N 1993. Minimizing stress during physiological monitoring.In Refinement and Reduction in Animal Testing Niemi SM, Willson JE (eds), 56-69. ScientistsCenter for Animal Welfare, Greenbelt, MD"Restraint itself affects the physiological functioning of the animal, measurement error andvariability are introduced into the data."Bush M, Custer R, Smeller J, Bush LM 1977. Physiologic measures of nonhuman primatesduring physical restraint and chemical immobilization. Journal of the American VeterinaryMedical Association 171, 866-869"Of 56 physically restrained primates, 30 (54%) experienced severe metabolic acidosis. .. Theanimals had more rapid respiration and pulse rates, higher rectal temperatures, and larger basedeficit."

Cope FW, Polis BD 1959. Increased plasma glutamic-oxalacetic transaminase activity inmonkeys due to nonspecific stress effect. Journal of Aviation Medicine 30, 90-94"There can be a rise in SGO-T [serum glutamic-oxalacetic transaminase] in monkeys due tononspecific stress such a fright, handling or clinical procedures."Crockett CM, Bowers CL, Sackett GP, Bowden DM 1993. Urinary cortisol responses oflongtailed macaques to five cage sizes, tethering, sedation, and room change. American Journalof Primatology 30, 55-74“Cortisol levels remained ... elevated 2-4 weeks after catheterization. After the catheters wereremoved, the cortisol levels dropped rapidly although they remained slightly elevated throughthe recovery phase."Ferin M, Carmel PW, Warren MP, Himsworth RL, Frantz AG 1976. Phencyclidine sedation as atechnique for handling rhesus monkeys: Effects on LH, GH, and prolactin secretion. Proceedingsof the Society for Experimental Biology and Medicine 151, 428-433"These [restraint] monkeys, however, are readily alarmed, and it may be difficult to obtainstable control levels for hormones which are easily influenced by stress."Fuller. G. B., Hobson WC, Reyes FI, Winter JSD, Faiman C 1984. Influence of restraint andketamine anesthesia on adrenal steroids, progesterone, and gonadotropins in rhesus monkeys.Proceedings of the Society for Experimental Biology and Medicine 175, 487-490"Determination of basal circulating hormone levels in nonhuman primates presents a problemsince handling or restraint of the animal for venipuncture may introduce sufficient stress tochange hormonal secretion. .. Each bleeding was made in conscious [female] monkeys afterrestraining the animal for 2 to 4 min with the squeeze mechanism of the [home] cage. The armwas manipulated through an opening in the cage mesh and the blood sample taken." Serumcortisol concentrations and adrenal androgens significantly increased from the initial bleedingto the second bleeding after 30 minutes. "Ketamine does not modify the stress-induced increaseof either cortisol or adrenal androgens."Gauquelin-Koch G, Blanquie J-P, Florence G, Milhaud C, Gharib C 1996. Hormonal response torestraint in rhesus monkeys. Journal of Medical Primatology 25, 387-396"These experiments indicate clearly that placement in a restraining chair represents a stimulusof different systems in monkeys. The responses observed in the present study are predominantlypsychoendocrine responses to unconditioned emotional stimuli associated with the chairrestraintsituation, despite the fact that they were acclimated to this system."Golub MS, Anderson JH 1986. Adaptation of pregnant rhesus monkeys to short-term chairrestraint. Laboratory Animal Science 36, 507-511"Heart rate and blood pressure values recorded immediately after the blood sampling [inrestraint chair] did not decline with repetition of this procedure."Goncharov NP, Taranov AG, Antonichev A, Gorlushkin V, Aso T, Ckan S, Diczfalusy E 1979.Effects of stress on the profile of plasma steroids in baboons (Papio hamadyas). ActaEndocrinologica 90, 372-384Restraint stress affects testosterone, progesterone, and oestradiol.15

16Goosen DJ, Davies JH, Maree M, Dormehl IC 1984. The influence of physical and chemicalrestraint on the physiology of the chacma baboon (Papio ursinus). Journal of MedicalPrimatology 13, 339-351Restraint leads to leukocytosis.Hayashi KT, Moberg GP 1987. Influence of acute stress and the adrenal axis on regulation of LHand testosterone in the male rhesus monkey (Macaca mulatta). American Journal of Primatology12, 263-273"Acute restraint stress appears to cause the transient stimulation of LH release. ... While thestress-stimulated release of corticosteroids failed to affect the LH response to GnRHadministration, it did act directly on the testes to prevent the normal release of testosterone."Ives M, Dack GM 1956. "Alarm reaction" and normal blood picture in Macaca mulatta. Journalof Laboratory Clinical Medicine 47, 723-729Authors observed an elevated White Blood Cell Count as "alarm reaction" to physical restraint.Kaplan JR, Adam MR, Bumsted P 1983. Heart rate changes associated with tethering ofcynomolgus monkeys. Laboratory Animal Science 38, 493 (Abstract)"The results suggest that some amount of cardiovascular (and perhaps hormonal) disturbancemay persist in tethered animals, even if several weeks are allowed for 'habituation'."Landi MS, Kissinger JT, Campbell SA, Kenney CA, Jenkins EL 1990. The effects of four typesof restraint on serum alanine aminotransferase and asparate aminotransferase in the Macacafascicularis. Journal of the American College of Toxicology 9, 517-523"All methods of restraint resulted in elevation in AST and ALT over time."Line SW, Markowitz H, Morgan KN, Strong S 1991. Effect of cage size and environmentalenrichment on behavioral and physiological responses of rhesus macaques to the stress of dailyevents. In Through the Looking Glass Novak MA, Petto AJ (eds), 160-179. AmericanPsychological Association, Washington, DC"Restraint with the cage-squeeze mechanism and confinement in a transfer box were bothassociated with significant increases in plasma cortisol. ... Repeated exposure to brief restraintdid not lead to habituation of the heart-rate response."Loomis MR, Henrickson RV, Anderson JH 1980. Effects of ketamine hydrochloride on thehemogram of rhesus monkeys (Macaca mulatta). Laboratory Animal Science 30, 851-853"Restraining a monkey in its cage represents a stressful situation which may result in aphysiological leukocytosis and hemoconcentration in the sample collected."Manning PJ, Lehner NDM, Feldner MA, Bullock BC 1969. Selected hematologic, serumchemical, and arterial blood gas characteristics of squirrel monkeys (Saimiri sciureus).Laboratory Animal Care 19, 831-837Catching and restraint procedures resulted in respiratory alkalosis and metabolic acidosis.Sedation reduced, but did not eliminate this stress response.Mason JW 1972. Corticosteroid response to chair restraint in the monkey. American Journal ofPhysiology 222, 1291-1294"These experiments indicate clearly that placement in the restraining chair represents a potentstimulus to the pituitary-adrenal cortical system."

17Mason JW, Mougey EH 1972. Thyroid (plasma BEI) response to chair restraint in the monkey.Psychosomatic Medicine 34, 441-448"Study of 14 of these monkeys throughout a longer period of 8 weeks of chair restraint indicatedthat ... mean BEI levels remained significantly elevated through the third week. ... Acuteemotional arousal [enforced restraint] elicits stimulation of the pituitary-thyroid system in therhesus monkey."Mason JW, Wool MS, Wherry FE, Pennington LL, Brady JV, Beer B 1968. Plasma growthhormone response to avoidance in the monkey. Psychosomatic Medicine 30, 760-773The “psychological response to the venipuncture procedure ['forcibly restrained on rubbermattress in order to perform venipuncture'] may be a major determinant of 'baseline' variabilityin growth hormone levels. The liability of this system appears to be such that venipunctureeffects may occur within the period of a few minutes required for a single venipuncture."McNamee GA, Wannemacher RW, Dinterman RE, Rozmiarek H, Montrey RD 1984. A surgicalprocedure and tethering system for chronic blood sampling, infusion, and temperaturemonitoring in caged nonhuman primates. Laboratory Animal Science 34, 303-307"The stress of chairing the monkeys may result in a significant decrease in hemoglobin,hematocrit, and lymphocyte concentration with an accompanying neutrophilia. In addition,chair-restrained monkeys tend to develop lower leg edema and decubital ulcers on long-termstudies."Morrow-Tesch JL, McGlone JJ, Norman RL 1993. Consequences of restraint stress on naturalkiller cell activity, behavior, and hormone levels in rhesus macaques (Macaca mulatta).Psychoendocrinology 18, 383-395Animals were chair restrained and samples taken after 1, 2 and 3 hours. "WBC and thepercentage of neutrophils increased during the restraint period, while the percent lymphocytesand monocytes decreased. NK [natural killer cell] activity also decreased over time afterrestraint whereas plasma cortisol and ß-endorphin levels increased significantly."Morton WR, Knitter GH, Smith PM, Susor TG, Schmit K 1987. Alternatives to chronic restraintof nonhuman primates. Journal of the American Veterinary Medical Association 191, 1282-1286"Despite attention to details of conditioning and daily assessments of the animals' health status,chronic chair restraint is accompanied by inherent problems such as skin abrasions, necrosis ofthe ischial callosities, position-dependent edema, inguinal hernia, rectal prolapse, and laryngealair sacculitis."Myers BA, Mendoza SP, Cornelius CE 1988. Elevation of plasma glucagon levels in response tostress in squirrel monkeys: Comparison of two subspecies (Saimiri sciureus boliviensis andSaimiri sciureus sciureus). Journal of Medical Primatology 17, 205-214Enforced restraint leads to an elevation of plasma glucagon levels.Nakamura RK, Coates R, Crawford H, Friedman D 1982. A flexible restraint chair for thecynomolgus monkey (Macaca fascicularis). Journal of Medical Primatology 11, 178-185"There is a general consensus that restraint chairs should be used only where necessary, sincethey inherently cause monkeys physical and emotional stress." Authors found "that the animalsshowed restless sleeping patterns which persisted despite our attempts to adapt the animals tothe chairs slowly. It was soon evident that the restlessness resulted from the rapid developmentof chafing ta the neck, a breakdown of tissue in the ischial pads, and lesions at the base of thetail."

Norman RL, McGlone J, Smith CJ 1994. Restraint inhibits luteinizing hormone secretion in thefollicular phase of the menstrual cycle in rhesus macaques. Biology of Reproduction 50, 16-26Chair restraint affects LH and ACTH in rhesus macaques.Norman RL, Smith CJ 1992. Restraint inhibits luteinizing hormone and testosterone secretion inintact male rhesus macaques: Effects of concurrent naloxone administration.Neuroendocrinology 55, 405-415Enforced restraint inhibits luteinizing hormone and testosterone secretion.Puri CP, Puri V, Anand-Kumar TC 1981. Serum levels of testosterone, cortisol, prolactin andbioactive luteinizing hormone in adult male rhesus monkeys following cage-restraint oranaesthetizing with ketamine hydrochloride. Acta Endocrinologica 97, 118-124Single-housed, adult male rhesus macaques were restrained in their home cages for bloodcollection at 20 minute intervals. While testosterone levels significantly declined, serum cortisolconcentrations significantly increased over a one-hour sampling period.Quadri SK, Pierson C, Spies HP 1978. Effects of centrally acting drugs on serum levels in rhesusmonkeys. Neuroendocrinology 27, 136-147Immobilization on restraint cross induced progressive increase in prolactin concentration.Rabot S, Fisco M, Martin F, Blanquie JP, Popot F, Bensaada M, Vaissade P, Searby N, Szylit O1997. Effects of chair-restraint on gastrointestinal transit time and colonic fermentation in malerhesus monkey (Macaca mulatta). Journal of Medical Primatology 26, 190-195"Chair-restraint induced a 2.5-fold acceleration of the gastrointestinal transit time, whichpersisted throughout the 7 day postrestraint period, and an increase of the fecal dry mattercontent. "Reinhardt V, Liss C, Stevens C 1995. Restraint methods of laboratory nonhuman primates: Acritical review. Animal Welfare 4, 221-238http://www.awionline.org/Lab_animals/biblio/aw6metho.htm"Published information provides scientific evidence that traditional, involuntary restrainttechniques of research non-human primates are intrinsically a source of distress resulting fromfear."Schnell CR, Wood JM 1993. Measurement of blood pressure, heart rate, body temperature, ECGand activity by telemetry in conscious unrestrained marmosets. Proceedings of the 5th Federationof European Laboratory Animal Science Association Symposium, 107-111Restraining well habituated marmosets by hand significantly increased heart rate and bloodpressure even after the animals were returned to their home cages.Todd HE, Shideler SE, Laughlin LS, Overstreet JW, Pohl CR, Byrd W, Lasley BL 1999.Application of an enzyme immunoassay for urinary follicle-stimulating hormone to describe theeffects of an acute stressor at different stages of the menstrual cycle in female laboratorymacaques. American Journal of Primatology 48, 135-151Capture and restraint “occurring during the luteal-follicular transition not only resulted in acuteperturbations of FSH but also led to abnormalities in the subsequent menstrual cycle in 50% ofthe cases."18

Torii R, Kitagawa N, Nigi H, Ohsawa N 1993. Effects of repeated restraint stress at 30-minuteintervals during 24-hours on serum testosterone, LH and glucocorticoids levels in male Japanesemonkeys (Macaca fuscata). Experimental Animal 42, 67-73"30-min intervals sampling [using "compulsory restraint"] serum testosterone levels decreasedand glucocorticoid levels increased, respectively, immediately after the start of blood sampling."Verlangieri AJ, De Priest JC, Kapeghian JC 1985. Normal serum biochemical, hematological,and EKG parameters in anesthetized adult male Macaca fascicularis and Macaca arctoides.Laboratory Animal Science 35, 63-66Author underscores undesirable variations in serum biochemical and hematological parametersin macaques and suggests that incongruities between values presented in different reports maybe due to a variety of factors including the method of restraint during handling procedures.Wheeler MD, Schutzengel RE, Barry S, Styne DM 1990. Changes in basal and stimulatedgrowth hormone secretion in the aging rhesus monkeys: A comparison of chair restraint andtether and vest sampling. Journal of Clinical Endocrinology and Metabolism 71, 1501-1507Animals who "were adapted to chair restraint" appeared calm, but they showed consistentlyhigher cortisol levels than "free moving" tethered animals.Yasuda M, Wolff J, Howard CF 1988. Effects of physical and chemical restraint on intravenousglucose tolerance test in crested black macaques (Macaca nigra). American Journal ofPrimatology 15, 171-180Restrained monkeys "appeared relaxed, but glucose clearance and insulin secretion wereimpaired" and cortisol values increased.(8) Queue Effect, Sequential TreatmentFox MW 1986. Laboratory Animal Husbandry: Ethology, Welfare and Experimental Variables.State University of New York Press, Albany, NY“The 'queue' effect of treating animals sequentially is an often overlooked experimentalvariable."Flow BL, Jaques JT 1997. Effect of room arrangement and blood sample collection sequence onserum thyroid hormone and cortisol concentrations in cynomolgus macaques (Macacafascicularis). Contemporary Topics in Laboratory Animal Science 36(1), 65-68Sequence of blood collection [as determined by room arrangement] affected serum cortisol andthyroxine levels.(9) Unfamiliar EnvironmentCrockett CM, Bowers CL, Shimoji M, Leu M, Bellanca RU, Bowden DM 1993. Appetite andurinary cortisol responses to different cage sizes in female pigtailed macaques. American Journalof Primatology 31, 305"Appetite during the first three days in the new room was moderately suppressed."19

20Crockett CM, Bowers CL, Shimoji M, Leu M, Bowden DM, Sackett GP 1995. Behavioralresponses of longtailed macaques to different cage sizes and common laboratory experiences.Journal of Comparative Psychology 109, 368-383Monkeys who were moved to a new room and to a lesser extent to a new, clean cage showed"disrupted sleep the 1st night and suppressed activity, especially self-grooming, the next day."Davenport MD, Lutz CK, Tiefenbacher S, Novak MA, Meyer JS 2007. A rhesus monkey modelof self-injury: Effects of relocation stress on behavior and neuroendocrine function. BiologicalPsychiatry, in press"Twenty adult male rhesus macaques were exposed to the stress of relocation to a new housingarrangement in a newly constructed facility. .. Our results indicate that relocation is asignificant stressor for rhesus macaques and that this stressor triggers an increase in self-bitingbehavior as well as sleep disturbance in monkeys previously identified as suffering from SIB."Herndon JG, Turner JJ, Perachio AA, Blank MS, Collins DC 1984. Endocrine changes inducedby venipuncture in rhesus monkeys. Physiology and Behavior 32, 673-676Blood collection in a transport box resulted in elevated GH and cortisol values. "The presentdata suggest that such responses may complicate interpretation of GH and cortisolmeasurements derived from samples collected by venipuncture."Lindburg DG, Coe J 1995. Ark design update: Primate needs and requirements. In Conservationof Endangered Species in Captivity Gibbons E, Durrant B, Demarest A (eds), 553-570. SUNYPress, Albany"Wherever possible, every effort should be made to design in ways that bring the treatment to theanimal, instead of the reverse. Removal for any purpose exposes the animal to overly novel,frequently noxious, and always stressful, stimuli."Line SW, Clarke AS, Markowitz H 1987. Plasma cortisol of female rhesus monkeys in responseto acute restraint. Laboratory Primate Newsletter 26(4), 1-3http://www.brown.edu/Research/Primate/lpn26-4.html#line"Confinement in a transfer box was a significant event, as measured by cortisol response, eventhough this condition was presumably intrinsically less stressful than manual restraint. .. Noveltyalone can be a significant source of stress for laboratory primates.”Line SW, Morgan KN, Markowitz H, Strong S 1989. Heart rate and activity of rhesus monkeysin response to routine events. Laboratory Primate Newsletter 28(2), 9-12http://www.brown.edu/Research/Primate/lpn28-2.html#lineAdult female rhesus macaques responded with a significant, protracted increase in heart rate tobeing placed in transfer boxes while their dirty cages were replaced with clean ones. "The meanheart rate remained elevated for two hours after completion of the procedure.... Theseobservations are important to note if one is to avoid confounding the physiological andbehavioral effects of experimental manipulations with those induced by routine husbandry."Line SW, Markowitz H, Morgan KN, Strong S 1991. Effect of cage size and environmentalenrichment on behavioral and physiological responses of rhesus macaques to the stress of dailyevents. In Through the Looking Glass Novak MA, Petto AJ (eds), 160-179. AmericanPsychological Association, Washington, DC

21Adult, single-housed female rhesus macaques responded with a significant rise in heart rate tobeing removed from their home cage and replaced after the cage had been cleaned. "Once thecage change was completed and the technicians left the room, it was several hours before heartrates returned to the expected level."Mason JW 1972. Corticosteroid response to chair restraint in the monkey. American Journal ofPhysiology 222, 1291-1294Animals who were restrained in an unfamiliar environment showed significantly higher urinarycortisol levels than animals who were familiar with the environment in which they wererestrained.Mason JW, Mougey EH, Kenion CC 1973. Urinary epinephrine and norepinephrine responses tochair restraint in the monkey. Physiology and Behaviour 10, 801-803Animals who were restrained in an unfamiliar environment showed significantly higher urinarycatecholamine levels than animals who were familiar with the environment in which they wererestrained.Mitchell G, Gomber J 1976. Moving laboratory rhesus monkeys (Macaca mulatta) to unfamiliarhome cages. Primates 17, 543-547"The results of this study should serve as a warning to those who wish to observe behavior ortake physiological measurements on monkeys. Removing an animal from its home cage prior tomonitoring anything biological will probably affect the event being monitored. Behavioral andalmost certainly physiological distress occur following removal from the home cage."Phoenix CH, Chambers KC 1984. Sexual behavior and serum hormone levels in aging rhesusmales: Effects of environmental change. Hormones and Behavior 18, 206-215"Cortisol levels [of single-housed subjects] were significantly higher immediately [one hour]after the move [to another cage in a nearby building] than they were on the first day of bleedingbefore the move."Reinhardt V, Cowley D, Eisele S, Scheffler J 1991. Avoiding undue cortisol responses tovenipuncture in adult male rhesus macaques. Animal Technology 42, 83-86http://www.awionline.org/Lab_animals/biblio/at83.htmSix adult rhesus males were: a) habituated to actively cooperate during venipuncture away fromthe homecage in a treatment squeeze cage, and b) trained to actively cooperate duringvenipuncture in the homecage. The magnitude of cortisol increase was significant when themales were venipunctured in the hallways but not when they were venipunctured in thehomecage. "It was concluded that venipuncture per se was not a physiologically distressingevent. It became distressing only when it was associated with a temporary removal from thehomecage."Schapiro SJ, Nehete PN, Perlman JE, Sastry KJ 1997. A change in housing condition leads torelatively long-term changes in cell-mediated immune responses in adult rhesus macaques.American Journal of Primatology 42, 146"A change in housing condition results in changes in immune responses, even after subjects hadspent up to eight months in the new housing and regardless of whether the change was tosolitary or pair housing."

22(10) Double-tier Cage ArrangementBaskerville M 1999. Old World Monkeys. In The UFAW [Universities Federation for AnimalWelfare] Handbook on the Care and Management of Laboratory Animals Seventh Edition PooleT, English P (eds), 611-635. Blackwell Science, Oxford, UK"Captive primates like to move upwards and look down on unfamiliar humans, and ideally thecage height should allow this. Two tier caging should be avoided.”Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 9.5. Multi-Tier Caging. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/variables.html#multi-tier

23"In a quantitative study I did on 20 pair-housed cynos, the animals spent 94 percent of theirwaking time in the upper part of the vertically arranged double cage. All food was given in thebottom section, yet the animals would bring the food to the upper part and consume it there. Themonkeys preference along the gradient of height was unequivocal!I observed squirrel monkeys in vertically arranged double cages and also found that theanimals clearly preferred the upper half of their cages. The only time they went to the bottomhalf was when they retrieved a toy or picked through the bedding for treats.When visiting facilities that have their pair-housed macaques kept in vertically arrangeddouble-cages, I repeatedly got the impression that subordinate partners are disadvantaged inthis caging system, with dominant animals preventing subordinates from spending as much timein the upper section as they would like to."Box HO, Rohrhuber B 1993. Differences in behaviour among adult male, female pairs of cottontoptamarins in different conditions of housing. Animal Technology 44, 19-30http://www.awionline.org/Lab_animals/biblio/at-box.htmAnimals living in upper-row cages were more active and engaged in more close contactamicable behavior than animals living in lower-row cages.Clough G 1982. Environmental effects on animals used in biomedical research. BiologicalReviews 57, 487-523"The intensity of light in animal cages is likely to be the most variable environmental factor inthe average animal room."European Commission 2002. The Welfare of Non-human Primates - Report of the ScientificCommitte on Animal Health and Animal Welfare. European Commission, Strasbourg, Francehttp://europa.eu.int/comm/food/fs/sc/scah/out83_en.pdf“Primates should not be placed in double-tiered caging unless the arrangement permitsadequate vertical movement for the animal."Heger W, Merker H-J, Neubert D 1986. Low light intensity decreases the fertility of Callithrixjacchus. Primate Report 14, 260http://www.awionline.org/Lab_animals/biblio/pr14-2.htm"Improvement of the light fixtures in both rooms doubled the lighting force and increased thebreeding rate during the following 12 months approximately 20% in the upper and 130% in thelower cages."European Commission 2002. The Welfare of Non-human Primates - Report of the ScientificCommittee on Animal Health and Animal Welfare. European Commission, Strasbourg, France“Primates should not be placed in double-tiered caging unless the arrangement permitsadequate vertical movement for the animal."Mahoney CJ 1992. Some thoughts on psychological enrichment. Lab Animal 21(5), 27,29,32-37"The sanitation tray, which runs the length of the room beneath the upper tier of cages, reducessignificantly the amount of light from ceiling-mounted fixtures that can penetrate to the lowercage tier; animals in the lower tier are thus relegated to a permanent state of semi-gloom."Mulder JB 1976. Behavior patterns of laboratory animals. Lab Animal 5(5), 22-28"Placing of the cage on a rack even further reduces the available light. During experimentation,care must be exercised to use cages of the ... same placement to avoid variations in lighting. Ifthis is not done, the investigator may be measuring behavioral rather than experimental results."

National Research Council 1998. The Psychological Well-Being of Nonhuman PrimatesNational Academy Press, Washington, DChttp://books.nap.edu/books/0309052335/html/index.html“Wild marmosets and tamarins only occasionally descent to the ground and in captivity prefer tobe above caregiving personnel. Therefore, it is advisable not to house these primates in two-tiercages. ... Under natural conditions, many primates spend much of their lives aboveground andescape upward to avoid terrestrial threats. Therefore, these animals might perceive the presenceof humans above them as particularly threatening. ... Even macaques, which some describe assemiterrestrial, spend most of the day in elevated locations and seek the refuge of trees at night.”Reinhardt V 1989. Evaluation of the long-term effectiveness of two environmental enrichmentobjects for singly caged rhesus macaques. Lab Animal 18(6), 31-33http://www.awionline.org/Lab_animals/biblio/la-eval.htm"The proportion of time spent with the pipes was three times greater for animals living in lowerrowcages than for animals living in upper-row cages. ... In the elevated position, the lightexposure was increased, a fact that made the pipes of particular value for the lower-row cagesanimals."Reinhardt V, Reinhardt A 1999. The monkey cave: The dark lower-row cage. LaboratoryPrimate Newsletter 38(3), 8-9http://www.brown.edu/Research/Primate/lpn38-3.html#cave"The typical lower-row cage provides a cave-like housing environment which may impair wellbeing,invalidate research data, and undermine good housekeeping."Reinhardt V, Reinhardt A 2000. The lower row monkey cage: An overlooked variable inbiomedical research. Journal of Applied Animal Welfare Science 3, 141-149http://www.awionline.org/Lab_animals/biblio/jaaws1.htm"A survey of 96 primatological articles revealed that cage location of research monkeys isusually not mentioned (98%), in spite of the fact that the environment of upper- and lower-rowhoused animals markedly differs in terms of light quality, light intensity and living dimension.Not accounting for these uncontrolled variables may increase variability of data and,consequently, the number of experimental animals needed to obtain statistically acceptableresults."Ross PW, Everitt JI 1988. A nylon ball device for primate environmental enrichment. LaboratoryAnimal Science 38(4), 481-483"We feel that macaques fare better when they are housed in cages on the upper tier or racks.This may relate to better interactions with the animal care technicians when they are housed inthis position."Schapiro SJ, Stavisky R, Hook M 2000. The lower-row cage may be dark, but behaviour doesnot appear to be affected. Laboratory Primate Newsletter 39(1), 4-6http://www.brown.edu/Research/Primate/lpn39-1.html#darkThe situation of 3 upper-row single-caged females was compared with that of 6 lower-rowsingle-caged females under undisturbed conditions... Mean light levels at nine different positionswithin the cage were significantly lower in bottom-row cages than in upper-row cages. "Lessthan 8% of light readings in lower-row cages were higher than the lowest light level readings atthe same position in the upper-row cages. .... There were no statistically significant differences24

25in behavior.” The mean percent time spent in abnormal behavior was 0.7 for upper-row cagedsubjects versus 1.6 for lower-row caged subjects.Schapiro SJ, Bloomsmith M 2001. Lower-row caging in a two-tiered housing system does notaffect the behaviour of young, singly housed rhesus macaques. Animal Welfare 10, 387-394"Although lower-row cages are significantly darker than upper-row cages at our facility, thedata from the present study demonstrate that the diminished lighting and other supposeddisadvantages experienced by lower-row-housed monkeys have few behavioural consequences"[under undisturbed conditions].Seier JV, Loza J, Benjamin L 2004. Housing and stereotyped behaviour: Some observationsfrom an indoor colony of vervet monkeys (Chlorocebus aethiops). Folia Primatologica75(Supplement 1), 332 (Abstract)”Both sexes housed in the upper rows spent less time engaging in stereotyped behaviour.”Shimoji M, Bowers CL, Crockett CM 1993. Initial response to introduction of a PVC perch bysingly caged Macaca fascicularis. Laboratory Primate Newsletter 32(4), 8-11http://www.brown.edu/Research/Primate/lpn32-4.html#pvcSingle-housed "monkeys spent significantly more time clinging to the cage wall ("suspended") inthe absence of the perch. ... Monkeys in lower level cages averaged somewhat more time on theperch than those in upper cages."Shively CA 2001. Psychological well-being of laboratory primates at Oregon Regional PrimateResearch Center. Web site link in Willamette Week, March 21, 2001http://www.wweek.com/html2/shivreport.html"We have observed lower body weights in animals housed in lower tier cages."Woodbeck T, Reinhardt V 1991. Perch use by Macaca mulatta in relation to cage location.Laboratory Primate Newsletter 30(4), 11-12http://www.brown.edu/Research/Primate/lpn30-4.html#perchSingle-housed "animals living in lower-row cages spent an average of 31.6% of the timeperching on their pipes while animals living in upper-row cages perched only 6.9% of the time.Access to the vertical dimension of the cage was more important for the lower-row cagedmonkeys who continuously live close to the ground, in the horizontal dimension of the room."(11) Neighbor EffectAureli F, Seres M, Whitten PL, de Waal FB 2001. Living conditions affect stress levels ofcaptive chimpanzees. American Journal of Primatology 54(Supplement), 67-68 (Abstract)“Stress levels in captive chimpanzees are not affected by population density per se (chimpanzeesuse behavioural coping strategies), but when coupled with high Neighbor Effect stress levelsincrease. If many groups need to live in close proximity, it is better to house chimpanzees inlarge compounds."Baker KC, Aureli F 1996. The neighbor effect: Other groups influence intragroup agonisticbehavior in captive chimpanzees. American Journal of Primatology 40, 283-291Hearing the vocalizations of neighboring groups increased the likelihood of intragroup fighting."It may be indicated to construct corrals at a distance from each other to avoid this undesirableneighbor effect."

26Coe CL 1991. Is social housing of primates always the optimal choice? In Through the LookingGlass Novak MA, Petto AJ (eds), 78-92. American Psychological Association, Washington, DC“Introduction of female subjects into the housing area had a significant effect on otherphysiological systems, including the immune systems, of these male pairs. For example, bothdominant and subordinate males showed a month-long decline in the natural killer-cell activityfollowing the psychological stimulation evoked by housing two females in cages adjacent to thecages of the male pairs."Kurth B, Bryant D 1998. Pairing female Macaca fascicularis. Laboratory Primate Newsletter37(4), 3http://www.brown.edu/Research/Primate/lpn37-4.html#kurthTwenty-nine previously single-caged adult female long-tailed macaques were paired with eachother in vertical, double-cage configuration. "Neighboring pairs were often charging each otheracross the grid panel. ... To avoid this, pairs were transferred to a horizontal configuration afterthe first month."Lipman NS 1992. Large colonies vs. small colonies. In Implementation Strategies for ResearchAnimal Well-Being: Institutional Compliance with Regulations Krulisch L (ed), 145-150.Scientist Center for Animal Welfare and WARDS, Bethesda, MD"It is important to recognize that visual contact between incompatible conspecifics can lead toproblems such as anorexia and stereotypic behavior. Therefore our caregivers and veterinarystaff pay close attention to the cage arrangement [of the single-caged animals] within eachroom".Wallis J, King BJ 1986. The effect of female proximity and social interaction on the menstrualcycle of crab-eating monkeys (Macaca fascicularis). Primates 27(1), 83-94"Close physical contact and social interaction between female crab-eating monkeys affects thereproductive cycle: females with a history of irregular and/or unusually long cycles beganexhibiting more normal cycling patterns when placed in proximity to a regularly cycling female.Irregular controls continued to show cycles that were abnormally long."(12) Observer Effect, Presence of PersonnelBoinski S, Gross TS, Davis JK 1999. Terrestrial predator alarm vocalizations are a valid monitorof stress in captive brown capuchins (Cebus apella). Zoo Biology 18, 295-312"We have most commonly ... documented TPAs [terrestrial predator alarms] being produced inassociation with the entrance into or presence of humans in colony rooms. Most predictablythose humans are research technicians associated with manipulative research projects involvingthe capuchins. ... Mean TPA production was correlated to fecal cortisol and behavioraldisorders."Bowers CL, Crockett CM, Bowden DM 1998. Differences in stress reactivity of laboratorymacaques measured by heart period and respiratory sinus arrhythmia. American Journal ofPrimatology 45, 245-261"Exposure to an unfamiliar technician with capture gloves stimulated cardiac reactivity morestrongly than an intense sound. ... Behavior responses to the glove indicated that all subjectsconsistently perceived this 'ecologically relevant' stimulus as threatening."

27Line SW, Morgan KN, Markowitz H, Strong S 1989. Heart rate and activity of rhesus monkeysin response to routine events. Laboratory Primate Newsletter 28(2), 9-12http://www.brown.edu/Research/Primate/lpn28-2.html#line“Variations in heart rate and activity are closely associated with human activity in the room."Line SW 1995. Effects of observation technique on the behavior of adult rhesus macaques.Contemporary Topics in Laboratory Animal Science 34, 61-65"During videotaped sessions, movement was higher in frequency and duration, while aggressivebehavior was lower" and stereotyped locomotion higher in frequency than during direct liveobservations.Malinow MR, Hill JD, Ochsner AJ 1974. Heart rate in caged rhesus monkeys (Macaca mulatta).Laboratory Animal Science 24, 537-540“The rapid increase of 80 beats/min recorded when someone entered the room and tapped thecages is most probably related to the action of the autonomic nervous system and may explainthe high heart rates reported in most studies of restrained or anesthetized monkeys. Thus, whenthe results of cardiovascular studies in rhesus monkeys are interpreted, the variables introducedby the sympathetic or parasympathetic nerves should be considered."Manuck SB, Kaplan JR, Clarkson TB 1983. Behavioral induced heart rate reactivity andatherosclerosis in cynomolgus monkeys. Psychosomatic Medicine 45, 95-108The presence of the experimenter [without glove!] dramatically increased heart rate in about50% of animals studied.Reinhardt V 1997. Refining the traditional housing and handling of laboratory rhesus macaquesimproves scientific methodology. Primate Report 49, 93-112http://www.awionline.org/Lab_animals/biblio/pr-refi.htm“The macho-type person is out of place in the animal room because s/he triggers stress or evendistress reactions. Typically, the animal will freak out and hide in a back corner of the cagewhen such a person comes into their room."Reinhardt V 1999. Pair-housing overcomes self-biting behavior in macaques. Laboratory PrimateNewsletter 38(1), 4http://www.brown.edu/Research/Primate/lpn38-1.html#pairSeven single-caged subjects exhibited self-biting behavior predictably in the presence ofpersonnel.Schnell CR, Wood JM 1993. Measurement of blood pressure, heart rate, body temperature, ECGand activity by telemetry in conscious unrestrained marmosets. Proceedings of the 5th Federationof European Laboratory Animal Science Association Symposium, 107-111"After event A [presence of a person], we observed a twofold increase in activity and a markedincrease in CT [temperature], MAP [blood pressure] and HR [heart rate]."Schnell CR, Wood JM 1993. Measurement of blood pressure and heart rate by telemetry inconscious, unrestrained marmosets. American Journal of Physiology 264, H1509-1516During the weekend, daytime values of heart rate and blood pressure were significantly lower,and motor activity was higher. "The higher motor activity suggests greater social interactionswhen the marmosets are undisturbed. The lower MAP [blood pressure] and HR [heart rate]suggest that the animals may be less anxious and feel better in this situation."

28Tatoyan SK, Cherkovich GM 1972. The heart rate in monkeys (Baboons and Macaques) indifferent physiological states recorded by radiotelemetry. Folia Primatologica 17, 255-266"In the presence of man the heart rate is always increased, in spite of the fact that the monkeysappear to be calm."Tinklepaugh OL 1928. The self-mutilation of a male Macacus rhesus monkey. Journal ofMammalogy 9, 293-300A drastic case of observer-induced self-biting of a male rhesus macaques is described.(13) NoiseBaldwin AL, Schwartz GE, Hopp DH 2007. Are investigators aware of environmental noise inanimal facilities and that this noise may affect experimental data? Journal of the AmericanAssociation for Laboratory Animal Science [Contemporary Topics in Laboratory AnimalScience] 46(1), 45-51”Because faculty are the least aware of noise as a potential problem but are primarilyresponsible for designing experiments, research involving animals may be confounded by noiseas an unknown variable. This effect may lead to unnecessary numbers of animals being requiredto achieve statistical significance and possibly to erroneous interpretation of results. On thebasis of the findings of this survey, we present recommendations for improving the environment,particularly for decreasing the noise level, in animal facilities.”Patterson-Kane EG, Farnworth MJ 2006. Noise exposure, music, and animals in the laboratory:A commentary based on Laboratory Animal Refinement and Enrichment Forum (LAREF)discussions. Journal of Applied Animal Welfare Science 9, 327-332"Evidence supports the use of quiet music during nonhuman animals' activity periods, if thispractice is introduced with an awareness of the risks to welfare and research."Pines MK, Kaplan G, Rogers LJ 2004. Stressors of common marmosets (Callithrix jacchus) inthe captive environment: Effects on behaviour and cortisol levels. Folia Primatologica75(Supplement), 317-318 (Abstract)Salivary cortisol samples, collected using a cotton bud with banana on the tip, doubled following30 minutes of exposure to playing radio (70-80 dB) or loud construction work (70-80 dB).Despite being sheltered from rain while outdoors, the marmosets moved indoors voluntarilywhen it was raining. ”There was no change in cortisol levels following the non-traumatic deathof a cage/room mate, however, cortisol levels doubled (and remained elevated for at least fivedays) following the accidental injury and death of a cage/room mate in the absence of any otherdisturbing event. Involvement of room-mates in non-invasive experiments was also stressful, withcortisol levels doubling. Activity levels and time spent on the floor of the cage decreases, butthere was no change in other stress-indicative behaviours. It would seem that the marmosetsmight be using a passive coping technique to deal with stressors over which they have nocontrol. The results suggest that marmosets are negatively affected by noise and any kind ofevent adversely affecting a room-mate.“

Refinement29(1) DefinitionRefinement is the attempt to enhance animal welfare and control extraneous variables thatmay increase research data variability.Russell WMS, Burch RL 1959. The Principles of Humane Experimental Technique. Methuen,Londonhttp://altweb.jhsph.edu/publications/humane_exp/het-toc.htm"Refinement means any decrease in the incidence or severity of inhumane procedures applied tothose animals which still have to be used."(2,a) Unstructured SpaceBayne K, McCully C 1989. The effect of cage size on the behavior of individually housed rhesusmonkeys. Lab Animal 18(1), 25-28A moderate increase of unstructured cage space does not affect stereotypical behaviors inindividually caged rhesus macaques.Boot R, Leussink AB, Vlug RF 1985. Influence of housing conditions on pregnancy outcome incynomolgus monkeys (Macaca fascicularis). Laboratory Animal Science 19, 42-47More successful pregnancies were recorded for females housed individually in large cages thanfor females housed in small cages.Brent L 1992. The effects of cage size and pair housing on the behavior of captive chimpanzees.American Journal of Primatology 27, 20"Environmental manipulation was higher and inactivity lower in the [furnished] large singlecage 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 DM 2000. Behavior, appetite, and urinary cortisol responsesby adult female pigtailed macaques to cage size, cage level, room change, and ketamine sedation.American Journal of Primatology 52, 63-80A moderate increase of unstructured cage space does not affect abnormal behaviors inindividually caged pig-tailed macaques.Daschbach NJ, Schein MW, Haines DE 1983. Cage-size effect on locomotor, grooming andagonistic behaviors of the slow loris (Nycticebus coucang). Applied Animal Ethology 9, 317-330"Results of the experiments in this study indicate that slow lorises kept in larger [furnished]cages will be more active than those housed in [furnished] cages approaching recommendationsfor size proposed by the U.S. National Research Council."Kitchen AM, Martin AA 1996. The effects of cage size and complexity on the behaviour ofcaptive common marmosets, Callithrix jacchus jacchus. Laboratory Animals 30, 317-326"Stereotyped behaviours, which occurred in the small [furnished] cages, were never exhibited inthe large [furnished] cages. We conclude that the welfare of captive marmosets is enhanced bythe provision of larger and more complex cages."

30Line SW, Morgan KN, Markowitz H, Strong S 1990. Increased cage size does not alter heart rateor behavior in female rhesus monkeys. American Journal of Primatology 20, 107-113A moderate increase of the dimensions of standard cages that lack any structures for climbing,perching, swinging or other activities does not affect the behavior of individually caged rhesusmacaques.Mallapur A, Waran N, Sinha A 2005. Use of enclosure space by captive lion-tailed macaques(Macaca silenus) housed in Indian zoos. Journal of Applied Animal Welfare Science 8, 175-185"Captive lion-tailed macaques used the edge zone — the space closest to the visitor areas —when their ... environments were deficient in appropriate environmental stimuli."Paulk HH, Dienske H, Ribbens LG 1977. Abnormal behavior in relation to cage size in rhesusmonkeys. Journal of Abnormal Psychology 86, 87-92"Observations were made of 24 monkeys that were introduced singly into a [barren] small and a[barren] large test cage. In a large cage .. less stereotyped locomotion was shown than in asmall cage."Williams LE, Steadman A, Kyser B 2000. Increased cage size affects Aotus time budgets andpartner distances. American Journal of Primatology 51(Supplement), 98 (Abstract)"Aotes spp. housed in typical, small, laboratory cages appear to be sedentary animals that spendlarge amounts of time sitting alone or in physical contact with social partners. ... The Aotus,housed as pairs or family groups, were moved from cages measuring 0.63m x 1.5m x 0.76m tolarger housing measuring 1.5m x 3m x 2m. Perches and nest boxes were provided in bothhousing conditions. ... Results indicate that Aotus will disperse and use the cage area provided.Changes in time budgeting are indicative of more relaxed animals, spending less time huddledwith family members or in their nest box [alone], and spending more time eating and drinking."(2,b) Structured SpacePhoto by Moshe Bushmitz

Erwin J 1977. Factors influencing aggressive behavior and risk of trauma in the pigtail macaque(Macaca nemestrina). Laboratory Animal Science 27, 541-547"Provision of cover ... reduced aggression among members of stable groups."Günther MM 1998. Influence of habitat structure on jumping behaviour in Galago moholi. FoliaPrimatologica 69(Supplement), 410 (Abstract)"These results suggest that support material [perches], as well as height, influences thebehaviour of G. maholi and these should be taken into consideration in behavioural andbiomedical studies as well as in the construction of cage facilities. Studies which do not takethese factors into account are to some extent vitiated."Maninger N, Kim JH, Ruppenthal GC 1998. The presence of visual barriers decreases agonismin group housed pigtail macaques (Macaca nemestrina). American Journal of Primatology 45,193-194“Bite, grab and chase were found to be significantly greater [among members of harem groupsof 23 pig-tailed macaques] when visual barriers were absent compared to when they werepresent."McCormack K, Megna NL 2001. The effects of privacy walls on aggression in a captive groupof rhesus macaques (Macaca mulatta). American Journal of Primatology 54(Supplement), 50-51”Preliminary results suggest that non-contact aggression (vocalizations, fear grimaces, chases,and threats) is significantly reduced after the introduction of the privacy walls (p

32Reinhardt V 1989. Evaluation of the long-term effectiveness of two environmental enrichmentobjects for singly caged rhesus macaques. Lab Animal 18(6), 31-33http://www.awionline.org/Lab_animals/biblio/la-eval.htm"While perching, the monkeys sat in front of the cage for 95% of the time, in the middle or rearof the cage for 5% of the time. The proportion of time spent with the pipes was three timesgreater for animals living in lower-row cages than for animals living in upper-row cages. In theelevated position, the light exposure was increased, a fact that made the pipes of particular valuefor the lower-row cages animals."Reinhardt V 1990. A perch for caged macaques. Humane Innovations and Alternatives inAnimal Experimentation 4, 134-135http://www.awionline.org/Lab_animals/biblio/h134.htmPerches are "particularly attractive for animals during the daily cleaning of their cages becausethey offer a dry, comfortable place to sit while the floors of their cages are sprayed with water."Ricker RB, Williams LE, Brady AG, Gibson SV, Abee CR 1995. Environmental enhancementfor laboratory-housed squirrel monkeys: Fifteen-year retrospective analysis of procedures.Contemporary Topics in Laboratory Animal Science 34(4), 55 (Abstract)”Cut pieces of PVC pipe (12 in diameter) were hung in each run as a hide box, allowing eyecontact to be broken between disputing animals. This decreased fight wounds by 60%."Shimoji M, Bowers CL, Crockett CM 1993. Initial response to introduction of a PVC perch bysingly caged Macaca fascicularis. Laboratory Primate Newsletter 32(4), 8-11http://www.brown.edu/Research/Primate/lpn32-4.html#pvcSingle-housed "monkeys spent significantly more time clinging to the cage wall ("suspended") inthe absence of the perch. ... 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-housed male cynos] primates stoppedexhibiting stereotypical and self-injurious behaviors." The two animals "were free ofstereotypical behavior for a little over two years."Westergaard GC, Izard MK, Drake JD, Suomi SJ, Higley JD 1999. Rhesus macaque (Macacamulatta) group formation and housing: Wounding and reproduction in a specific pathogen free(SPF) colony. American Journal of Primatology 49, 339-347"When forming new rhesus macaque breeding groups, divided corrals that provide for socialand visual separation of individuals lead to lower rates of traumatic wounding than do undividedcorrals."Wolff A 1989. Polyvinyl chloride piping as perch material for squirrel monkeys. LaboratoryPrimate Newsletter 28(1), 7http://www.brown.edu/Research/Primate/lpn28-1.html#pvc"An additional unexpected benefit of the PVC piping has been a decrease in dorsal tail-headabrasions, frequently seen in squirrel monkeys that sit on the stainless steel flooring of standardprimate cages."

(2,c) Playpen, Outdoor Housing, Exercise Cage33Baker KC, Ross SK 1998. Outdoor access: The behavioral benefits to chimpanzees. AmericanJournal of Primatology 45, 166 (Abstract)"When compared to the results of ameliorative environmental enrichment techniques furnishedto the indoor-housed subjects, the small outdoor groups of [two or three] chimpanzees showedbroader and more dramatic improvements in well-being." Animals with outdoor access showedsignificantly less abnormal behavior (e.g., coprophagy, regurgitation/reingestion), less yawning,and more self-grooming.Bayne K, Dexter S, Suomi S 1992. A preliminary survey of the incidence of abnormal behaviorin rhesus monkeys (Macaca mulatta) relative to housing condition. Lab Animal 21(5), 38-46“The greatest frequency of overall abnormal behavior and stereotypic exploratory behavior wasin 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-directed behavior."Brent L, Lee DR, Eichberg JW 1991. Evaluation of a chimpanzee enrichment enclosure. Journalof Medical Primatology 20, 29-34http://www.awionline.org/Lab_animals/biblio/jmp20-2.htmChimpanzees were given access to a complex new outdoor playground. "Activity andenvironmental manipulation increased while abnormal and self directed behaviors decreased."Bryant CE, Rupniak NMJ, Iversen SD 1988. Effects of different environmental enrichmentdevices on cage stereotypies and autoaggression in captive cynomolgus monkeys. Journal ofMedical Primatology 17, 257-269http://www.awionline.org/Lab_animals/biblio/jmp17-2.htm"Stereotypy and autoaggression were markedly reduced in the playpen, but reappeared on returnto the home cage."

34Clarke AS, Juno CJ, Maple TL 1982. Behavioral effects of a change in the physical environment:a pilot study of captive chimpanzees. Zoo Biology 1, 371-380A group of chimpanzees was translocated from a laboratory environment to a naturalistic manmadeisland. Stereotyped and self-directed behaviors were dramatically reduced on the island.Fontenot MB, Wilkes MN, Lynch CS 2006. Effects of outdoor housing on self-injurious andstereotypic behavior in adult male rhesus macaques (Macaca mulatta). Journal of the AmericanAssociation for Laboratory Animal Science [Contemporary Topics in Laboratory AnimalScience] 45(5), 35-43"Our findings suggest that self-biting and self-directed stereotypic behavior in rhesus macaqueswith a history of self-injurious behavior is significantly reduced by outdoor housing" incorncribs equipped with perches and toys. The outdoor housing provided a 114% increase infloor area for single-housed animals and a 364% to 837% increase in floor area for grouphousedanimals.Fried J, Whitehouse M 1992. A pre-post occupancy comparison of activity budgets and habitatutilization in a group of captive mandrills (Mandrillus sphinx). American Journal of Primatology27, 28 (Abstract)"For the group as a whole, feeding, traveling and object oriented behaviors increased, andstereotypic 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 reduced in the juvenile [group-housed] gorillain the larger and more natural environment."Honess PE, Marin C, Brown AP, Wolfensohn SE 2005. Assessment of stress in non-humanprimates: application of the neutrophil activation test. Animal Welfare 14, 291-295"All macaques were group-housed indoors in either a traditional caging system of three linkedmodules of typical reinforced stainless steel two-tier laboratory cages, or in open-roomscontaining either these cages with the fronts removed or no caging at all. ... Animals housed in atraditional caging system produced a significantly lower leukocyte response than animalshoused in open-rooms, indicating that 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 Conference Proceedings, 66 (Abstract)"Overall, after the move to the larger [structurally enriched] facility, there was an increase inactivity, a decrease in stereotypical behaviour, and an increase in threat behavior."Kessel AL, Brent L 1995. An activity cage for baboons, Part I. Contemporary Topics inLaboratory Animal Science 34(6), 74-79Single-housed "baboons provided with a large enriched activity cage [during two days eachmonth] display dramatic changes in behavior typically considered to represent positivepsychological well-being. ... The home cages and the activity cage were located in the sameroom, and provided visual, olfactory, and auditory access to other baboons."Kessel AL, Brent L 1997. Behavioural effects of transferring singly housed baboons to outdoorsocial groups. In Proceedings on the 2nd International Conference on EnvironmentalEnrichment Holst B (ed), 142-147. Copenhagen Zoo, Frederiksberg

35"Moving singly housed baboons to an enriched outdoor enclosure had significant effects on allbehaviors analyzed. Abnormal behavior, cage directed activities, and self-directed activities alldecreased in the corn cribs. Inactivity, locomotion, and normal behavior, as well as enrichmentdirected activities and social behavior all increased in the corn cribs."Leu M, Crockett CM, Bowers CL, Bowden DM 1993. Changes in activity levels of singlyhoused longtailed macaques when given the opportunity to exercise in a larger cage. AmericanJournal of Primatology 30, 327 (Abstract)"Over a period of 36 days, each [single-housed] animal had 15 min per day access to amulticompartmental [large] exercise cage." Locomotion increased while stereotypical behaviordecreased when the animals were in the exercise cage.Maple TL, Finlay TW 1987. Post-occupancy evaluation in the zoo. Applied Animal BehaviourScience 18, 5-18"We investigated the effects of translocating great apes from barren cages to innovativenaturalistic habitats. ... For both gorillas and orangutans, the new environment had the effect ofreducing the variety and frequency of aggressive interactions. ... Some behaviors, such a playbiting,were recorded for the first time in the new enclosure. Both gorillas were prone toregurgitation and re-ingestion in their former cages. However, in the naturalistic environmentsthese abnormal behaviors were never observed."Marriott BM, Marriott RW, Norris J, Lee D 1993. A semi-natural habitat for housing small,nonhuman primates. Journal of Medical Primatology 22, 348-354http://www.awionline.org/Lab_animals/biblio/jmp22-3.htmA semi-natural habitat was designed to house a group of squirrel monkeys. Animals maintainedin this environment were "healthy, and none of the animals exhibited locomotor stereotypies.”McGuffey LH, McCully CL, Bernacky BJ, Blaney SM 2002. Incorporation of an enrichmentprogram into a study protocol involving long-term restraint in macaques. Lab Animal 31(10), 37-39"In our experience, the provision of periodic intervals of unrestricted activity directly correlatedwith an increased tolerance during relatively more extended periods of [chair] restraint."O'Neill PL 1989. Short-term and long-term benefits of environmental enrichment on laboratoryrhesus monkeys (Macaca mulatta). American Zoo and Aquarium Association RegionalConference Proceedings, 616-625The animals were transferred from their barren group cage to a more spacious playroomequipped with climbing /perching structures and swings for one hour per day, five days a week:The animals showed a decline in the frequency of three [out of four] behavioral disorders in theplaypen. This therapeutic effect was nullified back in the barren homecage."Pines MK, Kaplan G, Rogers LJ 2007. A note on indoor and outdoor housing preferences ofcommon marmosets (Callithrix jacchus). Applied Animal Behaviour Science 108(3-4), 348-353"When given free access to move between their home cage and outdoors, the marmosets spent70% of their day in the outdoor cage."Seier JV, Loza J, Benjamin L 2004. Housing and stereotyped behaviour: Some observationsfrom an indoor colony of vervet monkeys (Chlorocebus aethiops). Folia Primatologica75(Supplement), 332 (Abstract)

36The animals “spent most time in stereotypies when in unenriched single cages. This wassignificantly reduced by the provision of either an exercise cage or a foraging log. Nostereotyped behaviour was observed in the largest most enriched cages.“Storey PL, Turner PV, Tremblay JL 2000. Environmental enrichment for rhesus macaques: Acost-effective exercise cage. Contemporary Topics in Laboratory Animal Science 39(1), 14-16“Increased visual attentiveness by other animals, decreased self-directed biting and hairpicking, and improved food consumption was observed when rhesus macaques were permittedaccess to an exercise cage for several hours daily."Tustin GW, Williams LE, Brady AG 1996. Rotational use of a recreational cage for theenvironmental enrichment of Japanese macaques (Macaca fuscata). Laboratory PrimateNewsletter 35(1), 5-7http://www.brown.edu/Research/Primate/lpn35-1.html#tustinThe rotational use of a “recreation cage” resulted in increased use of enrichment devices and adecrease in stereotypical behaviors.Wilkes MN, Lynch CS, Fontenot MB 2006. Outdoor housing decreases self-injurious andstereotypic behavior in adult male rhesus macaques (Macaca mulatta). American Journal ofPrimatology 68(Supplement), 106 (Abstract)Access to an outdoor area decreased self-injurious and stereotypical behaviors in adult malerhesus who had been single-caged or group-housed indoors.(3) Inanimate and Feeding EnrichmentBaker KC 1997. Straw and forage material ameliorate abnormal behaviors in adult chimpanzees.Zoo Biology 16, 225-236"In an [successful] effort to reduce abnormal behaviors, especially regurgitation andreingestion, and promote higher activity levels [locomoting and playing], straw and scatteredforage material were added to the enclosures of 13 indoor-housed chimpanzees living in pairsand trios."Baker KC, Springer DA 2006. Frequency of feeding enrichment and response of laboratorynonhuman primates to unfamiliar people. Journal of the American Association for LaboratoryAnimal Science [Contemporary Topics in Laboratory Animal Science] 45(1), 69-73"The data presented support the hypothesis that levels of treat feeding influence monkeys'receptivity to unfamiliar people."Bayne K, Dexter SL, Mainzer H, McCully C, Campbell G, Yamada F 1992. The use of artificialturf as a foraging substrate for individually housed rhesus monkeys (Macaca mulatta). AnimalWelfare 1, 39-53http://www.awionline.org/Lab_animals/biblio/aw1-39.htm"An increasing trend in time spent foraging with a concomitant decline in aberrant behaviourover a time period of six months was particularly noteworthy [in the single-housed subjects]."Bayne K, Dexter S, Suomi S 1992. A preliminary survey of the incidence of abnormal behaviorin rhesus monkeys (Macaca mulatta) relative to housing condition. Lab Animal 21(5), 38-46"The greatest frequency of overall abnormal behavior and stereotypic exploratory behavior wasin 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-directed behavior."

Bayne K, Mainzer H, Dexter SL, Campbell G, Yamada F, Suomi SJ 1991. The reduction ofabnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with aforaging/grooming board. American Journal of Primatology 23, 23-35All of the single-housed "animals foraged from the board to the point that a significant reductionin the level of abnormal behavior was noted."Bennett BT, Spector MR 1989. The use of naturally occurring manipulanda to improve thepsychological well-being of singly housed baboons. Journal of the American Veterinary MedicalAssociation 194, 1782 (Abstract)Single-housed animals demonstrated a marked reduction of stereotypy when they had corn-onthe-cob.Bloomsmith MA, Alford PL, Maple TL 1988. Successful feeding enrichment for captivechimpanzees. American Journal of Primatology 16, 155-164Four feeding techniques were simultaneously implemented. "Agonistic, abnormal, and groomingbehaviors were significantly reduced."Boccia ML 1989. Long-term effects of a natural foraging task on aggression and stereotypies insocially housed pigtail macaques. Laboratory Primate Newsletter 28(2), 18-19http://www.brown.edu/Research/Primate/lpn28-2.html#maria"Two months following the introduction of the foraging task stereotypies remained depressed,and hairpulling remained rare. In addition, bedding exploration and other types of explorationremained elevated, and agonistic behaviors remained low."Boccia ML, Hijazi AS 1998. A foraging task reduces agonistic and stereotypic behaviors inpigtail macaque social groups. Laboratory Primate Newsletter 37(3), 1-5http://www.brown.edu/Research/Primate/lpn37-3.html#bocciaTime spent foraging increased, while agonistic and abnormal behavior (e.g., hairpulling) andstereotypies (e.g., pacing ) decreased.Boinski S, Gross TS, Davis JK 1999. Terrestrial predator alarm vocalizations are a valid monitorof stress in captive brown capuchins (Cebus apella). Zoo Biology 18, 295-312"Our results are consistent with the interpretation that in conditions of low environmentalenrichment the study subjects were more stressed, and therefore more reactive to the presence ofa threatening terrestrial stimulus (human observer), than when in more enriched conditions."Brent L, Eichberg JW 1991. Woodchip bedding as enrichment for captive chimpanzees.American Journal of Primatology 24, 91-92"Abnormal behavior and environmental manipulation were significantly lower during thewoodchip [not mixed with food] condition."Brent L, Long KE 1995. The behavioral response of individually caged baboons to feedingenrichment and the standard diet: A preliminary report. Contemporary Topics in LaboratoryAnimal Science 34(2), 65-69"Increasing foraging opportunities in this study reduced abnormal behaviors from 16.4% of thedata points in the baseline condition to 4.9% and 5.7% in the chow [normal feeding condition]and feeder condition, respectively."37

38Brent L, Belik M 1997. The response of group-housed baboons to three enrichment toys.Laboratory Animals 31, 81-85"Abnormal, cage-directed, inactive and self-directed behaviours all significantly decreased afterthe [simultaneous] provision of the toys."Brown DL, Gold KC 1997. Effects of straw bedding on non-social and abnormal behavior ofcaptive lowland gorillas (Gorilla gorilla gorilla). In Proceedings on the 2nd InternationalConference on Environmental Enrichment Holst B (ed), 27-35. Copenhagen Zoo, Frederiksberg"Two individuals were frequently observed to hold their ears or head while the exhibit was in anunbedded condition. This behavior virtually disappeared in the enriched condition. ... Of theeight individuals found to engage in coprophagy, five individuals were observed to exhibit thisbehavior in solely the unbedded condition." Individuals who engaged in regurgitationreingestiondemonstrated lower levels of this behavior in the bedded condition.Chamove AS, Anderson JR, Nash VJ 1984. Social and environmental influences on selfaggressionin monkeys. Primates 25, 319-325“It is clear that enriched environmental conditions reduced SA [self-aggression]. Allowingmonkeys to forage through clean woodchips, even when there is no obvious incentive,substantially reduced the level of this abnormal behavior."Crockett CM, Bellanca RU, Heffernan KS, Ronan DA, Bonn WF 2001. Puzzle Ball foragingdevice for laboratory monkeys. Laboratory Primate Newsletter 40(1), 4-7http://www.brown.edu/Research/Primate/lpn40-1.html#ball“The empty Puzzle Balls were associated with a reduction [approximately 60%] in abnormalbehavior."Eaton GG, Kelley ST, Iliff-Sizemore SA 1993. Rawhide 'chew-bones' reduce abnormal behaviorin individually housed adult rhesus macaques. American Journal of Primatology 30, 308(Abstract)"Self-clasp showed a significant decline when the rawhide bones were present. We conclude thatrawhide chew-bones are an effective, and relatively inexpensive method of enriching theenvironment of individually housed rhesus macaques."Honess PE, Marin CM 2006. Enrichment and aggression in primates. Neuroscience andBiobehavioral Reviews 30, 413-346"There is considerable evidence that primates housed under impoverished conditions developbehavioural abnormalities, including, in the most extreme example, self-harming behaviour. Thishas implications for all contexts in which primates are maintained in captivity from laboratoriesto zoos since by compromising the animals' psychological well-being and allowing them todevelop behavioural abnormalities their value as appropriate educational and research modelsis diminished. This review examines the extensive body of literature documenting attempts toimprove living conditions with a view to correcting behavioural abnormalities and housingprimates in such a way that they are encouraged to exhibit a more natural range and proportionof behaviours, including less self-directed and social aggression. The results of housing, feeding,physical, sensory and social enrichment efforts are examined with specific focus on their effecton aggressive behaviour and variation in their use and efficacy. It is concluded that whileinappropriate or poorly distributed enrichment may encourage aggressive competition,enrichment that is species, sex, age and background appropriate can dramatically reduceaggression, can eliminate abnormal behaviour and substantially improve the welfare of primatesmaintained in captivity."

Kessel AL, Brent L 1998. Cage toys reduce abnormal behavior in individually housed pigtailmacaques. Journal of Applied Animal Welfare Science 1, 227-234"Providing multiple manipulable toys as enrichment for [single-caged] pigtail macaques waseffective in reducing abnormal behavior" during 30- min observation session.Lam K, Rupniak NMJ, Iversen SD 1991. Use of a grooming and foraging substrate to reducecage stereotypies in macaques. Journal of Medical Primatology 20, 104-109http://www.awionline.org/Lab_animals/biblio/jmp20-1.htm"Stereotyped behaviours were reduced by up to 73%.”Maki S, Alford PL, Bloomsmith MA, Franklin J 1989. Food puzzle device simulating termitefishing for captive chimpanzees (Pan troglodytes). American Journal of Primatology19(Supplement), 71-78"Significant reductions of abnormal behavior and significant increases in activity occurred withthe pipe feeder's availability.”Meunier LD, Dukting JT, Landi MS 1989. Modification of stereotypic behavior in rhesusmonkeys using videotapes, puzzlefeeders, and foraging boxes. Laboratory Animal Science 39,479 (Abstract)"Results of this study demonstrate that foraging boxes and puzzle feeders can reduce stereotypicbehavior significantly [in single-housed subjects].”Murphy DE 1976. Enrichment and occupational devices for orang utans and chimpanzees.International Zoo News 137(23.5), 24-26http://www.awionline.org/Lab_animals/biblio/izn-mur.htmSubjects were provided with an artificial termite mount. “The most encouraging result was areduction in the female's stereotyped pacing. The environmental enrichment of the chimp exhibithas resulted in a decrease in observable coprophagy, a diversification of the activities, and aprobable improvement in the physical and psychological condition of the animals."Nadler RD, Herndon JG, Metz B, Ferrer AC, Erwin J 1992. Environmental enrichment by variedfeeding strategies for individually caged young chimpanzees. In Chimpanzee Conservation andPublic Health: Environments for the Future Erwin J, Landon JC (eds), 137-145.Diagnon/Bioqual, Rockville"Providing an ear of unhusked corn on alternate days, in addition to laboratory chow, resultedin more time spent contacting food [primarily the corn] an hour after feeding than feedinglaboratory chow alone. Seven of eight [single-housed] animals exhibited less stereotypy on thedays they received the ear of corn. Stereotypical behavior, which occurs at relatively lowfrequencies under natural conditions, was reduced somewhat when the animals were fed three[rather than one] meals."Neu K, Lambeth S, Toback E, Schapiro S 2001. Hay can be used to decrease feces smearing ingroups of captive chimpanzees. American Journal of Primatology 54(Supplement), 78 (Abstract)Feces smearing on the walls decreased significantly when hay was present compared to whenno hay was available.Poffe A, Melotto S, Gerrard PA 1995. Comparison of four environmental enrichment strategiesin captive common marmosets (Callithrix jacchus). Primate Report 42, 24-2539

40"Access to the puzzles was accompanied by increase in social interaction and activity anddecrease 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 alterbehaviour."Preilowski B, Reger M, Engele H 1988. Combining scientific experimentation with conventionalhousing: A pilot study with rhesus monkeys. American Journal of Primatology 14, 223-234Manipulatory activity required by the apparatus reduced motor stereotypies but not self-biting.Pyle DA, Bennett AL, Zarcone TJ, Turkkan. J. S., Adams RJ, Hienz RD 1996. Use of two foodforaging devices by singly housed baboons. Laboratory Primate Newsletter 35(2), 10-15http://www.brown.edu/Research/Primate/lpn35-2.html#pyle"Stereotypical behaviors are reduced [in single-housed subjects] when the devices are present.In addition, the foraging devices elicited species-typical behaviors such as foraging andgrooming, even after food appeared to be absent from the devices."Roberts RL, Roytburd LA, Newman JD 1999. Puzzle feeders and gum feeders as environmentalenrichment for common marmosets. Contemporary Topics in Laboratory Animal Science 38(5),27-31“Gum feeders and Puzzle-Feeders loaded with waxmoth larvae are useful for reducing therates of pacing and inactivity" in single-housed and in pair-housed marmosets.Steen Z 1995. Effects of enriched food acquisition on activity budgets of two tamarin species atAdelaide Zoo. International Zoo News 42, 284-298http://www.awionline.org/Lab_animals/biblio/izn-ste.htmSimple bamboo pipe feeder is described and tested in group-housed animals. "The aim of thestudy was to [successfully] increase foraging time with an increasing number of feeding devices[brawn bowl, bamboo pipe]. ... Prior to the study large amounts of fur were found in the nestingbox of the golden tamarins. The zoo vet suspected that this was a result of overgrooming. Duringand after the study the overgrooming apparently ceased because the animals had something elseto do."Taylor TD 2002. Feeding enrichment for red-handed tamarins. The Shape of Enrichment 11(2),1-3http://www.enrichment.org/articles/112Tamarin.pdfAccess to a 'feeding basket' [stuffed with straw mixed with their normal feed and hung from aperch] and suspended sticks smeared with acacia gum increased feeding activities whilereducing the incidence of stereotypy [primarily somersaulting], hyperactivity, coprophagy andexcessive grooming and scent marking in a 3-adult-member group.Watson L 1992. Effect of an enrichment device on stereotypic and self-aggressive behaviors insingly-caged macaques: A pilot study. Laboratory Primate Newsletter 31(3), 8-10http://www.brown.edu/Research/Primate/lpn31-3.html#watson"A [temporary] reduction in some behavior pathology was noted, possibly due to replacing thestereotypic behaviors with activities directed toward the feeder."Weld K, Erwin J 1990. Provision of manipulable objects to cynomolgus macaques promotesspecies-typical behavior. American Journal of Primatology 20, 243 (Abstract)

41"A different pet toy was provided to each [single-caged] monkey" during six weeks. "Selfdirectedabnormal behavior was reduced or eliminated in all subjects ... but increased afterremoval of the toys."Wiard J 1992. Reduction of regurgitation and reingestion (R&R) in lowland gorillas at theOklahoma City Zoo. Gorilla Gazette 6(3), 6-7"The addition of browse or hay to the diet of captive gorilla reduces the occurrence of R&R[regurgitation-reingestion]. Novelty items tend to reduce R&R [only] for short periods of time."(4) Acoustical EnrichmentBrent L, Weaver D 1996. The physiological and behavioral effects of radio music on singlyhoused baboons. Journal of Medical Primatology 25, 370-374http://www.awionline.org/Lab_animals/biblio/jmp25-3.htmVocalization [of the single-housed subjects] was twice as high when the radio was off. Bloodpressure did not vary with radio condition, but the heart rate was significantly lower when theradio was playing.Howell S, Roeder E, Nelson C, Fritz J, Schwandt M 2002. The effect of music on the behavior ofcaptive chimpanzees (Pan troglodytes). American Journal of Primatology 57(Supplement), 83-84 (Abstract)"Results suggest music has a significant effect on behavior of captive chimpanzees. It resulted indecreased aggression and active exploratory behavior and increased inactive resting and socialbehavior (principally social grooming). .. We suggest music may have a calming effect onbehavior and good potential as therapeutic environmental enrichment.”McDermott J, Hauser MD 2007. Nonhuman primates prefer slow tempos but dislike musicoverall. Cognition 104, 654-668Both tamarins and marmosets preferred slow tempo to fast temp music, and when allowed tochoose between slow tempo musical stimuli and silence they preferred silence.Rukstalis M, French JA 2005. Vocal buffering of the stress response: exposure to conspecificvocalizations moderates urinary cortisol excretion in isolated marmosets. Hormones andBehavior 47, 1-7“For many species, the presence of a significant social partner can lessen the behavioral andphysiological responses to stressful stimuli. This study examined whether a single, individuallyspecific, signature vocalization (phee call) could attenuate the physiological stress response thatis induced in marmosets by housing them in short-term social isolation. .. Isolated marmosetsexposed to a familiar pair mate's vocalization showed significantly lower levels of urinarycortisol than when exposed to unfamiliar marmoset vocalizations (P

42"The purpose of this study was to test the effects of 2 different types (vocal versus instrumental)and 2 genres (classical vocal versus 'easy-listening' vocal) of music on social behavior in 31female and 26 male chimpanzees (Pan troglodytes). Results indicated that instrumental musicwas more effective at increasing affiliative behavior in both male and female chimpanzees,whereas vocal music was more effective at decreasing agonistic behavior. A comparison of 2genre of vocal music indicated that easy-listening (slower tempo) vocal music was more effectiveat decreasing agonistic behavior in male chimpanzees than classical (faster tempo) vocal music.Agonistic behavior in females remained low (

43"These results suggest that simple, unstructured affiliation between humans and chimpanzeeshas a powerful impact on well-being, promoting activity and relaxed conspecific interactionsand ameliorating undesirable behaviors [e.g., abnormal behaviors]."Bayne K, Dexter SL, Suomi SJ 1991. Social housing ameliorates behavioral pathology in Cebusapella. Laboratory Primate Newsletter 30(2), 9-12http://www.brown.edu/Research/Primate/lpn30-2.html#bayneChange from single- to group-housing "effectively reduced stereotypic behaviors; however, italso was associated with more passive behaviors... The concurrent shifts in these components ofthe behavioral repertoire suggests that the animals were in a calmer state when housedsocially."Bayne K, Dexter SL, Strange GM 1993. The effects of food treat provisioning and humaninteraction on the behavioral well-being of rhesus monkeys (Macaca mulatta). ContemporaryTopics in Laboratory Animal Science 32(2), 6-9“The effects of human interaction and food supplementation appear to be protracted, resulting ina 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 behavioral course of introductions. American Journal of Primatology 45, 171 (Abstract)Stereotyped rocking declined in newly integrated individuals.Boccia ML, Reite M, Laudenslager ML 1989. On the physiology of grooming in a pigtailmacaque. Physiology and Behavior 45, 667-670When the subject received grooming from others, heart rate was significantly lower than duringself grooming, as well as during other behaviors.Bourgeois SR, Brent L 2005. Modifying the behaviour of singly caged baboons: evaluating theeffectiveness of four enrichment techniques. Animal Welfare 14, 71-81Seven singly caged adolescent [mean age: 4.2 years] male baboons were studied. "Analysis ofbaseline behaviour verified substantial durations of abnormal behaviour [9.8/30- minobservations (33% of time)]. We tested the effectiveness of ... positive reinforcement training(PRT), food enrichment [fruits, frozen fruit/juice, foraging devices], non-food enrichment [toys],and social enrichment (pair/trio). .. The social enrichment condition resulted in the mostpositive behavioural changes, including ... near elimination of abnormal behaviours [0.7/30-minobservation (2% of time)]. Significant reduction in total abnormal behaviour levels were alsofound for other types of enrichment, but only social enrichment and PRT were effective inreducing whole-body stereotypies. ... Animal enrichment (human or conspecific stimulation), asopposed to inanimate enrichment, provides optimal means of behaviour modification for singlycaged baboons.”Bushong D, Schapiro SJ, Bloomsmith MA 1992. Self-aggression in nonhuman primates: Areview of its development/possible causes, methods of therapeutic treatment, and its relevance tothe zoo situation. American Zoo and Aquarium Association Regional Conference Proceedings,723-728"Social enrichment appears to be the most effective method of reducing the development orfrequency of abnormal behaviors.” After the animals ”were moved from single- to pair-housing,preliminary analyses of individual behavior indicated that there was a decrease in time spent inself-aggressive behaviors."

44Choi GC 1993. Humans enrich the lives of lab baboons. WARDS Newsletter 4, 3-7 & 13"The reduction in cage painting and banging was dramatic and remarkable" after the singlehousedanimals received more attention from the attending personnel.Coe CL, Franklin D, Smith ER, Levine S 1982. Hormonal responses accompanying fear andagitation in the squirrel monkey. Physiology and Behavior 29, 1051-1057"The presence of a social partner reduced signs of behavioral disturbance."Coelho AM, Carey KD, Shade RE 1991. Assessing the effects of social environment on bloodpressure and heart rates of baboon. American Journal of Primatology 23, 257-267In the social companion condition, a subject was able to have visual, tactile, and auditoryinteractions with his companion through the wire mesh walls of the specially designed cages."When animals were housed with social companions their blood pressures were consistentlylower than when they were either housed individually or with social strangers. ... Measurementsof cardiovascular physiology obtained under social housing may more closely model normalphysiology than ... individual housing."Eaton GG, Kelley ST, Axthelm MK, Iliff-Sizemore SA, Shiigi SM 1994. Psychological wellbeingin paired adult female rhesus (Macaca mulatta). American Journal of Primatology 33, 89-99Paired females show strong preference to spend time in close proximity; agonistic behaviors arevery infrequent. Health measures, body weight gains, reproduction and immune responses do notdiffer between dominant, subordinate, and single-housed females. Paired females spend less timeengaged in abnormal behavior than single-housed females."Fritz P, Fritz J 1979. Resocialization of chimpanzees. Journal of Medical Primatology 8, 202-221"With the exception of Tim, stereotyped behaviors in other individuals decreased almostimmediately upon introduction of a compatible cage mate and continued to decrease associalization proceeded."Gonzalez CA, Coe CL, Levine S 1982. Cortisol responses under different housing conditions infemale squirrel monkeys. Psychoneuroendocrinology 7, 209-216Plasma levels of cortisol "were significantly lower in pair-housed females than in those living ina social group or individually. The increment in cortisol levels after stress (handling and etheranesthesia) also was smaller in females housed in pairs." Dominant and subordinate partners offemale pairs did not differ in their plasma cortisol levels.Goodwin J 1997. The application, use, and effects of training and enrichment variables withJapanese snow macaques (Macaca fuscata) at the Central Park Wildlife Center. American Zooand Aquarium Association Regional Conference Proceedings, 510-515A training protocol is briefly described which allows the keepers through vocal and visual cuesto herd the animals to a holding area. Training sessions were "deterring stereotypic andabnormal behaviour - such as excessive grooming and fur-pulling."Goosen C 1988. Studies of disturbed behaviour in macaques. In Biomedical Research inPrimates. Proceedings of the TNO Symposium Jonker M (ed), 67-74Stereotyped locomotion amounted to about 20% of the time when subjects were housed solitary.The amount of time was reduced to about 4% when the subjects had one or more social partners.

45Gunnar MR, Gonzalez CA, Levine S 1980. The role of peers in modifying behavioral distressand pituitary-adrenal response to a novel environment in year-old rhesus monkeys. Physiologyand Behavior 25, 795-798Infant rhesus macaques were captured from their social group and placed in an unfamiliarenvironment for 24 hours either (a) alone or (b) with another infant from the same group. Whentested alone, the animals exhibited significantly more signs of distress - agitation, distressvocalization - than when they were tested with a companion, indicating that the companion had astress-buffering effect.Gust DA, Gordon TP, Brodie AR, McClure HM 1994. Effect of a preferred companion inmodulating stress in adult female rhesus monkeys. Physiology and Behavior 55, 681-684"Adult female rhesus monkeys exhibited a profound stress response when removed from theirsocial group to a novel environment. Recovery time [of T cell subsets] was significantlyenhanced by the presence of a preferred companion."Gwinn LA 1996. A method for using a pole housing apparatus to establish compatible pairs amongsquirrel monkeys. Contemporary Topics in Laboratory Animal Science 35(4), 61 (Abstract)Pair formation protocol in a pole-and-collar housing system is described. "Pair housing theanimals has not interfered with research. During nine treatments with an identical testcompound, singly housed animals lost significantly more weight on average than did pair housedanimals."Hartner MK, Hall J, Penderghest J, White E, Watson S, Clark L 2000. A novel approach togroup-housing male cynomolgus macaques in a pharmaceutical environment. ContemporaryTopics in Laboratory Animal Science 39(4), 67 (Abstract)"Twenty percent of our primates are maintained in a single-housed environment. Of those ..animals, 40% exhibited moderate to marked degrees of self-directed activity; i. e., hairpulling.By contrast, none of the pair or group-housed animals exhibited these behaviors. ... Theseprimates are now more receptive to handling and training, and will therefore be better animalmodels, as noted by a marked decrease in vocalization and self-directed behavior duringpole/collar capture and chair restraint procedures."Hennessy MB 1984. Presence of companion moderates arousal of monkeys with restricted socialexperience. Physiology and Behavior 33, 393-398When placed in a novel environment for 30 minutes, juvenile squirrel monkeys emittedsignificantly more high-pitched vocalizations when tested alone than when tested in the presenceof the companion. A significant elevation of plasma cortisol was observed only when animalswere exposed to the novel environment alone.Kessel AL, Brent L 1997. Rehabilitating a rheboon (Macaca mulatta x Papio hamadryascynocephalus), from single housing to social housing: A case study. American Journal ofPrimatology 42, 121 (Abstract)Abnormal behavior was reduced from 46% of observation time in the single-housed condition to4% after introduction to an enclosure with ten other rhesus females.Kessel A, Brent L 2001. The rehabilitation of captive baboons. Journal of Medical Primatology30, 71-80

46“Eleven baboons who had been singly housed indoors for an average of 5 years were moved tooutdoor social groups in an attempt to provide a more species-typical environment and reducehigh levels of abnormal behavior. ... Abnormal behavior decreased significantly from an averageof 14% of the observation time in the single cages to 3% in the sixth month of social housing.Cage manipulation and self-directed behaviors also significantly decreased."Line SW, Morgan KN, Markowitz H, Roberts J, Riddell M 1990. Behavioral responses of femalelong-tailed macaques (Macaca fascicularis) to pair formation. Laboratory Primate Newsletter29(4), 1-5http://www.brown.edu/Research/Primate/lpn29-4.html#line"Self-abusive behaviors were recorded for five of the ten subjects when singly housed, but werecompletely absent after pair formation."Lutz CK, Novak M 2005. Environmental enrichment for nonhuman primates: Theory andapplication. ILAR [Institute for Laboratory Animal Research] Journal 46(2), 178-191http://dels.nas.edu/ilar_n/ilarjournal/46_2/html/v4602lutz.shtml"Only social contact satisfies the goal of promoting a wide variety of species-typical activitieswhile at the same time reducing or preventing the development of abnormal behavior. .. Anumber of toys should be provided initially and rotated on a regular basis to maintain interest. ..At present, the most effective form of enrichment for captive primates is social housing."Mahoney CJ 1992. Some thoughts on psychological enrichment. Lab Animal 21(5), 27,29,32-37"Isolation 'wards' for ill animals and infectious study chambers can have windows ortransparent plastic panels between cages, providing visual communication without interferingwith ... air-flow."Mason WA 1960. Socially mediated reduction in emotional responses of young rhesus monkeys.Journal of Abnormal and Social Psychology 60, 100-110"Previous observations that social stimuli may function as a source of security and a means ofmitigating emotional distress in young primates are fully supported by the present results."Miller LC, Bard KA, Juno CJ, Nadler RD 1986. Behavioral responsiveness of youngchimpanzees (Pan troglodytes) to a novel environment. Folia Primatologica 47, 128-142"Extreme distress reported previously for chimpanzees and human children when tested alone ina novel situation was rarely observed in these tests when an attachment figure [humancaretaker] was present.”Minkel R 2007. Pair-housing eliminates compulsive hair pulling: a case report. LaboratoryAnimal Refinement and Enrichment Forum (electronic discussion group), September 27, 2007http://groups.yahoo.com/group/LAREF/members"At a previous institution we had a cyno — 'Grandpa' — who suffered from severe hair pulling.He had removed practically all hair from his body; all that was left was a patch in the middle ofhis back that he could not reach! He was not shy about hiding his idiosyncratic behavior at alland would contort into strange positions to do it. The veterinarians tried various treatments toalleviate the problem to no avail. We tried all the various enrichment devices we could find;they would only keep him occupied for a day or so. We pulled all the dividers from his cage togive him more space; no luck. We were reluctant to pair him as he was an older male who hadbeen singly housed for so long, but there was no other treatment option left.We tried two unsuccessful pairings and finally settled on a newly acquired juvenile malewho was very rowdy and active (Grandpa was quite the opposite: relaxed and sedate). The little

47guy, himself was on his second pair attempt. During his first attempt — all he did was try tostart a fight. To our great relief the new pair worked out just fine. This truly ”odd couple“ gotalong great from the start. Grandpa responded correctly, brought the little guy in line, andactually perked up. The most surprising part, however, was that Grandpa stopped hair pulling.He stopped completely, and all his hair had grown back in the course of several months.Three years later Grandpa had not resumed his old habit, even though his buddy hadbeen removed for research-related reasons one year after the original pair formation.”Missakian EA 1972. Effects of adult social experience on patterns of reproductive activity ofsocially deprived male rhesus monkeys (Macaca mulatta). Journal of Personality and SocialPsychology 21(1), 131-134Two of three males showed a decrease in both stereotyped locomotion and self-aggression afterbeing introduced into a group of rhesus macaques.National Research Council 1998. The Psychological Well-Being of Nonhuman PrimatesNational Academy Press, Washington, DChttp://fermat.nap.edu/books/0309052335/html/index.html"Social interactions are considered to be one of the most important factors influencing thepsychological well-being of most nonhuman primates. ... The common practice of housing rhesusmonkeys singly calls for special attention.”Reimers M, Schwarzenberger F, Preuschoft S 2007. Rehabilitation of research chimpanzees:Stress and coping after long-term isolation. Hormones and Behavior, in print“Permanent retirement from biomedical research in combination with therapeuticresocialization maximizing chimpanzees' situation control resulted in reduced fecal cortisolmetabolite levels. Our results indicate that chimpanzees can recover from severe socialdeprivation, and may experience resocialization as less stressful than solitary housing."Roberts SJ, Platt ML 2004. Pair-housing macaques with biomedical implants: a safe andpractical alternative to single-housing. American Journal of Primatology 62(Supplement), 96-97http://www.asp.org/asp2004/abstractDisplay.cfm?abstractID=734&confEventID=828”Recognition of the importance of social interaction for primate well-being has led to newUSDA guidelines recommending that animal facilities provide social enrichment for captiveprimates, as long as doing so does not endanger the animals or interfere with research goals.Group- or pair-housing is the best way to provide social enrichment, but many primates used inmedical research are housed singly because they have implants which may make them morevulnerable to inflicted injury. In addition, pairing adult male monkeys is often considered toodifficult and too impractical to attempt. The goal of this study was to evaluate these assumptions.Eight adult male rhesus macaques (Macaca mulatta) and two adult male crab-eating macaques(Macaca fascicularis) were evaluated for pairing and then housed with a compatible partner forup to three years. During the period of study, 9 of the 10 monkeys received cranial and scleralsearch coil implants. On average, each monkey was compatible with 69% of partners, and thishigh degree of compatibility allowed monkeys to be paired continuously within three weeks ofinitial evaluation. Moreover, the rate of implant failure during pair-housing (0.07 failures permonth) was not significantly different from the rate of implant failure when monkeys were singlyhoused(0.098). These data demonstrate that pair-housing provides a safe and practical socialalternative to single-housing for adult male macaques with biomedical implants.“

48Reinhardt V, Houser WD, Eisele S, Champoux M 1987. Social enrichment with infants of theenvironment for singly caged adult rhesus monkeys. Zoo Biology 6, 365-371http://www.awionline.org/Lab_animals/biblio/zb6-365.htm"Three adults exhibiting stereotypical behavior abandoned their peculiar habits after they hadlived with their young companions for four months."Reinhardt V, Houser W, Eisele S, Cowley D, Vertein R 1988. Behavior responses of unrelatedrhesus monkey females paired for the purpose of environmental enrichment. American Journalof Primatology 14, 135-140http://www.brown.edu/Research/Primate/lpn26-2.html#vik6 of 7 animals abandoned behavioral disorders within the first 4 ws of living together with acompanion.Reinhardt V, Houser WD, Cowley D, Eisele S, Vertein R 1989. Alternatives to single caging ofrhesus monkeys (Macaca mulatta ) used in research. Zeitschrift für Versuchstierkunde 32, 275-279http://www.awionline.org/Lab_animals/biblio/es32-2~1.htm“Pairing caged rhesus monkeys with compatible conspecifics does not interfere with a number ofcommon research protocols [e.g., headcap implantation, experimental surgery, bloodcollection].”Reinhardt V 1990. Social enrichment for laboratory primates: A critical review. LaboratoryPrimate Newsletter 29(3), 7-11http://www.brown.edu/Research/Primate/lpn29-3.html#rev"23% (54/237) of individually caged, but only 10% (38/382) of pair-housed rhesus monkeysrequired medical treatment."Reinhardt V 1999. Pair-housing overcomes self-biting behavior in macaques. Laboratory PrimateNewsletter 38(1), 4http://www.brown.edu/Research/Primate/lpn38-1.html#pairSubjects exhibited self-biting behavior predictably in the presence of personnel. ”The transfer toa compatible social-housing arrangement [isosexual pair-housing] effectively cured the [seven]rhesus subjects from the behavioral pathology of habitual self-biting.“Rukstalis M, French JA 2005. Vocal buffering of the stress response: exposure to conspecific.Hormones and Behavior 47, 1-7“For many species, the presence of a significant social partner can lessen the behavioral andphysiological responses to stressful stimuli. This study examined whether a single, individuallyspecific, signature vocalization (phee call) could attenuate the physiological stress response thatis induced in marmosets by housing them in short-term social isolation. .. Isolated marmosetsexposed to a familiar pair mate's vocalization showed significantly lower levels of urinarycortisol than when exposed to unfamiliar marmoset vocalizations (P

49Ruppenthal GC, Walker CG, Sackett GP 1991. Rearing infant monkeys (Macaca nemestrina) inpairs produces deficient social development compared with rearing in single cages. AmericanJournal of Primatology 25, 103-113In contrast to singly caged infants, pair-reared infants failed to show "rock/huddle/self clasp andstereotypy categories.“Schapiro SJ, Bushong D 1994. Effects of enrichment on veterinary treatment of laboratoryrhesus macaques (Macaca mulatta). Animal Welfare 3, 25-36http://www.awionline.org/Lab_animals/biblio/aw3-25.htm"Diarrhea-related problems typical for singly-housed animals and trauma-related problemstypical of group-housed animals were not as prominent in the pairs."Schapiro SJ, Nehete PN, Perlman JE, Sastry KJ 2000. A comparison of cell-mediated immuneresponses in rhesus macaques housed singly, in pairs, or in groups . Applied Animal BehaviourScience 68, 67-84“Social housing condition affects immune responses. While not unidirectional, these effectsgenerally suggest enhanced immune responses for socially housed animals. .. It is our contentionthat strong social relationships, particularly the affiliative interactions that characterize our pairhoused monkeys, may diminish the likelihood of severe infection with potentially diarrheainducingagents. ... Since rhesus monkeys live socially in nature, and the immune responses ofsingly housed animals differed from those housed socially, there is considerable motivation andjustification for suggesting that the use of singly housed rhesus macaques may complicateinterpretations of normal immunological responses."Schapiro SJ 2002. Effects of social manipulations and environmental enrichment on behaviorand cell-mediated immune responses in rhesus macaques. Pharmacology, Biochemistry andBehavior 73, 271-278"In general, enrichment of the inanimate environment with toys, structures, foraging devices,and/or videotapes increased the amount of species-typical behavior expressed by the monkeys,but did not affect their immune responses. Housing monkeys socially, on the other hand, not onlyresulted in increased time spent in species-typical activities, but also resulted in (1) decreases intime spent in abnormal behavior and (2) changes in a number of immune parameters."Schnell CR, Gerber P 1997. Training and remote monitoring of cardiovascular parameters innon-human primates. Primate Report 49, 61-70“Training of non-human primates to handling and experimental procedure will reduce thevariance and increase the significant level of observed changes, allows the measurement ofnormal physiological parameters and finally reduces the number of animals used in anexperiment.”Steinbacher EA, Setser JJ, Morris TD, Gumpf D 2006. Development and implementation of aprogram for the social housing of nonhuman primates on toxicology studies. AALAS 57thNational Meeting Official Program, 157 (Abstract)"We developed a step-wise procedure for social housing animals (cynomolgus and rhesus) intopairs, triads or quads based on the study design. Nonhuman primates that were socially housedshowed signs of better physical and psychological health, thereby greatly reducing abnormalbehaviors and stereotypies, such as self-biting, that could potentially compromise study data.Based on the success of our social housing program, all nonhuman primate studies longer than28 d will be socially housed unless otherwise approved by our institutional ACUC.”

50Thompson MA, Bloomsmith MA, Taylor LL 1991. A canine companion for a nursery-rearedinfant chimpanzee. Laboratory Primate Newsletter 30(2), 1-4http://www.brown.edu/Research/Primate/lpn30-2.html#dog"Reduction in rocking and other stress-related behaviors in the dog's presence is a strongargument for providing nursery-reared chimpanzees with dog companions. We have safelyhoused dogs with single infants as well as with small groups of infants, until infants reach aboutthree years of age.”Van Loo P, Skoumbourdis E, Reinhardt V 2006. Postsurgical pairing: a discussion by theRefinement & Enrichment Forum. Animal Technology and Welfare 5, 17-19http://www.awionline.org/Lab_animals/biblio/atw9.html”It is my experience with rhesus macaques that it is advisable to pair an animal after surgery assoon as possible with his or her compatible companion. We did this especially with animals afterone of them had head cap implant surgery. The animals recover better from the surgery stresswhen their familiar companion is with them than when they are alone."Wait C, Buchanan-Smith H, Morris K 2002. The effects of caretaker-primate relationships onprimates in the laboratory. Journal of Applied Animal Welfare Science 5, 309-319Group-housed "animals who had friendly relationships with caretakers were less disturbed byroutine husbandry procedures. .. Caretakers are much more likely to sustain scratches or bitesfrom animals who are fearful and aggressive toward them."Weed JL, Wagner PO, Byrum R, Parrish S, Knezevich M, Powell DA 2003. Treatment ofpersistent self-injurious behavior in rhesus monkeys through socialization: A preliminary report.Contemporary Topics in Laboratory Animal Science 42(5), 21-23Six individually caged males who engaged in persistent self-injurious behavior (SIB) werevasectomized and subsequently paired with females. The incidence of SIB was "markedlyreduced for all male monkeys after social pairing." One male engaged in severe SIB after 32months of pair-housing when he was temporarily removed from his partner for a procedure.Wolfle TL 1987. Control of stress using non-drug approaches. Journal of the AmericanVeterinary Medical Association 191, 1219-1221"Human interaction with monkeys and apes is essential for the well-being of the animal, datavalidity, and ease of handling." The 'social bond' with the animal "conveys to the animal a quietsense of assurance on which coping strategies can be developed for dealing with other stressfulaspects of the laboratory."(6) Natural WeaningCary M, Valentine B, Hill W 2000. The effect of mother-infant separation in captive baboons ontime intervals to first postpartum estrus, confirmed pregnancy and subsequent parturition.AALAS 51st National Meeting Official Program, 126-127"It is generally thought that early forced-weaning of infants would reduce the time fromparturition to the first fertile postpartum estrus thus maximizing reproductive efficiency. ... Froma survey of 23 animal records we determined the following values for mothers of both forced andnaturally weaned infants: days to first postpartum cycle and days from first postpartum cycle toconfirmed pregnancy. Mothers of naturally-weaned animals (those with infants) first cycled at174 ± 31 days and were confirmed pregnant 26 ± 13 days after this. Conversely, mothers offorce-weaned infants (weaning at 180 ± 16 days) first cycled at 187 ± 8 days and were confirmedpregnant 55 ± 26 days later. From these observations we suggest that both groups (mothers of

51force-weaned versus naturally-weaned infants) require similar times to exhibit their firstpostpartum estrus, but mothers of naturally-weaned infants appear to breed back more quickly(approximately one cycle) than those of force-weaned infants."International Primatological Society 1993. IPS International guidelines for the acquisition, careand breeding of nonhuman primates, Codes of Practice 1-3. Primate Report 35, 3-29http://pin.primate.wisc.edu/ips/codes.txt"A young monkey should not normally be separated from its mother at an early age (i.e., at 3-6months) but should remain in contact for one year to 18 months, in most species. There isunlikely to be any greater productivity through early weaning, in seasonally breeding species,such as rhesus monkeys. Even in non-seasonal breeders, any slight increase in productivity mustbe offset against the resulting behavioural abnormalities of the offspring."Mason WA 1991. Effects of social interaction on well-being: Development aspects. LaboratoryAnimal Science 41, 323-328"Captive animals will be served best if developing individuals are raised at least throughweaning by their biological mothers and have the experience of living in a social group thatapproximates the size and age-sex composition of the group in which they would develop innature. ... It seems unlikely, however, that peer experience alone can provide a practicalalternative to mother-rearing."Valentine B, Cary M, Stanley J, White G, Wallis J 1999. The timing of mother-infant separationand its effect on postpartum estrus and subsequent conception in captive baboons. AmericanJournal of Primatology 49, 110 (Abstract)"There was no correlation between infant removal age and duration until next conception. ...Postpartum cyclicity usually resumed before infant removal. Subsequent conception, however,was not significantly influenced by infant removal. This study indicates that early forced weaningdid not accomplish the goal of increased reproductive output. These findings - in addition to theconcern for proper psychological development - suggest the better strategy is to allow infants tobe naturally weaned by mothers."Wallis J, Valentine B 2001. Early vs. natural weaning in captive baboons: The effect on timingof postpartum estrus and next conception. Laboratory Primate Newsletter 40(1), 10-13http://www.brown.edu/Research/Primate/lpn40-1.html#wean"We examined the details of 73 recorded pregnancies of 45 adult females. ... The results of thisstudy indicate that forced infant weaning did not improve reproductive productivity in ourcolony of baboons. In fact, the data indicate that most females resumed their reproductive cycleswell before infant removal and, when given the opportunity for natural weaning, the femalesconceived while their previous infants were still dependent upon them. .. The potential benefits ofallowing infants to remain with their mothers throughout childhood are obvious."

(7) Working with Cooperative Animals52Bentson KL, Capitanio JP, Mendoza SP 2003. Cortisol responses to immobilization with Telazolor ketamine in baboons (Papio cynocephalus/anubis) and rhesus macaques (Macaca mulatta).Journal of Medical Primalogy 32, 148-160"The injection and blood sampling process increased cortisol levels in monkeys not trained toextend an arm but exerted no effect on cortisol in trained macaques.”Bloomsmith MA, Marr MJ, Maple TL 2007. Addressing nonhuman primate behavioral problemsthrough the application of operant conditioning: Is the human treatment approach a usefulmodel? Applied Animal Welfare Science 102(3-4), 205-222"Training by the systematic application of operant conditioning has been widely applied in thecare, management, exhibition, and study of nonhuman primates and many other species, but isless often used to control problematic animal behavior such as stereotyped behavior or selfinjuriousbehavior... Virtually all the techniques found to be effective treatments of stereotypyand self-injurious behavior in humans are directly applicable to similar behaviors in captivenonhuman primates. Thus the human work can serve as a model for how we can enhance ourattempts to address behavioral problems in captive nonhuman primates."

53Cross N, Pines MK, Rogers LJ 2004. Saliva sampling to assess cortisol levels in unrestrainedcommon marmosets and the effect of behavioral stress. American Journal of Primatology 62,107-114"We report a method for taking saliva samples from unrestrained, captive marmosets (Callithrixjacchus) to assess levels of free cortisol. Saliva samples can be obtained reliably, without anyhabituation, by encouraging the marmosets to lick and chew a cotton-wool bud coated inbanana. Saliva is thus left on the bud. We also tested sweetened fruit-drink crystals and anumber of other substances, but none of these attracted all of the marmosets, and even flavorsthat were effective once soon lost their attraction. .. A first experiment showed that themarmosets exhibited a rise in salivary cortisol levels in response to social isolation. A secondexperiment showed elevation of cortisol during a period when the marmosets were disturbed byincreased human activity and noise levels in the building in which they were housed. Hence, thismethod of saliva sampling is a convenient, noninvasive means of assessing cortisol levels inmarmosets.“Elvidge H, Challis JRG, Robinson JS, Roper C, Thorburn GD 1976. Influence of handling andsedation on plasma cortisol in rhesus monkeys (Macaca mulatta). Journal of Endocrinology 70,325-326"The present study shows that it is possible by long-term regular training to achieve meancortisol values which are significantly lower than in untrained or anaesthetized animals."Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housingand Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London, UKhttp://scienceandresearch.homeoffice.gov.uk/animal-research/legislation/"The least distressing method of handling is to train the animal to co-operate in routineprocedures. Advantage should be taken of the animal's ability to learn."Iliff SA, Friscino BH, Anderson LC 2004. Refinement of study design using positivereinforcement training in macaques. Folia Primatologica 75(Supplement), 282-283 (Abstract)”Implementation of Positive Reinforcement Training (PRT) to refine and modify studyprocedures conducted with rhesus macaques results in enhanced welfare for both animals andcaregivers. Capitalizing on the macaques intelligence and their capability to learn and performtasks with appropriate motivation, PRT can reduce or eliminate the need for sedatives orrestraint. PRT is useful for standard husbandry procedures such as feeding and transferringanimals between cages. It can also be used to facilitate sample collection from animals.Standard pharmacokinetic or metabolism study paradigms for evaluation of pharmaceutical testcompounds require frequent collection of blood, bile and/or other body fluids from animalsinstrumented with catheters and subcutaneous access ports. Collection of these samples can betechnically challenging, time consuming and potentially stressful for both personnel and theanimals. However, when PRT is used to conduct sampling procedures in the animals homeenclosure, stress is minimized as evidenced by lower cortisol levels.”Klein HJ, Murray KA 1995. Part C. Restraint. In Nonhuman Primates in Biomedical Research -Biology and Management Bennett BT, Abee CR, Henrickson R (eds), 286-297. Academic Press,New York, NY"The importance of training and adaptation cannot be overemphasized. This not only reducesstress to the animal but promotes safety and quality data collection."

54Lambeth SP, Hau J, Perlman JE, Martino M, Schapiro SJ 2006. Positive reinforcement trainingaffects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes).American Journal of Primatology 68, 245-256"Positive reinforcement training (PRT) techniques have received considerable attention for theirstress reduction potential in the behavioral management of captive nonhuman primates.However, few published empirical studies have provided physiological data to support thisposition. To address this issue, PRT techniques were used to train chimpanzees (Pantroglodytes) to voluntarily present a leg for an intramuscular (IM) injection of anesthetic.Hematology and serum chemistry profiles were collected from healthy chimpanzees (n=128) ofboth sexes and various ages during their routine annual physical examinations over a 7-yearperiod. Specific variables potentially indicative of acute stress (i.e., total white blood cell (WBC)counts, absolute segmented neutrophils (SEG), glucose (GLU) levels, and hematocrit (HCT)levels) were analyzed to determine whether the method used to administer the anesthetic(voluntary present for injection vs. involuntary injection) affected the physiological parameters.Subjects that voluntarily presented for an anesthetic injection had significantly lower mean totalWBC counts, SEG, and GLU levels than subjects that were involuntarily anesthetized by moretraditional means."Lambeth SP, Hau J, Perlman JE, Schapiro SJ 2006. Positive reinforcement training andphysiological responses in chimpanzees. AALAS [American Association for Laboratory AnimalScience] 57th National Meeting Official Program, 160 (Abstract)"A subset of variables potentially indicative of acute stress were analyzed to determine if themethod of adminstration of anesthetic (voluntary present for injection compared withnonvoluntary injection) and/or the method of obtaining the blood sample (voluntary comparedwith anesthesized) affected these physiogical parameters. Those subjects that voluntarilypresented for an anesthetic injection and/or venipuncture differed significantly on many of theseparameters from those subjects that were nonvonluntarily anesthetized by more traditionalmeans or whose blood was obtained following anesthesia. This data set objectively demonstratesthat positive reinforcement training for behaviors relevant to the blood sampling processsignificantly affects some of the physiological measures correlated with stress responses incaptive chimpanzees."McKinley J, Buchanan-Smith HM, Morris K 2002. Training common marmosets (Callithrixjacchus) to co-operate during routine laboratory procedures: Reliability and time investment.XIXth Congress of the International Primatological Society, Abstracts, 183-184."Nine pairs of ... marmosets were target trained to allow in-homecage weighing" and six pairswere trained to provide urine samples on request. Behavioural data showed that "increasedpositive interactions with humans as a consequence of training reduced stress as indicated bysignificantly less scent-marking, self-scratching and tsk and phee vocalisation. ... Data collectionwith trained animals was significantly faster than using standard techniques."Michael RP, Setchell KDR, Plant TM 1974. Diurnal changes in plasma testosterone and studieson plasma corticosteroids in non-anaesthetized male rhesus monkeys (Macaca mulatta). Journalof Endocrinology 63, 325-335Authors evaluated plasma corticosteroid concentrations in male rhesus macaques who "weretrained to enter voluntarily a restraining apparatus" and permitted venipuncture withoutshowing signs of stress. Basal cortisol values were 30% lower than previously reported fordifferent, untrained animals.

55National Research Council 1998. The Psychological Well-Being of Nonhuman PrimatesNational Academy Press, Washington, DChttp://fermat.nap.edu/books/0309052335/html/index.html“Procedures that reduce reliance on forced restraint and that reduce invasiveness are lessstressful for animals and staff, safer for both, and generally more efficient.”Prentice ED, Zucker IH, Jameton A 1986. Ethics of animal welfare in research: The institution'sattempt to achieve appropriate social balance. The Physiologist 29, 1&19-21"Physical restraint procedures should be used on awake animals only after alternativeprocedures have been considered and found to be inadequate. If a restraint will be utilized theanimal should be trained or conditioned to the restraining device, using positive reinforcement.”Prescott MJ, Buchanan-Smith HM 2007. Training laboratory-housed non-human primates, part I:a UK survey. Animal Welfare 16(1), 21-36Training using positive reinforcement is increasingly recognised as a valuable tool for thehumane and effective management and use of laboratory-housed non-human primates. A surveywas carried out on the use of training and other learning processes (socialisation, habituationand desensitisation) in over half of UK establishments using and breeding primates. There iswidespread awareness of training as a refinement technique but it not used as widely or as fullyas it might be. We conclude that there is opportunity for refinement of common scientific,veterinary and husbandry procedures (such as blood and urine collection, injection, capturefrom the group and weighing) through use of positive reinforcement training, especially whencombined with appropriate socialisation, habituation and desensitation. Recommendations onbest practice, training techniques and staff education are given.Reinhardt V 1992. Improved handling of experimental rhesus monkeys. In The Inevitable BondDavis H, Balfour AD (eds), 171-177. Cambridge University Press, Cambridge, UKhttp://www.awionline.org/Lab_animals/biblio/bond.htmThe significant increase of serum cortisol concentration associated with involuntary manual ormechanical restraint during venipuncture was absent in females who were trained to voluntarilycooperate during the procedure.Schnell CR, Gerber P 1997. Training and remote monitoring of cardiovascular parameters innon-human primates. Primate Report 49, 61-70http://www.awionline.org/Lab_animals/biblio/pr49-6~1.htm"We could prove that marmosets can be trained to participate willingly in cage restraint and tourine sampling by the use of appropriate (banana milk-shake) rewards. Under this prospect, theyshowed no behavioral and cardiovascular signs of distress." The "training of non-humanprimates to handling and experimental procedure will reduce the variance and increase thesignificant level of observed changes, allows the measurement of normal physiologicalparameters and finally reduces the number of animals used in an experiment."Smith CC, Ansevin A 1957. Blood pressure of the normal rhesus monkey. Proceedings of theSociety for Experimental Biology and Medicine 96, 428-432"Most [single-housed] monkeys could be trained to sit quietly" during blood pressuremeasurements. "The procedure used in handling the monkeys was an important factor insecuring reproducible blood pressure measurement."

56Smith M, Barley J, Down N, Francis R, Feurtado M, Kerwin A, Patterson-Kane E, Sherwin C,Reinhardt V 2005. Catching animals who have escaped from their primary enclosure: Adiscussion by the Laboratory Animal Refinement & Enrichment Forum. Animal Technology andWelfare 4(1), 41-44http://www.awionline.org/Lab_animals/biblio/atw4.html"Capturing rodents, nonhuman primates and birds who have escaped from their primaryenclosure does not need to be a chaotic event and does not necessitate the use of stress-inducing,possibly injurious methods in most cases. The application of basic ethological principles pluscompassion can make a big difference, turning the recapture procedure into a harmless eventboth for the escapee and for the personnel."Tiefenbacher S, Lee B, Meyer JS, Spealman RD 2003. Noninvasive technique for the repeatedsampling of salivary free cortisol in awake, unrestrained squirrel monkeys. American Journal ofPrimatology 60, 69-75”Individually housed adult male squirrel monkeys were trained to chew on dental rope attachedto a pole, from which saliva was extracted by centrifugation and analyzed for cortisol. .. Eight ofnine monkeys readily acquired the task, reliably providing adequate saliva samples for theassay. .. The described sampling technique provides a reliable and sensitive means for repeatedmeasurement of HPA activity in unrestrained, awake squirrel monkeys.“Schwindaman D 1991. The 1985 animal welfare act amendments. In Through the Looking GlassNovak MA, Petto AJ (eds), 26-32. American Psychological Association, Washington, DC“To reduce the stress and pain of laboratory animals, nontraumatic restraining techniques mustbe taught. ... We believe that teaching of procedural skills is crucial for maintaining highresearch standards within the laboratory.”Wall HS, Worthman C, Else JG 1985. Effects of ketamine anaesthesia, stress and repeatedbleeding on the haematology of vervet monkeys. Laboratory Animals 19, 138-144"10 adult [single-housed] non-pregnant females were trained to present a limb for unstressedsampling."(8) Treatment of Animals in their Home EnclosureNelms R, Davis BK, Tansey G, Raber JM 2001. Utilization of training techniques to minimizedistress and facilitate the treatment of a chronically ill macaque. AALAS 52nd National MeetingOfficial Program, 97-98 (Abstract)"In order to permit the more frequent measurement of blood glucose, at times up to eightmeasurements a day, with minimal or no distress to the animal, we trained the monkey [longtailedmacaque with unspecified gender] to voluntarily present the hand and accept a finger stickfor the collection of blood."Reinhardt V, Cowley D, Scheffler J, Vertein R, Wegner F 1990. Cortisol response of femalerhesus monkeys to venipuncture in homecage versus venipuncture in restraint apparatus. Journalof Medical Primatology 19, 601-606http://www.awionline.org/Lab_animals/biblio/jmp19.htmIn monkeys venipunctured in the restraint apparatus, cortisol concentrations were on average50% higher 15 minutes after venipuncture (p0.1).

57Reinhardt V, Cowley D, Eisele S, Scheffler J 1991. Avoiding undue cortisol responses tovenipuncture in adult male rhesus macaques. Animal Technology 42, 83-86http://www.awionline.org/Lab_animals/biblio/at83.htmSix adult males were: a) habituated to actively cooperate during venipuncture in a treatmentcage, and b) trained to actively cooperate during venipuncture in the homecage. The magnitudeof cortisol increase was significant when the males were venipunctured in the hallways but notwhen they were venipunctured in the homecage. "It was concluded that venipuncture per se wasnot a physiologically distressing event. It became distressing only when it was associated with atemporary removal from the homecage."Reinhardt V, Cowley D 1992. In-homecage blood collection from conscious stumptailedmacaques. Animal Welfare 1, 249-255http://www.awionline.org/Lab_animals/biblio/aw1blood.htmBlood collection of trained animals was not accompanied by an increase in serum cortisolconcentration.Thomsen R, Voigt CC 2006. Non-invasive blood sampling from primates using laboratory-bredblood-sucking bugs (Dipetalogaster maximus; Reduviidae, Heteroptera). Primates, 397-400"Primates are easily stressed by the conventional veterinary blood sampling routine andconsequently, measured blood parameters may be biased. In this study, we tested blood-suckingbugs (Dipetalogaster maximus) on one lemur and two ape species (Microcebus murinus, Pongoabelii, Pan paniscus) as an alternative, non-invasive technique for bleeding primates. Withintime periods of between 6 and 62 min we obtained blood volumes of 0.01-2.4 ml in 11 out of 12trials from all three species. Therefore, we conclude that these bugs represent a new, gentle andeffective tool for bleeding captive primates without stress."(9) Cage ArrangementReinhardt V 1997. Lighting conditions for laboratory monkeys: Are they adequate? AnimalWelfare Information Center Newsletter 8(2), 3-6http://www.nal.usda.gov/awic/newsletters/v8n2/8n2reinh.htm"The prevailing monkey cage arrangement makes adequate, that is uniform, illuminationimpossible, because the cages of upper-rows block the light from entering the cages of lowerrows.Caging all animals at the same level of the room is the only solution to the problem ofuneven lighting conditions."United States Department of Agriculture 1991. Title 9, CFR (Code of Federal Register), Part 3.Animal Welfare; Standards; Final Rule. Federal Register 56(32), 6426-6505http://www.nal.usda.gov/awic/legislat/awadog.htm“Lighting must be uniformly diffused throughout animal facilities and provide sufficientillumination to aid in maintaining good housekeeping practices, adequate cleaning, adequateinspection of animals, and for the well-being of animals.”

Environmental Enrichment58(1) DefinitionEnvironmental enrichment is the provision of stimuli that promote the expression of speciesappropriatebehavioral and mental activities.Bayne K 2000. Laboratory animal enrichment. In The IACUC (Institutional Animal Care andUse Committee) Handbook Silverman J, Suckow MA, Murthy S (eds), 465-480. CRC Press,New York, NY“Environmental enrichment is an environment in which complex stimuli are provided to alleviatethe occurrence of abnormal behaviors."United States Department of Agriculture 1991. Title 9, CFR (Code of Federal Register), Part 3.Animal Welfare; Standards; Final Rule. Federal Register 56(32), 6426-6505http://www.nal.usda.gov/awic/legislat/awadog.htm"The physical environment in the primary enclosures must be enriched by providing means ofexpressing noninjurious species-typical activities. .. Examples of environmental enrichmentinclude providing perches, swings, mirrors, and other increased cage complexities; providingobjects to manipulate; varied food items; using foraging or task-oriented feeding methods; andproviding interaction with the care giver or other familiar and knowledgeable person consistentwith personnel safety precautions."(2) Promoting Social BehaviorCanadian Council on Animal Care, Olfert ED, Cross BM, McWilliam AA 1993. Guide to theCare and Use of Experimental Animals, Volume 1, 2nd Edition. Canadian Council on AnimalCare, Ottawa, ONhttp://www.ccac.ca/en/CCAC_Programs/Guidelines_Policies/GUIDES/ENGLISH/toc_v1.htm"The social needs of animals used in research, teaching, or testing, should be given equalconsideration with environmental factors such as lighting, heating, ventilations andcontainment.. Particularly in the case of singly housed animals, daily observation provides analternative from of social contact .. and commonly facilitates handling .. Most animals shouldnot be housed singly unless required by medical condition, aggression, or dictates of the study.Singly housed animals should have some degree of social contact with others of their own kind.... In the interest of well-being, a social environment is desired for each animal which will allowbasic social contacts and positive social relationships. Social behaviour assists animals to copewith circumstances of confinement."European Commission 2002. The Welfare of Non-human Primates - Report of the ScientificCommitte on Animal Health and Animal Welfare. European Commission, Strasbourg, Francehttp://europa.eu.int/comm/food/fs/sc/scah/out83_en.pdf"Primates should not be housed singly unless fully justified by health considerations (for theanimal and human handler) or research procedures, as advised following an ethical reviewprocess. If primates have to be singly housed, the animals should have visual, olfactory andautitory contact with conspecifics.”

59European Economic Community 1986. Council Directive 86/609, Annex II Guidelines forAccommodation and Care of Animals. Official Journal of the European Communities L358, 7-28http://www.uku.fi/laitokset/vkek/Sopimus/convention.html“The performance of an animal during an experiment depends very much on its confidence inman, something which has to be developed. ... It is therefore recommended that frequent contactshould be maintained so that the animals become familiar with human presence and activity.Where appropriate, time should be set aside for talking, handling and grooming.”International Primatological Society 1993. IPS International guidelines for the acquisition, careand breeding of nonhuman primates, Codes of Practice 1-3. Primate Report 35, 3-29http://pin.primate.wisc.edu/ips/codes.txt“A compatible conspecific probably provides more appropriate stimulation ...than any otherpotential environmental enrichment factor.”National Research Council 1996. Guide for the Care and Use of Laboratory Animals NationalAcademy Press, Washington, DChttp://www.nap.edu/books/0309053773/html/“Animals should be housed with the goal of maximizing species-specific behaviors andminimizing stress-induced behaviors. For social species, this normally requires housing incompatible pairs or groups.”National Research Council 1998. The Psychological Well-Being of Nonhuman PrimatesNational Academy Press, Washington, DChttp://fermat.nap.edu/books/0309052335/html/index.html"Social interactions are considered to be one of the most important factors influencing thepsychological well-being of most nonhuman primates. ... The common practice of housing rhesusmonkeys singly calls for special attention [p. 99] ... Every effort should be made to house these[singly caged] animals socially (in groups or pairs), but when this is not possible, the need forsingle housing should be documented by investigators and approved by the IACUC. ... Theanimal technician's and caregiver's roles are pivotal to the social support of primates,particularly animals that are singly caged.”United States Department of Agriculture 1991. Title 9, CFR (Code of Federal Register), Part 3.Animal Welfare; Standards; Final Rule. Federal Register 56(32), 6426-6505http://www.nal.usda.gov/awic/legislat/awadog.htmThe environmental enhancement plan "must include specific provisions to address the socialneeds of nonhuman primates of species known to exist in social groups in nature. ... Examples ofenvironmental enrichment include ... providing interaction with the care giver or other familiarand knowledgeable person consistent with personnel safety precautions.”(2,1,a) Group-housing: Practical IssuesAlford PL, Bloomsmith MA, Keeling ME, Beck TF 1995. Wounding aggression during theformation and maintenance of captive, multimale chimpanzee groups. Zoo Biology 14, 347-359"There is more wounding and more severe wounding in groups composed of older, sociallyexperienced males than in groups composed of younger socially inexperienced males, many ofwhom also had extensive visual exposure to one another before grouping."

60Baker KC, Seres M, Aureli F, de Waal FBM 2000. Injury risks among chimpanzees in threehousing conditions. American Journal of Primatology 51, 161-175"Over a two-year period all visible injuries to 46 adult males, 64 adult females, and 25 immaturechimpanzees were recorded. ... Housing included ... groups of up to 12 individuals, and smallerindoor-outdoor runs for pairs and trios. ... Compound-housed chimpanzees incurred the highestlevel of minor wounding, but serious wounding levels were not affected by housing condition. ...Overall, this study indicates that maintaining chimpanzees in pairs and trios would not be aneffective means for reducing injuries. The management of wounding in chimpanzee colonies isinfluenced more by the sex and rearing composition of a colony."Bellinger LL, Hill EG, Wiggs RB 1992. Inexpensive modifications to nonhuman primate cagesthat allow social grouping. Contemporary Topics in Laboratory Animal Science 31(3), 10-12"These two design modifications [PVC tunnels and stainless steel tunnels connecting twoadjacent cages] allow us to inexpensively modify existing caging to meet the USDA regulationsof social grouping."Bernstein IS 1989. Breeding colonies and psychological well-being. American Journal ofPrimatology 19 (Supplement), 31-36Valuable discussion of relatively safe group-housing management practices.Bloomsmith MA 1989. Interaction between adult male and immature captive chimpanzees:Implications for housing chimpanzees. American Journal of Primatology 19(Supplement), 93-99"These observations suggest that captive adult male chimpanzees have the potential to developaffiliative relationships with immature conspecifics. Housing adult males in groups along withinfants may be an important way of increasing the social complexity of the males' environments."Boyce WT, O'Neill-Wagner PL, Price CS, Haines MC, Suomi SJ 1998. Crowding stress andviolent injuries among behaviorally inhibited rhesus macaques. Health Psychology 17, 285-289A rhesus group of 36 animals was kept during 6 'warm' months in a large outdoor enclosure,during 6 'cold' months confined in a building. "During the 6-month period of confinement stress,a fivefold acceleration in [medically-attended] injury incidence was found."Catlow G, Ryan PM, Young RJ 1998. Please don't touch, we're being enriched! In Proceedingsof the 3rd International Conference on Environmental Enrichment Hare VJ, Worley E (eds), 209-217. Shape of Enrichment, San Diego, CA“Non-interference in their social lives is an important form of environmental enrichment.”Rather than locking the chimpanzees into their indoor cages every evening, an average of 17hours a day the animals were given continuous access to their whole area and to each other.“The males became more tolerant towards one another, and started to socialise as a unit. ... Farmore normal behaviours are present and the afternoon tension for both animal and keeper hasceased."Caws C, Aureli F 2001. Coping with short-tem space restriction in chimpanzees. Primate Eye 74,9http://www.psgb.org/Meetings/Spring2001.html"During the indoor period the chimpanzees showed no increase in aggression, grooming, andsubmissive greeting, nor changed their proximity to adult males. However, the percentage ofaggressive events that involved more than 2 individuals was significantly lower during theindoor period. In addition, 36 dyads were identified as “highly aggressive” during the controlperiod; aggression was reduced in these dyads during the indoor period. These results confirm

61previous evidence that chimpanzees do not increase aggression during space restriction.Furthermore, they seem to inhibit aggression by not joining ongoing conflicts and by selectivelydecreasing the targeting of common ‘victims’."Dazey J, Kuyk K, Oswald M, Marenson J, Erwin J 1977. Effects of group composition onagonistic behavior of captive pigtailed macaques (Macaca nemestrina). American Journal ofPhysical Anthropology 46, 73-76Females showed significantly less aggression in the presence of adult males [one male pergroup] than they did in female-only groups.Elton RH 1979. Baboon behavior under crowded conditions. In Captivity and Behavior Erwin J,Maple T, Mitchell G (ed), 125-139. Van Nostrand Reinhold, New York, NYCrowding produced sharp increases in aggression, noticeable increase in tension and generalactivity. ”Social disintegration [e.g., vicious aggression, social withdrawal accompanied by selfdirectedbehaviors], as well as individual pathology [e.g., "pulling of hair out of other animals(by the handful) and eating it"; chewing fingers], was the end result of the crowding in thisgroup of baboons.“Erwin J 1977. Factors influencing aggressive behavior and risk of trauma in the pigtail macaque(Macaca nemestrina). Laboratory Animal Science 27, 541-547"Provision of cover reduced aggression among members of stable groups.”Erwin J 1979. Aggression in captive macaques: Interaction of social and spacial factors. InCaptivity and Behavior Erwin J, Maple T, Mitchell G (eds), 139-171. Van Nostrand, New York,NYProviding a male-dominated group access to two rooms rather than one allowed some animalsto be out of the dominant male's sight. Loss of the male's control over his group resulted in adramatic increase in aggression among the females.Ha JC, Robinette RL, Sackett GP 1999. Social housing and pregnancy outcome in captivepigtailed macaques. American Journal of Primatology 47, 153-163"A greater number of moves decreased the probability of a viable birth and increased gestationlength and the need for clinical treatment of the dam, while increased group size decreasedgestation length. Increased moves and group size may increase stress by continuously shufflingsocial relationships, keeping females from establishing social hierarchies, and reducing groupstability. Low group stability may increase aggression by making females more likely to attackother females without knowing the opponent's social position or physical abilities."Hartner MK, Hall J, Penderhest J, Clark LP 2001. Group-housing subadult male cynomolgusmacaques in a pharmaceutical environment. Lab Animal 30(8), 53-57A carefully designed, successful group-formation and group-housing protocol of five 3.5+ yearsold previously single-caged cynos is described in detail. "Not only can the social complexity ofthe animals' interactions be increased, but also routine tasks can be accomplished with ease. Theanimals are easy to handle, restrain, and chair train, and they readily accept biomedicalresearch project requirements. ... Through the maintenance of touch gates and constant visualcontact during the study [requiring single-housing for over a month], we were able to regroupthe animals [without accidents] within 24 hours. .. Since we began the program, the animalshave transitioned through puberty and subadult stages .. and are now cohabitating as adults."

62Judge PG, de Waal BM, Paul KS, Gordon TP 1994. Removal of a trauma-inflicting alphamatriline from a group of rhesus macaques to control severe wounding. Laboratory AnimalScience 44, 344-350"Results identify an unusual outbreak of serious wounding by the alpha matriline of a largecaptive group [of rhesus macaques] and indicate that identification and removal of the animalsresponsible can be an effective management procedure for controlling such injuries.“Judge P, Griffaton N, Fincke A 2001. No effect of acute crowding on the behavior of hamadryasbaboons (Papio hamadryas). American Journal of Primatology 54(Supplement), 68-69 (Abstract)Aggressive, submissive, affiliative and self-directed responses of the six adults - two males andfour females - were recorded in their small indoor quarters versus large outdoor section of theirenclosure. Agonistic behavior, and "scratching, an indicator of anxiety in primates, did notincrease during crowding. .. Perhaps male hamadryas baboons exert such a controllinginfluence that conflict management among the other group members is unnecessary duringcrowding."Kaplan JR, Manning P, Zucker E 1980. Reduction of mortality due to fighting in a colony ofrhesus monkeys (Macaca mulatta). Laboratory Animal Science 30, 565-570"Mortality resulting from fighting [17 deaths per 100 females per year] in a breeding colony ofrhesus monkeys living in groups was an important management problem. It was found that thecause of the fighting was the social disruption resulting from a breeding protocol which requiredthe regular removal of pregnant animals from groups and introduction of nonpregnant females."Maninger N, Kim JH, Ruppenthal GC 1998. The presence of visual barriers decreases agonismin group housed pigtail macaques (Macaca nemestrina). American Journal of Primatology 45,193-194"Instances of bite, grab and chase were found to be significantly greater [among members ofharem groups] when visual barriers were absent compared to when they were present."O'Neill-Wagner PL 1996. Facilitating social harmony in a primate group. American Zoo andAquarium Association Regional Conference Proceedings, 323-325"Installing an inexpensive electric net fencing system offered safe and innovative separation totwo groups of monkeys in the field enclosure. Animals with incentive to transfer between areassuccessfully penetrated the electric net fence by leaping over it, or darting through the meshopenings at the risk of being zapped by a pulsating (high voltage, low amperage) electric shock.This challenging, yet penetrable fence was functional to monkeys in the following ways. Thesocially evicted males were able to leave their natal group when the time was approaching.When responses by animals on the other side of the fence indicated that it was safe to return,they would do so. This system functions in a positive way by providing evidence of tensionbetween and within groups, offering escape routes during aggressive interactions, [and]reducing the potential for injuries."Porton I, White M 1996. Managing an all-male group of gorillas: Eight years of experience at theSt. Louis Zoological Park. American Zoo and Aquarium Association Regional ConferenceProceedings, 720-728"Our experience suggests that a gorilla bachelor group is a viable and indeed a desirablealternative to solitary housing of 'emigrated' captive males."

63Reinhardt V, Reinhardt A, Houser WD 1986. Hair pulling-and-eating in captive rhesus monkeys.Folia Primatologica 47, 158-164http://www.awionline.org/Lab_animals/biblio/pr14-1.htmIt was concluded that hair pulling and eating is an aggressive behavioral disorder reflectingadjustment problems to a stressful [group-housing] environment.Reinhardt V, Reinhardt A, Eisele S, Houser WD, Wolf J 1987. Control of excessive aggressivedisturbance in a heterogeneous troop of rhesus monkeys. Applied Animal Behaviour Science 18,371-377"Chronic harassment in a troop of rhesus monkeys was related to two animals. The carefullysupervised removal of these individuals brought harmony back into the group."Reinhardt V 1990. Catching Individual Rhesus Monkeys Living in Captive Groups (videotape).Wisconsin Regional Primate Research Center, Madison, WIA simple capture-chute design is demonstrated. Using vocal commands, a single person swiftlycatches all members of a trained rhesus breeding group one-by-one in a transport box withoutcausing any disturbance.Reinhardt V 1993. Nonspecific diarrhea in the alpha-male of a breeding troop: A case report.Laboratory Primate Newsletter 32(1), 4http://www.brown.edu/Research/Primate/lpn32-1.html#poop"Bob's prompt recovery from intractable diarrhea upon being removed from his troop suggeststhat asserting his role as alpha-animal constituted a chronic social challenge that may havealtered his resistance to facultative pathogens and/or autonomic neural tone, to producediarrhea."Rolland RM 1991. A prescription for psychological well-being. In Through the Looking GlassNovak MA, Petto AJ (eds), 129-134. American Psychological Association, Washington, DC"By far the most common physical problem that I treat as clinical veterinarian is traumasustained by macaques in group-housing situations."White G, Hill W, Speigel G, Valentine B, Weigant J, Wallis J 2000. Conversion of canine runsto group social housing for juvenile baboons. AALAS 51st National Meeting Official Program,126 (Abstract)"Our Division recently converted two rooms equipped with 10 stainless steel, elevated floorcanine runs into rooms providing social housing for young baboons. The detachable walls wereremoved to create larger primary enclosures and tops were fitted with stainless steel panels toprovide complete containment.”Wolfensohn S, Peters A 2005. Refinement of neuroscience procedures using non humanprimates. Animal Technology and Welfare 4, 49-50It is demonstrated that long-tailed macaques with cranial implants can be group-housed withoutundue risk. "Contrary to initial expectations we have not found any increased incidence ininfection due to the presence of other animals or foraging substrate."

(2,1,b) Group-housing: Group Formation/Introduction/Integration64Baboons (Papio spp.)Else JG, Tarara R, Suleman MA, Eley RM 1986. Enclosure design and reproductive success ofbaboons used for reproductive research in Kenya. Laboratory Animal Science 36, 168-172"The [75] females were introduced first to the cage and given an opportunity to stabilize. The [6]males, whose canine teeth had been cut, were paired for at least one week prior to placementwith females. Eight animals were removed within the first month due to fight wounds and generalincompatibility.”Wallis J, Hartley D 2001. Comparing two methods of forming large social groups of captivebaboons (Papio spp.). American Journal of Primatology 54(Supplement), 54-55 (Abstract)The formation of a large group of previously singly caged baboons [unspecified sex] was mostsuccessfully accomplished gradually, by first allowing individuals to live in small groups.Capuchin monkeys (Cebus apella)Bayne K, Dexter SL, Suomi SJ 1991. Social housing ameliorates behavioral pathology in Cebusapella. Laboratory Primate Newsletter 30(2), 9-12http://www.brown.edu/Research/Primate/lpn30-2.html#bayneNo serious aggression was associated with group formation of two females and four males.Cooper MA, Thompson RK, Bernstein IS, de Waal FBM 1997. The integration of stranger malesinto a group of tufted capuchin monkeys (Cebus apella). American Journal of Primatology 42,10 (Abstract)"The introductions were noteworthy for their early lack of both aggression and affiliation.Unlike the macaque model, in which aggression occurs immediately and relationships are settledquickly, the social integration of male capuchins was a gradual process."Fragaszy D, Baer J, Adams-Curtis L 1994. Introduction and integration of strangers into captivegroups of tufted capuchins (Cebus apella). International Journal of Primatology 15, 399-420"Two to four unfamiliar animals were housed together for 3-5 days in one room of each residentgroup's two-room cage, while the resident group remained in the other room. Following theacclimation period, we permitted the resident group to mix with the newcomers in the full cage.No morbidity from aggression occurred at the time of introductions or during several monthsfollowing. Introductions of adult females can be carried out with acceptable risk to thenewcomers provided that careful monitoring occurs, so that the onset of severe aggressioninstigated by resident females toward new females can be avoided [by temporarily dividing thegroup for a few days]; juveniles can be introduced with minimal risk, and adult males can beintroduced into groups lacking resident adult males with minimal risk."Wolff A, Ruppert G 1991. A practical assessment of a non-human primate exercise program.Lab Animal 20(2), 36-39Five females and three males were transferred once a week to an exercise pen for several hours.Aggressive interactions were never observed throughout a 9-week study period.

Chimpanzees (Pan spp.)65Bloomsmith MA, Lambeth SP 1996. Managing aggression in multi-male, multi-femalechimpanzee groups. American Zoo and Aquarium Association Regional ConferenceProceedings, 449-452"We found that wounding aggression was minimal during introductions of females to males orother females, and during male-male introductions of formerly single-caged adolescent andyoung adult males having long-term prior visual familiarity. Serious wounding occurred duringmale-male introductions, particularly when there were major discrepancies in their ages andsocial experience.”Bloomsmith MA, Baker KC, Ross SK, Lambeth SP 1998. Enlarging chimpanzee social groups:The behavioral course of introductions. American Journal of Primatology 45, 171 (Abstract)New group members were introduced behind mesh. Subsequent full physical contact did notfurther increase agonism. All 42 introductions of chimpanzees in already established groupswere successful.Fritz J, Howell S 2001. Captive chimpanzee social group formation. In Special Topics inPrimatology Volume 2 Brent L (ed.), 172-203. The American Society of Primatologists, SanAntonio, TX"Forming new social groups of captive chimpanzees requires appropriate facilities, aknowledgeable staff, planning, and careful observations." A well-tested socialization system isreviewed which "includes a gradual acclimation of unfamiliar chimpanzees and introductions ina controlled setting. The process has been used to form hundreds of different social groupswithout serious injuries.... Most of our 35 males live in one of seven all-male groups. While thereis considerable potential for male-male aggression among adults, we have found males to bequite social and, in most cases, able to live compatibly with other males. We developed thissocial group strategy to provide males with increased opportunities to form strong social bondswith other males as is common among wild chimpanzees and as a management technique toprevent pregnancy." The authors share extremely valuable first-hand experiences and outlinepractical recommendations for the careful establishment of new social units without undue riskof stress, distress and injury.Hartner MK, Hall J, Penderhest J, Clark LP 2001. Group-housing subadult male cynomolgusmacaques in a pharmaceutical environment. Lab Animal 30(8), 53-57A carefully designed, successful group-formation protocol of five 3.5+ years old previouslysingle-caged male long-tailed macaques is described in detail.McDonald S 1994. The Detroit Zoo Chimpanzees Pan troglodytes: exhibit design, groupcomposition and the process of group formation. International Zoo Yearbook 33, 235-247"All adults were introduced to each other first through mesh and then physically. Before allphysical introductions, the chimpanzees involved were fed double their normal morning rationsand then fed a single ration ten minutes prior to the start of the introduction. Play items werescattered throughout the day room. ... Following the dyadic/triadic introductions, an adultfemale group was formed and the [two] males were added later. All 11 Chimpanzees weresuccessfully integrated into one social group.”

66McNary JK 1992. Integration of chimpanzees (Pan troglodytes) in captivity. In The Care andManagement of Chimpanzees (Pan troglodytes) in Captive Environments Fulk R, Garland C(eds), 88-100. North Carolina Zool Society, Asheboro, NCClear recommendation of how to introduce new chimpanzees to a core group and how to form anew group.Pazol K, McDonald S, Baker K, Smuts B 1998. Placing hand-reared chimpanzees (Pantroglodytes) into adult social groups: A technique for facilitating group integration. LaboratoryPrimate Newsletter 37(3), 11-13http://www.brown.edu/Research/Primate/lpn37-3.html#smuts"This study suggests that prior housing with socially experienced adult females can facilitate theintegration of hand-reared infants into naturalistic social groups."Gorillas (Gorilla spp.)Catlow G 1990. Introducing Killa-Killa. Gorilla Gazette 4(1), 8-10The successful introduction procedure of an adult female to a group of two adult females andone adult male gorilla is described in detail.Chatfield JJ 1990. Notes on the introduction of an aggressive male gorilla at the Los AngelesZoo. Proceedings of the Columbus Zoo Gorilla Workshop, 2-4The integration of a conspicuously aggressive adult gorilla into an established group of younganimals plus one adult female is described. "The introduction took close to two years and lots ofpatience and effort. The end result proved that is was all worthwhile and certainly the risks [bitewound inflicted on the adult female requiring surgery] were justified." The male was toleranttoward the young animals.Downman M 1998. The formation of a bachelor group of gorillas at Loro Parque. InternationalZoo News 45, 208-211http://www.awionline.org/Lab_animals/biblio/izn-dow.htmSuccessful bachelor group formation protocol is described.Enciso AE, Calcagno JM, Gold KC 1999. Social interactions between captive adult male andinfant lowland gorillas: Implications regarding kin selection and zoo management. Zoo Biology18, 53-62“Infants may be introduced into non-natal groups without being attacked or physically harmedby dominant males, but their subsequent relationships with these males may lack the close,affiliative interactions that enhance infant social development.”Jendry C 1989. Gorilla introductions. Gorilla Gazette 3(3), 5-6A well-tested introduction protocol is outlined step-by-step.Johnstone-Scott R 1992. The integration of Julia. International Zoo News 39(6), 18-26http://www.awionline.org/Lab_animals/biblio/izn-joh.htmSuccessful integration of an adult female gorilla into an established breeding group is described.McCann CM, Rothman JM 1999. Changes in nearest-neighbor association in a captive group ofWestern Lowland gorillas after the introduction of five hand-reared infants. Zoo Biology 18,261-278

67The integration of five hand-reared infants into a group of 5 females and 1 male was successfuland without incident. "Findings lend strong support to the importance of peer groups and thepresence of a silverback male for facilitating the integration of hand-reared infants intoestablished groups.”Meder A 1985. Integration of hand-reared gorilla infants in a group. Zoo Biology 4, 1-12Zoo-born gorilla infants "could best be introduced into a group when about 1.5 to 2 years old;when younger or older, social integration becomes more difficult. An introduction to adultfemales in a small cage until strong social relations are formed leads to a smoother socialintegration in the whole group afterward and takes less time than socializing the infants tojuveniles. Allowing the infants to explore the group's main enclosure alone and before they jointhe group permanently leads to better spacial orientation for them and helps to lessen theiruneasiness in the new social situation. Providing the infants with a shelter within the group'senclosure, which gives them access to the group but is inaccessible to the adults, reduces tensionand thus aggression toward them.”Winslow S, Ogden J. J., Maple TL 1990. Socialization of an adult male lowland gorilla (Gorillagorilla gorilla). Proceedings of the Columbus Zoo Gorilla Workshop, 195-204Successful group formation process of an adult male, an adult female, and a juvenile female isoutlined.Macaques (Macaca spp.)Asvestas C, Reininger M 1999. Forming a bachelor group of long-tailed macaques (Macacafascicularis). Laboratory Primate Newsletter 38(3), 14http://www.brown.edu/Research/Primate/lpn38-3.html#groupThe careful establishment of a compatible group of 24 male long-tailed macaques is described."The worst injuries were a split lip and a bite to the leg, both of which healed up quickly.”Bernstein IS, Gordon TP 1977. Behavioral research in breeding colonies of Old World monkeys.Laboratory Animal Science 27, 532-540“The simultaneous release of all animals has proven to produce the fewest injuries and the mostrapid social integration. The addition of individuals to such a colony results in the mobbing ofadults, often with severe consequences. Once a group is established, one should avoid addinganimals no matter how desirable this might appear. If new groups are to be established, it is farless damaging to the stability of the colony to divide a group along matrilineal lines than toremove any particular age class.”Clarke AS, Czekala NM, Lindburg DG 1995. Behavioral and adrenocortical responses of malecynomolgus and lion-tailed macaques to social stimulation and group formation. Primates 36,41-46"Males were exposed to a mirror, then visually exposed to conspecific neighbors in all pairwisecombinations, and then formed into conspecific groups [of 3 animals each]. Following groupformation [urinary] cortisol values showed a decreasing trend in the cynomolgus, but not in thelion-tails. The cynomolgus rapidly adapted to group living and relations between them wereprimarily affiliative. In contrast, no affiliative behavior was ever observed in the lion-tail group,which appeared to be highly stressed by group living and was eventually disbanded.“

68Clarke MR, Blanchard JL 1994. All-male social group formation: Does cutting canine teethpromote social integration? Laboratory Primate Newsletter 33(2), 5-8http://www.brown.edu/Research/Primate/lpn33-2.html#clarkeGroups of rhesus males were formed by releasing future group members in same enclosure.Within the first five months one of 26 animals died and two were killed due to trauma resultingfrom fighting.Good GP, Sassenrath EN 1980. Persistent adrenocortical activation in female rhesus monkeysafter new breeding group formation. Journal of Medical Primatology 9, 325-334"Persistent elevated adrenocortical responsiveness to ACTH has been demonstrated in femalerhesus monkeys as long as 13 weeks after relocation into new single male breeding groups.”Gust DA, Gordon TP, Wilson ME, Brodie AR, Ahmed-Ansari A, McClure HM 1991. Formationof a new social group of unfamiliar female rhesus monkeys affects the immune and pituitaryadrenocortical systems. Brain, Behavior, and Immunity 5, 296-307Eight females were introduced. “Dominance rank was established within 48 h by noncontactthreats and chases and was unchanged throughout the study. Only two minor wounds wererecorded." The animals showed physiological stress responses during the first 9 weeks aftergroup formation.Jensen GD, Blanton FL, Gribble DH 1980. Older monkeys' (Macaca radiata) response to newgroup formation: Behavior, reproduction and mortality. Experimental Gerontology 15, 399-406"A group of younger bonnets (5 males and 33 females under 10 yrs of age) suffered 11%mortality in the first three months after new group formation, the death all due to trauma.”Kessler MJ, London WT, Rawlins RG, Gonzales J, Martines HS, Sanches J 1985. Managementof a harem breeding colony of rhesus monkeys to reduce trauma-related morbidity and mortality.Journal of Medical Primatology 13, 91-98Mortality rates per year were reduced from 13.4% to 3.5% "when monkeys were maintained inpermanent harems to which returning females were reintroduced compared to new social groupsformed from aggregates of unfamiliar animals."Line SW, Morgan KN, Roberts JA, Markowitz H 1990. Preliminary comments on resocializationof aged macaques. Laboratory Primate Newsletter 29(1), 8-12http://www.brown.edu/Research/Primate/lpn29-1.html#lineEach rhesus monkey [6 males and 7 females] was introduced to group members in a series ofbrief pair tests. The incidence of serious injury was 62% including one fatality.Meshik VA 1994. Group formation in adult Japanese macaques. International Zoo News 41(3),5-9http://www.awionline.org/Lab_animals/biblio/izn-mes.htm"Starting with submissive animals, individuals from the first group [2 females and 1 male] wereintroduced step by step to the second [resident] group [3 females and 1 male]. A new group wassuccessfully formed without severe fighting. There were practically no aggressive acts."Reinhardt V 1991. Group formation of previously single-caged adult rhesus macaques for thepurpose of environmental enrichment. Journal of Experimental Animal Science 34, 110-115http://www.awionline.org/Lab_animals/biblio/es34-1.html

69“Future group members [same sex, 6 females and 6 males] were given ample opportunity tophysically interact with each other on a one-to-one basis and were considered ready for groupformation only when they had demonstrated compatibility and clear-cut dominancesubordinationrelationships.” Persistent aggressive interactions made it imperative to disbandboth groups shortly after group formation.Rhine RJ, Cox RL 1989 How not to enlarge a stable group of stumptailed macaques (Macacaarctoides). In Housing, Care and Psychological Well-being of Captive and Laboratory PrimatesSegal EF (ed), 255-269. Noyes Publications, Park Ridge, NJ"The best advice, based on our experience ... is to combine groups, or introduce adult animals,only as a very last resort, and then with great care and assiduous monitoring."Schapiro SJ, Lee-Parritz DE, Taylor LL, Watson L, Bloomsmith MA, Petto AJ 1994. Behavioralmanagement of specific pathogen-free rhesus macaques: Group formation, reproduction, andparental competence. Laboratory Animal Science 44, 229-234Initial group formation was amicable. “During the first breeding season, there were outbreaksof severe aggression, leading to the permanent removal of three [of seven] males and 17 [of 50]females."Stahl D, Herrmann F, Kaumanns W 2001. Group formation of a captive all-male group of liontailedmacaques (Macaca silenus). Primate Report 59, 93-108http://www.dpz.gwdg.de/pr/pr59/stahl.pdf6 adults were brought together simultaneously. They “showed no fights or other seriousaggression during the first encounter on the first day. Aggression rates were high only duringthe first hour after introduction .... Afterwards, the aggression level remained within a similarlow level ... The development of the social relationships within the first days suggests that thereis a certain degree of social compatibility between male lion-tailed macaques.. .. After four days,the zoo decided to remove Heiner from the group. The animal did not show conspiciousaggressive behaviour but it was thought that he was not compatible. .... Four weeks after thegroup establishment Nepomuk died because of a chronic, subacute gastritis. Two months later,another monkey, Smokie, died because of a bacterial infection. To prevent further risks the groupwas disbanded at the end of December 1995.“Westergaard GC, Izard MK, Drake JD, Suomi SJ, Higley JD 1999. Rhesus macaque (Macacamulatta) group formation and housing: Wounding and reproduction in a specific pathogen free(SPF) colony. American Journal of Primatology 49, 339-347Initially small groups were formed consisting of one male and up to eight females. Subsequentlylarger groups [about 3 males and 21 females] were formed by releasing group memberssimultaneously or incrementally" When forming rhesus macaque breeding groups from partialgroups and strangers, a staged group formation method leads to lower traumatic wounding ratesthan does a rapid formation method in which all individuals are put together at once. Whenforming new rhesus macaque breeding groups, divided corrals that provide for social and visualseparation of individuals lead to lower rates of traumatic wounding than do undivided corrals."Orangutans (Pongo pygmaeus)Hamburger L 1988. Introduction of two young orangutans, Pongo pygmaeus, into an establishedfamily group. International Zoo Yearbook 27, 273-278Successful re-introduction of two hand reared young orangutans into a family group isdescribed.

Watts E 1997. Introductions. In Orangutan Species Survival Plan Husbandry Manual Sodaro C(ed), 69-84. Atlanta Orangutan SSP (Species Survival Plan), Atlanta, GAGroup integration and re-introduction techniques are described and valuable recommendationsmade.Squirrel monkeys (Saimiri spp.)King JE, Norwood VR 1989. Free-environment rooms as alternative housing for squirrelmonkeys. In Housing, Care and Psychological Well-being of Captive and Laboratory PrimatesSegal EF (ed), 102-114. Noyes Publications, Park Ridge"Individual and gang cages were removed from two conventional colony rooms and the monkeys[11 females and 5 males] were simply released into the rooms. Immediately following theestablishment of these two free-environment rooms, a few monkeys incurred sprains and brokenteeth, probably resulting from falls. ... Two deaths resulted from attacks by other monkeys.”Mendoza SP 1991. Sociophysiology of well-being in nonhuman primates. Laboratory AnimalScience 41, 344-349The formation of same-sex groups “is rarely accompanied by injurious aggression. Onceunisexual groups have stabilized, formation of larger heterosexual groups generally proceedssmoothly.”Vermeer J 1997. The formation of a captive squirrel monkey group. International Zoo News 44,146-149http://www.awionline.org/Lab_animals/biblio/izn-ver.htm"It is important that all females of a new [heterosexual] group are related to each other, that is,that they come from the same natal group. The introduction of unfamiliar females to a smallgroup with several females can result in much aggression with severe injury.” The minimumnumber of breeding females in a group should be five to seven. A maximum of two adult malesshould be added to these females. Groups of up to ten males can be formed without manyproblems.Williams LE, Abee CR 1988. Aggression with mixed age-sex groups of Bolivian squirrelmonkeys following single animal introductions and new group formations. Zoo Biology 7, 139-145"When introducing new animals to an established group, the new animals should be unfamiliarwith one another so as not to form competing 'teams'. Additions to groups should include enoughanimals so that aggression from the resident group will be diffused, not concentrated on one ortwo animals." New groups should be followed for a number of hours, even after an initial declinein agonistic interactions.Vervet monkeys (Cercopithecus aethiops)Else JG 1985. Captive propagation of vervet monkeys (Cercopithecus aethiops) in harems.Laboratory Animal Science 35, 373-375Animals were placed in ten single-male harem groups. This "resulted in considerable fightingamong the females. Each group was gradually reduced over a one year period to 2-4 femaleswith their young. Three adult females died during the [three year] study. All had been underfairly continual harassment."70

(2,2,a) Pair-housing: Practical Issues, Time Budget71Baker K, Bloomsmith M, Schoof V, Neu K, Maloney M, Griffis C, Marinez M, Clay A 2005.Compairing pair-housing options for caged rhesus macaques (Macaca mulatta). AmericanJournal of Primatology 66(Supplement), 180 (Abstract)”Baseline behavioral data were collected on 20 singly-housed adult rhesus macaques, 6 malesand 14 females, all mother reared. Isosexual pairs were then formed, and pairs were housed inthree form of pair caging balanced for order (6-8 weeks per phase): FC (full contact: sharingadjacent cages), PC (protected contact: access through perforated panels), and IC (intermittentcontact: full pairings separated several days/week).“ While all forms of pair housing increasedaffiliative behavior, levels were lower in the protected contact than full contact or intermittentcontact housing condition. Levels of inactivity and anxiety-related behaviors were higher in theprotected than in the full contact or intermittent contact condition, and full contact reducedanxiety-related behaviors from baseline. Full contact and intermittent contact decreasedinactivity and increased aggression which occurred at higher level in the intermittent than in thepartial contact housing condition. Abnormal behavior was affected only in females, with adecrease from baseline only in the intermittent, and higher levels in the partial than in the fullcontact condition. ”Results suggest that periodic separation may not detract from the benefits ofpair housing for rhesus macaques, but protected contact housing may, balanced only bydecreased aggression.“Basile BM, Hampton RR, Chaudhry AM, Murray EA 2007. Presence of a privacy dividerincreases proximity in pair-housed rhesus monkeys. Animal Welfare 16(1), 37-39"We observed twenty-five pairs of rhesus macaques (Macaca mulatta) both with and without thepresence of a privacy divider. Monkeys spent significantly more time in the same half of the paircagewhen the divider was in place. Subjects were fifty adult rhesus macaque monkeys agedbetween 5 and 13 years, housed in socially compatible pairs consisting of 18 male/male pairs, 2female/female pairs, and 5 male/female pairs. We conclude that the increase in proximityassociated with the presence of the privacy dividers reflects an increase in social toleranceand/or attraction. A privacy divider may provide a safe haven and give monkeys the ability todiffuse hostile situations before they escalate."

72Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 5.1. PairFormation and Pair-Housing of Monkeys. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/soc-hous.html"The PI who does research with our pair-housed rhesus insists that cage companions beseparated during the night and on weekends, so that they cannot fight and injure each otherwhile nobody is around. I would love to keep the animals together also during the night, butcannot argue with the PI because I really don’t know if that would jeopardize the safety of theanimals. In our facility, compatible companions are allowed to remain together also during thenight, on weekends and holidays. This applies for both female and male pairs, as well as for allanimals who have head cap implants. It has never happened that we found paired animalsinjured or bruised when entering their room in the early morning. I think there is no special riskwhen pairs spend the night together without being supervised.We also keep our male and female rhesus pairs together 24/7 and encounter no problemsrelated to aggression during the night.At our facility, after pairs have been established, they are housed togetheruninterruptedly. This includes male and female isosexual pairs, and each species housed here,including rhesus, pigtails, sooty mangabeys, squirrel monkeys, chimps, and cynos. We have notnoticed that paired companions fight during the night, on weekends and holidays when nobody isaround."Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 5.3.1. Post-Operative Care. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/buffer-post-op”It is my experience with rhesus macaques that it is advisable to pair-house an animal aftersurgery as soon as possible with his or her compatible companion. We do this especially withpairs, after one of them had cranial implant surgery. It is the investigator's and my ownimpression that the animals recover better from the surgery stress when their familiarcompanion is with them than when they are alone.Close to 95 percent of our cyno population is pair-housed. The animals are subjected to alot of orthopedic procedures. There have never been problems with the re-pairing of the animalsafter surgery. We partition the pairs cage with a transparent panel, which we remove after thetreated companion has fully recovered from anesthetic effects (usually 24 hours). It has neverhappened that animals who had no surgery showed any negative behavioral reactions towardtheir temporarily probably weaker cage mates.“Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 8.9. Pair-Housed Monkeys with Head Cap Implants. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/safety.html#head-caps”Our university tries to pair all rhesus macaques regardless of cranial implants. Normally thepairs are established before they have undergone surgery for head caps, but we havesuccessfully paired primates after surgery as well. Over a period of ten years, we have had noincidents of damage to the implants. We have more problems, with coils of head caps breaking,in single-housed than in pair-housed rhesus. The head caps of pair-housed animals are cleaner— as they groom each other — than those of individually caged animals.We have ten pair-housed male rhesus and long-tailed macaques with head caps. Theanimals were 3 to 6 years old at the time of pair formation. They are presently approximately 10

73years old. Some of them had head caps before they were paired, others got them afterwards. Itdidn't seem to matter. In my experience, pair-housing does not create a risk factor when theanimals have head cap implants. In all the time I've been working with these monkeys, they'venever damaged one another's head caps.“Brent L 1992. The effects of cage size and pair housing on the behavior of captive chimpanzees.American Journal of Primatology 27, 20 (Abstract)Paired subjects spent approximately 11% of the observation time in socially directed behaviors.Coe CL, Rosenblum LA 1984 Male dominance in the bonnet macaque. In Social Cohesion.Essays Toward a Sociophysiological Perspective Barchas PR, Mendoza SP (eds), 31-64.Greenwood Press, Westport“During the first week [after formation of 5 male/male pairs], the males spent a mean 29 percentof the observation time within arm's reach, engaging in mutual grooming or passive bodycontact."Coe CL, Franklin D, Smith ER, Levine S 1982. Hormonal responses accompanying fear andagitation in the squirrel monkey. Physiology and Behavior 29, 1051-1057Dominant and subordinate partners of male pairs did not differ in their plasma cortisol levels.Crockett CM 1998. Psychological well-being of captive nonhuman primates. In Second NatureShepherdson DH, Mellen JD, Hutchins M (eds), 129-152. Smithsonian Institution Press,Washington, DC“Adult female long-tailed macaques benefit from social enrichment through pairing with otherfemales. Adult males also have social needs, although they are more likely to express themtoward females. Many males ignore or behave aggressively toward other males, although somemale pairs are highly compatible. Housing longtailed macaque males in paired caging withwidely spaced grooming-contact bars prevents aggressive pursuits and increases the successrate of male pairing."Eaton GG, Kelley ST, Axthelm MK, Iliff-Sizemore SA, Shiigi SM 1994. Psychological wellbeingin paired adult female rhesus (Macaca mulatta). American Journal of Primatology 33, 89-99Paired females spend in close proximity approximately 80% of the time during the night, and40% of the time during the day. They engage in social interactions approximately 17% of thetime. “Health measures, body weight gains, reproduction and immune responses do not differbetween dominant, subordinate, and single-housed females. Paired females spend less timeengaged in abnormal behavior than single-housed females.”Gonzalez CA, Coe CL, Levine S 1982. Cortisol responses under different housing conditions infemale squirrel monkeys. Psychoneuroendocrinology 7, 209-216Dominant and subordinate partners of female pairs did not differ in their plasma cortisol levels.Gwinn LA 1996. A method for using a pole housing apparatus to establish compatible pairsamong squirrel monkeys. Contemporary Topics in Laboratory Animal Science 35(4), 61Pair housing has not interfered with research. “During nine treatments with an identical testcompound, singly housed animals lost significantly more weight on average than did pair housedanimals."

74Hotchkiss CE, Paule MG 2003. Effect of pair housing on operant behavior task performance byrhesus monkeys. Contemporary Topics in Laboratory Animal Science 42(4), 38-40"In conclusion, pair-housing monkeys is feasible for studies involving operant behavior testingas a model for a variety of complex brain functions. However, housing condition may affect sometest parameters, and this effect must be taken into consideration during experimental design."Jackson MJ 2001. Environmental enrichment and husbandry of the MPTP-treated commonmarmoset. Animal Technology 52, 21-28"One disadvantage of isosexual pairing that we have encountered is that temporary separationof the pair (e.g. for behavioural monitoring) can precipitate fighting on re-introduction. If thisoccurs we have found that a gradual re-association process, utilising adjacent cages to permitvisual and audio contact, and supervised free running together, facilitates re-pairing."McDonald KM, Ratajeski MA 2005. Pair-housing of monkeys on behavioral studies. AALAS56th National Meeting Official Program, 133 (Abstract)"After periods of separation, we did not observe the animals to act aggressively towards oneother when re-paired, and injury to head holder implants was never observed."Murray L, Hartner M, Clark LP 2002. Enhancing postsurgical recovery of pair-housednonhuman primates (M. fascicularis). Contemporary Topics in Laboratory Animal Science41(4), 112-113 (Abstract)"In many facilities, postsurgical protocol in the nonhuman primate requires individual housingfor a period of 2-10 days. ... Our goal was to allow [15 adult females] same-day return of thepostoperative [placement of vascular access port] candidate to its paired environment. ...Change in hierarchy status, self-traumatic events, weight loss or diarrhea did not occur in any ofthese animals, and the incision sites healed unremarkably. The animals ate and drank normally,and received their postoperative treatments without problem (readily accepted oral medication)... We conclude that this practice of quick return to group status postoperatively can besuccessfully employed, and it is a "best practice" when working with these laboratory animals."Majolo B, Buchanan-Smith H 2001. Psychological wellbeing of common marmoset (Callithrixjacchus) females living in same-sex pairs. Primate Eye 74, 9-10http://www.psgb.org/Meetings/Spring2001.htmlThe behaviour of female pairs of common marmosets resembles that of females living in familygroups suggesting that this method of housing does not compromise their welfare."Reinhardt V, Cowley D, Eisele S, Vertein R, Houser WD 1988. Pairing compatible femalerhesus monkeys for the purpose of cage enrichment has no negative impact on body weight.Laboratory Primate Newsetter 27(1), 13-15http://www.brown.edu/Research/Primate/lpn27-1.html#pair“Keeping singly housed adult female rhesus monkeys in compatible pairs for the purpose of cageenrichment does not affect the animals' general health status as reflected in body weight."Reinhardt V, Dodsworth R 1989. Facilitated Socialization of Previously Single Caged AdultRhesus Macaques (videotape with accompanying text). Wisconsin Regional Primate ResearchCenter, Madison, WIThirty scenes depict different adult rhesus monkeys [and one adult, male stump-tailed macaque],each paired with a compatible companion for up to two years. The following pair combinationsand research situations are shown: adult male/male, adult female/female, adult male/juvenilemale, adult female/juvenile female; experiments requiring headcap implants, tethering, or in-

75home cage blood collection. Presenting for in-homecage injection. Paired companions interactwith each other in various species-typical ways (e.g., grooming, huddling, mounting, playing,yielding, sharing food) and make use of perches and gnawing sticks. "Representing an everychanging,yet predictable stimulus, a compatible companion does not lose its boredom-reducingvalue over time."Reinhardt V, Houser WD, Eisele S 1989. Pairing previously singly caged rhesus monkeys doesnot interfere with common research protocols. Laboratory Animal Science 39, 73-74"Our experiences indicate that facilitated socialization of previously singly caged rhesusmonkeys offers an inexpensive method of environmental enrichment that is practicable undercommon management situations and numerous research conditions."Reinhardt V 1990. Time budget of caged rhesus monkeys exposed to a companion, a PVC perchand a piece of wood for an extended time. American Journal of Primatology 20, 51-56After 1.5 years paired partners spent an average of 23.5% of the time interacting with thecompanion. Females were socially more active than males.Reinhardt V, Cowley D, Scheffler J, Vertein R 1990. Living continuously with a compatiblecompanion is not a distressing experience for rhesus monkeys. Laboratory Primate Newsletter29(2), 16-17http://www.brown.edu/Research/Primate/lpn29-2.html#rhesusPaired females had serum cortisol concentrations that did not differ from single-housed females."Dominant animals had cortisol concentrations that did not differ from those of theirsubordinate companions, indicating that neither dominant nor subordinate partners experiencedsocial distress."Reinhardt V 1991. Social enrichment for aged rhesus monkeys that have lived singly for manyyears. Animal Technology 43, 173-177http://www.awionline.org/Lab_animals/biblio/at173.htm"There is widespread concern that aged rhesus monkeys who have been housed singly for a longtime would do better living alone than sharing a cage with a companion. Ten female and fivemale rhesus monkeys, 22 to 33 years old and deprived of physical contact with any otherconspecific for more than 10 years, were socialized with weaned infants or with each other usingtwo standard methods of pairing. Pairs were compatible in every case throughout a one yearfollow-up period.”Reinhardt V, Pape R, Zweifel D 1991. Multifunctional cage for macaques housed in pairs or insmall groups. American Association for Laboratory Animal Science Bulletin 30(5), 14-15Double-cage units were modified to provide optimal housing conditions for pair-housedmacaques. Perch installation allows normal operation of the squeeze-back; a privacy paneloffers visual seclusion.Reinhardt V, Reinhardt A 1991. Impact of a privacy panel on the behavior of caged femalerhesus monkeys living in pairs. Journal of Experimental Animal Science 34, 55-58http://www.awionline.org/Lab_animals/biblio/es34-5~1.htm"Paired partners spent significantly more time in close proximity when the privacy panel wasprovided. At the same time, they were more engaged in affiliative interactions while theincidence of agonistic interactions tended to decrease."

76Reinhardt V, Hurwitz S 1993. Evaluation of social enrichment for aged rhesus macaques.Animal Technology 44, 53-57http://www.awionline.org/Lab_animals/biblio/at44.htmThe 31-36 years old "subjects preferred to stay in close proximity with their companion eventhough this reduced their available cage space. They spent on average 21% of the timeinteracting with the companion. Sharing a cage with a compatible conspecific did not jeopardizethe subjects' general health, as reflected in their body weight development."Reinhardt V 1994. Social enrichment for previously single-caged stumptail macaques. AnimalTechnology 5, 37-41http://www.awionline.org/Lab_animals/biblio/at37.htmFemale pairs and male pairs engaged in non-injurious species-typical activities 25% and 17% ofthe time.Reinhardt V 1994. Continuous pair-housing of caged Macaca mulatta: Risk evaluation.Laboratory Primate Newsletter 33(1), 1-4http://www.brown.edu/Research/Primate/lpn33-1.html#vic"Pairs were compatible in 88% of cases during the follow-up period of 1 to 6.3 years. Therewere no indications that long-term compatibility of male pairs was less than that of femalepairs.”Reinhardt V 1994. Pair-housing rather than single-housing for laboratory rhesus macaques.Journal of Medical Primatology 23, 426-431http://www.awionline.org/Lab_animals/biblio/jmp23.htmFirst-year compatibility was 88% in adult female-female pairs, 80% in adult male-male pairs.Adult-infant pairs were compatible in 92% of 15 male-infant pairs, and in 94% in 65 femaleinfantpairs. The incidence of serious injury was 0.7% (2/272) during the first year after pairformation.Reinhardt V 1996. Frequently asked questions about safe pair-housing of macaques. AnimalWelfare Information Center Newsetter 7(1), 11http://www.nal.usda.gov/awic/newsletters/v7n1/7n1reinh.htmNine frequently asked questions regarding safe pair-housing protocols for macaques areaddressed.Reinhardt V, Reinhardt V 2000. Meeting the “social space” requirements of pair-housedprimates. Laboratory Primate Newsletter 39(1), 7http://www.brown.edu/Research/Primate/lpn39-1.html#vik“Social space is the space required by a subordinate partner to buffer potential social tension,by increasing the distance to a dominant counterpart. At a minimum, pair-housed animalsshould be allocated at least twice the cage space that is legally required for single-housing.”Reinhardt V 2002. Addressing the social needs of macaques used for research. LaboratoryPrimate Newsletter 41(3), 7-10http://www.brown.edu/Research/Primate/.lpn41-3.html#vik"The present paper summarizes the author’s experiences transferring a colony of rhesusmacaques (Macaca mulatta) from individual- to pair-caging. ... The implementation of pairhousingas standard caging at Wisconsin RPRC was not excessively expensive in terms of worktime and material. It was not a hindrance to active research; rather it improved the animals’behavioral health and made them more species-representative research models. A total of 726

77pairs were formed involving 817 different animals, yet no indication was found that thisrendered research data collected from them useless due to confounding variables such as stressor disease."Roberts SJ, Platt ML 2005. Effects of isosexual pair-housing on biomedical implants and studyparticipation in male macaques. Contemporary Topics in Laboratory Animal Science 44(5), 13-18"Social housing has been shown to contribute to the psychological well-being and physicalhealth of captive primates, and this factor has led to United States Department of Agricultureguidelines requiring facilities to address the social needs of primate species known to livesocially in nature as long as doing so does not endanger the animals or interfere with researchgoals. Although pair-housing is the best way to provide social enrichment, many researchers andfacilities are hesitant to implement it, particularly in biomedical research contexts whereimplanted devices or behavioral performance might be compromised. In order to study theeffects of pair-housing on biomedical implants and study participation, we collected data from agroup of isosexually pair-housed male macaques (adult and subadult) with 1) cranial and eyeimplants and 2) controlled access to water as means of motivating subjects to participate inpsychophysical studies. Implants, study participation, and weight gain were not adverselyaffected by pair-housing. Our results support the use of pair-housing as social enrichment formacaques with biomedical implants and controlled access to water." Consistent directionaldominance behavior served to assess potential partner compatibility. Of 15 rhesus diads, 12[80%] were compatible. One cyno diad was also tested and was compatible. Compatibility wasascertained over a period of 0.8 - 3.3 years." One monkey, however, occasionally exhibitednoninjurious self-biting when someone other than his usual handler took him out of his cage, andtwo other monkeys occasionally placed in their cages when agitated."Schapiro SJ, Bloomsmith MA, Kessel AL, Shively CA 1993. Effects of enrichment and housingon cortisol response in juvenile rhesus monkeys. Applied Animal Behaviour Science 37, 251-263"Social housing condition [single vs. pair] also did not affect cortisol."Schapiro SJ, Bloomsmith MA, Porter LM, Suarez SA 1996. Enrichment effects on rhesusmonkeys successively housed singly, in pairs, and in groups. Applied Animal Behaviour Science48, 158-172"Subjects were more socially oriented when pair-housed than when living in small groups.Subjects used enrichment less frequently when housed in groups. The data suggest that thepresence of a social partner(s) led to more beneficial changes in behavior than did the provisionof inanimate enhancements.”Sheehan J, Ziegelhofer T, Henn S, Miyamoto M, Vanterpool I 2005. A novel caging method forcollecting telemetry data from pair-housed monkeys. AALAS [American Association forLaboratory Animal Science] 56th National Meeting Official Program, 117 (Abstract)Caging method is described that allows telemetric measurements [ECG and blood pressure] oflong-tailed macaques housed in pairs. "The first method consisted of modifying the current cagesto add a wire mesh tunnel constructed above the two adjacent cages, with sliding doors on eitherend so the monkeys could be intermittently paired. The second method for improvement withthese modified cages was to compare results if we permanently placed a telemetered and a nontelemeteredpair of monkeys in the cages and collected data using the distributed receiver arraywhich allows for two receivers to be configured to one animal." No differences were noted in thedata collected nor were any artifacts created by application of the second uninterrupted pairhousingmethod.

78Shively CA 2001. Psychological well-being of laboratory primates at Oregon Regional PrimateResearch Center. Web site link in Willamette Week March 21, 2001http://www.wweek.com/html2/shivreport.html"I was exposed to no protocols that required social isolation during my visit to the ORPRC.Rather, investigators were not giving priority to the social needs of the monkeys. For example,monkeys in virus studies at other institutions are housed socially with animals with similar virusload. Animals on timed mating protocol do not need to be housed alone. Animals in protocolsrequiring food restriction can be pair housed and separated from cagemates for 8 hrs during theday when food is accessible. They can be socially housed the other 16 hrs/day. ... The IACUCshould use its authority to decline approval of protocols that do not demonstrate a detaileddefense of single caging.”Yanagihara Y, Matsubayashi K, Matsuzawa T 1994. Environmental enrichment in Japanesemonkeys: Feeding device [Japanese text with English summary]. Primate Research 10, 95-104“The two monkeys spent the night in same living unit, while they spontaneously separated fromeach other in the different units during feeding time.(2,2,b) Pair-housing: Pair formationBaboons (Papio spp.)Bourgeois SR, Brent L 2005. Modifying the behaviour of singly caged baboons: evaluating theeffectiveness of four enrichment techniques. Animal Welfare 14, 71-81Seven singly caged adolescent [mean age: 4.2 years] male baboons were studied. Pairs wereformed by introducing sedated partners in the same cage. "Pairing was successful for all sevenindividuals, with no serious injuries or overt aggression observed."Jerome CP, Szostak L 1987. Environmental enrichment for adult, female baboons (Papioanubis). Laboratory Animal Science 37, 508-509"Each baboon was placed in a cage with another baboon for 3-4 hours, two or three times perweek. The same pairs consistently visited each other in either animal's cage. No significantaggression occurred.”Gorillas (Gorilla spp.)Gould JE 1990. Conspecific introduction, socialization, and attempts to breed a solitary-raised,silverback male gorilla. Proceedings of the Columbus Zoo Gorilla Workshop, 56-79“His introduction to the adult female conspecific Muke was very successful." The careful pairformation procedure is described.

Macaques (Macaca spp.)79Abney DM, Weed JL 2006. Methods for successfully pair housing adult male rhesus macaques(Macaca mulatta). American Journal of Primatology 68(Supplement), 59 (Abstract)The successful same-sex pairing of 34 male rhesus macaques is described. ”Animals weresocialized in different age combinations, consisting of adult/adult, adult/sub-adult, andadult/juvenile. .. The pairs started with a clear panel, allowing the animals to see one another,but not touch. Next, they were given a mesh panel, which allowed finger touch access.Grooming bars were the final panel used before the pair was given full, un-restricted access.Pairs were deemed successful if no serious fighting or injury occurred within one weeks time.Out of 56 rhesus socializations attempted which included at least one adult, 34 were successful(61%)."Anonymous 2006. Pair formation and reintroduction of temporarily separated partners — Adiscussion on the Laboratory Animal Refinement & Enrichment Forum. Laboratory PrimateNewsletter 45(1), 11-12http://www.brown.edu/Research/Primate/lpn45-1.html#pair"To sum up, it seems advisable to monitor the reintroduction of temporarily separated partnersvery carefully, and if possible, to allow the animals to first recognize each other before they arereunited as a pair. There is no good reason to believe that male cynos are less suitable forisosexual pair-housing than rhesus. If and how experimentally-induced pathophysiologicalprocesses affect the compatibility of pairs needs to be explored."Byrum R, St. Claire M 1998. Pairing female Macaca nemestrina. Laboratory PrimateNewslettere 37(4), 1http://www.brown.edu/Research/Primate/lpn37-4.html#byrumTwenty-four adult pig-tailed macaques were successfully transferred from single- to pairhousingarrangements following the establishment of rank relationships during a semi-contactfamiliarization period. "We have observed no serious fighting and wounding in our pairs,neither at the moment of introduction nor during follow-up observations of up to two years.”Coe CL, Rosenblum LA 1984 Male dominance in the bonnet macaque. In Social Cohesion.Essays Toward a Sociophysiological Perspective Barchas PR, Mendoza SP (eds), 31-64.Greenwood Press, Westport, CT

80“The establishment of dominance relations occurred at pair formation. The aggressive incidentswere limited, usually involving threats and pursuit behavior. .. More typically, one animalsubmitted and indicated his subordinate status through communicative gestures. In the first weekfollowing pair formation, the occurrence of aggressive behavior subsided almost entirely.”Crockett CM, Bowers CL, Bowden DM, Sackett GP 1994. Sex differences in compatibility ofpair-housed adult longtailed macaques. American Journal of Primatology 32, 73-94Newly formed pairs were separated for 17 hrs and subsequently reintroduced daily during a 23-day study. No female pair but seven [47%] male pairs were separated because of fighting andwounding.Crockett CM, Lee GH, Thom JP, Bentson KL 2005. Does temperament similarity predictcompatibility of same-sex and opposite-sex rhesus macaques paired in grooming/contact?American Journal of Primatology 66(Supplement), 58 (Abstract)Partner compatibility was not significantly associated with temperament.Doyle LA, Baker KC, Cox LD 2008. Physiological and behavioral effects of social introductionon adult male rhesus macaques. American Journal of Primatology 70, 1-9Potential partners of four adult rhesus macaque pairs were first familiarized in cages in whichpartners were separated by a panel consisting of bars spaced 2 cm apart. The eight males wereall implanted with biotelemetry devices for remote heart rate monitoring. After 24 hours, asneither persistent aggression nor wounding was observed, each pre-familiarized pair wasintroduced into full contact by removing the barred panel. All four introductions were successfuland subjects showed no physiological (fecal cortisol concentration and heart rate) or behavioralsigns (pathological behavior) of stress, or psychological indices of distress (depressive/anxietyrelatedbehavior) not only during the introduction process but also over a follow-up period of 18months. No overt aggression was displayed at all during the first two hours following pairformation. Aggressive interactions were minimal thereafter. Only one bite laceration wasincurred 14 weeks after pair formation. The partners of this pair were maintained in the homecage with the barred panel to allow wound healing; they were subsequently placed again intofull contact with no further complications. "The results of this study may be of practical use fordesigning and monitoring social introductions and suggest that managers should not dismiss thefeasibility of successful pairing of adult male rhesus macaques."Eaton GG, Kelley ST, Axthelm MK, Iliff-Sizemore SA, Shiigi SM 1994. Psychological wellbeingin paired adult female rhesus (Macaca mulatta). American Journal of Primatology 33, 89-99Partners were paired after noncontact familiarization. Pairs were compatible in 86% of 21cases.Line SW, Morgan KN, Markowitz H, Roberts J, Riddell M 1990. Behavioral responses of femalelong-tailed macaques (Macaca fascicularis) to pair formation. Laboratory Primate Newsletter29(4), 1-5http://www.brown.edu/Research/Primate/lpn29-4.html#linePotential partners were familiarized in a noncontact situation prior to pairing. Five of six pairstested were compatible during a five to six months study period.

81McLean M, Morris J, Watson E, Gavetti D, Marshall S 2006. Retrospective evaluation of pairhousingjuvenile and adult cynomolgus macaques in a pharmaceutical environment. AALAS57th National Meeting Official Program, 148 (Abstract)"Our experience and data suggest that pair formation in juvenile and adult cynomolgus maleand female macaques has been successful and as allowed us to provide social housing in apharmaceutical environment."McMillan J, Maier A, Tully L, Coleman K 2003. The effects of temperament on pairing successin female rhesus macaques. American Journal of Primatology 60(Supplement), 95 (Abstract)“We assessed temperament in these monkeys, along with their two partners, by measuring theirreaction to novel objects (e.g., a brightly colored novel toy) presented to them in their homecages. Every monkey received a score from 0-6 based on her reaction to the novelty. ..Temperament scores were more similar between the focal monkeys and their successful partnerthan their unsuccessful partner. These results suggest that assessing temperament with a simpletesting paradigm may be useful in forming successful pairs.“Niemeyer C, Eaton, GG, Kelley ST1998. Practical aspects of the program to promotepsychological well-being in nonhuman primates at the Oregon RPRC. In Proceedings of theThird International Conference on Environmental Enrichment Hare VJ, Worley E (eds), 345-354. The Shape of Enrichment, San Diego, CA”New pairs are formed by moving both [pre-familiarized] individuals to a new location becausemonkeys housed in individual cages appear to become territorial about their cages.”Reaves ME, Cohen J 2005. Primate pairing under less than ideal circumstances. Tech Talk 10(5),1-2"Of the six male cynomolgus monkeys in our group, we were able to create three stable pairs.The animals share food, and although we have had some minor bumps and bruises, there havebeen no serious injuries. We later reproduced these results with our vervet colony and after thequarantine process with all new arrivals."Reinhardt V, Houser WD, Eisele S, Champoux M 1987. Social enrichment with infants of theenvironment for singly caged adult rhesus monkeys. Zoo Biology 6, 365-371http://www.awionline.org/Lab_animals/biblio/zb6-365.htm"Twenty-nine weaned rhesus monkey infants were removed from breeding troops to avoidovercrowding and were placed with unfamiliar singly caged adults... Pairs were compatible in90% of cases. Compatibility depended neither on the sex, age, and origin of the adult nor on thesex of the infant.”Reinhardt V 1989. Behavioral responses of unrelated adult male rhesus monkeys familiarizedand paired for the purpose of environmental enrichment. American Journal of Primatology 17,243-248"Potential companions were first given the opportunity to establish clear-cut rank relationshipsduring a 5-day period of noncontact familiarization. Only then were they paired in a differentdouble cage. Rank relationships were confirmed within the first 6 minutes after pairing withoutthe occurrence of any biting and fighting. It stands to reason that the risk of injury, intrinsicallyassociated with pairing, can be minimized if only those dyads are selected whose partners showunequivocal signs of an established rank relationship during a period of noncontactfamiliarization.”

82Reinhardt V 1991. Agonistic behavior responses of socially experienced, unfamiliar adult malerhesus monkeys (Macaca mulatta) to pairing. Laboratory Primate Newsletter 30(1), 5-7http://www.brown.edu/Research/Primate/lpn30-1.html#vik"The present data demonstrate that unfamiliar adult male rhesus monkeys may generally bepaired directly with each other without undue risk provided partners have previously lived withanother male companion. This is congruent with the findings made with adult females.”Reinhardt V 1994. Social enrichment for previously single-caged stumptail macaques. AnimalTechnology 5, 37-41http://www.awionline.org/Lab_animals/biblio/at37.htm10 females and 6 males were isosexually introduced following the establishment of rankrelationships during a three-day non-contact familiarization period. "Pair formations did notentail serious antagonism; instead companions engaged in conciliatory interactions."Watson LM 2002. A successful program for same- and cross-age pair-housing adult and subadultmale Macaca fascicularis. Laboratory Primate Newsletter 41(2), 6-9http://www.brown.edu/Research/Primate/lpn36-2.html#watsonIsosexual pairs of adult males, adult male/juvenile male and adult females were established andpair compatibility ascertained throughout follow-up periods of 1 month to 3 years. Partnerswere introduced after a supervised noncontact familiarization period in a specific pair formationcage. Of 31 adult male pairs tested, 29 [94%] were compatible; two pairs had to be separatedbecause "one animal in each pair sustained injuries during minor fighting."Marmosets (Callithrix spp.)Majolo B, Buchanan-Smith HM, Morris K 2001. Factors affecting the successful pairing ofunfamiliar common marmoset (Callithrix jacchus) females. Primate Eye 73, 12-13 (Abstract)http://www.psgb.org/Meetings/Winter2000.html46 marmoset female pairs were formed. “The success rate was 83%. ... Aggression is lower ifone member of the pair is not yet sexually mature... Pairing unfamiliar common marmosetfemales can be accomplished safely to avoid single housing when natural social grouping is notfeasible.“Squirrel monkeys (Saimiri spp.)Gwinn LA 1996. A method for using a pole housing apparatus to establish compatible pairs amongsquirrel monkeys. Contemporary Topics in Laboratory Animal Science 35(4), 61 (Abstract)Successful pair formation protocol in a pole-and-collar housing system is described.Vervet monkeys (Cercopithecus spp.)Dansie C, Galvao AV, McKain J, Despain KE 2004. African Green nonhuman primateenrichment. AALAS 55th National Meeting Official Program, 129 (Abstract)“Selected pairs are housed with plexi-panels between them for at least one week. At the end ofthis adaptive periods, pairs are allowed access to each other by removal of the grated panelsseparating them for a supervised period of one hour. The daily amount of time monkeys accesseach other is increased gradually until transition to pair-housing is complete.”

83Gerald MS, Weiss A, Ayala JE 2006. Artificial colour treatment mediates aggression amongunfamiliar vervet monkeys (Cercopithecus aethiops): a model for introducing primates withcolourful sexual skin. Animal Welfare 15(4), 363-369"Painting the scrotum dark led to more aggression when these males were paired with darkcoloured males and less aggression when these males were paired with pale coloured males.These findings suggest a practical and inexpensive means of reducing the likelihood ofaggression when introducing new animals."(2,3) Grooming-Contact CagingCrockett CM, Bellanca RU, Bowers CL, Bowden DM 1997. Grooming-contact bars providesocial contact for individually caged laboratory macaques. Contemporary Topics in LaboratoryAnimal Science, 53-60Pair formation of adult long-tailed macaques was accomplished by using widely spaced, verticalgrooming-contact bars that allow physical contact [but no copulation] but prevent pursuit byone animal into the other's cage. Pair compatibility was 100% in all cases except unfamiliarmale pairs (86%).Crockett CM, Koberstein D, Heffernan KS 2001. Compatibility of laboratory monkeys housed ingrooming-contact cages varies by species and sex. American Journal of Primatology54(Supplement), 51-52 (Abstract)“Grooming contact is achieved through widely spaced vertical bars that permit grooming butnot aggressive pursuit."The following pair compatibility was found:Macaca fascicularis: male-female 97%, female-female 89%, male-male 63%Papio cynocephalus: male-female 88%, female-female 57%M. nemestrina: male-female 78%, male-male 57%%, female-female 53%M. mulatta: male-male 45%. "The majority of male-male pairs involved juveniles, so MMcompatibility percentages may overestimate compatibility of adult male pairs."Crockett CM, Lee GH, Thom JP 2006. Sex and age predictors of compatibility in groomingcontactcaging vary by species of laboratory monkey. International Journal of Primatology27(Supplement), 417 (Abstract)Adult rhesus pairs were significantly less likely to be fully compatible (16%) than adult baboonpairs (64%), adult pig-tailed pairs (51%) and adult long-tailed pairs (67%).(2,4) Positive Interaction with Humans

Abney D, Conlee K, Cunneen M, Down N, Lang T, Patterson-Kane E, Skoumbourdis E,Reinhardt V 2006. Human-animal relationship in the research lab: a discussion by theRefinement and Enrichment Forum. Animal Technology and Welfare 5(2), 95-98http://www.awionline.org/Lab_animals/biblio/atw11.html"I think an affectionate human-animal relationship makes a huge difference for the animalsbecause it helps them overcome anxiety and fear in disturbing or distressing situations." "Thestress resulting from a neutral or negative relationship between investigator/technician andanimal is bound to affect the research data collected from the animal subject, but the researchindustry is not yet taking this methodological flaw seriously."Anonymous 2006. Primate passion — An interview with Karen MacLeod, RVT, AALASNorthern California Branch Technologist of the Year 2006. Lab Animal 35(9), 6When asked how she deals with attachment to animals in her care: ”Its hard because I ampassionate about what I do and because our animals are long-term. It is important to beattached and there are certainly days when I am in tears, but I think if I ever felt unaffected byeuthanizing our animals, it would be time for me to leave. As hard as it is to be passionate aboutwhat I do, I think it is a serious job requirement.“Anonymous 2003. Personnel / Animal Relationships: Affectionate or Neutral: A Discussion.Laboratory Primate Newsletter 42(1), 14-15http://www.brown.edu/Research/Primate/lpn42-1.html#relation“Having a close relationship with your animals is necessary to regard them as living beings,rather than biological test tubes. As such, you are more careful and patient, and will think moreabout what the procedures mean to the animals. You will get more creative in finding animalfriendly alternatives for the procedures you need to do on the animals. You will thus increase thewell-being of your animals and, by doing so, make better research subjects and increase thevalidity of the test results. .. There was a consensus that the emotional attachment provides anassurance that the animals receive optimal care, both physically and behaviorally. .. Concernwas expressed that establishing an affectionate relationship with experimental subjects andknowing them as individuals would hamper ones impartiality and capacity to be objective whenobserving and registering their behavior. A caregiver strongly objected: It seems to me that weget hung up on trying to divorce our emotions from what we hope to be our objectivity. I do notthink that any normally functioning human being in the world does anything for any reason otherthan emotional. Sure, research is done to answer questions, but isn't the premise of all researchto make human (or animal) lives better? If you want to make lives better, it's because ofemotion, not because you are logically attached to life.”Baker KC 1997. Human interaction as enrichment for captive chimpanzees: A preliminaryreport. American Journal of Primatology 42, 92 (Abstract)Simple, unstructured affiliation between humans and chimpanzees has a powerful impact onwell-being, promoting activity and relaxed conspecific interactions and ameliorating behavioraldisorders.Bayne K 2002. Development of the human-research animal bond and its impact on animal wellbeing.ILAR [Institute for Laboratory Animal Research] Journal 43(1), 4-9http://dels.nas.edu/ilar_n/ilarjournal/43_1/Development.shtml84

85The various roots of human-animal bonding in the research laboratory setting are reviewed."The development of these relationships is enriching to both personnel and animals inasmuch aspeople who care about their animals are committed to promoting and ensuring the well-being ofthose animals."Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 2.3.1.Affection for Animals. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/basic.html#rel"Animal care personnel and researchers should be encouraged to develop affectionaterelationships with their animals. Having such a relationship assures that you regard the animalsas living beings, rather than biological test tubes. As such, you will be more careful and morepatient. You will think more about what the experimental procedure implies to the animals. Youwill get more creative in refining procedures that are normally stressful or distressing to theanimals. You will thus enhance their well-being and, by doing so, you will increase the scientificvalidity of the research results.If you are not kind to your animals, make no attempt to enrich their boring, oftendepressing living quarters by addressing species-typical behavioral and social needs, and nevershow any kind of affection towards them (for example by offering them food treats from time totime), then I really don't think that you should work in an animal research laboratory.“Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 2.3.2. GivingAnimals Names. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/basic.html#name”Naming the animals helps me realize that I am working with sentient beings who deserve myconsideration of their well-being. I guess, we can all relate much better to names than tonumbers, and we tend to treat named versus numbered animals accordingly. The naming ofanimals in research labs could serve as a safeguard for optimal animal care.We have an investigator who is against the naming of rabbits assigned to her researchprotocol. The PI is afraid that, when bonding with her research subjects, we add a variable thatis detrimental to performing research. Our staff feels that this is an antiquated mentality and weare all standing strong in our position of naming all animals in our charge!“Bayne K, Dexter SL, Strange GM 1993. The effects of food treat provisioning and humaninteraction on the behavioral well-being of rhesus monkeys (Macaca mulatta). ContemporaryTopics in Laboratory Animal Science 32(2), 6-9"The effects of human interaction and food supplementation appear to be protracted, resulting ina reduction of pathology [behavioral disorders] even after the enrichment is removed."Bennett BT 1990. Alternative methodologies. In Essentials for Animal Research: A Primer forResearch Personnel Bennett BT, Brown MJ, Schofield JC (eds), 13-25. National AgriculturalLibrary, Beltsville, MDhttp://research.ucsb.edu/connect/acc/esalt.htm"Almost every animal commonly used in the laboratory responds positively to a little tenderloving care. It's inexpensive, readily portable, safe even at the highest doses and spreads rapidlythrough the staff."

86Boccia ML, Broussard C, Scanlan J, Laudenslager ML 1992 Practice makes predictable. In TheInevitable Bond Davis H, Balfour AD (eds), 153-170. Cambridge University Press, Cambridge,UK"In our laboratory, we have made it a point to minimize the human-animal interactions,assuming that by minimizing interactions, we optimize experimental conditions by eliminatingconfounding handling effects. The results presented here, however, suggest that it may benecessary to reverse this thinking."Choi GC 1993. Humans enrich the lives of lab baboons. WARDS Newsletter Summer, 3-7 & 13"The reduction in cage painting and banging was dramatic and remarkable" after the singlehousedanimals received more attention from the attending personnel.European Economic Community 1986. Council Directive 86/609, Annex II Guidelines forAccommodation and Care of Animals. Official Journal of the European Communities L358, 7-28http://www.uku.fi/laitokset/vkek/Sopimus/convention.html“The performance of an animal during an experiment depends very much on its confidence inman, something which has to be developed. It is therefore recommended that frequent contactshould be maintained so that the animals become familiar with human presence and activity.”Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housingand Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London, UKhttp://scienceandresearch.homeoffice.gov.uk/animal-research/legislation/“Where appropriate, time should be set aside for handling and grooming. All staff, bothscientific and technical, should be sympathetic, gentle and firm when dealing with the animals.”Jensvold ML 2007. Promoting positive interactions between chimpanzees (Pan troglodytes) andcaregivers. Laboratory Primate Newsletter 46(1), 1-4"We tested our contention that when caregivers use chimpanzee behavior, more positiveinteractions result.Mahoney CJ 1992. Some thoughts on psychological enrichment. Lab Animal 21(5), 27,29,32-37“A spark of compassion in any one person towards the animals can be fanned into flames ofempathy with the right encouragement, without destroying the primary research goals. In myexperience [as attending veterinarian] it is utterly impossible, however, to make an uncaringperson caring. Such people are not suited for this line of work (p. 35). .. There should be nosharp demarcation between 'good guys' and 'bad guys.' All employees, to some extent must sharethe work. Nonhuman primates are quick to forget, or perhaps forgive, the momentary fear orresentment they feel towards a human being who has just subjected them to an unpleasantexperience if a strong bond of trust already exists with that person.”Morton DB, Jennings M, Buckwell A, Ewbank R, Godfrey C, Holgate B, Inglis I, James R, PageC, Sharman I, Verschoyle R, Westall L, Wilson AB 2001. Refining procedures for theadministration of substances. Laboratory Animals 35, 1-41“Where substances are administered infrequently but on a long-term basis handling the animalsduring routine daily husbandry will help reduce stress when subsequently dosing them. Ingeneral, staff should be encouraged to handle animals as much as possible."National Research Council 1996. Guide for the Care and Use of Laboratory Animals NationalAcademy Press, Washington, DChttp://www.nap.edu/books/0309053773/html/

“The animal technician's and caregiver's roles are pivotal to the social support of primates,particularly animals that are singly caged. ... When they must be housed alone, other forms ofenrichment should be provided to compensate for the absence of other animals, such as safe andpositive interaction with the care staff.”National Research Council 1998. The Psychological Well-Being of Nonhuman PrimatesNational Academy Press, Washington, DChttp://fermat.nap.edu/books/0309052335/html/index.html“Interactions between humans and nonhuman primates can be made less stressful by adherenceto routine schedules and procedures, familiarity with handlers and researchers through positiveinteractions outside [sic] the handling context.”Reese EP 1991. The role of husbandry in promoting the welfare of laboratory animals. InAnimals in Biomedical Research Hendriksen CFM, Koeter HBWM (eds), 155-192. Elsevier,Amsterdam, The Netherlands“An important, and often neglected, source of social enrichment, especially when animals mustbe isolated from conspecifics, is attention from caretakers and technicians. That many scientistslack detailed information about their animals, especially their behavior, is distressing andreflects a serious disregard for the single most important element of their research. The animalis the key to the entire experiment. ... The proper handling of laboratory animals is as essentialto the collection of valid data as it is to the animals' comfort and well-being. The more theanimal is handled properly, the more docile it becomes, especially if handling begins at an earlyage. Conversely, the more an animal is mishandled, the more difficult, frightened, andaggressive it is likely to become ... Successful shaping requires the right attitude, a thoroughunderstanding of the individual animal and of the task to be performed, and clinical skills. Thereis only one 'right' attitude, and that is respect for the individual animal. ... My students mustname their animals, and I do not let them put an animal in the apparatus until they show me itwill eat from their hands.”Reinhardt V 2003. Compassion for animals in the laboratory: Impairment or refinement ofresearch methodology. Journal of Applied Animal Welfare Science 6, 123-130http://www.awionline.org/Lab_animals/biblio/jaaws10.html“Compassion for animals used in research, testing and teaching should not be regarded assubjective but as a sound methodological base for scientifically valid animal research.”Russow L-M 2002. Ethical implications of the human-animal bond. ILAR Journal 43(1), 33-37http://dels.nas.edu/ilar_n/ilarjournal/43_1/Implications.shtml"Researchers must continue to question the barriers that have traditionally been errected againstforming HABs in the name of objectivity and to investigate seriously the ways in which fosteringthe formation of HABs can promote animal welfare without compromising the scientificrespectability of research."Sokol KA 1993. Commentary: Thinking like a monkey - "primatomorphizing" an environmentalenrichment program. Lab Animal 22(5), 40-45“We encouraged animal caretakers to visit the animals at times other than their normal routinesto reinforce positive interactions and associations. Instead of identifying the monkeys by just atattoo number, we gave them names. Thus, we could refer to them as individuals and betteridentify them.”87

Southey ER, Baldwin CM 2006. Socialisation of rhesus macaques at CFM. Animal Technologyand Welfare 5(2), 119-122The Centre for macaques in England is an example of best practice in the care and welfare ofold world primates in addition to an evolving centre for the education and training of peopleworking in the area of primate research. Husbandry techniques and socialisation of themacaques are described. Socialisation comprises of hand feeding through cage room and lobbybars, going into the playpen to hand out food and sitting in with the animals and interacting on acloser basis.Wolfle TL 1987. Control of stress using non-drug approaches. Journal of the AmericanVeterinary Medical Association 191, 1219-1221“Human interaction with monkeys and apes is essential for the well-being of the animal, datavalidity, and ease of handling.” The 'social bond' “conveys to the animal a quiet sense ofassurance on which coping strategies can be developed for dealing with other stressful aspectsof the laboratory.”Wolfle TL 2002. Introduction. ILAR [Institute for Laboratory Animal Research] Journal 43(1), 1-3http://dels.nas.edu/ilar_n/ilarjournal/43_1/introduction.shtml"I was encouraged not to assign names to the many rhesus monkeys in my charge. I wasadmonished that the animals are research subjects, not pets. The concern was that having namesfor the animals might blur this distinction between a research subject and a pet.... It did not seempossible to remain distant - emotionally isolated - from the animals. In fact, the inevitablecloseness that resulted from those intimate interactions was precisely what made us capable ofdoing what we were asked to do. ... Eventually, we all came to know that F49 was Sam, A12 wasRosie, and Z13 was Curious. ... Such attachments are the results of compassionate people doingtheir job right."(3) Promoting Intelligent Behavior: Positive Reinforcement TrainingHome Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housingand Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London, UKhttp://scienceandresearch.homeoffice.gov.uk/animal-research/legislation/“The least distressing method of handling is to train the animal to co-operate in routineprocedures. Advantage should be taken of the animal's ability to learn."Prentice ED, Zucker IH, Jameton A 1986. Ethics of animal welfare in research: The institution'sattempt to achieve appropriate social balance. The Physiologist 29, 1,19-21"Physical restraint procedures should be used on awake animals only after alternativeprocedures have been considered and found to be inadequate. If a restraint will be utilized theanimal should be trained or conditioned to the restraining device, using positive reinforcement,prior to the beginning of the experiment"(3,1) Basic RecommendationsBaumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 7.2. Injectionand Blood Collection—How to minimize Stress Reactions. Washington, DC: Animal WelfareInstitutehttp://www.awionline.org/pubs/LAREF/working.html#training88

89”If the animals are under stress while you are working with them, there is a great risk that theyshow aggressive reactions to you, in an attempt to get away from the stressful situation. One ofthe conditions of successful and safe positive reinforcement training is a stress-free workenvironment, both for the animal and for you. This means, neither the animal nor you should beunder the emotional influence of fear, apprehension or frustration. These emotions aredangerous when your handle monkeys or, for that matter, any other animals.You should reach a stage when you know that you can trust the trainee while you workwith him or her. This does not mean that you should not be alert, but any traces of mistrust andfear puts you into a seriously dangerous position. Do not work with an animal, unless you havetrust in him or her! For your additional safety, you will always have to make sure that yourinteraction with the trainee will not be disturbed or disrupted by any unexpected event, such aspersonnel entering the room or loud personnel passing in hallways.“Chambers DR, Gibson TE, Bindman L, Guillou PJ, Herbert WJ, Mayes PA, Poole TB, Wade AJ,Wood RKSBC 1992. Guidelines on the Handling and Training of Laboratory Animals.Universities Federation for Animal Welfare, Potters Bar, UKVery helpful outline of what has to be taken into consideration when training animals tocooperate during handling procedures. "Non-human primates, particularly the larger macaques,vervets, baboons and apes, are readily trained to cooperate in procedures such as presenting anarm for blood collection."Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housingand Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London, UKhttp://scienceandresearch.homeoffice.gov.uk/animal-research/legislation/“ The least distressing method of handling is to train the animal to co-operate in routineprocedures. Advantage should be taken of the animal's ability to learn."Klein HJ, Murray KA 1995. Part C. Restraint. In Nonhuman Primates in Biomedical Research -Biology and Management Bennett BT, Abee CR, Henrickson R (eds), 286-297. Academic Press,New York, NY“The importance of training and adaptation cannot be overemphasized. This not only reducesstress to the animal but promotes safety and quality data collection."Laule GE, Desmond T 1998. Positive reinforcement training as an enrichment strategy. InSecond Nature Shepherdson DH, Mellen JD, Hutchins M (eds), 302-313. SmithsonianInstitution Press, Washington, DCPrinciples of positive reinforcement training are clearly outlined and applications reviewed."Animals are reinforced with pleasurable rewards for the desired behavioural response.Operationally, this means that positive alternatives are exhausted before any kind of negativereinforcement is used." Punishment "is only appropriate in a situation that is life threatening forperson or animal. ... Positive reinforcement training does not require any food deprivation. ...This training regime relies on voluntary cooperation by the animal to be successful."Laule G 1999. Training laboratory animals. In The UFAW [Universities Federation for AnimalWelfare] Handbook on the Care and Management of Laboratory Animals Seventh Edition PooleT, English P (eds ), 21-27. Blackwell Science, Oxford, UKVery helpful discussion of positive reinforcement training for cooperation during procedures."By making the shift to a more positive reinforcement-based system, the welfare of the animals issignificantly enhanced while providing better (less stressed) research models for the biomedicalcommunity."

T-W-Fiennes RN 1972. Primates - General. In The UFAW Handbook on the Care andManagement of Laboratory Animals Fourth Edition Universities Federation for Animal Welfare(ed), 374-375. Churchill Livingstone, London, UK“Chimpanzees and baboons, are intelligent and sensitive. If handled with sympathy andunderstanding they can become more than research tools - even cooperative partners inexperimentation. To achieve this, a little time .. must be spent on conditioning the animals. Achimpanzee, for instance, will sit quietly and hold his arm out for a blood sample to be taken. ...An animal treated unsympathetically is liable to become aggressive and uncooperative;furthermore, unless care is taken over its comfort and needs, it is liable to become stressed andthe results of the experiment may be vitiated for this reason."(3,2) Species-specific RecommendationsBaboons (Papio spp.)Levison PK, Fester CB, Nieman WH, Findley JD 1964. A method for training unrestrainedprimates to receive drug injection. Journal of the Experimental Analysis of Behavior 7, 253-254Training technique by which an adult, single-housed male baboon learned to offer his armthrough a pothole and accept intramuscular injection in this home cage is described and theresult demonstrated with a photo. Injection was reliably obtained after approximately nine onehourtraining sessions.Turkkan JS, Ator NA, et al 1989. Beyond chronic catheterization in laboratory primates. InHousing, Care and Psychological Well-being of Captive and Laboratory Primates Segal EF (ed),305-322. Noyes Publications, Park Ridge, NJTraining protocols are described to ensure cooperation of single-housed baboons during bloodpressure measurement and during oral drug dosing in the homecage.Chimpanzees (Pan troglodytes)Bloomsmith MA, Laule GE, Alford PL, Thurston RH 1994. Using training to moderatechimpanzee aggression during feeding. Zoo Biology 13, 557-566"Positive reinforcement training techniques were applied to reduce a dominant malechimpanzee's aggression and chasing during meals. Verbal commands and food reinforcers wereused to train him to sit and remain seated while other group members received and ate theirshare of produce."Bloomsmith MA, Stone AM, Laule GE 1998. Positive reinforcement training to enhance thevoluntary movement of group-housed chimpanzees within their enclosure. Zoo Biology 17, 333-341Positive reinforcement was applied to train groups of chimpanzees to move voluntarily into theindoor portions of their enclosures at the request of trainers and to be briefly restricted to thoseareas.Kessel-Davenport AL, Gutierrez T 1994. Training captive chimpanzees for movement in atransport box. The Newsletter 6(2), 1-2http://www.awionline.org/Lab_animals/biblio/jo-6.htm90

91Training technique is described. "Thirty-seven [group-housed] captive chimpanzees weretrained using operant conditioning to enter a transfer box." [Age and sex of subjects is notprovided.]Lambeth SP, Perlman JE, Schapiro SJ 2000. Positive reinforcement training paired withvideotape exposure decreases training time investment for a complicated task in femalechimpanzees. American Journal of Primatology 51(Supplement), 79-80 (Abstract)“Five females were exposed to a 10-minute videotape of female chimpanzees being positivelyreinforced for successfully urinating into a cup. Immediately following videotape exposure, thesesubjects participated in a training session." On average experimental and control subjectsreceived 56 minutes of training. "Subjects with videotape exposure successfully responded to thecommand to urinate in significantly less time than did controls."Laule GE, Thurston RH, Alford PL, Bloomsmith MA 1996. Training to reliably obtain blood andurine samples from a diabetic chimpanzee (Pan troglodytes). Zoo Biology 15, 587-591Training techniques are described to gain the cooperation of a 3-year old female chimpanzee inobtaining blood and urine samples. "The first blood draw occurred during the 18th trainingsession, with a total of 275 minutes invested prior to that. The first successful [urine] collectionoccurred in session 4 in less than 4 min after a total of 42 min of training time."Laule G 1999 Training laboratory animals. In The UFAW [Universities Federation for AnimalWelfare] Handbook on the Care and Management of Laboratory Animals Seventh Edition PooleT, English P (eds ), 21-27. Blackwell Science, Oxford, UKVery helpful discussion of positive reinforcement training for cooperation during procedures."By making the shift to a more positive reinforcement-based system, the welfare of the animals issignificantly enhanced while providing better (less stressed) research models for the biomedicalcommunity."Perlman JE, Thiele E, Whittaker MA, Lambeth SP, Schapiro SJ 2004. Training chimpanzees toaccept subcutaneous injections using positive reinforcement training techniques. AmericanJournal of Primatology 62(Supplement), 96 (Abstract)http://www.asp.org/asp2004”Positive reinforcement training techniques were used to train four socially-housed, adultchimpanzees to present their abdomen for a subcutaneous injection. .. Subjects had beenpreviously trained to present body parts for inspection, including the abdomen. For the presentstudy, subjects were trained to 1) present the abdomen, 2) tolerate a pinch of the skin, 3) acceptthe subcutaneous insertion of a needle, and 4) remain stationary while the contents of the syringewere injected. Three of the four chimpanzees were reliably trained to voluntarily accept thesubcutaneous injection. A mean of 98 minutes of training time was required for the animals toreliably accept penetration and injection of up to 10 cc through a 25-gauge needle. Trainingsessions lasted 5 to 8 minutes and 13 - 20 sessions (mean = 17) were required to achievereliable performance.“Russell JL, Taglialatela JP, Hopkins WD 2006. The use of positive reinforcement training inchimpanzees (Pan troglodytes) for voluntary presentation for IM injections. American Journal ofPrimatology 68(Supplement), 122 (Abstract)"Positive reinforcement has been used to gain the cooperation of captive primates for researchand management needs. In this study, ten chimpanzees .. were trained to present forintramuscular (IM) injections. Clicker training was used to teach subjects to present their legand accept an injection. .. Subjects reached criterion for presenting for a touch from a needle in

927 to 44 training sessions. .. These results suggest that through the use of positive reinforcement,chimpanzees can be quickly and reliably trained to present for injections as part of a researchprotocol requiring multiple accesses."Schapiro SJ, Perlman JE, Thiele E, Lambeth S 2005. Training nonhuman primates to performbehaviors useful in biomedical research. Lab Animal 34(5), 37-42Training protocols are described and the time investments to achieve cooperation for semencollection [7 subjects: 29-453 minutes], subcutaneous [2 subjects: 90-104 minutes; 1 subjectcould not be trained] and intramuscular injection [39 subjects: 0.1-396 minutes; 43 subjectscould not be trained] are presented.Spragg SDS 1940. Morphine addiction in chimpanzees. Comparative Psychology Monographs15, 1-132Author provides formal description of training four unrestrained chimpanzees to approach aninvestigator and accept an injection of physiological saline solution. The training comprised acombination of adaptation, desensitization, and shaping, with fruit, praise, and patting asreinforcers. "It is the writer's contention that this preliminary adaptation to the injectionsituation was an important factor for the experiment; it obviated many undesirable aspectswhich would have appeared if it had been necessary to inject the animals by force."Videan EN, Fritz J, Murphy J, Borman R, Smith HF, Howell S 2005. Training captivechimpanzees to cooperate for an anesthetic injection. Lab Animal 34(5), 43-48Training protocol is described in detail and the time investment presented.Videan EN, Fritz J, Murphy J, Howell S, Heward CB 2005. Does training chimpanzees topresent for injection lead to reduced stress? Laboratory Primate Newsletter 44(3), 1-2http://www.brown.edu/Research/Primate/lpn44-3.html#videan"Subjects were 17 captive chimpanzees living at the Primate Foundation of Arizona, aged 10.6to 34.5 years at the time of the study. The sample included 8 males and 9 females. Eleven of thesubjects were trained, using positive reinforcement techniques, over 21 months (Videan et al.,2005). Individuals were trained to present an arm or leg to the cage mesh for anestheticinjection, using the verbal cues “arm” and “leg”. Training procedures were transferred fromthe trainer to either the colony manager or the assistant colony manager, after behaviors wereunder stimulus control, in 5 of the trained subjects. .. When all trained individuals were pooled,trained subjects exhibited significantly lower levels of cortisol than untrained (U=7, p

Gorillas (Gorilla spp.)93Bettinger T, Kuhar C, Sironen A, Laudenslager M 1998. Behavior and salivary cortisol ingorillas housed in an all male group. AZA Annual Conference Proceedings, 242-246Gorillas were successfully trained to voluntarily chew on the cotton plugs then return them to thecaretaker.Bond M 1991. How to collect urine from a gorilla. Gorilla Gazette 5(3), 12-13Training technique is clearly described. Mandara "not only urinates on demand but has beenknown to go get a drink of water if we happen to ask for a sample when her bladder is empty.”Brown CS 1997. Training gorillas (Gorilla gorilla gorilla) for noninvasive semen collection.Proceedings American Association of Zoo Veterinarians, 201-203"Appropriate behaviors, in response to verbal prompts, were rewarded with praise and foodtreats. Collection of the first semen sample [from single-housed subjects] varied from 5-14months after the initiation of training, with collections occurring earliest on the animal thatappeared to have the best relationship with the trainer."Brown CS 1998 A Training Program for Semen Collection in Gorillas (video). Henry DoorlyZoo, Omaha, MBTraining technique to ensure cooperation of single-housed adult male gorillas during physicalexamination, injection, semen collection are described and very clearly demonstrated.Segerson L, Laule GE 1995. Initiating a training program with gorillas at the North CarolinaZoological Park. American Zoo and Aquarium Association Annual Conference Proceedings,488-489Technique is clearly described to facilitate wound treatment of an unrestrained, single-housedfemale.Macaques (Macaca spp.)

94Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 7.2. Injectionand Blood Collection—How to minimize Stress Reactions. Washington, DC: Animal WelfareInstitutehttp://www.awionline.org/pubs/LAREF/working.html#training”With positive reinforcement, I have trained adult female cynos to cooperate duringintramuscular injection in home cages that are not equipped with squeeze-backs. When they cantrust you, they readily learn to cooperate during this common procedure. These animals workwith rather than against me, which automatically implies that they show no fear or stressreactions during the procedure.“Bunyak SC, Harvey NC, Rhine Rj, Wilson MI 1982. Venipuncture and vaginal swabbing in anenclosure occupied by a mixed-sex group of stumptailed macaques (Macaca arctoides).American Journal of Primatology 2, 201-204By the end of five training sessions ”it was no longer necessary to net and restrain the females.Indeed, some of the females began voluntarily to approach the researcher and present forvaginal swabbing.”Clarke MR, Phillippi KM, Falkenstein JA, Moran EA, Suomi SJ 1990. Training Corral-livingRhesus Monkeys for Fecal and Blood Sample Collection (Videotape). Delta Primate ResearchCenter, Covington, LATraining technique is explained and the animals' reactions demonstrated.Down N, Skoumbourdis E, Walsh M, Francis R, Buckmaster C, Reinhardt V 2005. Pole-andcollartraining: A discussion by the Laboratory Animal Refinement and Enrichment Forum.Animal Technology and Welfare 4, 157-161http://www.awionline.org/Lab_animals/biblio/atw7.htmlExperiences with the pole-and-collar training training are shared. "Yes, most monkeys can betrained but some cannot, or let's say they should not be trained because their personality —which is presumably conditioned through negative experiences with people — is very difficult todeal with.".Friscino BH, Gai CL, Kulick AA, Donnelly MJ, Rockar RA, Aderson LC, Iliff SA 2003.Positive reinforcement training as a refinement of a macaque biliary diversion model. AALAS54th National Meeting Official Program, 101 (Abstract)"Animals that adapted to wearing jackets were surgically implanted with a biliary diversioncannula system, a venous cannula and three subcutaneous access ports. .. The animals [threefemales and nine male rhesus] were trained to present the pouch and to remain stationary whilethe catheters were accessed. The length of time required for training was variable betweenindividuals, but generally required three to four training sessions during a two-week period.These in-cage procedures precluded the need for chair or manual restraint of animals duringsample collection. Instead, positive reinforcement was used to reward the animals with food fortheir cooperation during sample collection. This has also increased the efficiency of conducingmetabolic studies and minimized the potential stress of sample collection for both the personneland animals."Goodwin J 1997. The application, use, and effects of training and enrichment variables withJapanese snow macaques (Macaca fuscata) at the Central Park Wildlife Center. American Zooand Aquarium Association Regional Conference Proceedings, 510-515Training protocol is briefly described which allows the keepers through vocal and visual cues toherd the animals to a holding area.

Heath M 1989. The training of cynomolgus monkeys and how the human/animal relationshipimproves with environmental and mental enrichment. Animal Technology 40(1), 11-22http://www.awionline.org/Lab_animals/biblio/at40heath.html“A relatively short, but predictable, course of routine handling and feeding enabled the monkeysto co-operate with their handlers and made working practices a lot easier, quicker and safer forboth the animals and technicians."Luttrell L, Acker L, Urben M, Reinhardt V 1994. Training a large troop of rhesus macaques tocooperate during catching: Analysis of the time investment. Animal Welfare 3, 135-140http://www.awionline.org/Lab_animals/biblio/aw5train.htm“Using a simple chute system and applying a training technique based on patience, all 45 troopmembers were successfully conditioned in less then 15 work-hours to voluntarily enter atransport cage one by one.”Phillippi-Falkenstein K, Clarke MR 1992. Procedure for training corral-living rhesus monkeysfor fecal and blood-sample collection. Laboratory Animal Science 42, 83-85Clear description of training technique. "By day 9, the male stopped resisting, and three of the[five] females extended their legs voluntarily."Reinhardt V 1990. Avoiding undue stress: Catching individual animals in groups of rhesusmonkeys. Lab Animal 19(6), 52-53http://www.awionline.org/Lab_animals/biblio/la-avoid.htmTraining technique is described. "We have successfully trained two heterogeneous rhesus troopsof 28 and 33 members. The catching procedure has become a routine that is no longerassociated with excitation and distress. It is now possible for one experienced person to catchanimals at any given time without extra help."Reinhardt V 1990. Catching Individual Rhesus Monkeys Living in Captive Groups (videotape).Wisconsin Regional Primate Research Center, Madison, WIUsing vocal commands, a single person swiftly catches all members of a trained rhesus breedinggroup one-by-one in a transport cage without causing any disturbance or stress.Reinhardt V 1996. Refining the blood collection procedure for macaques. Lab Animal 32(1), 32-35http://www.awionline.org/Lab_animals/biblio/la-refin.htmA training technique is described for ensuring the active cooperation of pair-housed/singlehousedadult male and female rhesus and stump-tailed macaques during in-homecagevenipuncture. Mean cumulative training time investment per individual was less than one hour.The training eliminated significant cortisol responses which typically occur during conventional,i.e., enforced blood collection.Reinhardt V, Cowley D 1990. Training stumptailed monkeys to cooperate during in-homecagetreatment. Laboratory Primate Newsletter 29(4), 9-10http://www.brown.edu/Research/Primate/lpn29-4.html#vikOne to 14 training sessions, each lasting for 1-5 minutes, were required to train adult, pair- andsingle-housed stump-tailed macaques of both sexes to cooperate during topical treatment in thehomecage.95

96Skoumbourdis EK 2008. Pole-and-collar-and-chair training. Laboratory Animal Refinement &Enrichment Forum (electronic discussion group) , January 24, 2008http://groups.yahoo.com/group/LAREF/members”All the monkeys I have pole/collar/chair trained have gone through an initial phase ofresistance both when the pole was being attached to the collar, and when they were first put intothe chair, but for the most part they finally did settle down and cooperate. All it takes ispatience and gentle determination on the part of the trainer.Trust in the trainer is the ultimate key for success. Nonhuman primates are intelligent;when they are free of apprehension or fear, they quickly figure out that it is much easier andeven rewarding for them to cooperate with you rather than resist. A successfully trained monkeywill have developed so much trust in you that he/she will never fight against you when you poleand chair him/her.To pole-collar-chair train a monkey can be a very rewarding process that is notnecessarily time-consuming. I have successfully trained 19 animals: two adult female rhesus,four adult male rhesus, five juvenile male rhesus, four adult female cynomolgus, and four adultmale cynomolgus.My quickest subject took just five days of training to reliably cooperate (I should mentionthat he was two years old and an angel!), while other animals have taken me well over a monthto get going — especially older rhesus who can be very stubborn and hard to food-motivate.Also, I have had some animals who were just never meant to be put in a chair. This is a realitythat both you and the investigators must acknowledge. You cannot force a monkey to cooperateand be relaxed in the chair. It's impossible. Sure, you can try, but you're not going to win.“Marmosets (Callithrix spp.)Anzenberger G, Gossweiler H 1993. How to obtain individual urine samples from undisturbedmarmoset families. American Journal of Primatology 31, 223-230"An apparatus and a method are described, which allow simultaneous urine collection from allindividual members of undisturbed marmoset families. By the end of the third week of training, itwas not unusual to collect urine samples from an entire family."McKinley J, Buchanan-Smith HM, Bassett L, Morris K 2003. Training common marmosets(Callithrix jacchus) to cooperate during routine laboratory procedures: Ease of training and timeinvestment. Journal of Applied Animal Welfare Science 6, 209-220Behaviours taught were target training to allow in homecage weighing and providing urinesamples from 12 pairs of marmosets. "Between 2 to 13, 10-minute training sessions establisheddesired behaviors. .. Trained animals proved extremely reliable, and data collection usingtrained animals was considerably faster than collection using current laboratory techniques."Smith TE, McCallister JM, Gordon SJ, Whittikar M. 2004. Quantitative data on training newworld primates to urinate. American Journal of Primatology 64(1), 83-930"This study assessed the effectiveness of operant conditioning in training three species ofcaptive callitrichid primates (Leontopithecus rosalia, Callithrix geoffroyi, and Saguinusimperator) to urinate on demand...Training sessions (30 min each) were conducted at dawnthrice weekly during five consecutive phases: habituation, control, training (animals wererewarded for urinating), maintenance (animals had reached a defined training criteria andcontinued to be rewarded for urinating), and collection (animals were rewarded for urinating,and the trainer entered the cage to collect the sample). The numbers of 30-min training sessionsrequired to train the three monkey species (L. rosalia, C. geoffroyi, and S. imperator) were five,six, and eight, respectively. For the three species, the mean number of urinations per animal was

97significantly greater during the training, maintenance, and collection phases compared to thecontrol phase... The entry of the trainer into the cage to collect the urine sample did not appearto alter urination behavior. We demonstrate that operant conditioning techniques, whichtypically incur minimal cost, time investment, and disturbance, can be used to increase thequantity of urine samples collected for physiological analysis, the proportion of animals thaturinate, and the speed of sample collection."Orangutans (Pongo pymgmaeus)Berman N, Greenblatt H 1989. Training Medical Behaviors in Orangutans at Brookfield Zoo(videotape). Chicago Zoological Society, Chicago, ILTraining technique is clearly described and demonstrated to ensure cooperation of two pairhousedfemale/male orangutans during daily insulin injection.Moore BA, Suedmeyer K 1997. Blood sampling in 0.2 Bornean orangutans at the Kansas CityZoological Gardens. Animal Keepers' Forum 24, 537-540Training technique is clearly described to ensure cooperation during in-homecage bloodcollection of adult, pair-housed female orangutans.Sakis (Pithecia spp.)Shideler SE, Savage A, Ortuño AM, Moorman EA, Lasley BL 1994. Monitoring femalereproductive function by measurement of fecal estrogen and progesterone metabolites in thewhite-faced saki (Pithecia pithecia). American Journal of Primatology 32, 95-108"Fist morning void urine was collected directly in a polypropylene container hand-held underthe female subject. A second container was held under the female to collect fecal material. [Thegroup-housed] females urinated and defecated within 5-20 min. Following sample collection,females were rewarded for their cooperation with more sunflower seeds."Spider monkeys (Ateles spp.)Hernándes-López L, Mayagoitia L, Esquivel-Lacroix C, Rojas-Maya S, Mondragón-Ceballos R1998. The menstrual cycle of the spider monkey (Ateles geoffroyi). American Journal ofPrimatol. 44, 183-195Four of the five females were trained to enter a small cage attached to the door of theirenclosure and to "allow a cotton swab to be introduced in the vagina. This procedure wasslightly modified [not described], and the animals were trained to be injected with ketamine" forsubsequent blood collection.Squirrel monkeys (Saimiri spp.)Panneton M, Alleyn S, Kelly N 2001. Chair restraint for squirrel monkeys. AALAS 52ndNational Meeting Official Program, 92 (Abstract)“Our facility has trained squirrel monkeys to cooperate during various procedures such ascapture from their homecage and chair restraint for periods not exceeding 1 h. ... Each squirrelmonkey is constantly supervised and given positive reinforcement during and after the trainingsessions. ... The initial training period starts at 5-10 min three times a week. Additional trainingsessions of 5-20 min are added until 1h of chair restraint is achieved. At this time, training isreduced to twice a week for 1 h and then once a week for maintenance.” Concerns are weightloss, chair abrasions and hypoglycemia.

98Tamarins (Saguinus spp.)Smith TE, McCallister JM, Gordon SJ, Whittikar M. 2004. Quantitative data on training newworld primates to urinate. American Journal of Primatology 64(1), 83-93"This study assessed the effectiveness of operant conditioning in training three species of captivecallitrichid primates (Leontopithecus rosalia, Callithrix geoffroyi, and Saguinus imperator) tourinate on demand...Training sessions (30 min each) were conducted at dawn thrice weeklyduring five consecutive phases: habituation, control, training (animals were rewarded forurinating), maintenance (animals had reached a defined training criteria and continued to berewarded for urinating), and collection (animals were rewarded for urinating, and the trainerentered the cage to collect the sample). The numbers of 30-min training sessions required totrain the three monkey species (L. rosalia, C. geoffroyi, and S. imperator) were five, six, andeight, respectively. For the three species, the mean number of urinations per animal wassignificantly greater during the training, maintenance, and collection phases compared to thecontrol phase... The entry of the trainer into the cage to collect the urine sample did not appearto alter urination behavior. We demonstrate that operant conditioning techniques, whichtypically incur minimal cost, time investment, and disturbance, can be used to increase thequantity of urine samples collected for physiological analysis, the proportion of animals thaturinate, and the speed of sample collection."Snowdon CT, Savage A, McConnell PB 1985. A breeding colony of cotton-top tamarins(Saguinus oedipus). Laboratory Animal Science 35, 477-480Group-housed females were conditioned to urinate into containers each morning for a foodreward.Vervet monkeys (Cercopithecus aethiops)Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 7.3. OralDrug Administration—How to minimize Stress Reactions. Washington, DC: Animal WelfareInstitutehttp://www.awionline.org/pubs/LAREF/working.html#oral-prim"Our vervet monkeys voluntarily swallow drugs when we mix these with their regular diet,consisting on pre-cooked maize, fortified with vitamins, minerals and other ingredients. The dryingredients are blended with water and form a stiff putty-like paste, which is an ideal vehicle formixing in test substances. If the flavor needs to be masked, there are a variety of possibilities,such as honey and syrup, depending on what the protocol permits. We usually administer thecompound in about a third of the morning feed. The bulk of the food is offered after this portionhas been consumed. Some substances we even mix into the entire bulk of the morning feed.Keeping the compound too long in cheek pouches or spitting it out has never been a problem.We have used this simple oral administration technique for pharmacokinetic studies verysuccessfully. Over a time period of 20 years, we have not had to deal with any substance that wecould not feed to the vervets, including bitter herbal mixtures in fairly high concentrations."Kelley TM, Bramblett CA 1981. Urine collection from vervet monkeys by instrumentalconditioning. American Journal of Primatology 1, 95-97Training technique is described. Six of eight group-housed males reliably produced clean urinesamples after a two-month period of training.

Woolly monkeys (Lagothrix spp.)99Logsdon S 1995. Use of operant conditioning to assist in the medical management ofhypertension in woolly monkeys. American Zoo and Aquarium Association RegionalConference Proceedings, 96-102Training technique is described. "Currently, two monkeys [one adult female and one adult male]have had their blood pressure measured in the group without being restrained."(4) Promoting Foraging and Food Processing Behavior(4,1) Foraging DevicesBayne K, Dexter SL, Mainzer H, McCully C, Campbell G, Yamada F 1992. The use of artificialturf as a foraging substrate for individually housed rhesus monkeys (Macaca mulatta). AnimalWelfare 1, 39-53http://www.awionline.org/Lab_animals/biblio/aw1-39.htmSubjects spent on average 15.7 minutes per 30 minute-observation sessions foraging from thedevice. "An increasing trend in time spent foraging with a concomitant decline in aberrantbehaviour over a time period of six months was particularly noteworthy."Bayne K, Mainzer H, Dexter SL, Campbell G, Yamada F, Suomi SJ 1991. The reduction ofabnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with aforaging/grooming board. American Journal of Primatology 23, 23-35All of the single-housed "animals foraged from the board to the point that a significant reductionin the level of abnormal behavior was noted.” Subjects spent on average 12.1 minutes foragingfrom the board per 30 minute-observation sessions.

100Bertrand F, Seguin Y, Chauvier F, Blanquié JP 1999. Influence of two different kinds offoraging devices on feeding behaviour of rhesus macaques (Macaca mulatta). FoliaPrimatologica 70, 207 (Abstract)A foraging device fitted on the ceiling of the cage (H), and a foraging device fitted on the front ofthe cage (V) and filled with pellets were tested in 12 individually housed animals. "The animalsmoved the pellets from the reserve to a hopper. ... We found that the amount of waste food wasup to 17 times lower in the V foraging device than in the control feeder and that the feeding timewas much longer with the foraging device than with the control feeder. Over 90% of the foodwas eaten within the first 15 minutes with the control feeder, whereas it took 60 or 75 minutes toreach this percentage using the foraging device, whether it was a V or an H one. Each puzzlerequired specific skills. Whichever the feeding device, the subjects ate their whole daily rationand their weight remained stable."Bjone SJ, Price IR, McGreevy PD 2006. Food distribution effects on the behaviour of captivecommon marmosets, Callithrix jacchus. Animal Welfare 15, 131-140"Both the cluster and dispersed feeder distributions increased foraging, and there was a trend ofreduced scratching and grooming."Blanchard M, Gruver S, Kirk P, McLain V, Zebrun M 2005. Look what's hanging around!Foraging feeder cup puzzles for cynomolgus macaques. Tech Talk 10(3), 3Foraging device is described and demonstrated. It is used by pair-housed cynos to retrieve theirdaily biscuit ration. No changes in body weights were noticed.Bloom KR, Cook M 1989. Environmental enrichment: Behavioral responses of rhesus to puzzlefeeders. Lab Animal 18(5), 25,27,29,31A commercial puzzle feeder loaded with 10 whole peanuts is tested in two single-housed adultmales. Average time spent foraging from the feeder was about 15 minutes.Bloomstrand M, Riddle K, Alford PL, Maple TL 1986. Objective evaluation of a behavioralenrichment device for captive chimpanzees (Pan troglodytes). Zoo Biology 5, 293-300Group-housed individuals spent on average 13 minutes per 120 minute-observation sessions"contacting" the puzzle box. "The most dominant males displayed the highest levels of overalluse of this enrichment device. It may be desirable to use this device in groups of animals withrelatively stable relationships and/or to increase the number of puzzles available to the group."Brent L, Eichberg JW 1991. Primate puzzleboard: A simple environmental enrichment device forcaptive chimpanzees. Zoo Biology 10, 353-360Treat-loaded transparent board with finger holes is attached to the top of the cage. Mean 'puzzleuse' during four 60-minute trials was 17%.Brent L, Long KE 1995. The behavioral response of individually caged baboons to feedingenrichment and the standard diet: A preliminary report. Contemporary Topics in LaboratoryAnimal Science 34(2), 65-69PVC pipe with finger holes, filled with a mixture of peanut butter and seeds. The mean amount offeeder use was 51 minutes per 60 minute observation sessions. "Increasing foragingopportunities in this study reduced abnormal behaviors from 16.4% of the data points in thebaseline condition to 4.9% and 5.7% in the chow [normal feeding condition] and feedercondition, respectively."

101Celli ML, Tomonagaa M, Udonob T, Teramotob M, Naganob K 2003. Tool use task asenvironmental enrichment for captive chimpanzees. Applied Animal Behaviour Science 81, 171-182“A device––honey in a bottle to be "fished" with artificial materials––that elicits tool use waspresented to six captive chimpanzees housed in pairs. The task successfully reduced inactivity byabout 52%, increased foraging opportunity from 0 to around 31% and elicited tool use andmanipulation. ... There was no statistical evidence of habituation to the device.”Corleto J 1997. A-mazing orangutans. The Shape of Enrichment 6(2), 9-10A food puzzle was constructed and modified several times to take into account the subject's highlevel of intelligence. "The results were everything I could have hoped for. Not only did hemaneuver the [food] items through the maze, he also did it with remarkable speed andconcentration."Crockett CM, Bellanca RU, Heffernan KS, Ronan DA, Bonn WF 2001. Puzzle Ball foragingdevice for laboratory monkeys. Laboratory Primate Newsletter 40(1), 4-7http://www.brown.edu/Research/Primate/lpn40-1.html#ball"Puzzle Balls are attached outside of the cage. .. Each animal was observed for 10 minutes aftersix pieces of cereal were placed in the ball. .. Overall, the subjects manipulated the Puzzle Ballduring 69.5% of the scan samples. ... Four of the seven subjects were able to successfully empty(eat plus spill) at least one type of Puzzle Ball in less than 10 minutes. (Most spilled about asmuch as they ate.) For the successful animals, it took an average of five minutes to empty thepuzzle. ...Even though the Puzzle Balls were empty during observations [four of seven cases], thesubjects manipulate them. ... We were pleased that the empty Puzzle Balls were associated with areduction in abnormal behavior."Evans HL, Taylor JD, Ernst J, Graefe JF 1989. Methods to evaluate the well-being of laboratoryprimates. Comparison of macaques and tamarins. Laboratory Animal Science 39, 318-323Single-caged long-tailed macaques took on average 8.7 seconds, paired tamarins took onaverage 15 seconds to retrieve one raisin from the pickup board [miniature ice cube trayattached to front of cage]. Experienced macaques emptied the commercial puzzle filled with thestandard food pellet ration within 20 minutes. "After a few days experience with the puzzle,macaques ate from both sources [puzzle feeder and conventional food cup] at the same time,showing no clear preference for either source. This indicates a motivation other than taste orcaloric need for performing the puzzle. The puzzle was not adaptable for tamarins since theydisplayed little or no appetite for any hard food items which could be pushed through the puzzle.Soft foods, such as grapes, raisins, marshmallows or marmoset diet were squeezed out throughthe small holes rather than being pushed through the maze of the puzzle."Fekete JM, Norcross JL, Newman JD 2000. Artificial turf foraging boards as environmentalenrichment for pair-housed female squirrel monkeys. Contemporary Topics in LaboratoryAnimal Science 39(2), 22-26"Five groups of pair-housed female squirrel monkeys were videotaped the week prior to, theweek following, and for 2 weeks during the enrichment phase, when treat-enhanced boards wereprovided for 2 h daily. During the first 30 min of daily enrichment, inactivity declined 35.3%,locomotion increased 3.8%, and board-related behavior occupied 36.3% of the activity budget;these changes were not evident after 1.5 h." Behavioral disorders were not altered by theforaging opportunity.

102Gilloux I, Gurnell J, Shepherdson D 1992. An enrichment device for great apes. Animal Welfare1, 279-289http://www.awionline.org/Lab_animals/biblio/aw1-279.htmThe animals could manipulate food items to the end of the pipe by poking sticks through holesdrilled along the side of the pipe facing them. When the food items reached the end of the pipe,the animals could reach them with their fingers through the welded mesh. No habituation to thefeeder was observed during 12 trials. Average time spent in 'feeder-oriented behaviour' during30 minute trials was approximately 8 minutes for [pair-housed] orangutans and [group-housed]chimpanzees and 5 minutes for [group-housed] gorillas.Glenn AS, Watson J 2007. Novel nonhuman primate puzzle feeder reduces food wastage andprovides environmental enrichment. AALAS [American Association for Laboratory AnimalScience] 58th National Meeting Official Program, 45 (Abstract)"The feeder dispenses monkey chow and fits on nonhuman primate group four quad rack cages... The original feeders dispensed 18 to 20 biscuits. At feeding time, the macaques removed all thebiscuits within 3 min, and those that were not eaten or stored in cheek pouches were pushed backthrough the feeder onto the room floor or dropped through the cage floor grid. .. Each feedertook approximately 1 h to make and cost approximately $60 in materials. .. Puzzle feederimplementation increased time spent foraging (approximately 20 min per biscuit), reduced foodwastage, and decreased clean-up time."Goodwin J 1997. The application, use, and effects of training and enrichment variables withJapanese snow macaques (Macaca fuscata) at the Central Park Wildlife Center. American Zooand Aquarium Association Regional Conference Proceedings, 510-515"Although the [commercial] primate puzzles proved to be a learning success, they were best usedsporadically to prevent the macaques from becoming bored with the puzzles."Kinsey JH, Jorgensen MJ, Platt DM, Hazen TJ 1996. Food puzzle feeders: Effects on self-bitingand stereotypy in individually housed monkeys. XVIth Congress of the InternationalPrimatological Society/XIXth Conference of the American Society of Primatologists, AbstractNo. 683Subjects were "observed not only when the food puzzle feeder had just been filled in the earlymorning but at several other time points throughout the day. ... There was no effect on selfaggression;however, a reduction in active stereotypic behavior was noted but only in the firsthour of each daily exposure."Lam K, Rupniak NMJ, Iversen SD 1991. Use of a grooming and foraging substrate to reducecage stereotypies in macaques. Journal of Medical Primatology 20, 104-109http://www.awionline.org/Lab_animals/biblio/jmp20-1.htm"Monkeys given fleece sprinkled with morsels of food did not groom the fleece, but foraged forlong periods (up to 27 min/h). Stereotyped behaviours were reduced by up to 73% by use of thefleece pad both alone and with foraging crumbles."LeBlanc D 1993. A simple device for stimulating gummivory in tamarins (Saguinus). AmericanZoo and Aquarium Association Regional Conference Proceedings, 212-219A simple, custom-made gum-tree was tested. "The artificial gum-tree was hung vertically fromthe top of the cage with two screw hooks, and placed ideally two or more feet from existingbranches and cage walls. All tamarins under 3.5 years in the study utilized the artificial gumtree.Older tamarins in general ignored this device, but did take gum arabic and diluted maplesyrup from a small food bowl."

Line SW, Markowitz H, Morgan KN, Strong S 1989. Evaluation of attempts to enrich theenvironment of single-caged non-human primates. In Animal Care and Use in BehavioralResearch: Regulation, Issues, and Applications Driscoll JW (ed), 103-117. Animal WelfareInformation Center, Beltsville, MD"Rhesus macaques removed monkey biscuits from a puzzle feeder "despite the fact that the samekind of food was available free-choice at the twice-daily feedings."Lutz CK, Farrow RA 1996. Foraging device for singly housed longtailed macaques does notreduce stereotypies. Contemporary Topics in Laboratory Animal Science 35(3), 75-78"All [ten] subjects manipulated the foraging boards, but stereotyped behaviors and activitylevels were not significantly affected by the presence of the boards." Subjects "used" the boardsapproximately 2 minutes per 30 minute-observation sessions. "No reduction in board usage wasobserved over time of day or on repeated presentation, indicating that there was no novelty effector reduction in motivation."Maki S, Alford PL, Bloomsmith MA, Franklin J 1989. Food puzzle device simulating termitefishing for captive chimpanzees (Pan troglodytes). American Journal of Primatology19(Supplement), 71-78"Significant reductions of abnormal behavior and significant increases in activity occurred withthe pipe feeder's availability. Species-typical tool-using activity occurred, and the use of the pipefeeder increased subjects' foraging and feeding activity toward more species-normative levels. ...Multiple puzzle devices should be available to group-housed animals to preclude ... aggressionarising from competition."Markowitz H 1979. Environmental enrichment and behavioral engineering for captive primates.In Captivity and Behavior Erwin J, Maple T, Mitchell G (eds), 217-238. Van NostrandReinhold, New York, NYFood dispensing apparatuses were developed and successfully implemented as feedingenrichment options for group-housed gibbons, siamangs and diana monkeys. "Frequently, oftenwith free food in their hands, they [gibbons] attempted to get the lights and levers to respond“and missed the opportunity to 'produce' food. "The problem of excess food lying around anddecaying on the floor had been reduced to a minimum."Maloney MA, Meiers ST, White J, Romano MA 2006 . Effects of three food enrichment itemson the behavior of black lemurs (Eulemur macaco macaco) and ringtail lemurs (Lemur catta) aththe Henson Robinson Zoo, Springfield, Illinois. Journal of Applied Animal Welfare Science 9,111-127"The lemurs' behavior appeared [sic] to be most affected by the food enrichment item thatrequired the most manipulation."Mentz I, Perret K 1999. Environmental enrichment bei Flachlandgorillas (Gorilla g. gorilla) -Beobachtungen zur Nahrungsaufnahme und zum Manipulationsverhalten. Der ZoologischeGarten 69, 1-15“Behavioural enrichment possibilities include greater dispersal of food as well as the providingof food boxes or raisin sticks. Each gorilla was engaged intensively with the raisin sticks [5.8%of day], but were especially responsive to the food boxes [15,2% of day]."103

104Molzen EM, French JA 1989. The problem of foraging in captive callitrichid primates:Behavioral time budgets and foraging skills. In Housing, Care and Psychological Wellbeing ofCaptive and Laboratory Primates Segal EF (ed), 89-101. Noyes Publications, Park RidgeThe group-housed animals had to hang from above, or sit on the covered bowl to obtain raisinsthat were mixed with ground corn cob. "The device reduced foraging yield and increasedforaging effort to levels similar to those observed in free-ranging populations. These dramaticchanges in behavioral profiles were produced even though the foraging device was supplementalto, rather than a replacement for, standard provisioning."Murchison MA 1992. Task-oriented feeding device for singly caged primates. LaboratoryPrimate Newsletter 31(1), 9-11http://www.brown.edu/Research/Primate/lpn31-1.html#taskA perforated hard plastic ball loaded with peanuts was attached to the outside of the cage. "Theanimals spent most of their time sitting on their cage perches. Manipulating the foraging devicewas the second most time-consuming activity [males 22%, females 8%]."Murchison MA 1994. Primary forage feeder for singly-caged macaques. Laboratory PrimateNewsletter 33(1), 7-8http://www.brown.edu/Research/Primate/lpn33-1.html#mark"Apparently the animals consumed nearly all the food retrieved from the forage feeders, leavingless on the cage floor to become contaminated. The animals spent significantly more timeforaging with the forage feeder than the standard feeder."Murchison MA 1995. Forage feeder box for single animal cages. Laboratory Primate Newsletter34(1), 1-2http://www.brown.edu/Research/Primate/lpn34-1.html#forageStandard feeder with small access holes rather than one big access hole. Time spent foragingduring the first hour after biscuit distribution increased from 51 seconds when 40 biscuits werepresented in the standard feeder [one large access hole] to 400 seconds when 40 biscuits werepresented in the forage feeder [four small access holes]. "There were no differences between thestandard and forage feeders in number of biscuits fed and consumed." More biscuits fell on thecage floor and beneath the cage on the floor of the room in the standard feeder situation than inthe forage feeder situation.Murphy DE 1976. Enrichment and occupational devices for orang utans and chimpanzees.International Zoo News 137(23.5), 24-26http://www.awionline.org/Lab_animals/biblio/izn-mur.htm"A heavy metal cylinder, 60 cm long and 45 cm in diameter, was capped on each end and boltedto a platform. Three 8 cm holes in the cylinder allowed access to the inside. A short section of arubber hose was chained near one hole in the cylinder. The chimps were able to use the hose asa tool in a manner similar to fishing for termites or opening a beehive in the wild. Thechimpanzees rapidly emptied the container of their morning meal with ingenious manipulationand intense interest. .... Chimps and orangs manipulated their feeders even though ample foodwas available. On days when the device could be operated by the orang utans, they wereobserved climbing in the structure about thirty per cent more often than when the device was notoperating. There was an apparent increase in general activity. The most encouraging result wasa reduction in the female's stereotyped pacing. The environmental enrichment of the chimpexhibit has resulted in a decrease in observable coprophagy.”

105Novak MA, Kinsey JH, Jorgensen MJ, Hazen TJ 1998. Effects of puzzle feeders on pathologicalbehavior in individually housed rhesus monkeys. American Journal of Primatology 46, 213-227"Manipulation of the puzzle feeder was associated with a reduction in pacing and rocking in allsubjects; but this effect was transient, occurring only during the first hour after the puzzle feederwas filled with treats. Puzzle feeder manipulation had no effect on self-injurious behavior.”Nishimura S 2006. Owl monkey enrichment ideas. Tech Talk 11(1)"One enrichment item we use is a small suet basket. We place pieces of fresh fruits, dried fruits,nuts, and ice cubes inside the basket and hang it inside the cages and kennels. The holes in thesuet basket are too small for the Aotus to reach through, so they spend a good amount of timetrying to manipulate the food pieces with their fingers and teeth.Another form of enrichment used is a small plastic baskets filled with hay, pine shavings, or SaniChips to which we add a few nuts, cereal pieces, or mealworms." These two items increaseforaging time.O'Connor E, Reinhardt V 1994. Caged stumptailed macaques voluntarily work for ordinary food.In Touch 1(1), 10-11http://www.awionline.org/Lab_animals/biblio/tou-food.htm"Dan spent 286 seconds retrieving 12 biscuits from the food puzzle after leaving 21 freelyavailable dish-biscuits untouched."Perret K, Büchner S, Adler HJ 1998. Beschäftigungsprogramme für Schimpansen (Pantroglodytes) im Zoo. Der Zoologische Garten 68, 95-111An effective feeding enrichment program for group-housed chimpanzees is described andassessed. The program resulted in a more than two-fold increase in time spent foraging (23.6%vs. 57.4% per day).Poffe A, Melotto S, Gerrard PA 1995. Comparison of four environmental enrichment strategiesin captive common marmosets (Callithrix jacchus). Primate Report 42, 24-25"Access to the puzzles was accompanied by increase in social interaction and activity anddecrease 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 alterbehaviour."Preilowski B, Reger M, Engele H 1988. Combining scientific experimentation with conventionalhousing: A pilot study with rhesus monkeys. American Journal of Primatology 14, 223-234"The testing apparatus ... was connected to a computer that controlled the test and thedistribution of regular monkey chow as reward." Manipulatory activity required by theapparatus reduced motor stereotypies but not self-biting in single-housed subjects.Prist. P., Pizzutto CS, Hashimoto C 2004. Woven vine balls and baskets as feeding enrichmentfor howler monkeys. Shape of Enrichment 14(2), 1-2http://www.enrichment.org/articles/142Howlers.pdf"Our results showed that the animals spent more time foraging when the feeder balls were used[compared to the baskets], since it was more difficult to reach the leaves. The monkeys alsoexplored each of the baskets and stopped spending most of their time on the floor. We concludedthat these two enrichment ideas increased the animals' activity through play and exploration,and also increased their use of vertical space and reduced their time on the floor. Thesebehaviors are more species-typical and appropriate for arboreal monkeys."

106Reinhardt V 1992. Foraging for commercial chow. Laboratory Primate Newsletter 31(2), 10http://www.brown.edu/Research/Primate/lpn31-2.html#chowWhile sitting on swings, platforms or other elevated structures, or clinging to the mesh,individual animals seize a piece of chow and retrieve it through the mesh of the ceiling. “Thissimple 'food puzzle' not only promotes non-injurious foraging skills but also keeps the floorrelatively clean by avoiding undue spoilage of food. The animals only work for food that theyactually eat."Reinhardt V 1993. Enticing nonhuman primates to forage for their standard biscuit ration. ZooBiology 12, 307-312http://www.awionline.org/Lab_animals/biblio/zb12-30.htmOrdinary feeder-boxes were converted into food puzzles by remounting them onto the mesh of thefront of the cages, away from original access holes. The total amount of time [pair-housed] adultmale rhesus macaques engaged in gathering the standard biscuit ration was 141 times higher atfood puzzles [42.2 min] than at feeder-boxes [0.3 min].Reinhardt V 1993. Evaluation of an inexpensive custom-made food puzzle used as primaryfeeder for pair-housed rhesus macaques. Laboratory Primate Newsletter 32(3), 7-8http://www.brown.edu/Research/Primate/lpn32-3.html#food"Working for their standard food rather than collecting it from freely accessible food boxes didnot impair the [pair-housed] animals' body weight maintenance, suggesting that their generalhealth was not impaired by the new feeding technique."Reinhardt V 1993. Promoting increased foraging behaviour in caged stumptailed macaques.Folia Primatologica 61, 47-51"Simply remounting the food box [of single-housed subjects] a few centimeters away from theaccess hole resulted in a 69-fold increase in total time engaged in [biscuit ration] foodretrievingactivities."Reinhardt V 1993. Using the mesh ceiling as a food puzzle to encourage foraging behaviour incaged rhesus macaque (Macaca mulatta). Animal Welfare 2, 165-172http://www.awionline.org/Lab_animals/biblio/aw3mesh.htm"Daily commercial dry food rations consisting of 33 bar-shaped or 16 star-shaped biscuits peranimal were placed on the mesh ceiling of the cages instead of in the feed-boxes. This induced an80-fold increase and 289-fold increase, respectively, in foraging time" in the pair-housed males.Reinhardt V 1994. Caged rhesus macaques voluntarily work for ordinary food. Primates 35, 95-98http://www.awionline.org/Lab_animals/biblio/primat~1.htmIndividuals spent on average 32 sec retrieving biscuits from the ordinary food box, and 673 secretrieving biscuits from the food puzzle. "It was inferred that the animals voluntarily worked forordinary food, with the expression of foraging activities serving as its own reward."Riviello MC 1995. The use of feeding board as an environmental enrichment device for tuftedcapuchin monkeys (Cebus apella). Primate Report 42, 23-24http://www.awionline.org/Lab_animals/biblio/pr42-2~2.htm"Results show that the feeding board [on which seeds were scattered] were almost always in use[during 30-minute observations]” by the group-housed animals.

107Schapiro SJ, Suarez SA, Porter LM, Bloomsmith MA 1996. The effects of different types offeeding enhancements on the behaviour of single-caged, yearling rhesus macaques. AnimalWelfare 5, 129-138http://www.awionline.org/Lab_animals/biblio/aw5-129.htm"Enrichment use" in minutes/observation hour was as follows: Turf mats 25.8 minutes; Acrylicpuzzles 22.1 minutes; Produce 17.4 minutes; Frozen juice 14.6 minutes.Spector M, Kowalczky MA, Fortman JD, Bennett BT 1994. Design and implementation of aprimate foraging tray. Contemporary Topics in Laboratory Animal Science 33(5), 54-55"Excreta trays have been modified to include [small] foraging trays. The trays are placed underthe cages. Videotape observation of [single-housed] 24 animals indicates the trays provide from30 to over 120 min of foraging activity."(4,2) SubstratesAnderson JR, Chamove AS 1984. Allowing captive primates to forage. In Standards inLaboratory Animal Management. Proceedings of a Symposium 253-256. UniversitiesFederation Animal Welfare, Potters Bar, UKhttp://www.awionline.org/Lab_animals/biblio/ufaw-2~1.htmA woodchip litter substrate reduces abnormal behaviours, primarily self-aggression, andencourages foraging, even in the absence of grain.Baker KC 1997. Straw and forage material ameliorate abnormal behaviors in adult chimpanzees.Zoo Biology 16, 225-236"In an [successful] effort to reduce abnormal behaviors, especially regurgitation andreingestion, and promote higher activity levels [locomoting and playing], straw and scatteredforage material were added to the enclosures of 13 indoor-housed chimpanzees living in pairsand trios."Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 4.3. FeedingEnrichment. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/enrich.html#feed-prim”Wood shavings in the catch pans provide an ideal substrate to foster foraging activities. Ondays when we change the pans — three times a week — we sprinkle sunflower seeds on theshavings. Our rhesus and squirrel monkeys then search with their fingers through the litter andpull the seeds through the floor grids, eat them or store them in their cheek pouches. Since wechange the pans, rather than dump the bedding, we don’t have any drainage problems in therooms. This feeding enrichment technique doesn’t require undue extra work time in our colonyof approximately 130 monkeys. I'd say the benefit of being able to provide even a brief period of"natural" foraging behavior for our caged primates is worth the little additional time it takes toput the bedding in the pans and add a handful of seeds.“Blois-Heulin C, Jubin R 2004. Influence of the presence of seeds and litter on the behaviour ofcaptive red-capped mangabeys Cercocebus torquatus torquatus. Applied Animal BehaviourScience 85, 340-362"The addition of both litter and seeds induced a significant decline in self-directed activities anda significant increase in search for food. The presence of litter, with or without seeds, induceddiversification of occupation of space."

108Boccia ML 1989. Long-term effects of a natural foraging task on aggression and stereotypies insocially housed pigtail macaques. Laboratory Primate Newsletter 28(2), 18-19http://www.brown.edu/Research/Primate/lpn28-2.html#maria"A supplementary feeding of ... sunflower seeds were dispersed throughout the cage in thewoodchip bedding ... 4-6 hours after the group was fed their daily ration of chow and fruit. ...Two months following the introduction of the foraging task ... stereotypies remained depressed,and hairpulling remained rare. ... Exploration remained elevated, and agonistic behaviorsremained low."Brown DL, Gold KC 1997. Effects of straw bedding on non-social and abnormal behavior ofcaptive lowland gorillas (Gorilla gorilla gorilla). In Proceedings on the 2nd InternationalConference on Environmental Enrichment Holst B (ed), 27-35. Copenhagen Zoo, Frederiksberg,Denmark"Two individuals were frequently observed to hold their ears or head while the exhibit was in anunbedded condition. This behavior virtually disappeared in the enriched condition. ... Of theeight individuals found to engage in coprophagy, five individuals were observed to exhibit thisbehavior in solely the unbedded condition."Bryant CE, Rupniak NMJ, Iversen SD 1988. Effects of different environmental enrichmentdevices on cage stereotypies and autoaggression in captive cynomolgus monkeys. JournalMedical Primatology 17, 257-269http://www.awionline.org/Lab_animals/biblio/jmp17-2.htm"Of the many activities available in the playpen, those that consistently captured the attention ofall the [single-housed] animals throughout the 3-week observation period were foraging [inwoodchip litter scattered with sunflower seeds placed below the grid floor of the cage]."Burt DA, Plant M 1990. Observations on a caging system for housing stump-tailed macaques.Animal Technology 41, 175-179http://www.awionline.org/Lab_animals/biblio/at-burt.htm"The removal of metal grids at the bottom of the cage and the introduction of direct access to asubstrate mixed with cereals and seeds, had a beneficial effect on the psychological well-being ofthe [single-housed] macaques by allowing foraging and, in our experience, up to 60% of ourmacaques' day is now spent in this pursuit."Byrne GD, Suomi SJ 1991. Effects of woodchips and buried food on behavior patterns andpsychological well-being of captive rhesus monkeys. American Journal of Primatology 23, 141-151The addition of woodchips increased exploration and feeding levels. Burial of regular monkeychow in woodchips had little effect on behavior beyond that of the woodchips alone, increasingexploration and decreasing passivity. The addition of sunflower seeds to the woodchipsencouraged increased feeding and exploration and led to decreased passivity and socialinteraction. No effect on abnormal behavior.Chamove AS 2001. Floor-covering research benefits primates. Australian Primatology 14(3), 16-19http://www.lisp.com.au/~primate/arnold.htm“The basic study involved scattering the smallest food items we could find either onto the barefloor or into some substrate... Aggression was reduced. .. Food intake was more evenlydistributed. ... We found NO bad effects ... The monkeys were foraging 14% of the time through

109the wood-chips looking for and eating grain even though that same grain was available fromhoppers full of the stuff nearby."Combette C, Anderson JR 1991. Réponses à deux techniques d’enrichissement environmentalchez deux espèces de primates en laboratoire (Cebus apella, Lemur macaco). Cahiersd'Ethologie 11, 1-16"Locomotion almost doubled in the lemurs when small food items were added to the litter, butonly the [group-housed] capuchins engaged in foraging activities to any extent."Grief L, Fritz J, Maki S 1992. Alternative forage types for captive chimpanzees. LaboratoryPrimate Newsletter 31(2), 11-13http://www.brown.edu/Research/Primate/lpn31-2.html#grief"Chicken scratch, because it is small and harder to find [in the litter], elicited the most foragingof the three foods ['sweet feed', popcorn]. It is very encouraging to see the chimpanzees stillforaging late in the day for these small kernels. In addition, for subjects such as our blindanimal, who had one of the highest foraging scores in our study, this [inexpensive] enrichmentcannot be overemphasized."Lutz CK, Novak MA 1995. Use of foraging racks and shavings as enrichment tools for groups ofrhesus monkeys (Macaca mulatta). Zoo Biology 14, 463-474Antagonism decreased when the animals had to search for food in wood shavings.Mahoney CJ 1992. Some thoughts on psychological enrichment. Lab Animal 21(5), 27,29,32-37Pans from rabbit cages can be used as foraging trays. "We fill the trays with wood chips or othertypes of bedding scattered with crushed maize, rice, or raisins, and attach them to the undersideof the cage floors with bungie cords, thereby providing the animals with hours of searchingactivity."Stegenga L 1993. Modifying spider monkey behavior with the use of environmental variables.The Shape of Enrichment 2(3), 3-4"During baseline observations, the monkeys spent 7.3% of the time feeding, but when leaveswere added to the enclosure, feeding activities increased to 13.1% of the time. ... When theleaves were added to the enclosure, playtime was more significant."(4,3) Produce

110Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 4.4.Coconuts. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/enrich.html#coconuts"Rhesus don’t care much about coconuts, but stump-tailed macaques are fascinated by them anddo not get tired ”working“ on them until the last morsel has disappeared in the drop pan. Itnever occurred that one of the monkeys somehow became injured while processing a nut.I give whole coconuts to our individually caged cynos. More than anything, they likethem for grooming purposes. It gives them something else to do besides bite themselves. I alsohad a female who carried her coconut around as if it was a baby, constantly clutching it to herchest, and lip smacking to it, grooming it, etc. She was a chronic alopecia case. The coconutalleviated some — unfortunately not all — of her stereotypical hair pulling behavior."Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 4.3. FeedingEnrichment. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/enrich.html#feed-prim”I have given whole watermelons to group-housed rhesus, cynos, bonnet and stump-tailedmacaques for several years without noticeable adverse effects. It would be a waste of time to cutthe melons into small pieces. The monkeys first gnaw a hole into the rind and then ”dig“ into thesoft and juicy part. They really like this and are kept busy until the last morsel has been eaten.They usually discard the rind, but before they do so they thoroughly remove any soft materialand eat it. This usually creates quite a mess, but I don’t mind cleaning it up, because the animalsenjoy this type of feeding enrichment so much.We give whole pumpkins to rhesus and cynos in both single- and group-housedenvironments. I would say that this is one of the most effective foraging device we have evergiven our animals. All of them spent hours processing their pumpkin!I give whole corn with the husk to our pair- and group-housed rhesus and baboons. Theylove it, and I enjoy observing them "peel and eat," leaving a big mess after they have finished.They gnaw the cob into little pieces that finally fall through the grid floor on the pans. I cannotsay whether they actually also eat pieces of the cob, but we have never encountered any healthrelatedproblem. I don't mind cleaning up the mess; its worth the treat!We use corn on the cob for all our caged cynos, rhesus and vervets. The animals give theimpression that they love processing and eating the corn. They typically pick the kennels bothwith their hands and their teeth. When they are done, they proceed gnawing on the cob. I don’tknow if they actually ingest pieces of it. Even if they do, we have never encountered any clinicalproblems.“Beirise JH, Reinhardt V 1992. Three inexpensive environmental enrichment options for grouphousedMacaca mulatta. Laboratory Primate Newsletter 31(1), 7-8http://www.brown.edu/Research/Primate/lpn31-1.html#three"We distributed the following enrichment materials on the floor once a week, each on a differentday: (1) 1 kg roasted peanuts in their shells; (2) 32 ears of hard corn; (3) one non-corrugatedcardboard box. ... After a habituation period of 8 weeks, [2-hour] behavioral observations weremade. ...The corn was the most effective eliciter of foraging activity, engaging the animals about77% of the time. Next in effectiveness was the box (65%) and finally the peanuts (47%)."

111Bennett BT, Spector MR 1989. The use of naturally occurring manipulanda to improve thepsychological well-being of singly housed baboons. Journal of the American Veterinary MedicalAssociation 194, 1782 (Abstract)The single-housed animals demonstrated a marked reduction of cage stereotypy during the timethey had the corn to manipulate.Nadler RD, Herndon JG, Metz B, Ferrer AC, Erwin J 1992. Environmental enrichment byvaried feeding strategies for individually caged young chimpanzees. In ChimpanzeeConservation and Public Health: Environments for the Future Erwin J, Landon JC (eds), 137-145. Diagnon/Bioqual, Rockville, MDProviding an ear of unhusked corn daily or on alternate days, in addition to laboratory chow,resulted in more time spent contacting food [primarily the corn] an hour after feeding [34% &55%] than feeding laboratory chow alone [8% & 5%]. Seven of eight [single-housed] animalsexhibited less stereotypy on the days they received the ear of corn. Stereotypical behavior, whichoccurs at relatively low frequencies under natural conditions, was reduced somewhat when theanimals were fed three [vs. one] meals."Waugh C 2002. Coconuts as enrichment item for macaques.Wisconsin Primate Research Center,University of Wisconsin-Madison, Primate Enrichment Forum (electronic discussion group),October 24, 2002"I give whole coconuts, and have had them last a long time (days/weeks), until we exchange themwith new ones (they are really durable). I have had one male cyno break one open by throwing itaround his cage for a few days in a row, and even then it just cracked - he loved the milk andcontinued to amuse himself by trying to get to the fleshy part inside until we eventually had totake it away from him because it got kind of gross! More than anything, I think they like them forgrooming purposes - it gives them something else to do besides bite themselves. I also had afemale cyno who carried her coconut around like it was a baby, constantly clutching it to herchest, and lip smacking to it, grooming it, etc. She was a chronic alopecia case, and the coconutaided in her problem somewhat also. In my experience, it is a cheap, quite helpful, andinteresting alternative!”(4,4) Ice and WaterAnderson JR, Peignot P, Adelbrecht C 1992. Task-directed and recreational underwaterswimming in captive rhesus monkeys (Macaca mulatta). Laboratory Primate Newsletter 31(4),1-4http://www.brown.edu/Research/Primate/lpn31-4.html#swim"Facilitating thermoregulation and increasing [solitary and social] play are two reasons toconsider a swimming facility to be a cheap and clean environmental enrichment."Anonymous 2006. Is a swimming pool safe for macaques? A discussion. Laboratory PrimateNewsletter 45(3), 13http://www.brown.edu/Research/Primate/lpn45-3.html#swimExperience suggest that the provision of a shallow swimming pool provides an effective, safeenvironmental enrichment option for macaques.Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 8.7.Swimming Pools for Macaques. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/safety.html#swim

112”We give our pair-housed cynos ”bathtubs,“ filled with 30 to 40 cm deep warm water, a fewtimes a week, and have never encountered any problems other than a lot of splashing. Somemonkeys take luxurious baths, others climb a perch and jump into the water, others sit on theside walls and drag their hands in the water, and others wash their fruit in the water. Usually themonkeys make a real mess within the first half hour, and yes they do urinate/defecate in thewater. We empty the tubs after about two hours, if the monkeys haven’t done it alreadythemselves — which is often the case.There are a few published articles on the use of swimming pools for rhesus, long-tailedand Japanese macaques. None of these papers mention any safety or hygienic problems.“Fritz J, Howell S 1993. The disappearing ice cube. Laboratory Primate Newsletter 32(1), 8http://www.brown.edu/Research/Primate/lpn32-1.html#iceIce ”cubes are distributed across the floor, hidden in high plastic barrels (we call these igloos),tucked into corners of the cages, etc. As the animals come out, the excitement of the hunt startsand continues until the last ice cube is found. Hoarders clutch them to their chests, ... others filltheir mouths and carry the cubes to the top of the cage, where they lay them down and watchcarefully as the cubes get smaller and smaller. Still others have learned to skate through thepuddles, making mad dashes in order to slide further and further.“ No detrimental effects havebeen found of providing the ice cubes.Gilbert SG, Wrenshall E 1989. Environmental enrichment for monkeys used in behavioraltoxicology studies. In Housing, Care and Psychological Wellbeing of Captive and LaboratoryPrimates Segal EF (ed), 244-254. Noyes Publications, Park Ridge, NJ"The pools [stainless-steel frame with 3/8” Plexiglas sides] have been a tremendous success withthe younger [cynomolgus] monkeys, who adapt easily to water and are instinctively goodswimmers. They will swim under water with their eyes open looking for the raisins and playingwith each other."Hazlewood SJ 2001. From beagles to marmosets - The development of a marmoset breedingcage. Animal Technology 52, 149-152A “water bath was found to be of little interest to the marmosets, other than to use it as a toilet!"McNulty J 1993. Enrichment for primates in a toxicology facility. Laboratory Primate Newsletter32(2), 16http://www.brown.edu/Research/Primate/lpn32-2.html#judiIce cubes have "been given to hundreds of monkeys, and we found no ill effects (e.g., brokenteeth)."Parks KA, Novak MA 1993. Observations of increased activity and tool use in captive rhesusmonkeys exposed to troughs of water. American Journal of Primatology 29, 13-25"These results suggest that exposure to water sources may elicit a broad spectrum of speciestypicalactivity and may be a simple and inexpensive way to enrich the environment of captive[group-housed] rhesus monkeys. ... Standing water was more effective than running water inincreasing exploration and object manipulation."Poulsen E 1994. Monkeys on ice. The Shape of Enrichment 3(1), 7"I spent an hour or so shoveling fresh, clean new snow into a huge plastic bin and dumped thelot on the floors of each small primate and prosimian indoor enclosure... The event was atremendous success"

113Rademacher A 1997. Gorilla treats served poolside. The Shape of Enrichment 6(3), 11"Initially, [Rocky, the gorilla], was hesitant and seemed a bit irritated at this presentation offood [floating on the pool's surface], but eventually he waded into the water and retrieved thetreats. Rocky will now wade into the pool when food items are tossed in; we no longer need tofloat them on the surface. He even makes use of the pool occasionally during our hot Arkansassummers, sitting on the bottom, with his arms stretched along the pool's edge.”Schafer J 2005. Primate popsicles. Tech Talk 10(3), 4"When the frozen enrichment treats were first provided to our rhesus macaques, they showed agreat deal of interest and worked steadily at removing the food from the ice. After severalmonths of using this enrichment, the primates still enjoy their frozen treats."Steele TL, Butler NA, Segar MT, Olson SM 1995. Preferences for food location and foragingrequirements in white-handed gibbons. American Zoo and Aquarium Association RegionalConference Proceedings, 151-158"Mixing ice with the food [in buckets] reduced eating time slightly but substantially increasedforaging time. Foraging was much more extensive from the top bucket and significantly morefood was gathered from this source than from the bottom bucket. The dominance of the maleduring feeding suggests that more than one food source should be available for multipleanimals."(4,5) Food Preparation and Feeding ScheduleKerridge FJ 2005. Environmental enrichment to address behavioral differences between wild andcaptive black-and-white ruffed lemurs (Varecia variegata). American Journal of Primatology 66,71-84"Behavioral enrichment experiments were carried out in which whole rather than chopped fruitwas provided and presented in a more naturalistic manner [whole fruit suspended by sisal orjute from wooden polses]. ... Manual manipulation of dietary items increased. Time spent feedingalso increased significantly. .. The novel feeding method successfully stimulated the animals to

114use their hands to obtain and process fruit. It also necessitated bipedal and tripedal suspension... The enrichment increased the time spent feeding to levels similar to those seen in the wild."Parks KA, Novak MA 1993. Observations of increased activity and tool use in captive rhesusmonkeys exposed to troughs of water. American Journal of Primatology 29, 13-25"These results suggest that exposure to water sources may elicit a broad spectrum of speciestypicalactivity and may be a simple and inexpensive way to enrich the environment of captive[group-housed] rhesus monkeys. ... Standing water was more effective than running water inincreasing exploration and object manipulation."Potratz KR, Boettcher C 2006. Rhesus diet smoothies. Tech Talk 11(4), 5There are a number of situations in which non-human primates need a special diet to provideadditional calories. The receipe for a Chow Smoothie for Rhesus macaques is described andconsists in incorporating the animal's regular food, tailoring the smoothie to the individualanimal's needs, and adding specific supplements, medications, and different flavors. Thesmoothie was tested on 40 Rhesus macaques ranging in age from 2 to 25 years.Poulsen E 1994. Monkeys on ice. The Shape of Enrichment 3(1), 7"I spent an hour or so shoveling fresh, clean new snow into a huge plastic bin and dumped thelot on the floors of each small primate and prosimian indoor enclosure... The event was atremendous success."Rademacher A 1997. Gorilla treats served poolside. The Shape of Enrichment 6(3), 11"Initially, Rocky was hesitant and seemed a bit irritated at this presentation of food [floating onthe pool's surface], but eventually he waded into the water and retrieved the treats. Rocky willnow wade into the pool when food items are tossed in; we no longer need to float them on thesurface. He even makes use of the pool occasionally during our hot Arkansas summers, sittingon the bottom, with his arms stretched along the pool's edge."Steele TL, Butler NA, Segar MT, Olson SM 1995. Preferences for food location and foragingrequirements in white-handed gibbons. American Zoo and Aquarium Association RegionalConference Proceedings, 151-158"Mixing ice with the food [in buckets] reduced eating time slightly but substantially increasedforaging time. Foraging was much more extensive from the top bucket and significantly morefood was gathered from this source than from the bottom bucket. The dominance of the maleduring feeding suggests that more than one food source should be available for multipleanimals."(5) Promoting Arboreal Behavior(5,1) The Importance of Access to Vertical Dimension of SpaceBernstein IS, Draper WA 1964. The behaviour of juvenile rhesus monkeys in groups. AnimalBehaviour 12, 84-91Subjects spent 48%-72% of the time in the upper one-third of the compound.Bloomsmith MA, Lambeth SP, Haberstroh MD 1999. Chimpanzee use of enclosures. AmericanJournal of Primatology 49, 36Group-housed chimpanzees spent 43% of their time off the ground.

115Buchanan-Smith HM 1991. A field study on the red-bellied tamarin, Saguinus l. labiatus, inBoliva. International Journal of Primatology 12, 259-276Tamarins spent 90% of their time in the upper half of their 186 cm-high cages when observationswere made from a hide.Clarence WM, Scott JP, Dorris MC, Paré M 2006. Use of enclosures providing verticaldimension by captive rhesus monkeys (Macaca mulatta) involved in biomedical research.JAALAS [Contemporary Topics in Laboratory Animal Science], 45(5), 31-34"The monkeys visited more often and occupied for longer time regions at or above human eyelevel [perches and top home cage] than lower regions." The total percentage of time spent in thetop home cage was found to be significantly greater than in the bottom home cage."European Commission 2002. The Welfare of Non-human Primates - Report of the ScientificCommitte on Animal Health and Animal Welfare. European Commission, Strasbourg, Francehttp://europa.eu.int/comm/food/fs/sc/scah/out83_en.pdf"Enclosures for nonhuman primates should be equipped with one or more elevated restingsurfaces (to a position higher than the level at which they perceive threatening factors, e.g.,humans) and installed in such a way that an animal can sit on them comfortably. Perches orshelves should be provided in all cages. Arboreal species should be given adequate verticalspace to allow the expression of normal locomotory behaviour. Primates should not be placed indouble-tiered caging unless the arrangement permits adequate vertical movement for theanimal."Goff C, Howell SM, Fritz J, Nankivell B 1994. Space use and proximity of captive chimpanzees(Pan troglodytes) mother/offspring pairs. Zoo Biology 13, 61-68"Results confirmed the importance of vertical cage dimension and suggested the provision ofhorizontal substrates above the enclosure floor is important."Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housingand Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London, UKhttp://scienceandresearch.homeoffice.gov.uk/animal-research/legislation/"The use of space by primates means that cage volume is important. Virtually all show a verticalflight reaction. Cage height should allow for this and should permit the animals to stand erect,jump and climb, and to sit on a perch without head or tail touching the cage."International Primatological Society 1993. IPS International guidelines for the acquisition, careand breeding of nonhuman primates, Codes of Practice 1-3. Primate Report 35, 3-29http://pin.primate.wisc.edu/ips/codes.txt"The vertical dimension of the cage is of importance [because of the vertical flight response] andcages where the monkey is able to perch above human eye level are recommended."Kaumanns W, Schönmann U 1997. Requirements for cebids. Primate Report 49, 71-91"Arboreal species need ... enclosures which allow a differentiated moving in the verticaldimension. They should be able to use spatial positions which are above the level ... ofthreatening humans or potential dangerous events in their environment. Cage positions in akeeping room below the eye level of human can be a source of permanent stress, because theyare incompatible with adaptive tendencies of arboreal primates to avoid risks by using higherparts of the habitat."

116MacLean E, Roberts Prior S 2006. View from the top. AWI (Animal Welfare Institute) Quarterly55(3), 7http://www.awionline.org/quarterly/view_from_top.html"Across both conditions, monkeys showed a strong preference for the upper-row cage indicatingthat elevation was more important than illumination in guiding location preference. Althoughmonkeys did increase the amount of time that they spent in the lower row during periods ofreversed lighting, this trend was not significant. Nonetheless, we do not interpret this result asevidence that sufficient lighting is not important to captive monkeys. Rather, we believe thatmonkeys' consistent preference for the upper-row reflects the paramount importance of access toelevated space."National Research Council 1998. The Psychological Well-Being of Nonhuman PrimatesNational Academy Press, Washington, DChttp://fermat.nap.edu/books/0309052335/html/index.html"Under natural conditions, many primates spend much of their lives aboveground and escapeupward to avoid terrestrial threats. Therefore, these animals might perceive the presence ofhumans above them as particularly threatening. ... Even macaques, which some describe assemiterrestrial, spend most of the day in elevated locations and seek the refuge of trees at night.... Optimal use of available cage space might well depend more on the placement of perches,platforms, moving and stationary supports, and refuges than on cage size itself."Reinhardt V, Liss C, Stevens C 1996. Space requirement stipulations for caged nonhumanprimates in the United States: A critical review. Animal Welfare 5, 361-372http://www.awionline.org/Lab_animals/biblio/aw4space.htm"Having no stimulatory value, space alone does not enhance an animal's environment. ... Legalspace requirements for non-human primates are not adequate unless they stipulate that sufficientheight be provided to accommodate properly placed elevated structures."Ross SR, Lukasb KE 2006. Use of space in a non-naturalistic environment by chimpanzees (Pantroglodytes) and lowland gorillas (Gorilla gorilla gorilla) . Applied Animal Behaviour Science96, 143-152"Chimpanzees preferred the highest tier of the enclosure and the gorillas preferred the floorlevel. Both species showed preferences for doorways, corners and the mesh barriers adjacent tokeeper areas."Taylor L, Owens A 2004. Enclosure use by aged squirrel monkeys (Saimiri sciureus). AmericanJournal of Primatology 62(Supplement), 85 (Abstract)http://www.asp.org/asp2004/abstractDisplay.cfm?abstractID=800&confEventID=808A group of squirrel monkeys was translocated from an indoor exhibit to an outdoor enclosure."The monkeys were scored most often among the largest and highest branches in the tallest treein the enclosure (17.7% ). .. None were ever scored on the ground, despite the water sourcebeing there and the insect foraging opportunities.”Westlund K Preference of the vertical dimension of cyno pairs living in high cages. LaboratoryAnimal Refinement and Enrichment Forum (electronic discussion group), November 28, 2002"In a quantitative study I did on pair-housed cynos the animals spent 95% of their waking time inthe upper part of the cage (being housed in a system that resembles a double-tier system, butwith vertical access to upper and lower sections) - which suggests that their preference along thegradient of height is unequivocal! No bedding was provided on any of the cage floors, and all

117food was given in the bottom section. Even so, animals would bring the food to the upper partand consume it there."(5,2) Elevated StructuresAbee CR 1985. Medical care and management of the squirrel monkey. In Handbook of SquirrelMonkey Research Rosenblum LA, Coe CL (ed), 447-488. Plenum Press, New York, NY"Squirrel monkeys .... lack ischeal callosities and therefore are prone to the development of soresif they are not provided with suitable structures on which to climb and perch. Squirrel monkeysprefer a flat, shelf-type surface for sleeping, but animals using such perches frequently developpressure ulcers on the dorsal aspect of the tail. By using large-diameter plastic pipe (1.5 inch), ahighly desirable perch can be provided. These perches have a broad surface yet are sufficientlycontoured to avoid tail sores."Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 4.17. VerticalSpace Enhancement. Washington, DC: Animal Welfare Institutehhttp://www.awionline.org/pubs/LAREF/enrich.html#vertical-prim"Most of the primates' natural environment is "fixed.“ Even a tree is "fixed;“ it's only at the endof branches where a monkey in nature would have the sensation of anything like a swingingperch. A fixed perch is a great thing for a monkey. We used to hang numerous swings andmovable raised structures into the enclosure of our group-housed cynos, but we could see veryclearly that they prefer the stable perches or platforms. Our animals very rarely used ropes orswings. The only ones using those elements were babies and juveniles.In the caging systems we use there is no bottom tier. All cages are 0.6 m off of the floor.Each cage is furnished with a 1 m high perch; so it is pretty much at human eye level — 1.6 mheight. It seems to me that the animals feel relaxed when they sit on their perch and can meet meat eye level. A low perch has little or no value as a ”safe“ resting location from our monkeyspoint of view."

Bayne K, Hurst JK, Dexter SL 1992. Evaluation of the preference to and behavioral effects of anenriched environment on male rhesus monkeys. Laboratory Animal Science 42, 38-45"With simultaneous exposure, the single-housed subjects spent the greatest portion of theinteractive time [30 minute-observation sessions] on the perch [16.8%], the second greatestamount of time spent divided approximately equally between interacting with the Kong [5.0%]and Tug-A-Toy [4.9%], and the least amount of time spent manipulating the grooming board[0.4%]."Brinkman C 1998. Usefulness of swings for macaques. Primate Enrichment Forum (electronicdiscussion group), August 17, 1998"I have used swings with cynos and pigtails... My impression is that adult animals do not reallyuse them, that is, to 'swing'. Young animals like moving things, be they swings, or othersuspended items. My adults did not even use the swings much to perch on; my explanation is thaton a swing, you simply cannot easily relax. Animals cannot really sit on them, and especiallywith the cynos, you can see almost continuous movement in the tail, compensating in balance."Crockett CM, Bellanca RU, Bowers CL, Bowden DM 1997. Grooming-contact bars providesocial contact for individually caged laboratory primates. Contemporary Topics LaboratoryAnimal Science 36(6), 53-60"Monkeys in upper cages averaged 48%±27% SD of the time on the perch, compared with40%±25% SD for monkeys in lower cages."Davis E 2006. More fun with a barrel full of monkeys: A nonhuman primate swing made byrecycling plastic barrels. Laboratory Primate Newsletter 45(3), 9-11http://www.brown.edu/Research/Primate/lpn45-3.html#swing"The NIH Shared Animal Facilities’ enrichment program has developed a primate swing createdfrom recycling our discarded plastic 30- and 55-gallon detergent barrels. These swings are easyto construct and are effective in increasing our animals’ behavioral repertoires. Additionally,these swings are safe, portable, non-toxic, easy to sanitize, and almost indestructible. We haveused these barrels in our socially-housed monkey runs for over three years, and they are stillgoing strong!"Dexter SL, Bayne K 1994. Results of providing swings to individually housed rhesus monkeys(Macaca mulatta). Laboratory Primate Newsletter 33(2), 9-12http://www.brown.edu/Research/Primate/lpn33-2.html#bayneThe single-housed adult test subjects manipulated the swings but showed little inclination toactually use them for swinging.European Commission 2002. The Welfare of Non-human Primates - Report of the ScientificCommitte on Animal Health and Animal Welfare. European Commission, Strasbourg, Francehttp://europa.eu.int/comm/food/fs/sc/scah/out83_en.pdfComprehensive updated recommendations on the species-appropriate care of nonhumanprimates."Enclosures for nonhuman primates should be equipped with one or more elevated restingsurfaces (to a position higher than the level at which they perceive threatening factors, e.g.,humans) and installed in such a way that an animal can sit on them comfortably. Perches orshelves should be provided in all cages.”118

119Günther MM 1998. Influence of habitat structure on jumping behaviour in Galago moholi. FoliaPrimatologica 69(Supplement), 410 (Abstract)There was a statistically significant preference for wooden versus PVC perches and for highversus low perches. "These results suggest that support material as well as height, influencesthe behaviour of G. maholi. Studies which do not take these factors into account are to someextent vitiated."Howell SM, Mittra E, Fritz J, Baron J 1997. The provision of cage furnishings as environmentalenrichment at the Primate Foundation of Arizona. The Newsletter 9(2), 1-5http://www.awionline.org/Lab_animals/biblio/jo-5.htm"Adults infrequently used 'moving' furnishings (e.g., swinging ropes, hanging tubes, etc...) andseemed to prefer 'stable' horizontal furnishings (e.g., benches, logs) above the enclosure floor."Kopecky J, Reinhardt V 1991. Comparing the effectiveness of PVC swings versus PVC perchesas environmental enrichment objects for caged female rhesus macaques. Laboratory PrimateNewsletter 30(2), 5-6http://www.brown.edu/Research/Primate/lpn30-2.html#vikSingle-housed subjects' "preference for perches was probably related to the fact that perches,unlike swings, are fixed structures permitting continuous relaxed postures rather than short-termbalancing. Moreover, perches, unlike swings, permit the animals to sit right in front of the cagewith optimal visual control of the environment outside of the cage."Millere KE, Laszlo K, Suomi SJ 2006. Using recycled barrel swings vs. Prima-Hedrons inprimate enclosures. Laboratory Primate Newsletter 45(3), 12http://www.brown.edu/Research/Primate/lpn45-3.html#swing2"To document the utility of using recycled barrel swings vs. Prima-Hedrons as enrichmentobjects, we observed a socially housed group of 28 tufted capuchins (Cebus apella). .. We foundno significant difference in the average frequency of use of hanging Prima-Hedrons vs. hangingbarrels."Neveu H, Deputte BL 1996. Influence of availability of perches on the behavioral well-being ofcaptive, group-living mangabeys. American Journal of Primatology 38, 175-185"A total deprivation of perches yielded an increase in aggressive behaviors and locomotion, anda decrease in cohesiveness. Placing perches progressively in the experimental cage restored thelevel of all the variables to levels found in the control cage [with five perches]. ... Therefore,perches constitute a necessary feature of an adequate environment for mangabeys."O'Neill-Wagner PL 1994. When trying to get your monkeys to behave, try perches. In Touch1(2), 6-8http://www.awionline.org/Lab_animals/biblio/tou-pegg.htmThe group-housed animals preferred perches at high elevation over perches at low elevation.Ochiai T, Matsuzawa T 1999. Environmental enrichment for captive chimpanzees (Pantroglodytes): Introduction of climbing frames 15 m high. Reichorui Kenkyu/Primate Research15, 289-296"Tall climbing frames were introduced into an outdoor compound for captive chimpanzees as away of environmental enrichment. ... Chimpanzees spent 81% of the observation time on theclimbing structures. ... All chimpanzees used the climbing structure throughout the day with littleindividual difference."

120Phillippi-Falkenstein K 1998. Usefulness of swings for macaques. Primate Enrichment Forum(electronic discussion group), August 19, 1998"In group runs, corncribs and corrals, swings provide a dimension of environmental complexityfor rhesus and pig-tailed macaques. The swings are primarily used by young animals, whileadults rarely use them. Tire swings seem to be the favorite. It has been my experience that theanimals - even juveniles - do not benefit from swings when housed in 'small' standard cages:They simply don't use them."Plesker R, Herzog A 2001. Prima hedrons, puzzle feeders and television as environmentalenrichment for captive African Green Monkeys. Primate Eye 74, 4 (Abstract)http://www.psgb.org/Meetings/Spring2001.html"The prima hedrons had no significant effect on any of the behaviours investigated. These wereinfrequently used as objects for playing, resting or observation."Reinhardt V 1989. Evaluation of the long-term effectiveness of two environmental enrichmentobjects for singly caged rhesus macaques. Lab Animal 18(6), 31-33http://www.awionline.org/Lab_animals/biblio/la-eval.htmSingly caged monkeys spent 28% of the 120 min observation time with the PVC pipe. “Whileperching, the monkeys sat in front of the cage for 95% of the time, in the middle or rear of thecage for 5% of the time. ... The proportion of time spent with the pipes was three times greaterfor animals living in lower-row cages than for animals living in upper-row cages. .. In theelevated position, the light exposure was increased, a fact that made the pipes of particular valuefor the lower-row caged animals."Reinhardt V, Pape R 1991. An alternative method for primate perch installation. Lab Animal20(8), 47-48http://www.awionline.org/Lab_animals/biblio/la-an.htmModification of squeeze cages is described allowing the installation of a perch that does notinterfere with the normal operation of the cage.Reinhardt V 1990. Comparing the effectiveness of PVC perches versus wooden perches asenvironmental enrichment objects for singly caged rhesus monkeys. Laboratory PrimateNewsletter 29(1), 13-14http://www.brown.edu/Research/Primate/lpn29-1.html#comp"One half of each cage was provided with a PVC pipe, the other with an oak branch." Bothperches had the same diameter and were installed in the same manner. During one-hourobservation sessions, single-caged subjects showed no clear preference but spent on average19% of the time on the PVC pipe and another 24% of the time on the oak branch.Reinhardt V 1992. Environmental enrichment branches that do not clog drains. LaboratoryPrimate Newsletter 31(2), 8http://www.brown.edu/Research/Primate/lpn31-2.html#branch"More than 700 caged rhesus and stump-tailed macaques housed in 29 rooms have been exposedto red oak perches and/or loose branch segments for a period of six months. Drains did not clogin any of the 29 rooms during this time although the animals gnawed the wood extensively."Reinhardt V 1992. Space utilization by captive rhesus macaques. Animal Technology 43, 11-17http://www.awionline.org/Lab_animals/biblio/at.htm

"The area covered by the floor was 3 times larger than that covered by elevated structures;nonetheless the animals were located significantly more often (89.8% of 108 scan samples) onelevated structures than on the floor (8.6% of 108 scan samples). ... The higher an animal's rankposition, the more pronounced was its habit to utilize high-level (>130 cm above floor)structures of the pen, while low ranking animals had to be content with low-level structures (40cm above floor) and the floor. .. All members of the group would inevitably take to elevated siteswhenever they heard or saw fear-inducing personnel. ... The animals huddled together withregularity on high-level structures but never on low-level structures or on the floor. ... It wasconcluded that laboratory rhesus macaques prefer the vertical dimension over the horizontaldimension as primary living space."Reinhardt V 2003. Legal loophole for subminimal floor area for caged macaques. Journal ofApplied Animal Welfare Science 6, 53-56http://www.awionline.org/Lab_animals/biblio/jaaws9.html"The USDA regulations pertaining to the minimum space requirements of nonhuman primatesand the fitting of elevated resting surfaces are contradictory. They implicitly condone theprevailing perch design that allows maximal usage of animal room space by stacking the cageson top of each other but fails to address the animals minimal spatial needs for normal posturaladjustments with freedom of movement. An amendment to the regulations is needed to clarifythat perches, ledges, swings, or other suspended fixtures have to be installed in such a way thatthey do not block part of the minimum floor space that is needed by an animal to make speciestypicalpostural adjustments with freedom of movement."Ricker RB, Williams LE, Brady AG, Gibson SV, Abee CR 1995. Environmental enhancementfor laboratory-housed squirrel monkeys: Fifteen-year retrospective analysis of procedures.Contemporary Topics in Laboratory Animal Science 34(4), 55 (Abstract)"Two types of perching material were tried: polyvinyl chloride and hemp (rope). The PVC waspreferred by the animals and was set up in multiple levels, allowing use of vertical as well ashorizontal space."Schmidt EM, Dold GM, McIntosh JS 1989. A perch for primate squeeze cages. LaboratoryAnimal Science 39, 166-167Modification of single squeeze-cages is described allowing the installation of a perch that doesnot interfere with the normal operation of the cage. "The monkeys make use of their perch forfeeding, grooming and sleeping" for 30% to 95% of the day.Seier JV 2000. Usefulness of wooden material for environmental enrichment for rhesusmacaques. Primate Enrichment Forum (electronic discussion group), February 12, 2000"We have been using wood extensively in our vervet monkey colony (about 300 monkeys,indoors) and communal cages we make climbing apparatus from wood. Wood perches forresting were also installed but they use the metal perches equally well. ...The vervets use thewood as described for other species, stripping the bark and climbing. They eventually reduceand medium branches to a single pole. We find this desirable since it keeps them occupied forhours. ... They do not loose interest in the wood as they do in other objects which we have tried.... There is obviously the problem of sanitation but we replace the wood regularly and autoclaveit before we place inside the cage (luckily we have a very large autoclave). Clogging of drainsand mould has not occurred, neither have problems such as injury through splintering. ... Weconsider wood as our most important enrichment tool."121

122Shimoji M, Bowers CL, Crockett CM 1993. Initial response to introduction of a PVC perch bysingly caged Macaca fascicularis. Laboratory Primate Newsletter 32(4), 8-11http://www.brown.edu/Research/Primate/lpn32-4.html#pvcThe height of the cage is important for allowing the animals to withdraw from potentiallystressful or alarming situations. “Monkeys spent significantly more time clinging to the cagewall in the absence of the perch. ... Monkeys in lower level cages [26% of daytime] averagedsomewhat more time on the perch than those in upper cages [14% of daytime]. ... There was lessstereotypy when the perch was present."Smith K, St. Claire M, Byrum R, Harbaugh S, Harbaugh J, Erwin J 2003. Use of space, cagefeatures, and manipulable objects by laboratory primates: individual differences and speciesvariability. American Journal of Primatology 60(Supplement), 76-77 (Abstract)”Rhesus (74%), longtailed (71%), vervets (94%), and patas (82%) significantly exceeded theexpected rate of perch use (25%), while pigtailed (28%) did not differ from expectation.”Taylor LL 1998. Promoting species typical behavior in Coquerel's sifakas (PropithecusVerreauxi Coquereli). American Zoo and Aquarium Association Regional ConferenceProceedings, 599-603"The sifakas rarely were observed on the ground, preferring to locomote on vertical substratesand rest on vertical and horizontal elevated substrates. ...If vertical surfaces were absent fromcaptive habitats, these rare lemurs could not display their preferred mode of arboreallocomotion.”Taylor L, Owens A 2004. Enclosure use by aged squirrel monkeys (Saimiri sciureus). AmericanJournal of Primatology 62(Supplement), 85http://www.asp.org/asp2004/abstractDisplay.cfm?abstractID=800&confEventID=808A group of squirrel monkeys was translocated from an indoor exhibit to an outdoor enclosure.“Static substrates were preferred (64.3%). Dynamic substrates, like rope walkways, were usedprimarily during locomotion (33.8%) from one static location to another.”van Wagenen G 1950. The monkeys. In The Care and Breeding of Laboratory Animals Farris EJ(ed), 1-42. John Wiley, New York, NY"Sitting on the board [approximately 1 m off the ground], facing the center of the room, is thefavorite position of the monkeys. At this height these intensely alert animals have a better view ofactivities within the room, and they can meet visitors on the same eye level. ... and they sleep onthe board at night."Watson DSB 1991. A built-in perch for primate squeeze cages. Laboratory Animal Science 41,378-379Perch installation design for single squeeze-back cages is described. "Independent of gender themonkeys were seen using their perches more than 84% of the time."Watson SL, Shively CA 1996. Effects of cage configuration on behavior in cynomolgusmacaques. XVIth Congress of the Internatational Primatological Society/XIXth Conference ofthe American Society of Primatologists, Abstract No. 674"Stereotypies occurred more often in the STD [standard single cage] than in the VE [verticallyenhanced;probably with perche(s)]. ... The results indicate that VE cages provide more suitableindividual housing environments for nonhuman primates than STD cages."

123Watson SL, Gray A, Taylor E, Johnson B, Fahm B, McGee A, Bingham W, Banks P 2002.Efficacy of environmental enrichment for garnett's bushbaby (Otolemur garnettii). AmericanJournal of Primatology 57, 38-39“Bushbabies interacted with swinging/climbing apparati significantly more than withmanipulanda.... All animals spent significantly more time at the top than at the bottom of theircages (t(17)=3.3, p=.004). ... These results suggest that provision of vertical space andswinging/climbing opportunities may be more effective forms of enrichment for bushbabies thanprovision of manipulanda.“Williams LE, Abee CR, Barnes SR, Ricker RB 1988. Cage design and configuration for anarboreal species of primate. Laboratory Animal Science 38, 289-291Squirrel monkeys preferred a PVC pipe perch (rigid) over rope perches (non-rigid). For anarboreal animal, a higher perch may be perceived as safer." Perches decreased the propensityfor tail ulcers associated with floor contact. "With only one perch level, males were forced tospend a large percentage of their time sitting on the floor rather than the main perches [whichwere occupied by females]."Wolff A 1989. Polyvinyl chloride piping as perch material for squirrel monkeys. LaboratoryPrimate Newsletter 28(1), 7http://www.brown.edu/Research/Primate/lpn28-1.html#pvc"An additional unexpected benefit of the PVC piping has been a decrease in dorsal tail-headabrasions, frequently seen in squirrel monkeys that sit on the stainless steel flooring of standardprimate cages."Woodbeck T, Reinhardt V 1991. Perch use by Macaca mulatta in relation to cage location.Laboratory Primate Newsletter 30(4), 11-12http://www.brown.edu/Research/Primate/lpn30-4.html#perchSingle-housed "animals living in lower-row cages spent an average of 31.6% of the timeperching on their pipes while animals living in upper-row cages perched only 6.9% of the time.Access to the vertical dimension of the cage was more important for the lower-row cagedmonkeys who continuously live close to the ground, in the horizontal dimension of the room."(6) Promoting Object-oriented Behavior(6,1) Commercial Toysphoto by Peggy O’Neill-Wagner

Anonymous 1991. The psychological well-being of primates. Primate News 25(Fall), 3-5"The problems with all these devices is that they are expensive to purchase (foraging boards cost$60 each) and to maintain (they require many hours to fill and clean). ... We could live with theexpense if we were certain that these devices really improve the well-being of the animals. Itseems, however, that after a short time the animals lose interest in foraging boards, and fleeceboards, just as they lose interest in balls and toys."Bayne K 1989. Nylon balls re-visited. Laboratory Primate Newsletter 28(1), 5-6http://www.brown.edu/Research/Primate/lpn28-1.html#ball"Approximately 10% of the [single-housed] monkeys in a room utilize the ball at any giventime."Bayne K, Hurst JK, Dexter SL 1992. Evaluation of the preference to and behavioral effects of anenriched environment on male rhesus monkeys. Laboratory Animal Science 42, 38-45"With simultaneous exposure, the single-housed subjects spent the greatest portion of theinteractive time [30 minute-observation sessions] on the perch [16.8%], the second greatestamount of time spent divided approximately equally between interacting with the Kong [5.0%]and Tug-A-Toy [4.9%], and the least amount of time spent manipulating the grooming board[0.4%]."Bayne K, Dexter SL, Hurst JK, Strange GM, Hill EE 1993. Kong toys for laboratory primates:Are they really an enrichment or just fomites? Laboratory Animal Science 43, 78-85"The use of simple toys for environmental enrichment of laboratory primates is an economicalmeans of increasing the complexity of the cage environment to a limited degree. The limitationspresented by this method of enrichment include the finite ways in which a simple device can elicitnormative behaviors and the relatively rapid habituation to the device." It was demonstrated thatmicrobial growth can persist on enrichment devices - such as Kong toys - after they have beensanitized in a commercial cagewasher.Bloomsmith MA, Finlay TW, Merhalski JJ, Maple TL 1990. Rigid plastic balls as enrichmentdevices for captive chimpanzees. Laboratory Animal Science 40(3), 319-322"The mean percentage of ball-use time for all subjects during the study [first ten hours afterinitial presentation] was 7.1%. ... Age and housing effects were obtained, with younger animalsand those housed in more barren environments exhibiting higher levels of ball use. It isconcluded that the balls were worthwhile additions to the chimpanzee environments with usestabilizing at a mean of 2.5% of the subjects' time."Brent L, Stone AM 1998. Destructible toys as enrichment for captive chimpanzees. Journal ofApplied Animal Welfare Science 1, 5-14Nine singly caged chimpanzees were provided with eight different toys made of plastic, vinyl, orcloth one at a time or several at once. The toys remained in the cages an average of three days."The chimpanzees varied greatly in their interest in the toys. One subject rarely contacted thetoys and others used them a great deal and quickly destroyed them."Cardinal BR, Kent SJ 1998. Behavioral effects of simple manipulable environmental enrichmenton pair-housed juvenile macaques (Macaca nemestrina). Laboratory Primate Newsletter 37(1),1-3http://www.brown.edu/Research/Primate/lpn37-1.html#kent“Toy use declined with time, indicating that rotation of toys ... may increase use."124

Crockett CM, Bielitzki JT, Carey A, Velez A 1989. Kong toys as enrichment devices for singlycagedmacaques. Laboratory Primate Newsletter 28(2), 21-22http://www.brown.edu/Research/Primate/lpn28-2.html#kong"Providing objects such as Kong toys ... is mildly enriching to some of the monkeys. Periodicallyremoving and reintroducing the toys would increase their enrichment value."Hamilton P 1991. Enrichment toys and tools in recent trials. Humane Innovations andAlternatives in Animal Experimentation 5, 272-277"When toys were left with an animal for several days, the individual became accustomed to anddesinterested in the toy."Kessel AL, Brent L 1998. Cage toys reduce abnormal behavior in individually housed pigtailmacaques. Journal of Applied Animal Welfare Science 1, 227-234Providing multiple “toys as enrichment for [single-caged] pigtail macaques was effective inreducing abnormal behavior" during 30-min observation session. "The use of the toys wasreduced over time."Line SW, Markowitz H, Morgan KN, Strong S 1989. Evaluation of attempts to enrich theenvironment of single-caged non-human primates. In Animal Care and Use in BehavioralResearch: Regulation, Issues, and Applications Driscoll JW (ed), 103-117. Animal WelfareInformation Center, Beltsville, MD"Our experience with cage toys suggests that after a very short time (a few days or less), mostmacaques will lose interest in the objects that are offered."Novak MA, Musant A, Munroe H, O'Neill PL, Price C, Suomi SJ 1993. Old, socially housedrhesus monkeys manipulate objects. Zoo Biology 12, 285-298"More than 10% of the [group-housed] females' time was spent in object [toy] manipulation. ...Socially housed rhesus monkeys ranging in age from 14 to 22 years showed steady rates ofobject manipulation, and their interest in familiar objects did not appear to wane over time. ...Several factors [for interpreting higher interaction rates in groups-housed than in single-housedanimals] should be considered, the first of which is social facilitation ... Failure to manipulateobjects in rhesus macaques appears to be more a function of individual housing than of old age."Paquette D, Prescott J 1988. Use of novel objects to enhance environments of captivechimpanzees. Zoo Biology 7, 15-23"Following their familiarization with the novel objects [rubber or plastic toys for smallchildren], the [group-housed] chimpanzees' manipulation frequency decreased whereas selfgroomingand abnormal behaviors were increased." The importance of a periodical substitutionof the objects was suggested to enhance their usefulness.Plesker R, Heller-Schmidth J, Hackbarth H 2006. Environmental enrichment objects for theimprovement of locomotion of caged rhesus macaques (Macaca mulatta). Laboratory PrimateNewsletter 45(1), 7-10http://www.brown.edu/Research/Primate/lpn45-1.html#pleskerJuveniles used the mobile objects [treadmill and rotating barrel] more than the adults. "Due tothe increase in locomotion, the amount of time spent in aggressive behavior significantlydecreased."125

126Pruetz JD, Bloomsmith MA 1992. Comparing two manipulable objects as enrichment for captivechimpanzees. Animal Welfare 1, 127-137http://www.awionline.org/Lab_animals/biblio/aw1-12.htm"Paper was used a mean 27 per cent of the available time [one hour], while the Kong Toys wereused a mean 10 per cent of the available time. ... Object use steadily declined over the first hourof exposure. ... Object use when the Kong Toy was present declined over the course of the study,but use of the paper remained consistent. ... The destructible wrapping paper was moreworthwhile enrichment object than the indestructible Kong Toy for the [group-housed] captivechimpanzees of this study."Shefferly N, Fritz J, Howell S 1993. Toys as environmental enrichment for captive juvenilechimpanzees (Pan troglodytes). Laboratory Primate Newsletter 32(2), 7-9http://www.brown.edu/Research/Primate/lpn32-2.html#jo”Whereas contact with the indestructible toy ball decreased over time, destructible objectsmaintained a consistent level of interest throughout the toys lifespan. ... Provision of both typesof toys did not result in significant differences in the time individuals spent in abnormal, oraggressive behavior. ... There were no health problems or injuries associated with thedestructible objects. No pieces of plastic were found in feces, indicating that none had beeningested.“Weick BG, Perkins SE, Burnett DE, Rice TR, Staley EC 1991. Environmental enrichmentobjects and singly housed rhesus monkeys: Individual preferences and the restoration of novelty.Contemporary Topics in Laboratory Animal Science 30(5), 18"We found that the extent of physical contact with the [Kong toy, Nylabone ring and Nylaboneball] toys habituated during a short time. ... The introduction of a different toy every Mondaywas accompanied by a restoration of the apparent novelty of the toys."(6,2) Wooden ObjectsBaumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 4.10. WoodenObjects. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/enrich.html#wood"I give our single-caged baboons 20 cm long gnawing sticks made of pecan branches. They lovethem! It takes one to two weeks for a stick to be ”widdled“ down to about half of its size."

127Eckert K, Niemeyer C, Anonymous , Rogers RW, Seier J, Ingersoll B, Barklay L, Brinkman C,Oliver S, Buckmaster C, Knowles L, Pyle S 2000. Wooden objects for enrichment: A discussion.Laboratory Primate Newsletter 39(3), 1-4http://www.brown.edu/Research/Primate/lpn39-3.html#wood"It seems that there is a general consensus that wooden objects provide inexpensive, safe, longtermand effective stimulation for the expression of non-injurious, species-typical behaviors suchas perching, gnawing, gouging, manipulating and playing" without causing health and hygienicproblems.Hienz RD, Zarcone TJ, Turkkan JS, Pyle DA, Adams RJ 1998. Measurement of enrichmentdevice use and preference in singly caged baboons. Laboratory Primate Newsletter 37(3), 6-10http://www.brown.edu/Research/Primate/lpn37-3.html#hienz"Baboons generally interacted less with Kongs than with logs or swings. This trend, however,was not consistent for each individual animal. Of the six baboons, three clearly "preferred" thelog (i.e., moved the log more than the other two devices), two preferred the swing, and onepreferred the Kong. Thus the trends expressed in the averaged data can be quite misleading."Hienz RD, Pyle DA, Frey JJ, Zarcone TJ, Adams RJ, Turkkan JS 2000. Enrichment device useby baboons during long-term vs. intermittent availability. Laboratory Primate Newsletter 39(2),1-3http://www.brown.edu/Research/Primate/lpn39-2.html#hienz"Four of the six baboons increased their [cherry] log use over the exposure period [104 days],while the remaining two baboons decreased their interactions with their logs over this period....When the logs were available only every other day, or every fourth day, log use wasconsiderably enhanced on those days. When the logs were withheld longer, log use declined tothe same level of use observed when the logs were continuously available. These results suggestthat leaving enrichment devices out of a monkey's cage for extended periods would not bebeneficial for generating greater use."Hienz RD, Jones A, Pyle DA, Johnson J 2002. Effectiveness of enrichment devices during briefperiods of social restriction in singly housed baboons. Laboratory Primate Newsletter 41(3), 1-3http://www.brown.edu/Research/Primate/lpn41-3.html#hienz"Data were collected on the animals’ (three singly caged adult males) daily biscuit intake andactivity levels as well as log activity prior to, during, and following social restriction (housed inseparate room in which no other animals are present), and also in the absence and presence of alog (hand-cut cherry hardwood logs; 9 cm diameter x 35 cm long). .. All three baboons in thecurrent study showed a marked decrease in activity during the brief periods of social restrictionwhen the log enrichment devices were not available. However, once these devices were provided,general activity increased again, with two of the three baboons increasing their activity levels tonear-normal. ... These findings present further support for the importance of enrichment devicesfor laboratory primates, showing that in the presence of such devices, the behavior of the animalis positively influenced. While the devices themselves were not manipulated greatly in this study,their presence affected the activity of the baboons."Line SW, Morgan KN 1991. The effects of two novel objects on the behaviour of singly cagedadult rhesus macaques. Laboratory Animal Science 41, 365-369Single-housed subjects engaged in stick use 5.8% of 15 minute-observations. The correspondingfigure for nylon ball use was 2%. "No adverse health effects of stick ingestion were noted amongthe subjects."

128Reinhardt V 1990. Time budget of caged rhesus monkeys exposed to a companion, a PVC perchand a piece of wood for an extended time. American Journal of Primatology 20, 51-5660 animals were exposed for at least 1.5 years to a compatible companion, a suspended plasticpipe, and a branch segment. Individuals spent an average of 23.5% of the time interacting withthe companion, 10.4% with the plastic pipe and 4.8% with the branch segment.Reinhardt V 1997. The Wisconsin Gnawing Stick. Animal Welfare Information CenterNewsletter 7(3-4), 11-12http://www.nal.usda.gov/awic/newsletters/v7n3/7n3reinh.htmThe sticks consist of branch segments cut of dead red oak trees. They are used by cagedmacaques about 5% of the time - more by young animals, less by adult animals - for gnawing,manipulating and playing. “Long-term exposure to the sticks has resulted in no recognizablehealth hazards."(6,3) MirrorsBaumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 4.5. Mirrors.Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/enrich.html#mirrors”All of our single-housed long-tailed macaques have mirrors mounted on swivels that areattached to the outside of their cages, low enough so that an animal can chose to either benddown and intentionally look into the mirror or to make no extra effort, hence not be confronted— bothered? — by the mirror reflection. Our monkeys use their mirrors frequently.Our rhesus love mirrors too. They like to check us out by looking at us through themirror. I guess they don't feel so threatened when they can look at us without being seen. Theyalso like to check out the room, by looking at the reflections in the mirror. We have one malewho never looks at people directly, but holds up a polished stainless steel mirror to watch peoplewho have just entered the room. Of course, we named him Mirror Man.We have found an acrylic sheet mirror that we can cut into different-size pieces. Some gethung on the walls, using double sided tape, while other pieces get hung right inside theenclosures, using zip ties. We also cut small pieces and give these directly to the primates. Ourrhesus macaques often combine the wall and hand mirrors to get extra viewing advantage! It’sreally fun to watch them. The acrylic leaves no sharp edges when it breaks; this means it is safefor the animals. We never encountered a problem.

129Our singly housed baboons get the most enjoyment from their mirrors, while pair- andgroup-housed animals show little interest in them.I have a male olive baboon in my charge who regularly sits for long periods at a timelooking at himself in a mirror. He is housed with two females but appears to prefer looking at hisown mirror reflection versus the nice tumescent females hovering around him! He also uses hismirror to see reflections of what is going on behind him, sitting diagonally with his back facingthe main traffic area for techs, as if he was spying on us! I do believe he is entertaining himselfquite a bit with the mirror.“Brent L, Stone AM 1996. Long-term use of television, balls, and mirrors as enrichment forpaired and singly caged chimpanzees. American Journal of Primatology 39, 139-145"Chimpanzees used televisions, balls, and mirrors for 0.27-1.53% of the observation time afterseveral years of exposure. ... Television and ball use were significantly higher than mirror use."Goode TL, McPherson H, Hughes J, Conboy T, Smith S, Bone A, Zimmerman W, Holder D,Klein H 1998. Evaluation of stainless steel reflective discs as enrichment devices for rhesusmonkeys (Macaca mulatta) housed in a toxicological facility. Contemporary Topics inLaboratory Animal Science 37, 100 (Abstract)"The enrichment device was used [probably by single-caged subjects] primarily formanipulation and banging. ... The usage of polished stainless steel discs declines over time andtherefore alternative methods of environmental enrichment and rotation of enrichment devicesshould be considered."Harris H 2002. Mirrors as enrichment for monkeys. Laboratory Animal Refinement andEnrichment Forum (electronic discussion group), November 13, 2002“Our African green monkeys (all males) and cynomolgus macaques use the mirrors more thanthe rhesus and squirrel monkeys. .. The mirrors are utilized by singly-caged, paired and grouphoused monkeys. They use them to look at themselves and at other things inside and outside theroom. We have had a few (less than 10) occurrences where the monkeys were too fearful or selfaggressiveto keep a mirror on their cage, but by far, the majority benefit from them. Themirrors, in my opinion, are one of our most useful object enrichment items."Harris HG, Edwards AJ 2004. Mirrors as environmental enrichment for African green monkeys.American Journal of Primatology 63, 459-467"Stainless steel circular mirrors were employed in an enrichment plan for 105 singly housedmale African green monkeys. We observed 25 randomly selected males to measure mirror useand to assess the mirrors' effectiveness as an enrichment item. We conducted additional mirrorusesurveys on all 105 males using fingerprint accumulation as an indicator (rated on a scale of0 to 4). Use was defined as either being in contact with the mirror (contact use (CU)) or lookingdirectly into the mirror without contact (non-contact use (NC)). Mirror-use data were collected10 months after the initial introduction of the mirrors and again at 16 months. The two timepoints were compared by paired t-tests. No significant difference in use was found between thetwo data collection points. On average, the monkeys used the mirrors 5.2% of the total timeintervals recorded (approximately 3 min/hr). Results from the five fingerprint-accumulationsurveys showed that 102 of 105 males (97%) had CU with their mirrors over the survey points.Based on the sustained use of the mirrors over a 6-month period, we concluded that the mirrorswere an effective enrichment tool that the vast majority of our monkeys routinely used.Habituation did not appear to occur even a year after the mirrors were introduced."

130O'Neill PL, Wright AC, Weed JL 1997. Curious response of three monkey species to mirrors.American Zoo and Aquarium Association Regional Conference Proceedings, 95-101One mirror was hung on the front of each subject's cage for a two-week study period. Pig-tailedmacaques contacted the mirror at a fairly constant rate of 12-18 times per hour. Rhesusmacaques were initially interested, but contact rate progressively dropped to only 6/h at the endof the second week. Long-tailed macaques showed little interest in the beginning, but contactrates reached those of pig-tailed macaques at the end of the study.(7) Promoting Curiosity Behavior(7,1) Television and VideosBloomsmith MA, Lambeth SP 2000. Videotapes as enrichment for captive chimpanzees (Pantroglodytes). Zoo Biology 19, 541-551”Individually housed subjects watched the videotapes more than socially housed subjects. Whenviewing time was averaged across all videotapes, the chimpanzees watched the monitor a meanof 38.4% of the time available. ... Subjects habituated to repeated presentations of thevideotapes, although the effect was small numerically. Although this type of enrichment did notextensively alter behavior, it did occupy a significant portion of the subjects activity budget."Bloomsmith MA, Lambeth SP, Perlamn JE, Hook MA, Schapiro SJ 2000. Control overvideotape enrichment for socially housed chimpanzees. American Journal of Primatology51(Supplement), 44-45 (Abstract)Social behavior and solitary play were higher in subjects with control over the onset ofvideotapes, while scratching [generally regarded as a sign of tension] was higher in thosegroups who lacked control. "The results indicate that giving chimpanzees control overvideotaped enrichment had limited, but positive, effects on behavior."Harris LD, Briand EJ, Orth R, Galbicka G 1999. Assessing the value of television asenvironmental enrichment for individually housed rhesus monkeys: A behavioral economicapproach. Contemporary Topics in Laboratory Animal Science 38(2), 48-53"The negative demand curve suggested that TV is not a valued commodity" for single-cagedanimals.Lambeth S, Bloomsmith M, Baker K, Perlman J, Hook M, Schapiro S 2001. Control overvideotape enrichment for socially housed chimpanzees: Subsequent challenge tests. AmericanJournal of Primatology 54(Supplement), 62-63 (Abstract)"The lower expression of stress–related behaviors by chimpanzees that took advantage of theopportunity to control the videotape apparatus implies that exerting control over theenvironment may have a generalized effect by lessening disturbance caused by mildlychallenging situations.“O'Neill-Wagner P 2001. Videotape exposure may facilitate recovery for monkeys in a clinicalsetting. American Journal of Primatology 54(Supplement), 59 (Abstract)”During videotape exposure monkeys did not remove their sutures. Animals that had previouslywithdrawn from food were observed eating during videotapes showing primates eating.“

131Platt DM, Novak MA 1997. Videostimulation as enrichment for captive rhesus monkeys(Macaca mulatta). Applied Animal Behaviour Science 52, 139-155The animals spent substantially more time watching selected videotapes than manipulating thejoystick.Plesker R, Herzog A 2001. Prima hedrons, puzzle feeders and television as environmentalenrichment for captive African Green Monkeys. Primate Eye 74, 4 (Abstract)http://www.psgb.org/Meetings/Spring2001.html"The access to television (mainly nature films) enhanced the observation behaviour of the wholegroup for a short time. Again, the adult males, but also the youngest offspring did not appear tobe interested."Rumbaugh DM, Washburn DA, Savage-Rumbaugh ES 1989. On the care of captivechimpanzees: Methods of enrichment. In Housing, Care and Psychological Wellbeing of Captiveand Laboratory Primates Segal EF (ed), 357-375. Noyes Publications, Park Ridge"Television can be a great source of environmental enrichment if the chimpanzee can perceivethe relevance of what it sees on the screen to the world it knows."(7,2) WindowsPhoto by Richard LynchBaumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 4.7.Windows. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/enrich.html#windows”We expose our squirrel monkeys to natural daylight via big windows during the summer. This issupplemented with artificial light in late fall and early spring, when the days are short, andthroughout the winter. Some of our squirrel monkeys will lie as close to the window as possibleand let the sun rays dance on their belly.I've seen the same behavior in our marmosets. As soon as the sunlight hits the window,the animals stop what they are doing, run over to the window ledge, and start stretching out andbasking in the sunrays. There is no doubt in my mind that exposure to natural light, especiallysunlight, is highly appreciated by the animals.All our rhesus macaques have access to one-way glass exterior windows mounted high

132above ground level. I very often see the animals gather up, attentively gazing out of the windowstowards the source of some noise, at caretakers, activities in the garden and birds. One wouldthink that exposure to daylight and the natural diurnal rhythm couldn’t be anything else but agood thing for these animals.“Lynch R, Baker D 2000. Primate Enrichment: A room with a view. Laboratory PrimateNewsletter 39(1), 12http://www.brown.edu/Research/Primate/lpn39-1.html#roomPairs were transferred to a play room with windows for 1½ hours every ten days. "During thepast year, we have observed that the primates spend about an hour of their time looking out thewindows."(8) Safety ConcernsEckert K, Niemeyer C, Anonymous , Rogers RW, Seier J, Ingersoll B, Barklay L, Brinkman C,Oliver S, Buckmaster C, Knowles L, Pyle S 2000. Wooden objects for enrichment: A discussion.Laboratory Primate Newsletter 39(3), 1-4http://www.brown.edu/Research/Primate/lpn39-3.html#wood"It seems that there is a general consensus that wooden objects provide inexpensive, safe, longtermand effective stimulation for the expression of non-injurious, species-typical behaviors suchas perching, gnawing, gouging, manipulating and playing" without causing health and hygienicproblems.Etheridge MA, O'Malley J 1996. Diarrhea and peritonitis due to traumatic perforation of thestomach in a rhesus macaque (hardware disease). Contemporary Topics in Laboratory AnimalScience 35(5), 57-78"Abdominal radiographic views indicated ingestion of approximately 20 pieces of wire that camefrom an old automobile tire hung in the outdoor monkey pen to provide environmentalenrichment."Hahn NE, Lau D, Eckert K, Markowitz H 2000. Environmental enrichment-related injury in amacaque (Macaca fascicularis): Intestinal linear foreign body. Comparative Medicine 50, 556-558"As a result of this incidence [ingested sisal rope pieces leading to multiple ulcerations,perforations, septic peritonitis] sisal rope enrichment devices were immediately removed fromall macaque cages in the facility."Mahoney CJ 1992. Some thoughts on psychological enrichment. Lab Animal 21(5), 27,29,32-37"Facilities must exercise caution when installing such climbing devices as vertically hanging orhorizontally suspended ropes and chains - these must not crisscross or be too slack, because ananimal can strangle its neck, limbs, or other body parts."Murchison MA 1993. Potential animal hazard with ring toys. Laboratory Primate Newsletter32(1), 1-2http://www.brown.edu/Research/Primate/lpn32-1.html#ring"Recently one animal, a 2-year-old pigtail macaque (Macaca nemestrina), approximate weight3.1 kg, became trapped inside a Nylaring. The ring went around the neck, across the body, andunder one arm. Since the animal was apparently unable to remove the ring, he was anesthetizedand the ring manually removed."

133Novak MA, Rulf A, Munroe H, Parks K, Price C, O'Neill PL, Suomi SJ 1995. Using a standardto evaluate the effects of environmental enrichment. Lab Animal 24(6), 37-42Monkeys maintained on pine wood shavings showed an increase in agonism, scratch, andstereotypy.Reinhardt V 1997. The Wisconsin Gnawing Stick. AWIC Newsletter 7(3-4), 11-12http://www.nal.usda.gov/awic/newsletters/v7n3/7n3reinh.htmAll 700 caged rhesus and 36 stumptailed macaques had continual access to gnawing sticks formore than 10 years. “Long-term exposure to the sticks has resulted in no recognizable healthhazards."Shefferly N, Fritz J, Howell S 1993. Toys as environmental enrichment for captive juvenilechimpanzees (Pan troglodytes). Laboratory Primate Newsletter 32(2), 7-9http://www.brown.edu/Research/Primate/lpn32-2.html#jo”Whereas contact with the indestructible toy ball decreased over time, destructible objectsmaintained a consistent level of interest throughout the toys lifespan. ... There were no healthproblems or injuries associated with the destructible objects. No pieces of plastic were found infeces, indicating that none had been ingested.“Tresz H 1997. Providing enrichment at no cost. The Shape of Enrichment 6(4), 1-4"Green pine cones can cause severe diarrhea. Keepers should work only with old, opened-uppinecones."Regulations and GuidelinesAmerican Society of Primatologists 2000. American Society of Primatologists guidelines for theethical treatment of nonhuman primates. ASP Bulletin 24(4), 4“ASP members hold the following general principles in common:1. The most important of these principles is that we accept the responsibility of stewardship fornonhuman primates, and this responsibility must [sic] be reflected in our husbandry practicesand research protocols whether in field, laboratory, or other setting.3. Research with nonhuman primates should avoid pain and distress at every opportunity.5. We should make use of information on a species natural history to improve management andenrich environments, because physical and psychological well-being are essential not only to thehealth of the animals but also to the validity of the research results.6. Finally, we recognize that our concern should be extended to nonhuman primates once theyhave become 'surplus' to our research needs. This obligation entails ensuring quality care to theend of their natural lives whenever possible. .. While recognizing that some professional believeeuthanasia is an acceptable way to deal with surplus animals in some cases, we strongly urgethat other solutions be found whenever possible.“Canadian Council on Animal Care 1984. Chapter XX: Non-human primates. In Guide to theCare and Use of Experimental Animals, Volume 2 Canadian Council on Animal Care (ed), 163-173. Canadian Council on Animal Care, Ottawa, ONhttp://www.ccac.ca/en/CCAC_Programs/Guidelines_Policies/GUIDES/ENGLISH/V2_84/CHXX.HTM"Any primate housed alone will probably suffer from social deprivation, the stress from whichmay distort processes, both physiological and behavioural."

134Canadian Council on Animal Care 1993. Guide to the Care and Use of Experimental Animals,Volume 1, 2nd Edition. Canadian Council on Animal Care, Ottawa, ONhttp://www.ccac.ca/en/CCAC_Programs/Guidelines_Policies/GUIDES/ENGLISH/V1_93/CHAP/CHVI.HTM"All animals must be observed at least once daily. .. The social needs of animals used inresearch, teaching, or testing, should be given equal consideration with environmental factorssuch as lighting, heating, ventilations and containment (caging). Particularly in the case ofsingly housed animals, daily observation provides an alternative from of social contact for theanimal and commonly facilitates handling in that the animal becomes accustomed to the humanpresence. .. Most animals should not be housed singly unless required by medical condition,aggression, or dictates of the study. Singly housed animals should have some degree of socialcontact with others of their own kind. .. In the interest of well-being, a social environment isdesired for each animal which will allow basic social contacts and positive social relationships.Social behaviour assists animals to cope with circumstances of confinment. .. Restraintprocedures should only be invoked after all other less stressful procedures have been rejected asalternatives. ... Physiological, biochemical and hormonal changes occur in any restraint animal... and investigators should consider how these effects will influence their proposedexperiments."Council of Europe 2006 Appendix A of the European Convention for the Protection ofVertebrate Animals Used for Experimental and Other Scientific Purposes (ETS No. 123) enactedJune 15, 2007. Strasbourg, France: Council of Europehttp://conventions.coe.int/Treaty/EN/Treaties/PDF/123-Arev.pdfProgressive regulations pertaining to the species-appropriate housing and handling of animalskept in research labs."Because the common laboratory non-human primates are social animals, they should behoused with one or more compatible conspecifics. .. Single housing should only occur if there isjustification on veterinary or welfare ground. Single housing on experimental grounds should bedetermined in consultation with the animal technician and with the competent person chargedwith advisory duties in relation to the well-being of the animals.Primates dislike being handled and are stressed by it; training animals to co-operateshould be encouraged, as this will reduce the stress otherwise caused by handling. Training theanimals is a most important aspect of husbandry, particularly in long-term studies. .. Trainingcan often be employed to encourage the animals to accept minor interventions, such as bloodsampling.The flight reaction of non-human primates from terrestrial predators is vertical, ratherthan horizontal; even the least arboreal species seek refuge in trees or on cliff faces. As a result,enclosure height should be adequate to allow the animal to perch at a sufficiently high level forit to feel secure. .. The minimum enclosure height for caged marmosets and tamarins is 1.5 m;the minimum enclosure height for caged squirrel monkeys, macaques, vervets and baboons is 1.8m. .. The structural division of space in primate enclosures is of paramount importance. It isessential that the animals should be able to utilise as much of the volume as possible because,being arboreal, they occupy a three-dimensional space. The make this possible, perches andclimbing structures should be provided.“Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housingand Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London, UKhttp://scienceandresearch.homeoffice.gov.uk/animal-research/legislation/"Experimental results may be influenced by environmental conditions. .... Unstableenvironmental conditions are likely to introduce avoidable variability into biological responses.

135To demonstrate any experimental response against such a variable background generates arequirement for greater animal usage if the result is to be statistically valid. Good control ofvariables ... can therefore contribute both to good science and to the minimisation of animal use... The shape of the cage and the furniture provided may be as important to the animal as theoverall size of the cage. ..All animals must be allowed to exercise. For the smaller species, thisshould usually be achieved by providing adequately sized cages or pens and sometimes playobjects. ... For larger species, special arrangements will usually be required for social contactas well as exercise. ... The behaviour of an animal during a procedure depends on the confidenceit has in its handler. This confidence is developed through regular human contact and, onceestablished, should be preserved. .. Where appropriate, time should be set aside for handling andgrooming. All staff, both scientific and technical, should be sympathetic, gentle and firm whendealing with animals. .. The least distressing method of handling is to train the animal to cooperatein routine procedures. Advantage should be taken of the animal's ability to learn."Institute of Laboratory Animal Resources 1980. Laboratory Animal Management: NonhumanPrimates. National Academy Press, Washington, DC"Lighting should be uniformly diffused throughout the area and provide adequate illuminationfor good house-keeping practices, adequate inspection of animals, and safe working conditionsfor personnel."Institute for Laboratory Animal Research 1992. Recognition and alleviation of pain and distressin laboratory animals. National Academy Press, Washington, DChttp://www.nap.edu/books/0309042755/html"The purposes of this book are to increase awareness of the sources and manifestations of stressand distress in laboratory animals and to increase ethical sensitivity in those who use and carefor them. (It might also, indirectly, help to reduce the number of animals needed for experimentalpurposes: uncontrolled pain or distress can increase variability in experimental data and sorequire the use of more animals in a study for it to achieve statistical significance.)Stress is the effect produced by external (i.e., physical or environmental) events or internal (i.e.,physiologic or psychologic) factors, referred to as stressors, which induce an alteration in ananimal's biologic equilibrium. ... Examples of potential stressors that cause psychological stress[include] fear, anxiety, boredom, loneliness, separation.Distress is an aversive state in which an animal is unable to adapt completely to stressors andthe resulting stress and shows maladaptive behaviors" such as “coprophagy, hair-pulling, selfbiting,and repetitive stereotyped movements. ... Such behaviors, like maladaptive ones, shouldbe interpreted as causing harm to the animal and producing unwanted variability in researchdata. ... The identification and control of these [environmental] stressors from the animals' orspecies' perspective constitute good husbandry and are a primary responsibility of all who carefor or use animals in a laboratory setting. ... Behavioral changes, however, are the earliest signsof stress or distress that most animal care staff and researchers are likely to confront. Skilledobservers who know the behavior of a particular species or strain of animal and of the individualanimals under their care could provide a reliable assessment of the state of the animals. Thatreliability is seriously compromised when few animal care staff and researchers are afforded thetime or training necessary for them to become skilled observers. ... Recognition, or anticipation,that a particular event will be perceived as an important stressor by an animal requiresknowledge not only of the stressor, but of the species-typical responses to situations and of theexperience of the particular animal. ... Stroking and handling by humans can be a practical andeffective technique for calming animals in situations where they are distressed, particularlyanimals that have been positively socialized by humans."

136International Primatological Society 1989. IPS International Guidelines for the acquisition, careand breeding of nonhuman primates. Primate Report 25, 3-27"Illumination should be uniform and sufficient for adequate inspection of animals and safeworking conditions for personnel, but not obtrusive to the well-being of the animals. .. Restraintprocedures should be used only when less stressful alternatives are not feasible. .. Primates ofmany species can be trained for sample procedures, such as presenting a limb for a bloodcollection, and such training is advocated whenever possible, using positive reinforcement."International Primatological Society 2007. IPS International Guidelines for the Acquisition, Careand Breeding of Nonhuman Primates. Bronx, NY: International Primatological Societyhttp://www.internationalprimatologicalsociety.org/docs/IPS_International_Guidelines_for_the_Acquisition_Care_and_Breeding_of_Nonhuman_Primates_Second_Edition_2007.pdf“There is an acute need for the training of professional and technical personnel in veterinarycare, psychological well-being, handling and general management of captive primates and therequirements of species and individuals. Well-trained, competent and motivated personnel canmake an enormous difference in improving the welfare of captive primates.Pair or group housing in an enclosure must be considered the norm for gregariousanimals, but only compatible (socially, virological status, etc.) animals should be kept together.Infectious disease study does not necessarily preclude the ability to keep primates in pairs orgroups in the same enclosure, without interfering with study validity. Many infectious diseasestudies are carried out in paired or grouped primates. the same is true of many other types ofstudies and procedures, such as pharmacokinetic studies and drug safety testing. .. Individualsubjects can be accessed for testing and manipulation through good enclosure design,separation chutes and training using positive reinforcement techniques. .. For experimentalanimals, where housing in groups is not possible, keeping them in compatible pairs is a viablealternative social arrangement. Single caging should only be allowed where there is anapproved protocol justification on veterinary or welfare grounds.A two-tiered system is not recommended as these cages are usually too small. The lowertiers do not allow primates to engage in their vertical flight response, are often darker, andanimals in the lower cages tend to receive less attention from attending personnel.Adequate space alone does not in itself provide for good welfare, but larger enclosuresallow greater complexity of cage furnishings and other enrichments, and greater flexibility formeeting social needs.Illumination of each cage should be uniform and sufficient for adequate inspection ofanimals.As animals like to work for their food, increasing processing time, increasing foraging,or providing puzzle feeders or other feeding devices is encouraged.Infants should not be separated from their natal group at an early age but should remainwith their mother until weaning age which varies greatly between species.Primates of many species can be quickly trained using positive reinforcement techniquesto cooperate with a wide range of scientific, veterinary and husbandry procedures. Such trainingis advocated whenever possible as a less stressful alternative to traditional methods usingphysical restraint. Techniques that reduce or eliminate adverse effects not only benefit animalwelfare but can also enhance the quality of scientific research, since suffering in animals canresult in physiological changes which are, at least, likely to increase variability in experimentaldata and, at worst, may even invalidate the research. Restraint procedures should be used onlywhen less stressful alternatives are not feasible."

137Medical Research Council 2004. MRC Ethics Guide: Best Practice in the Accomodation andCare of Primates used in Scientific Research. Medical Research Council, London, UKhttp://www.mrc.ac.uk/index/publications/publications-electronic_publications.htm"Primates must [sic] be provided with a complex and stimulating environment that promotesgood health and psychological well-being and provides full [sic] opportunity for socialinteractions, exercise and to express a range of behaviours appropriate to the species. .. Thevolume and height of the cage (or enclosure) are particularly important for macaques andmarmosets, which flee upwards when alarmed. Their cages and enclosures should be floor-toceilinghigh whenever possible, allowing the animals to move up to heights where they feelsecure. Double-tiered cages should not be used since they restrict the amount of vertical spaceavailable to the animals. Special justification should be given for using cages with grid floors(eg, compelling scientific or veterinary reasons) as this restricts the opportunity to providesubstrate and forage. In the case of macaques, cages should be linked to a play area orenclosure .. They should have unlimited access to this area unless it is necessary to confine themfor scientific, husbandry, veterinary or welfare purposes. Where security permits, theaccommodation should have natural light. .. Primates should be socially housed as compatiblepairs or groups, depending on their age and sex and the nature of the scientific procedures orstudy. .. Primates should not be singly housed unless there is exceptional scientific or veterinaryjustification. .. Cages and enclosures should be furnished to encourage primates to express theirfull [sic] range of behaviours. Depending on the species, this should normally include provisionfor resting, running, climbing, leaping and foraging. ..Shelves, ladders and branches should bemade from wood wherever possible even though they will have to be replaced more often. .. Thecage and enclosure should provide the animals with an area of privacy. .. To help preventboredom, novelty should be regularly introduced into the environment, for example, by rearrangingsome of the cage furniture. .. The MRC will require justification for the use ofscientific procedures that restrict the opportunity to forage. .. Positive reinforcement techniquesshould be used to train primates to cooperate with catching, handling, restraint and researchprocedures. The routine use of squeeze-back cages and nets should be actively discouraged.“National Center for the Replacement, Refinement and Reduction of Animals in Research. 2006NC3Rs Guidelines: Primate Accomodation, Care and Use. London: National Center for theReplacement, Refinement and Reduction of Animals in Researchhttp://www.nc3rs.org.uk/page.asp?id=277"The guidelines were developed by reviewing the published literature and through consultationwith the scientific community, veterinary and animal care staff, the Animals (ScientificProcedures) Inspectorate, and animal welfare organisations. They represent a framework forapplying and reviewing the expectations of the funding bodies in the humane [sic] use ofprimates. The guidelines set out contemporary best practice in the use of primates in biomedical,biological, veterinary and behavioural research, and include principles relating to the source,housing, capture, handling, restraint and training of primates. .. They are readily applicable tothe majority of research programmes using primates. .. Cages and enclosures should be floor toceiling high whenever possible, with adequate perching to allow all animals to move up toheights where they feel more secure. .. Double-tiered cages should not be used since they restrictthe amount of vertical space available to the animals. .. Where security permits, theaccomodation should have natural light. .. Primates should be socially-housed as compatiblepairs or groups. .. Primates should not be housed singly unless there is exceptional [sic]scientific or veterinary justification. .. The vertical and horizontal dimensions of the cage andenclosure should be exploited fully by incorporating shelves, logs, ladders, climbing structures,branches, hammocks, swings, ropes and objects to manipulate. .. Shelves, ladders and branchesshould be made from wood wherever possible. .. All primates should be given the opportunity to

138forage daily, by scattering food in litter or substrate on the floor, or in a tray, and by usingdevices that encourage foraging activity. .. Positive reinforcement techniques should be used totrain primates to cooperate with capture, handling, restraint and research procedures. Theroutine use of squeeze-back cages and nets should be actively discouraged.“National Health and Medical Research Council 2004. Australian Code of Practice for the Careand Use of Animals for Scientific Purposes 7th Edition. Australian Government PublishingService, Canberra, Australiahttp://www7.health.gov.au/nhmrc/publications/synopses/ea16syn.htm"People who use animals for scientific purposes have an obligation to treat them with respectand consider their welfare as an essential factor when planning and conducting studies."National Health and Medical Research Council Animal Welfare Committee 2003. Policy on theCare and Use of Non-Human Primates for Scientific Purposes. National Health and MedicalResearch Council, Canberra, Australiahttp://www7.health.gov.au/nhmrc/ethics/animal/issues/nonhuman.htm"Social interaction is paramount for well-being. Social deprivation in all its forms must beavoided. ... Animals that need to be individually caged, either for experimental or holdingpurpose (for example, aggressive adult males), must be given contact with conspecific animals.... Accomodation should provide an environment which is as varied as possible. It should meetthe behavioural requirements of the species being used and must provide access to an outsideenclosure for animals held long-term (that is, longer than six weeks). ... Emphasis must beplaced on environmental enrichment."National Research Council 1996. Guide for the Care and Use of Laboratory Animals, 7thEdition. National Academy Press, Washington, DChttp://www.nap.edu/books/0309053773/html/"Proper care, use, and humane treatment of animals used in research, testing, and education ..require scientific and professional judgment based on knowledge of the needs of the animals. .. Agood management program provides the environment, housing, and care that ... minimizesvariations that can affect research. .. Animals should be housed with the goal of maximizingspecies-specific behaviors and minimizing stress-induced behaviors. For social species, thisnormally requires housing in compatible pairs or groups. .. In general, lighting should bediffused throughout an animal holding area and provide sufficient illumination for the well-beingof the animals and to allow good housekeeping practices, adequate inspection of animals -including the bottom-most cages in racks - and safe working conditions for personnel."National Research Council 1998. The Psychological Well-Being of Nonhuman Primates.National Academy Press, Washington, DChttp://fermat.nap.edu/books/0309052335/html/index.htmlMeeting the criteria of psychological well-being implies:• "Appropriate social companionship.• Opportunities to engage in behavior related to foraging, exploration, and other activitiesappropriate to the species, age, sex, and condition of the animal.• Housing that permits suitable postural and locomotor expression.• Interactions with personnel that are generally positive and not a source of unnecessarystress.Procedures that reduce reliance on forced restraint ... are less stressful for animals and staff,safer for both, and generally more efficient. .. Social interactions are considered to be one of the

139most important factors influencing the psychological well-being of most nonhuman primates. ...Knowing that most primates benefit from social interactions, it should be obvious that they canbe harmed by a lack of social interaction. .. The common practice of housing rhesus monkeyssingly calls for special attention. .. Every effort should be made to house these [singly caged]animals socially (in groups or pairs), but when this is not possible, the need for single housingshould be documented by investigators and approved by the IACUC. ... Although the causes ofself-directed biting are poorly understood, prolonged individual housing is probably aninfluential contributing factor. ... To reduce the stress of physical restraint, many primates canbe trained for routine procedures. ... Under natural conditions, many primates spend much oftheir lives aboveground and escape upward to avoid terrestrial threats. Therefore, these animalsmight perceive the presence of humans above them as particularly threatening .. Even macaques,which some describe as semiterrestrial, spend most of the day in elevated locations and seek therefuge of trees at night ..Optimal use of available cage space might well depend more on theplacement of perches, platforms, moving and stationary supports, and refuges than on cage sizeitself. .. The animal technician's and caregiver's roles are pivotal to the social support ofprimates, particularly animals that are singly caged. .. Enrichment methods that have not beensubjected to empirical testing should be viewed simply as invalidated ideas, regardless of howwell intended they might be."Office of Laboratory Animal Welfare (OLAW) 2006 Enrichment for Nonhuman Primates.Bethesda, MD: Office of Laboratory Animal Welfarehttp://grants.nih.gov/grants/olaw/request_publications.htm"This book serves as an introduction to the basic behavior and environmental enrichment." Inbaboons "boredom, stress and, ultimately, problem behavior may result from confinement insmall enclosures, lack of enrichment activities, solitary housing ... Examples of abnormalbehavior patterns .... are hair eating and regurgitation. .. More severe problems, such as selfbiting,also have been reported in captive baboons. ... Captive chimpanzees may develop badhabits, including strange behaviors not normally seen in the wild. [e.g. hair plucking] ...Diarrhea may be a response to psychological stress. ... Because of the intrinsic social nature ofmacaques, pair or group housing of compatible animals is extremely important. ... Because ofthe animals' [macaques] tendency to flee upward when escaping a perceived threat, they benefitfrom perches, shelves or other structures that increase the three-dimensional space of theenclosure. Generally, older macaques prefer a non-moving shelf or perch, while the youngerones will readily use swings. ... Because the monkeys will chew on these toys, they should berelatively durable, such as heavy-duty dog toys. ... Rotating different toys in the enclosure andremoving them periodically will help to keep the toys novel and increase the animals' interest inthem. ... Abnormal behaviors are an undesirable consequence of captive housing, reflecting aninadequate environment for maintaining the animal. ... Redirection of an abnormal behavior[e.g., via fleece etc.] is not a 'cure' and should only be regarded as a temporary correction." ..."Self-injurious behaviors" ... "such as self hair-pulling and self-biting, often are the result ofunusual stress". They also occur in squirrel monkeys where "'pacing' may be eliminated byincreasing the animal's available travel paths by installing additional perches."Organisation for Economic Co-Operation and Development [OECD] 2000. Guidance Documenton the Recognition, Assessment, and Use of Clinical Signs as Humane Endpoints forExperimental Animals Used in Safety Evaluation [OECD Guidance Document No. 19 onHumane Endpoints]. OECD, Paris, Francehttp://www.olis.oecd.org/olis/2000doc.nsf/LinkTo/env-jm-mono(2000)7"A humane endoint can be defined as the earliest indicator in an animal experiment of severepain, severe distress, suffering, or impending death. .. Pain can be defined as an unpleasant

140sensory and emotional experience associated with actual or potential tissue damage, ordescribed in terms of such damage." Distress is "An aversive state resulting from maladaptationor inability to adapt to stressors. .. Distress is usually associated with a change in motility orlocomotion, and can result in stereotype behaviour. .. Retreat to a corner of the cage orexcessive struggling or vocalisation on dosing are examples of distress in anticipation of anexperimental procedure. .. If something is known to cause suffering in humans, it should beassumed to cause suffering in animals."Prentice ED, Zucker IH, Jameton A 1986. Ethics of animal welfare in research: The institution'sattempt to achieve appropriate social balance. The Physiologist 29, 1&19-21"Physical restraint procedures should be used on awake animals only after alternativeprocedures have been considered and found to be inadequate. If a restraint will be utilized theanimal should be trained or conditioned to the restraining device, using positive reinforcement,prior to the beginning of the experiment"Public Health Service (PHS) 1996. U.S. Government Principles for the Utilization and Care ofVertebrate Animals Used in Testing, Research, and Training. In Guide for the Care and Use ofLaboratory Animals National Research Council 117-118. National Academy Press, Washington,DChttp://grants.nih.gov/grants/olaw/references/phspol.htm#U.S.Government Principles"Unless the contrary is established, investigators should consider that procedures that causepain or distress in human beings may cause pain or distress in other animals."Smith JA, Boyd KM 2003. The Boyd Group of papers on: The use of non-human primates inresearch and testing. Animal Technology and Welfare 2, 89-97"Unless specifically justified, infants should remain with their mothers until they are no longerdependent on them. .. The minimum cage sizes for both marmosets and macaques detailed in theHome Office guidance (1989), and the European standards, are inadequate - particularly inrespect of vertical dimensions of cages - and do not reflect current best practices. ... Every effortshould be made to train non-human primates to accept routine scientific procedures, and sominimise the stress caused to the animals."USDA 2002. Animal Welfare Regulations Revised as of January 1, 2002 [Code of FederalRegulations, Title 9, Chapter 1, Parts 1-4 United States Department of Agriculture]. U.S.Government Printing Office, Washington, DChttp://www.access.gpo.gov/nara/cfr/waisidx_02/9cfrv1_02.html"Handling of all animals shall be done as expeditiously and carefully as possible in a mannerthat does not cause trauma, overheating, excessive cooling, behavioral stress, physical harm, orunnecessary discomfort. ... Deprivation of food or water shall not be used to train, work, orotherwise handle animals. .. Lighting must be uniformly diffused throughout animal facilities andprovide sufficient illumination to aid in maintaining good housekeeping practices, adequatecleaning, adequate inspection for animals, and for the well-being of the animals. .. Inadequatespace may be indicated by ... stress, or abnormal behavior patterns. .. Primary enclosures .. must[sic] provide sufficient space for the nonhuman primates to make normal postural adjustmentswith freedom of movement. .. These minimum space requirements must [sic] be met even ifperches and ledges, swings, or other suspended fixtures are placed in he enclosure. .. Researchfacilities must [sic] develop, document, and follow an appropriate plan for environmentalenhancement. .. The plan must [sic] include specific provisions to address the social needs ofnonhuman primates. .. The physical environment in the primary enclosures must be enriched byproviding means of expressing species-typical activities."

Zimmermann M 1987. Ethical principles for the maintenance and use of animal in neuroscienceresearch. Neuroscience Letters 73, 1"Animals are generally accepted to be sentient and capable of suffering, and to have speciesspecificrequirements of living. ... Maintenance of experimental animals should account forspecies-specific needs of accommodation, activity, feeding and social interactions to the degreepossible."SurveysBaker KC, Weed JL, Crockett CM, Bloomsmith MA 2007. Survey of environmentalenhancement programs for laboratory primates. American Journal of Primatology 69, 377-394"Here we report the results of a 2003 survey that was sent to individuals overseeing enrichmentprograms at a variety of primate research institutions. Data were obtained on the managementof 35,863 primates in 22 facilities. While most primates were reported to be housed socially(73%), social housing for indoor-housed primates appears to have changed little over the past10 years. Research protocol issues and social incompatibility were commonly cited constraints.Implementation of feeding, manipulanda, and structural enrichment was relativelyunconstrained, and contributions to these aspects of behavioral management generally includedindividuals in a wide variety of positions within a facility. In contrast, enrichment devices wereused on a less widespread basis within facilities, and positive reinforcement programs thatinvolved dedicated trainers were rare.""Social Housing: We focused on the indoor population to assess the current status ofefforts to reduce the use of single housing in research. With outdoor-housed primates excludedfrom the analysis, our sample included 17,663 individuals, 46% of which were housed socially.""Feeding Enrichment: All facilities included feeding enrichment in their plans. Nofacilities provided fewer than half (1-50%) of their nonhuman primates with feedingenrichment... Fruit was distributed at all facilities, nuts and seeds at 95%, vegetables at 91%,manufactured treats at 73%, and other items at 64% of facilities.""Manipulanda: All facilities employed manipulable objects. Of the categories ofmanipulanda provided as response choices, the items used most frequently were mirrors (100%),balls (95%), synthetic chew toys (86%), and hanging toys (86%). Rattles were provided at 68%of the facilities, wood at 59%, and bells at 18%.""Devices: Ninety-one percent of facilities reported the use of enrichment devices. Of thedevices offered as response choices, the most common were puzzle tube feeders (77% offacilities) and Astroturf foraging boards (77%), followed by puzzle balls (59%), fleece boards(36%) and other devices (36%).""Structural Enrichment: Most facilities reported providing structural enrichment to all oftheir animals. All facilities reported the use pf perches, 73% swings, 59% used barrels, 50%bedding/nesting materials, 36% exercise cages or playrooms."With respect to social housing, in the 1994 survey 38% of indoor-housed macaquespecies were housed socially. In the current survey, among these species, 44% of the individualsin cages wee housed socially. This comparison indicates that the use of social housing for cagedprimates has not expanded as substantially as many applied behavioral scientists would havehoped.Since the practice of single housing is a major risk factor for the development ofabnormal behavior, the continued prevalence of single housing perpetuates the need forintervention."141

142Bayne K 1989 Resolving issues of psychological well-being and management of laboratorynonhuman primates. In Housing, Care and Psychological Wellbeing of Captive and LaboratoryPrimates. Segal EF (ed), 27-39 . Noyes Publications, Park Ridge, NJ"The survey indicated that approximately 83% of adult captive primates at NIH are caged alone.As only 9% of scientists interviewed currently train their animals to go into transport cages, themajority use squeeze panels to transfer animals or to restrain them at the front of the cage. ..Themost frequent recommendations [of NIH scientists interviewed] were for larger and morecomplex cages."Prescott MJ, Buchanan-Smith HM 2007. Training laboratory-housed non-human primates, part I:a UK survey. Animal Welfare 16(1), 21-36Training using positive reinforcement is increasingly recognised as a valuable tool for thehumane and effective management and use of laboratory-housed non-human primates. A surveywas carried out on the use of training and other learning processes (socialisation, habituationand desensitisation) in over half of UK establishments using and breeding primates. There iswidespread awareness of training as a refinement technique but it not used as widely or as fullyas it might be. We conclude that there is opportunity for refinement of common scientific,veterinary and husbandry procedures (such as blood and urine collection, injection, capturefrom the group and weighing) through use of positive reinforcement training, especially whencombined with appropriate socialisation, habituation and desensitation. Recommendations onbest practice, training techniques and staff education are given.Reinhardt V 1994. Survey of environmental enhancement for research macaques. LaboratoryPrimate Newsletter 33(3), 1-2http://www.brown.edu/Research/Primate/lpn33-3.html#victorA survey of 11 facilities. The percentage of caged macaques permanently: a) exposed toenrichment objects ranged from 18% to 100% with a mean of 86%, b) housed in pairs or smallgroups ranged from 0% to 98% with a mean of 38%.Ethical ConsiderationsÖbrink KJ, Rehbinder C 1999. Animal definition: a necessity for the validity of animalexperiments? Laboratory Animals 22, 121-130"'Material and Methods' section mostly reveals an obvious or almost total lack of informationabout the animals. ... If a researcher, through carelessness or ignorance, should use moreanimals for a project than is necessary, it must be considered unethical. ...Without hesitation, itis a scientific demand that all factors that have not proven to be insignificant should be checked,controlled or kept constant."American Society of Primatologists 2000. American Society of Primatologists guidelines for theethical treatment of nonhuman primates. ASP Bulletin 24(4), 4"Despite their varied disciplines, ASP members hold the following general principles incommon:1. The most important of these principles is that we accept the responsibility of stewardship fornonhuman primates, and this responsibility must [emphasis added] be reflected in ourhusbandry practices and research protocols whether in field, laboratory, or other setting.5. We should make use of information on a species natural history to improve management andenrich environments, because physical and psychological well-being are essential not only to thehealth of the animals but also to the validity of the research results.”

143Arluke A 1994. The ethical socialization of animal researchers. Lab Animal 23(6), 30-35"In all but two of the 35 laboratories, newcomers faced a closed moral universe where issues ofmorality were defined institutionally, and hence rarely confronted by individuals. ... It wascontroversial or risky to admit to having ethical concerns, because to do so was tantamount toadmitting that there really was something morally wrong with animal experimentation, therebygiving 'ammunition to the enemy’.”Association of Veterinarians for Animal Rights 2005. Contemporary Veterinarian's Oath.Association of Veterinarians for Animal Rights, Davis, CAhttp://www.avar.org/"Being admitted to the profession of veterinary medicine, I solemnly swear to use my scientificknowledge and skills to protect the health and well-being of all nonhuman animals, to relievepain and suffering in nonhuman animals, to strengthen the understanding of the inherent needsand interests of all nonhuman animals, and to promote the preservation of wildlife and theirnatural environment. I will practice my profession conscientiously, with dignity, compassion,and integrity. I accept as a lifelong obligation the continual improvement of my professionalknowledge and competence. "Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 2.1. How toRefer to an Animal—Using the Proper Pronoun. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/basic.html#pron”As caregivers, we do not use the pronoun it when referring to an animal. An animal is not anobject! We do not think that calling an animal he or she encourages anthropomorphism, but thatit does acknowledge the fact that we are dealing with an individual sentient being who can feeldiscomfort, pain and distress in very similar ways as we do. Calling individual animals he or shehelps us deal with something that deep down, we are not really comfortable with — namely thefact that these animals have no choice about deciding whether they want to be used in researchand then killed.Referring to an animal as it is neither correct nor scientific, because it overlooks the factthat animals, just like humans, have a biological gender. Therefore, they should be referred toaccordingly with the correct pronouns he or she. When we label an animal with the incorrectpronoun it, we risk treating the animal like an inanimate object incapable of feeling discomfort,pain and distress.“Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007. Making Lives Easier for Animals in Research Labs - Chapter 2.2. Higher-Versus Lower-Order Species. Washington, DC: Animal Welfare Institutehttp://www.awionline.org/pubs/LAREF/basic.html#spec”It seems that Refinement in the use of animals for research includes choosing lower-orderspecies rather than higher-order species, presumably due to the assumption that the lower-orderanimals suffer less and that their use in experiments poses fewer ethical problems. Where do wedraw the line?For people who are using these terms, lower simply means less like humans, and highermeans more like humans. This terminology is tied in with the incorrect view of evolution as aladder of progress toward especially evolved beings, such as humans. How would animals, usedby humans for biomedical research, classify the human species? Of a high order? Crown of

144creation? Very unlikely!I think all animals deserve the same consideration, whether they are a rat ormouse — of presumed low order — or a dog or monkey — of presumed higher order. It seemsstrange to me to categorize animals into different orders and then treat them accordingly.“Canadian Council on Animal Care, Olfert ED, Cross BM, McWilliam AA 1993. Guide to theCare and Use of Experimental Animals, Volume 1, 2nd Edition. Canadian Council on AnimalCare, Ottawa, ONhttp://www.ccac.ca/en/CCAC_Programs/Guidelines_Policies/GUIDES/ENGLISH/toc_v1.htm"We are morally responsible for any living thing that we cause to be dependent upon us,including animals used in research, teaching and testing."Halpern-Lewis JG 1996. Understanding the emotional experiences of animal research personnel.Contemporary Topics in Laboratory Animal Science 35(6), 58-60"Animal research personnel should be encouraged to join in the pursuit of progress with therecognition that, in addition to knowledge and skills, primary attributes must be feelings ofcompassion and sensitivity toward animals. Because animals cannot speak for themselves, it isup to empathetic and caring personnel to see that they are treated humanely and with respect. Avariety of suggestions have been provided to enable research participants to perform necessarytasks without impeding experimental results or detracting from the integrity of the animal-humanrelationship. It is my belief that individuals who demonstrate caring behaviors while beingallowed appropriate outlets for expression will remarkably enrich the overall researchexperience of humans and animals alike."Herzog H 2002. Ethical aspects of relationships between humans and research animals. ILAR[Institute for Laboratory Animal Research] Journal 43(1), 27-32http://dels.nas.edu/ilar_n/ilarjournal/43_1/Ethical.shtml"More often than not, moral dilemmas are the result of good people trying to do the right thingwhen the right thing is unclear. ... I have spoken with some animal care staff who havecomplained about investigators who rarely set foot in their institution's animal colony and whoappear to regard research animals as organ repositories. In addition, some researchers showlittle understanding of the ethical problems faced by technicians. ... There is every reason tobelieve that individuals who care about their wards on a personal level actually treat theanimals better. .. Inevitably, individuals who work with animals in the context of biomedical andbehavioral research will sometimes form bonds with the animals with whom they interact. Whenan animal is transformed from ‘object’ to ‘pet,’ its moral status is changed. Although humanresearchanimal relationships may enhance the well-being of laboratory animals, they involve amoral cost to the human caretakers. Institutions should acknowledge the existence of these bondsand provide support mechanisms to help laboratory personnel deal with the moral challenges oftheir profession.”Mroczek NS 1994. Recognizing animal suffering and pain. Lab Animal 23(1), 27-31Highlights the "human conditioning to the incongruous position that considers animalsdissimilar to humans with respect to drive, need, or sensation, yet similar enough to be used asmodels for the study of humans themselves. ... Identification, sympathy, and positive regard by ascientist or animal care worker can, most of all, help to encourage optimum care and treatmentof animals in pain. Recognition of animals suffering and pain is made possible by feeling for andinterest in animals themselves, as sentient organisms, first and foremost, and feeling for andinterest in animal behavior in totality."

145Petto AJ, Buchanan-Smith H 1994. Psychological well-being and other projections of the humancondition: Their meaning for research activities with non-human primates. XVth Congress of theInternational Primatological Society, 359"The often cited paradox for researchers studying nonhuman primates is that we must considerthem sufficiently similar to us so that our studies will be valid and significant; at the same timewe must consider them sufficiently different that we can study them in ways that are ethicallyobjectionable for studying fellow humans."Public Health Service (PHS) 1996. U.S. Government Principles for the Utilization and Care ofVertebrate Animals Used in Testing, Research, and Training. In Guide for the Care and Use ofLaboratory Animals National Research Council 117-118. National Academy Press, Washington,DChttp://grants.nih.gov/grants/olaw/references/phspol.htm#principlePrinciple IV states that "Proper use of animals, including the avoidance or minimization ofdiscomfort, distress, and pain when consistent with sound scientific practices, is imperative.Unless the contrary is established, investigators should consider that procedures that cause painor distress in human beings may cause pain or distress in other animals."Reese EP 1991. The role of husbandry in promoting the welfare of laboratory animals. InAnimals in Biomedical Research Hendriksen CFM, Koeter HBWM (eds), 155-192. Elsevier,Amsterdam, The Netherlands"That many scientists lack detailed information about their animals, especially their behavior, isdistressing and reflects a serious disregard for the single most important element of theirresearch. ... The animal is the key to the entire experiment. ... There is only one 'right' attitude,and that is respect for the individual animal."Röder EL, Timmermans PJA 2002. Housing and care of monkeys and apes in laboratories:adaptations allowing essential species-specific behaviour. Laboratory Animals 36, 222-241"An animal is not a survival machine but a genetically programmed organism. A machine'survives' longest if it is maintained properly but not used. An animal, however, needs to use thefunctions that evolved for its survival, in order to keep those functions from decay anddeterioration. Whoever deliberately chooses a species because of its specific properties, in hisown interest should be expected to take care that these properties remain unimpaired."Reinhardt V 1996. Letter to the Editor. Lab Animal 25(5), 42"I was a bit surprised that the animals of my article lost their biological gender and werereferred to in the neuter gender, like things. Perhaps this sounds more scientific, but it actually isscientifically incorrect. Animals with neuter gender cannot reproduce. A female is a 'she' and notan 'it', and a male is a 'he' and not an 'it'."Schwindaman D 1991. The 1985 animal welfare act amendments. In Through the Looking GlassNovak MA, Petto AJ (eds), 26-32. American Psychological Association, Washington, DC"While we [veterinarians] pledge to take responsibility for the welfare of animals, we also vowto use scientific knowledge and skills for the advancement of medical knowledge. The wisecomposer of this oath saw no conflict between relieving animal suffering and advancing science.Indeed, there is none."

146Spaeth GL 1994. Editorial: Caring for animals, caring for ourselves. Ophthalmic Surgery 25,426"Our behavior to other creatures reflects our own characters. We are shaped by what we do.When we act uncaringly toward experimental animals we become uncaring human beings. Whatis the worth of medical miracles achieved at the cost of inflicting trauma on others that cannothelp but scar our own characters? When we act uncaringly towards experimental animals, wedamage ourselves. When we hurt experimental animals, we hurt ourselves."Traystman RJ 1987. ACUC, who needs it? The investigator's viewpoint. Laboratory AnimalScience 37 (Special Issue), 108-110“The academic and intellectual freedom to pursue these activities is crucial to the livelihood ofany investigator... Most investigators think only briefly about the care and handling of theiranimals and clearly have not made it an important consideration in their work. .. Allinvestigators consider themselves upstanding citizens of excellent ethical and moral character.Their feeling may be that since they are moral and ethical in every sense of the word, they arequite capable of monitoring their own animals without outside interference."Zbinden G 1985. Ethical consideration in toxicology. Food and Chemical Toxicology 23, 137-138"Toxicologists must realize that their important mission ... does not give them an unconditionallicense to kill as many animals as they wish and hide behind regulatory requirements, testingguidelines and bureaucratic prescriptions for good laboratory practice."

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