Refinement and Environmental Enrichment for Primates: Enrichment 1-3

Bibliographyon Refinement and Environmental Enrichment for Primates. Enrichment1-3


(1) Definition
(2) Promoting Social Behavior
(2,1,a) Group-housing: Practical Issues
(2,1,b) Group-housing: Group Formation/Introduction/Integration
(2,2,a) Pair-housing: Practical Issues, Time Budget
(2,2,b) Pair-housing: Pair formation
(2,3)   Grooming-Contact Caging
(2,4)   Positive Interaction with Humans
(3) Promoting Intelligent Behavior (positive reinforcement training)
(3,1) Basic Recommendations
(3,2) Species-specific Recommendations
(4) Promoting Foraging and Food Processing Behavior
(4,1) Foraging Devices
(4,2) Substrates
(4,3) Produce
(4,4) Ice and Water
(4,5) Food Preparation and Feeding Schedule
(5) Promoting Arboreal Behavior
(5,1) The Importance of Access to the Vertical Dimension of Space
(5,2) Elevated Structures

(6) Promoting Object-oriented Behavior
(7) Promoting CuriosityBehavior (watching videos; watching out of the window)
(8) Safety Concerns

Regulationsand Guidelines

Ethical Considerations

(1) Definition

Environmental enrichment providesmore species-adequate living and handling conditions thereby bufferingstress and distress responses to captivity.Environmental enrichmentis the provision of stimuli which promote the expression of species-appropriatebehavioral and mental activities in an understimulating artificialenvironment.

United States Department of Agriculture1991. Title9, CFR (Code of Federal Register), Part 3. Animal Welfare; Standards;Final Rule. Federal Register 56(No. 32), 6426-6505
"The physical environment in the primary enclosures mustbe enriched by providing means of expressing noninjurious species-typicalactivities. .. Examples of environmental enrichment include providingperches, swings, mirrors, and other increased cage complexities;providing objects to manipulate; varied food items; using foragingor task-oriented feeding methods; and providing interaction withthe care giver or other familiar and knowledgeable person consistentwith personnel safety precautions."

(2) PromotingSocial Behavior

Canadian Council on Animal Care, OlfertED, Cross BM, McWilliam AA 1993. Guideto the Care and Use of Experimental Animals, Volume 1, 2ndEdition. Canadian Council on Animal Care, Ottawa
"The social needs of animals used in research, teaching,or testing, should be given equal consideration with environmentalfactors such as lighting, heating, ventilations and containment(caging). Particularly in the case of singly housed animals, dailyobservation provides an alternative from of social contact forthe animal and commonly facilitates handling in that the animalbecomes accustomed to the human presence. .. Most animals shouldnot be housed singly unless required by medical condition, aggression,or dictates of the study. Singly housed animals should have somedegree of social contact with others of their own kind. ... Inthe interest of well-being, a social environment is desired foreach animal which will allow basic social contacts and positivesocial relationships. Social behaviour assists animals to copewith circumstances of confinement."

European Commission2002. The Welfare of Non-human Primates - Report of the ScientificCommitte on Animal Health and Animal Welfare. European Commission,Strasbourg, France
"Primates should not be housed singly unless fully justifiedby health considerations (for the animal and human handler) orresearch procedures, as advised following an ethical review process.If primates have to be singly housed, the animals should havevisual, olfactory and autitory contact with conspecifics."

European Economic Community 1986.Council Directive 86/609 on the Approximation of Laws, Regulations,and Administrative Provisions Regarding the Protection of AnimalsUsed for Experimental and Other Scientific Purposes, Annex IIGuidelinesfor Accommodation and Care of Animals. Official Journalof the European Communities L358 , 7-28
European guidelines for housing and handling of laboratoryanimals. "The performance of an animal during an experimentdepends very much on its confidence in man, something which hasto be developed. ... It is therefore recommended that frequentcontact should be maintained so that the animals become familiarwith human presence and activity. Where appropriate, time shouldbe set aside for talking, handling and grooming. The staff shouldbe sympathetic, gentle and firm when associating with the animals."

International Primatological Society1993. IPSInternational guidelines for the acquisition, care and breedingof nonhuman primates, Codes of Practice 1-3. Primate Report35, 3-29
" A compatible conspecific probably provides more appropriatestimulation to a captive primate than any other potential environmentalenrichment factor. ... Monkeys should, unless there are compellingreasons for not doing so, be housed socially. ... Young monkeyshould not normally be separated from its mother at an early age(i.e., at 3-6 months) but should remain in contact for one yearto 18 months, in most species. There is unlikely to be any greaterproductivity through early weaning, in seasonally breeding species,such as rhesus monkeys. Even in non-seasonal breeders, any slightincrease in productivity must be offset against the resultingbehavioural abnormalities of the offspring."

National Research Council 1996. Guide for theCare and Use of Laboratory Animals, 7th Edition="http:>. NationalAcademy Press, Washington
"Animals should be housed with the goal of maximizingspecies-specific behaviors and minimizing stress-induced behaviors.For social species, this normally requires housing in compatiblepairs or groups."

National Research Council 1998. ThePsychological Well-Being of Nonhuman Primates="http:>. NationalAcademy Press, Washington
"Social interactions are considered to be one of the mostimportant factors influencing the psychological well-being ofmost nonhuman primates. ... The common practice of housing rhesusmonkeys singly calls for special attention [p. 99] ... Every effortshould be made to house these [singly caged] animals socially(in groups or pairs), but when this is not possible, the needfor single housing should be documented by investigators and approvedby the IACUC. ... The animal technician's and caregiver's rolesare pivotal to the social support of primates, particularly animalsthat are singly caged."

United States Department of Agriculture1991. Title9, CFR (Code of Federal Register), Part 3. Animal Welfare; Standards;Final Rule. Federal Register 56(No. 32), 6426-6505
The environmental enhancement plan "must include specificprovisions to address the social needs of nonhuman primates ofspecies known to exist in social groups in nature. ... Examplesof environmental enrichment include ... providing interactionwith the care giver or other familiar and knowledgeable personconsistent with personnel safety precautions."

(2,1,a) Group-housing:Practical Issues

Alford PL, Bloomsmith MA, KeelingME, Beck TF 1995. Wounding aggression during the formation andmaintenance of captive, multimale chimpanzee groups. Zoo Biology14, 347-359
"There is more wounding and more severe wounding in groupscomposed of older, socially experienced males than in groups composedof younger socially inexperienced males, many of whom also hadextensive visual exposure to one another before grouping."

Baker KC, Seres M, Aureli F, de WaalFBM 2000. Injury risks among chimpanzees in three housing conditions.American Journal of Primatology 51, 161-175
"Over a two-year period all visible injuries to 46 adultmales, 64 adult females, and 25 immature chimpanzees were recorded.... Housing included compounds containing about 20 chimpanzees,interconnected indoor-outdoor runs for groups of up to 12 individuals,and smaller indoor-outdoor runs for pairs and trios. ... Compound-housedchimpanzees incurred the highest level of minor wounding, butserious wounding levels were not affected by housing condition.... Overall, this study indicates that maintaining chimpanzeesin pairs and trios would not be an effective means for reducinginjuries. 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 cages that allowsocial grouping. Contemporary Topics in Laboratory Animal Science31(3), 10-12
"These two design modifications [PVC tunnels and stainlesssteel tunnels connecting two adjacent cages] allow us to inexpensivelymodify existing caging to meet the USDA regulations of socialgrouping."

Bernstein IS 1989. Breeding coloniesand psychological well-being. American Journal of Primatology19(Supplement 1), 31-36
Valuable discussion of relatively safe group-housing managementpractices.

Bloomsmith MA 1989. Interaction betweenadult male and immature captive chimpanzees: Implications forhousing chimpanzees. American Journal of Primatology 19(Supplement1), 93-99
"These observations suggest that captive adult male chimpanzeeshave the potential to develop affiliative relationships with immatureconspecifics. Housing adult males in groups along with infantsmay be an important way of increasing the social complexity ofthe males' environments."

Boyce WT, O'Neill-Wagner PL, PriceCS, Haines MC, Suomi SJ 1998. Crowding stress and violent injuriesamong behaviorally inhibited rhesus macaques. Health Psychology17, 285-289
Rhesus group of 36 animals was kept during 6 'warm' monthsin a large outdoor enclosure, during 6 'cold' months confinedin a building. "During the 6-month period of confinementstress, a fivefold acceleration in [medically-attended] injuryincidence was found."

Catlow G, Ryan PM, Young RJ 1998.Please don't touch, we're being enriched! In Proceedings ofthe Third International Conference on Environmental EnrichmentHare VJ, Worley E (eds), 209-217. The Shape of Enrichment, SanDiego
"Enrichment often involves manipulation of animals' lives.However, non-interference in their social lives is an importantform of environmental enrichment for chimpanzees." Ratherthan locking the chimpanzees "into their indoor cages everyevening, an average of 17 hours a day" the animals were given"continuous access to their whole area and each other 24hours a day, except for routine cleaning. ... Almost from thebeginning [1991] the group changed. There appeared to be a calmingeffect with the group actually being unified. The males becamemore tolerant towards one another, and started to socialise asa unit. ... Far more normal behaviours are present and the afternoontension for both animal and keeper has ceased."

Caws C, Aureli F 2001. Copingwith short-tem space restriction in chimpanzees. PrimateEye 74, 9
"During the indoor period the chimpanzees showed no increasein aggression, grooming, and submissive greeting, nor changedtheir proximity to adult males. However, the percentage of aggressiveevents that involved more than 2 individuals was significantlylower during the indoor period. In addition, 36 dyads were identifiedas "highly aggressive" during the control period; aggressionwas reduced in these dyads during the indoor period. These resultsconfirm previous evidence that chimpanzees do not increase aggressionduring space restriction. Furthermore, they seem to inhibit aggressionby not joining ongoing conflicts and by selectively decreasingthe targeting of common `victims'."

Dazey J, Kuyk K, Oswald M, MarensonJ, Erwin J 1977. Effects of group composition on agonistic behaviorof captive pigtailed macaques (Macaca nemestrina). AmericanJournal of Physical Anthropology 46, 73-76
Females showed significantly less aggression in the presenceof adult males [one male per group] than they did in female-onlygroups.

Elton RH 1979. Baboon behavior undercrowded conditions. In Captivity and Behavior Erwin J,Maple T, Mitchell G (ed), 125-139. Van Nostrand Reinhold, NewYork
Crowding produced sharp increases in aggression, noticeableincrease in tension and general activity. "Social disintegration[e.g., vicious aggression, social withdrawal accompanied by self-directedbehaviors], as well as individual pathology [e.g., "pullingof hair out of other animals (by the handful) and eating it";chewing fingers], was the end result of the crowding in this groupof baboons."

Erwin J 1977. Factors influencingaggressive behavior and risk of trauma in the pigtail macaque(Macaca nemestrina). Laboratory Animal Science 27,541-547
"Provision of cover reduced aggression among members ofstable groups."

Erwin J 1979. Aggression in captivemacaques: Interaction of social and spacial factors. In Captivityand Behavior Erwin J, Maple T, Mitchell G (eds), 139-171.Van Nostrand, New York
Providing a male-dominated group access to two rooms ratherthan one allowed some animals to be out of the dominant male'ssight. 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 captive pigtailed macaques.American Journal of Primatology 47, 153-163
"A greater number of moves decreased the probability ofa viable birth and increased gestation length and the need forclinical treatment of the dam, while increased group size decreasedgestation length. Increased moves and group size may increasestress by continuously shuffling social relationships, keepingfemales from establishing social hierarchies, and reducing groupstability. Low group stability may increase aggression by makingfemales more likely to attack other females without knowing theopponent's social position or physical abilities."

Hartner MK, Hall J, Penderhest J,Clark LP 2001. Group-housing subadult male cynomolgus macaquesin a pharmaceutical environment. Lab Animal 30(8), 53-57
A carefully designed, successful group-formation and group-housingprotocol of five 3.5 + years old previously single-cagedcynos is described in detail. "Not only can the social complexityof the animals' interactions be increased, but also routine taskscan be accomplished with ease. The animals are easy to handle,restrain, and chair train, and they readily accept biomedicalresearch project requirements. ... Through the maintenance oftouch gates and constant visual contact during the study [requiringsingle-housing for over a month], we were able to regroup theanimals [without accidents] within 24 hours. .. Since we beganthe program, the animals have transitioned through puberty andsubadult stages .. and are now cohabitating as adults."

Judge PG, de Waal BM, Paul KS, GordonTP 1994. Removal of a trauma-inflicting alpha matriline from agroup of rhesus macaques to control severe wounding. LaboratoryAnimal Science 44, 344-350
"Results identify an unusual outbreak of serious woundingby the alpha matriline of a large captive group [of rhesus macaques]and indicate that identification and removal of the animals responsiblecan be an effective management procedure for controlling suchinjuries."

Judge P, Griffaton N, Fincke A 2001.No effect of acute crowding on the behaviorof hamadryas baboons (Papio hamadryas). American Journal of Primatology 54(Supplement1), 68-69
Aggressive, submissive, affiliative and self-directed responsesof the six adults - two males and four females - were recordedin their small indoor quarters versus large outdoor section oftheir enclosure. Agonistic behavior, and "scratching, anindicator of anxiety in primates, did not increase during crowding... Perhaps male hamadryas baboons exert such a controlling influencethat conflict management among the other group members is unnecessaryduring crowding."

Kaplan JR, Manning P, Zucker E 1980.Reduction of mortality due to fighting in a colony of rhesus monkeys(Macaca mulatta). Laboratory Animal Science 30,565-570
"Mortality resulting from fighting [17 deaths per 100females per year] in a breeding colony of rhesus monkeys livingin groups was an important management problem. It was found thatthe cause of the fighting was the social disruption resultingfrom a breeding protocol which required the regular removal ofpregnant animals from groups and introduction of nonpregnant females."

Maninger N, Kim JH, Ruppenthal GC1998. The presence of visual barriers decreases agonism in grouphoused pigtail macaques (Macaca nemestrina). AmericanJournal of Primatology 45, 193-194
"Instances of bite, grab and chase were found to be significantlygreater [among members of harem groups of 23 pig-tailed macaques]when visual barriers were absent compared to when they were present."

O'Neill-Wagner PL 1996. Facilitatingsocial harmony in a primate group. American Zoo and AquariumAssociation (AZA) Regional Conference Proceedings, 323-325
"Installing an inexpensive electric net fencing systemoffered safe and innovative separation to two groups of monkeysin the field enclosure. Animals with incentive to transfer betweenareas successfully penetrated the electric net fence by leapingover it, or darting through the mesh openings at the risk of beingzapped by a pulsating (high voltage, low amperage) electric shock.This challenging, yet penetrable fence was functional to monkeysin the following ways. The socially evicted males were able toleave their natal group when the time was approaching. When responsesby animals on the other side of the fence indicated that it wassafe to return, they would do so. This system functions in a positiveway by providing evidence of tension between and within groups,offering escape routes during aggressive interactions, [and] reducingthe potential for injuries."

Porton I, White M 1996. Managing anall-male group of gorillas: Eight years of experience at the St.Louis Zoological Park. American Zoo and Aquarium Association(AZA) Regional Conference Proceedings, 720-728
"Our experience suggests that a gorilla bachelor groupis a viable and indeed a desirable alternative to solitary housingof 'emigrated' captive males."

Reinhardt V, Reinhardt A, Houser WD1986. Hairpulling-and-eating in captive rhesus monkeys. Folia Primatologica47, 158-164
It was concluded that hair pulling and eating is an aggressivebehavioral disorder reflecting adjustment problems to a stressful[group-housing] environment.

Reinhardt V, Reinhardt A, Eisele S,Houser WD, Wolf J 1987. Control of excessive aggressive disturbancein a heterogeneous troop of rhesus monkeys. Applied AnimalBehaviour Science 18, 371-377
"Chronic harassment in a troop of rhesus monkeys was relatedto two animals. The carefully supervised removal of these individualsbrought harmony back into the group."

Reinhardt V 1990. Catching IndividualRhesus Monkeys Living in Captive Groups (Videotape). Availableon loan from Animal Care Audio-Visual Materials, WRPRC, 1220 CapitolCourt, Madison, WI 53715
A simple capture-chute design is demonstrated. Using vocalcommands, a single person swiftly catches all members of a trainedrhesus breeding group one-by-one in a transport box without causingany disturbance.

Reinhardt V 1993. Nonspecificdiarrhea in the alpha-male of a breeding troop: A case report.Laboratory Primate Newsletter 32(1), 4
"Bob's prompt recovery from intractable diarrhea uponbeing removed from his troop suggests that asserting his roleas alpha-animal constituted a chronic social challenge that mayhave altered his resistance to facultative pathogens and/or autonomicneural tone, to produce diarrhea."

Rolland RM 1991. A prescription forpsychological well-being. In Through the Looking Glass. Issuesof Psychological Well-being in Captive Nonhuman Primates NovakMA, Petto AJ (eds), 129-134. American Psychological Association,Washington DC
"By far the most common physical problem that I treatas clinical veterinarian is trauma sustained by macaques in group-housingsituations."

White G, Hill W, Speigel G, ValentineB, Weigant J, Wallis J 2000. Conversion of canine runs to groupsocial housing for juvenile baboons. AALAS 51st National MeetingOfficial Program, 126
"Our Division recently converted two rooms equipped with10 stainless steel, elevated floor canine runs into rooms providingsocial housing for young baboons. The detachable walls were removedto create larger primary enclosures and tops were fitted withstainless steel panels to provide complete containment. ... Ourgroup has trained the juvenile baboons [6 months to two yearsof age] to enter squeeze cages through guillotine openings availablein the front door of the primary enclosures."

Wolfensohn S, Peters A 2005. Refinementof neuroscience procedures using non human primates. AnimalTechnology and Welfare 4, 49-50
It is demonstrated that long-tailed macaques with cranial implantscan be group-housed without undue risk. "Contrary to initialexpectations we have not found any increased incidence in infectiondue to the presence of other animals or foraging substrate."

(2,1,b) Group-housing:Group Formation/Introduction/Integration

Baboons (Papio spp.)

Else JG, Tarara R, Suleman MA, EleyRM 1986. Enclosure design and reproductive success of baboonsused for reproductive research in Kenya. Laboratory AnimalScience 36, 168-172
"The [75] females were introduced first to the cage andgiven an opportunity to stabilize. The [6] males, whose canineteeth had been cut, were paired for at least one week prior toplacement with females. Eight animals were removed within thefirst month due to fight wounds and general incompatibility."

Wallis J, Hartley D 2001. Comparing two methods of forming large socialgroups of captive baboons (Papio spp.). American Journal of Primatology 54(Supplement1), 54-55
The formation of a large group of previously singly caged baboons[unspecified sex] was most successfully 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 pathologyin Cebus apella. LaboratoryPrimate Newsletter 30(2), 9-12
No serious aggression was associated with group formation oftwo females and four males.

Cooper MA, Thompson RK, BernsteinIS, de Waal FBM 1997. The integration of stranger males into agroup of tufted capuchin monkeys (Cebus apella). AmericanJournal of Primatology 42, 10
"The introductions were noteworthy for their early lackof 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 gradualprocess."

Fragaszy D, Baer J, Adams-Curtis L1994. Introduction and integration of strangers into captive groupsof tufted capuchins (Cebus apella). International Journalof Primatology 15, 399-420
"Two to four unfamiliar animals were housed together for3-5 days in one room of each resident group's two-room cage, whilethe resident group remained in the other room. Following the acclimationperiod, we permitted the resident group to mix with the newcomersin the full cage. No morbidity from aggression occurred at thetime of introductions or during several months following. Introductionsof adult females can be carried out with acceptable risk to thenewcomers provided that careful monitoring occurs, so that theonset of severe aggression instigated by resident females towardnew females can be avoided [by temporarily dividing the groupfor a few days]; juveniles can be introduced with minimal risk,and adult males can be introduced into groups lacking residentadult males with minimal risk."

Wolff A, Ruppert G 1991. A practicalassessment of a non-human primate exercise program. Lab Animal20(2), 36-39
Five females and three males were transferred once a week toan exercise pen for several hours. Aggressive interactions werenever observed throughout a 9-week study period.

Chimpanzees (Pan spp.)

Bloomsmith MA, Lambeth SP 1996. Managingaggression in multi-male, multi-female chimpanzee groups. AmericanZoo and Aquarium Association (AZA) Regional Conference Proceedings,449-452
"We found that wounding aggression was minimal duringintroductions of females to males or other females, and duringmale-male introductions of formerly single-caged adolescent andyoung adult males having long-term prior visual familiarity. Seriouswounding occurred during male-male introductions, particularlywhen there were major discrepancies in their ages and social experience."

Bloomsmith MA, Baker KC, Ross SK,Lambeth SP 1998. Enlarging chimpanzee social groups: The behavioralcourse of introductions. American Journal of Primatology45, 171
New group members were first introduced behind mesh fencing.Subsequent full physical contact did not further increase agonism.All 42 introductions of chimpanzees in already established groupswere successful.

Fritz J, Howell S 2001. Captive chimpanzeesocial group formation. In Special Topics in Primatology Volume2 - The Care and Management of Captive Chimpanzees Brent L(ed.), 172-203. The American Society of Primatologists, San Antonio
"Forming new social groups of captive chimpanzees requiresappropriate facilities, a knowledgeable staff, planning, and carefulobservations." A well-tested socialization system is reviewedwhich "includes a gradual acclimation of unfamiliar chimpanzeesand introductions in a controlled setting. The process has beenused to form hundreds of different social groups without seriousinjuries.... Most of our 35 males live in one of seven all-malegroups. While there is considerable potential for male-male aggressionamong adults, we have found males to be quite social and, in mostcases, able to live compatibly with other males. We developedthis social group strategy to provide males with increased opportunitiesto form strong social bonds with other males as is common amongwild chimpanzees and as a management technique to prevent pregnancy."The authors share extremely valuable first-hand experiences andoutline practical recommendations for the careful establishmentof new social units without undue risk of stress, distress andinjury.

Hartner MK, Hall J, Penderhest J,Clark LP 2001. Group-housing subadult male cynomolgus macaquesin a pharmaceutical environment. Lab Animal 30(8), 53-57
A carefully designed, successful group-formation protocol offive 3.5 + years old previously single-caged malelong-tailed macaques is described in detail.

McDonald S 1994. The Detroit Zoo ChimpanzeesPan troglodytes: exhibit design, group composition andthe process of group formation. International Zoo Yearbook33, 235-247
"All adults were introduced to each other first throughmesh and then physically. Before all physical introductions, thechimpanzees involved were fed double their normal morning rationsand then fed a single ration ten minutes prior to the start ofthe introduction. Play items were scattered throughout the dayroom. These strategies were employed in an attempt to reduce tensionfurther and provide distractions. Following the dyadic/triadicintroductions, an adult female group was formed and the [two]males were added later. All 11 Chimpanzees were successfully integratedinto one social group. The mesh and physical introductions onlyproduced five visible wounds, all minor and not requiring veterinaryattention."

McNary JK 1992. Integration of chimpanzees(Pan troglodytes) in captivity. In The Care and Managementof Chimpanzees (Pan troglodytes) in captive environmentsFulk R, Garland C (eds), 88-100. North Carolina Zool Society
Clear recommendation of how to introduce new chimpanzees toa core group and how to form a new group.

Pazol K, McDonald S, Baker K, SmutsB 1998. Placing hand-reared chimpanzees (Pan troglodytes)into adult social groups: A technique for facilitating group integration. Laboratory Primate Newsletter 37(3),11-13
"This study suggests that prior housing with sociallyexperienced adult females can facilitate the integration of hand-rearedinfants into naturalistic social groups."

Gorillas (Gorilla spp.)

Catlow G 1990. Introducing Killa-Killa.Gorilla Gazette 4(1), 8-10
The successful introduction procedure of an adult female toa group of two adult females and one adult male gorilla is describedin detail.

Chatfield JJ 1990. Notes on the introductionof an aggressive male gorilla at the Los Angeles Zoo. Proceedings:Columbus Zoo Gorilla Workshop, 2-4
The integration of a conspicuously aggressive adult gorillainto an established group of young animals plus one adult femaleis described. "The introduction took close to two years andlots of patience and effort. The end result proved that is wasall worthwhile and certainly the risks [bite wound inflicted onthe adult female requiring surgery] were justified." Themale was tolerant toward the young animals.

Downman M 1998. Theformation of a bachelor group of gorillas at Loro Parque.Int Zoo News 45, 208-211
Successful bachelor group formation protocol is described.

Enciso AE, Calcagno JM, Gold KC 1999.Social interactions between captive adult male and infant lowlandgorillas: Implications regarding kin selection and zoo management.Zoo Biology 18, 53-62
"Infants may be introduced into non-natal groups withoutbeing attacked or physically harmed by dominant males, but theirsubsequent relationships with these males may lack the close,affiliative interactions that enhance infant social development."

Jendry C 1989. Gorilla introductions.Gorilla Gazette 3(3), 5-6
A well-tested introduction protocol is outlined step-by-step.

Johnstone-Scott R 1992. Theintegration of Julia. International Zoo News 39(6),18-26
Successful integration procedure of an adult female gorillainto an established breeding group is described.

McCann CM, Rothman JM 1999. Changesin nearest-neighbor association in a captive group of WesternLowland gorillas after the introduction of five hand-reared infants.Zoo Biology 18, 261-278
The integration of five hand-reared infants into a group of5 females and 1 male was successful and without incident. "Findingslend strong support to the importance of peer groups [security/companionship]and the presence of a silverback male for facilitating the integrationof hand-reared infants into established groups."

Meder A 1985. Integration of hand-rearedgorilla infants in a group. Zoo Biology 4, 1-12
Zoo-born gorilla infants "could best be introduced intoa group when about 1.5 to 2 years old; when younger or older,social integration becomes more difficult. An introduction toadult females in a small cage until strong social relations areformed leads to a smoother social integration in the whole groupafterward and takes less time than socializing the infants tojuveniles. Allowing the infants to explore the group's main enclosurealone and before they join the group permanently leads to betterspacial orientation for them and helps to lessen their uneasinessin the new social situation. Providing the infants with a shelterwithin the group's enclosure, which gives them access to the groupbut is inaccessible to the adults, reduces tension and thus aggressiontoward them."

Winslow S, Ogden J. J., Maple TL 1990.Socialization of an adult male lowland gorilla (Gorilla gorillagorilla). Proceedings: Columbus Zoo Gorilla Workshop, 195-204
Successful group formation process of an adult male, an adultfemale, and a juvenile female is outlined.

Macaques (Macaca spp.)

Asvestas C, Reininger M 1999. Forming a bachelor group of long-tailed macaques(Macaca fascicularis).Laboratory Primate Newsletter 38(3), 14
The careful establishment of a compatible group of 24 malelong-tailed macaques is described. "The worst injuries werea split lip and a bite to the leg, both of which healed up quickly."

Bernstein IS, Gordon TP 1977. Behavioralresearch in breeding colonies of Old World monkeys. LaboratoryAnimal Science 27, 532-540
"In our experience, the simultaneous release of all animalshas proven to produce the fewest injuries and the most rapid socialintegration. The addition of individuals to such a colony resultsin the mobbing of adults, often with severe consequences. Oncea group is established, one should avoid adding animals no matterhow desirable this might appear. If new groups are to be established,it is far less damaging to the stability of the colony to dividea group along matrilineal lines than to remove any particularage class."

Clarke AS, Czekala NM, Lindburg DG1995. Behavioral and adrenocortical responses of male cynomolgusand lion-tailed macaques to social stimulation and group formation.Primates 36, 41-46
"Males were exposed to a mirror, then visually exposedto conspecific neighbors in all pairwise combinations, and thenformed into conspecific groups [of 3 animals each]. Followinggroup formation [urinary] cortisol values showed a decreasingtrend in the cynomolgus, but not in the lion-tails. The cynomolgusrapidly adapted to group living and relations between them wereprimarily affiliative. In contrast, no affiliative behavior wasever observed in the lion-tail group, which appeared to be highlystressed by group living and was eventually disbanded."

Clarke MR, Blanchard JL 1994. All-malesocial group formation: Does cutting canine teeth promote socialintegration? Laboratory Primate Newsletter 33(2), 5-8
Groups of rhesus males were formed by releasing future group membersin same enclosure. Within the first five months after group formationone of 26 animals died and two were killed due to trauma resultingfrom fighting.

Good GP, Sassenrath EN 1980. Persistentadrenocortical activation in female rhesus monkeys after new breedinggroup formation. Journal of Medical Primatology 9, 325-334
"Persistent elevated adrenocortical responsiveness toACTH has been demonstrated in female rhesus monkeys as long as13 weeks after relocation into new single male breeding groups."

Gust DA, Gordon TP, Wilson ME, BrodieAR, Ahmed-Ansari A, McClure HM 1991. Formation of a new socialgroup of unfamiliar female rhesus monkeys affects the immune andpituitary adrenocortical systems. Brain, Behavior, and Immunity5, 296-307
Eight females were introduced into an enclosure. "Dominancerank was established within 48 h by noncontact threats and chasesand was unchanged throughout the study. Only two minor woundswere recorded." The animals showed physiological stress responsesduring the first 9 weeks after group formation.

Jensen GD, Blanton FL, Gribble DH1980. Older monkeys' (Macaca radiata) response to new groupformation: Behavior, reproduction and mortality. ExperimentalGerontology 15, 399-406
"A group of younger bonnets (5 males and 33 females under10 yrs of age) suffered 11% mortality in the first three monthsafter new group formation, the death all due to trauma."

Kessler MJ, London WT, Rawlins RG,Gonzales J, Martines HS, Sanches J 1985. Management of a harembreeding colony of rhesus monkeys to reduce trauma-related morbidityand mortality. Journal of Medical Primatology 13, 91-98
Mortality rates per year were reduced from 13.4% to 3.5% "whenmonkeys were maintained in permanent harems to which returningfemales were reintroduced compared to new social groups formedfrom aggregates of unfamiliar animals."

Line SW, Morgan KN, Roberts JA, MarkowitzH 1990. Preliminarycomments on resocialization of aged macaques. LaboratoryPrimate Newsletter 29(1), 8-12
Each rhesus monkey [6 males and 7 females] was introduced togroup members in a series of brief pair tests. The incidence ofserious injury was 62% including one fatality.

Meshik VA 1994. Groupformation in adult Japanese macaques. International ZooNews 41(3), 5-9
"Starting with submissive animals, individuals from thefirst group [2 females and 1 male] were introduced step by stepto the second [resident] group [3 females and 1 male]. A new groupwas successfully formed without severe fighting. There were practicallyno aggressive acts."

Reinhardt V 1991. Groupformation of previously single-caged adult rhesus macaques forthe purpose of environmental enrichment. Journal of ExperimentalAnimal Science 34, 110-115
"Future group members [of the same sex, 6 females and6 males] were given ample opportunity to physically interact witheach other on a one-to-one basis and were considered ready forgroup formation only when they had demonstrated compatibilityand clear-cut dominance-subordination relationships." Persistentaggressive interactions made it imperative to disband both groupsshortly after group formation.

Rhine RJ, Cox RL 1989 How not to enlargea stable group of stumptailed macaques (Macaca arctoides).In Housing, Care and Psychological Well-being of Captive andLaboratory Primates Segal EF (ed), 255-269. Noyes Publications,Park Ridge
"The best advice, based on our experience with establishedgroups of stumptails, is to combine groups, or introduce adultanimals, only as a very last resort, and then with great careand assiduous monitoring."

Schapiro SJ, Lee-Parritz DE, TaylorLL, Watson L, Bloomsmith MA, Petto AJ 1994. Behavioral managementof specific pathogen-free rhesus macaques: Group formation, reproduction,and parental competence. Laboratory Animal Science 44,229-234
Initial group formation was amicable. "However, duringthe first breeding season, there were outbreaks of severe aggression,leading to the permanent removal of three [of seven] males and17 [of 50] females."

Stahl D, Herrmann F, Kaumanns W 2001.Group formation of a captive all-male groupof lion-tailed macaques (Macaca silenus). Primate Report 59, 93-108
"The [6 adult (5 years and older)] individuals were broughttogether simultaneously. .. .. The individuals showed no fightsor other serious aggression during the first encounter on thefirst day. Aggression rates were high only during the first hourafter introduction of the animals. Afterwards, the aggressionlevel remained within a similar low level during the whole observationperiod. .. The development of the social relationships withinthe first days suggests that there is a certain degree of socialcompatibility between male lion-tailed macaques.. .. After fourdays, the zoo decided to remove Heiner from the group. The animaldid not show conspicious aggressive behaviour but it was thoughtthat he was not compatible with the other animals in the group.Four weeks after the group establishment Nepomuk died becauseof a chronic, subacute gastritis. Two months later, another monkey,Smokie, died because of a bacterial infection. To prevent furtherrisks the group was disbanded at the end of December 1995."

Westergaard GC, Izard MK, Drake JD,Suomi SJ, Higley JD 1999. Rhesus macaque (Macaca mulatta)group formation and housing: Wounding and reproduction in a specificpathogen free (SPF) colony. American Journal of Primatology49, 339-347
Initially small groups were formed consisting of one male andup to eight females. Subsequently larger groups [about 3 malesand 21 females] were formed by releasing group members simultaneouslyor incrementally" When forming rhesus macaque breeding groupsfrom partial groups and strangers, a staged group formation methodleads to lower traumatic wounding rates than does a rapid formationmethod in which all individuals are put together at once. Whenforming new rhesus macaque breeding groups, divided corrals thatprovide for social and visual separation of individuals lead tolower rates of traumatic wounding than do undivided corrals."

Orangutans (Pongo pygmaeus)

Hamburger L 1988. Introduction oftwo young orangutans, Pongo pygmaeus, into an establishedfamily group. International Zoo Yearbook 27, 273-278
Successful re-introduction of two hand reared young orangutansinto a family group is described.

Watts E 1997. Introductions. In OrangutanSpecies Survival Plan Husbandry Manual Sodaro C (ed), 69-84.Atlanta Orangutan SSP [Species Survival Plan], Atlanta
Group integration and re-introduction techniques are describedand very valuable recommendations made.

Squirrel monkeys (Saimirispp.)

King JE, Norwood VR 1989. Free-environmentrooms as alternative housing for squirrel monkeys. 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 conventionalcolony rooms and the monkeys [11 females and 5 males] were simplyreleased into the rooms. Immediately following the establishmentof these two free-environment rooms, a few monkeys incurred sprainsand broken teeth, probably resulting from falls. ... Two deathsresulted from attacks by other monkeys."

Mendoza SP 1991. Sociophysiology ofwell-being in nonhuman primates. Laboratory Animal Science41, 344-349
The formation of same-sex groups of squirrel monkeys is rarelyaccompanied by injurious aggression. Once unisexual groups havestabilized, formation of larger heterosexual groups generallyproceeds smoothly.

Vermeer J 1997. Theformation of a captive squirrel monkey group. InternationalZoo News 44, 146-149
"It is important that all females of a new [heterosexual]group are related to each other, that is, that they come fromthe same natal group. The introduction of unfamiliar females toa small group with several females can result in much aggressionwith severe injury." The minimum number of breeding femalesin a group should be five to seven. A maximum of two adult malesshould be added to these females. Groups of up to ten males canbe formed without many problems.

Williams LE, Abee CR 1988. Aggressionwith mixed age-sex groups of Bolivian squirrel monkeys followingsingle animal introductions and new group formations. Zoo Biology7, 139-145
"When introducing new animals to an established group,the new animals should be unfamiliar with one another so as notto form competing 'teams'. Additions to groups should includeenough animals so that aggression from the resident group willbe diffused, not concentrated on one or two animals." Newgroups should be followed for a number of hours, even after aninitial decline in total agonistic interactions.

Vervet monkeys (Cercopithecusaethiops)

Else JG 1985. Captive propagationof vervet monkeys (Cercopithecus aethiops) in harems. LaboratoryAnimal Science 35, 373-375
Animals were placed randomly in ten single-male harem groupswith 5-10 females per enclosure. This "resulted in considerablefighting among the females. Each group was gradually reduced overa one year period to 2-4 females with their young. Three adultfemales died during the [three year] study. All had been underfairly continual harassment."

(2,2,a) Pair-housing:Practical Issues, Time Budget

Basile BM, Hampton RR, Chaudhry AM,Murray EA 2007. Presence of a privacy divider increases proximityin pair-housed rhesus monkeys. Animal Welfare 16(1), 37-39
"We observed twenty-five pairs of rhesus macaques (Macacamulatta) both with and without the presence of a privacy divider.Monkeys spent significantly more time in the same half of thepair-cage when the divider was in place. Subjects were fifty adultrhesus macaque monkeys aged between 5 and 13 years, housed insocially compatible pairs consisting of 18 male/male pairs, 2female/female pairs, and 5 male/female pairs. We conclude thatthe increase in proximity associated with the presence of theprivacy dividers reflects an increase in social tolerance and/orattraction. A privacy divider may provide a safe haven and givemonkeys the ability to diffuse hostile situations before theyescalate."

Baker K, Bloomsmith M, Schoof V, NeuK, Maloney M, Griffis C, Marinez M, Clay A 2005. Compairing pair-housingoptions for caged rhesus macaques (Macaca mulatta). AmericanJournal of Primatology 66(Supplement), 180 (Abstract)
"Baseline behavioral data were collected on 20 singly-housedadult rhesus macaques, 6 males and 14 females, all mother reared.Isosexual pairs were then formed, and pairs were housed in threeform of pair caging balanced for order (6-8 weeks per phase):FC (full contact: sharing adjacent cages), PC (protected contact:access through perforated panels), and IC (intermittent contact:full pairings separated several days/week)." While all formsof pair housing increased affiliative behavior, levels were lowerin the protected contact than full contact or intermittent contacthousing condition. Levels of inactivity and anxiety-related behaviorswere higher in the protected than in the full contact or intermittentcontact condition, and full contact reduced anxiety-related behaviorsfrom baseline. Full contact and intermittent contact decreasedinactivity and increased aggression which occurred at higher levelin the intermittent than in the partial contact housing condition.Abnormal behavior was affected only in females, with a decreasefrom baseline only in the intermittent, and higher levels in thepartial than in the full contact condition. "Results suggestthat periodic separation may not detract from the benefits ofpair housing for rhesus macaques, but protected contact housingmay, balanced only by decreased aggression."

*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 ResearchLabs - Chapter5.1. Pair Formation and Pair-Housing of Monkeys. Washington,DC: Animal Welfare Institute
"The PI who does research with our pair-housed rhesusinsists that cage companions be separated during the night andon weekends, so that they cannot fight and injure each other whilenobody is around. I would love to keep the animals together alsoduring the night, but cannot argue with the PI because I reallydon't know if that would jeopardize the safety of the animals.
In our facility, compatible companions are allowed to remain togetheralso during the night, on weekends and holidays. This appliesfor both female and male pairs, as well as for all animals whohave head cap implants. It has never happened that we found pairedanimals injured or bruised when entering their room in the earlymorning. I think there is no special risk when pairs spend thenight together without being supervised.
We also keep our male and female rhesus pairs together 24/7 andencounter no problems related to aggression during the night.
At our facility, after pairs have been established, they are housedtogether uninterruptedly. This includes male and female isosexualpairs, and each species housed here, including rhesus, pigtails,sooty mangabeys, squirrel monkeys, chimps, and cynos. We havenot noticed that paired companions fight during the night, onweekends and holidays when nobody is around."

*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 ResearchLabs - Chapter5.3.1. Post-Operative Care. Washington, DC: Animal WelfareInstitute
"It is my experience with rhesus macaques that it is advisableto pair-house an animal after surgery as soon as possible withhis or her compatible companion. We do this especially with pairs,after one of them had cranial implant surgery. It is the investigator'sand my own impression that the animals recover better from thesurgery stress when their familiar companion is with them thanwhen they are alone.
Close to 95 percent of our cyno population is pair-housed. Theanimals are subjected to a lot of orthopedic procedures. Therehave never been problems with the re-pairing of the animals aftersurgery. We partition the pairs cage with a transparent panel,which we remove after the treated companion has fully recoveredfrom anesthetic effects (usually 24 hours). It has never happenedthat animals who had no surgery showed any negative behavioralreactions toward their 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 ResearchLabs - Chapter8.9. Pair-Housed Monkeys with Head Cap Implants. Washington,DC: Animal Welfare Institute
"Our university tries to pair all rhesus macaques regardlessof cranial implants. Normally the pairs are established beforethey have undergone surgery for head caps, but we have successfullypaired primates after surgery as well. Over a period of ten years,we have had no incidents of damage to the implants. We have moreproblems, with coils of head caps breaking, in single-housed thanin pair-housed rhesus. The head caps of pair-housed animals arecleaner as they groom each other than those of individually cagedanimals.
We have ten pair-housed male rhesus and long-tailed macaques withhead caps. The animals were 3 to 6 years old at the time of pairformation. They are presently approximately 10 years old. Someof them had head caps before they were paired, others got themafterwards. It didn't seem to matter. In my experience, pair-housingdoes not create a risk factor when the animals 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 cagesize and pair housing on the behavior of captive chimpanzees.American Journal of Primatology 27, 20
Paired subjects spent approximately 11% of the observationtime in socially directed behaviors.

Coe CL, Rosenblum LA 1984 Male dominancein the bonnet macaque. In Social Cohesion. Essays Toward aSociophysiological Perspective Barchas PR, Mendoza SP (eds),31-64. Greenwood Press, Westport
"During the first week [after formation of 5 male/malepairs], the males spent a mean 29 percent of the observation timewithin arm's reach, engaging in mutual grooming or passive bodycontact."

Coe CL, Franklin D, Smith ER, LevineS 1982. Hormonal responses accompanying fear and agitation inthe squirrel monkey. Physiology and Behavior 29, 1051-1057
Dominant and subordinate partners of male pairs did not differin their plasma cortisol levels.

Crockett CM 1998. Psychological well-beingof captive nonhuman primates. In Second Nature - EnvironmentalEnrichment for Captive Animals Shepherdson DH, Mellen JD,Hutchins M (eds), 129-152. Smithsonian Institution Press, Washington
"Adult female long-tailed macaques benefit from socialenrichment through pairing with other females. Adult males alsohave social needs, although they are more likely to express themtoward females. Many males ignore or behave aggressively towardother males, although some male pairs are highly compatible. Housinglongtailed macaque males in paired caging with widely spaced grooming-contactbars prevents aggressive pursuits and increases the success rateof male pairing."

Eaton GG, Kelley ST, Axthelm MK, Iliff-SizemoreSA, Shiigi SM 1994. Psychological well-being in paired adult femalerhesus (Macaca mulatta). American Journal of Primatology33, 89-99
Paired females spend in close proximity approximately 80% ofthe time during the night, and 40% of the time during the day.They engage in social interactions approximately 17% of the time.Agonistic behaviors are very infrequent. "Health measures,body weight gains, reproduction and immune responses do not differbetween dominant, subordinate, and single-housed females. Pairedfemales spend less time engaged in abnormal behavior than single-housedfemales."

Gonzalez CA, Coe CL, Levine S 1982.Cortisol responses under different housing conditions in femalesquirrel monkeys. Psychoneuroendocrinology 7, 209-216
Dominant and subordinate partners of female pairs did not differin their plasma cortisol levels.

Gwinn LA 1996. A method for usinga pole housing apparatus to establish compatible pairs among squirrelmonkeys. Contemporary Topics in Laboratory Animal Science35(4), 61
"Pair housing the animals has not interfered with research.During nine treatments with an identical test compound, singlyhoused animals lost significantly more weight on average thandid pair housed animals."

Hotchkiss CE, Paule MG 2003. Effectof pair housing on operant behavior task performance by rhesusmonkeys. Contemporary Topics in Laboratory Animal Science42(4), 38-40
"In conclusion, pair-housing monkeys is feasible for studiesinvolving operant behavior testing as a model for a variety ofcomplex brain functions. However, housing condition may affectsome test parameters, and this effect must be taken into considerationduring experimental design."

Jackson MJ 2001. Environmental enrichmentand husbandry of the MPTP-treated common marmoset. Animal Technology(2

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