Bibliography on Refinement and Environmental Enrichment for Primates. Enrichment 1-3

Environmental Enrichment

(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 Curiosity Behavior (watching videos; watching out of the window)
(8) Safety Concerns

Regulations and Guidelines

Ethical Considerations




(1) Definition

Environmental enrichment provides more species-adequate living and handling conditions thereby buffering stress and distress responses to captivity.Environmental enrichment is the provision of stimuli which promote the expression of species-appropriate behavioral and mental activities in an understimulating artificial environment.

United States Department of Agriculture 1991. Title 9, 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 must be enriched by providing means of expressing noninjurious species-typical activities. .. Examples of environmental enrichment include providing perches, swings, mirrors, and other increased cage complexities; providing objects to manipulate; varied food items; using foraging or task-oriented feeding methods; and providing interaction with the care giver or other familiar and knowledgeable person consistent with personnel safety precautions."

(2) Promoting Social Behavior

Canadian Council on Animal Care, Olfert ED, Cross BM, McWilliam AA 1993. Guide to the Care and Use of Experimental Animals, Volume 1, 2nd Edition. Canadian Council on Animal Care, Ottawa
"The social needs of animals used in research, teaching, or testing, should be given equal consideration with environmental factors such as lighting, heating, ventilations and containment (caging). Particularly in the case of singly housed animals, daily observation provides an alternative from of social contact for the animal and commonly facilitates handling in that the animal becomes accustomed to the human presence. .. 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 social contact with others of their own kind. ... In the interest of well-being, a social environment is desired for each animal which will allow basic social contacts and positive social relationships. Social behaviour assists animals to cope with circumstances of confinement."

European Commission 2002. The Welfare of Non-human Primates - Report of the Scientific Committe on Animal Health and Animal Welfare. European Commission, Strasbourg, France
http://europa.eu.int/comm/food/fs/sc/scah/out83_en.pdf
"Primates should not be housed singly unless fully justified by health considerations (for the animal and human handler) or research procedures, as advised following an ethical review process. If primates have to be singly housed, the animals should have visual, 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 Animals Used for Experimental and Other Scientific Purposes, Annex II Guidelines for Accommodation and Care of Animals. Official Journal of the European Communities L358 , 7-28
European guidelines for housing and handling of laboratory animals. "The performance of an animal during an experiment depends very much on its confidence in man, something which has to be developed. ... It is therefore recommended that frequent contact should 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. The staff should be sympathetic, gentle and firm when associating with the animals."

International Primatological Society 1993. IPS International guidelines for the acquisition, care and breeding of nonhuman primates, Codes of Practice 1-3. Primate Report 35, 3-29
" A compatible conspecific probably provides more appropriate stimulation to a captive primate than any other potential environmental enrichment factor. ... Monkeys should, unless there are compelling reasons for not doing so, be housed socially. ... Young monkey should not normally be separated from its mother at an early age (i.e., at 3-6 months) but should remain in contact for one year to 18 months, in most species. There is unlikely 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 must be offset against the resulting behavioural abnormalities of the offspring."

National Research Council 1996. Guide for the Care and Use of Laboratory Animals, 7th Edition. National Academy Press, Washington
"Animals should be housed with the goal of maximizing species-specific behaviors and minimizing stress-induced behaviors. For social species, this normally requires housing in compatible pairs or groups."

National Research Council 1998. The Psychological Well-Being of Nonhuman Primates. National Academy Press, Washington
"Social interactions are considered to be one of the most important factors influencing the psychological well-being of most nonhuman primates. ... The common practice of housing rhesus monkeys 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 for single housing should be documented by investigators and approved by the IACUC. ... The animal 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(No. 32), 6426-6505
The environmental enhancement plan "must include specific provisions to address the social needs of nonhuman primates of species known to exist in social groups in nature. ... Examples of environmental enrichment include ... providing interaction with the care giver or other familiar and knowledgeable person consistent with personnel safety precautions."

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

Alford PL, Bloomsmith MA, Keeling ME, Beck TF 1995. Wounding aggression during the formation 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, socially experienced males than in groups composed of younger socially inexperienced males, many of whom also had extensive visual exposure to one another before grouping."

Baker KC, Seres M, Aureli F, de Waal FBM 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 adult males, 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-housed chimpanzees incurred the highest level 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 an effective means for reducing injuries. The management of wounding in chimpanzee colonies is influenced more by the sex and rearing composition of a colony."

Bellinger LL, Hill EG, Wiggs RB 1992. Inexpensive modifications to nonhuman primate cages that allow social grouping. Contemporary Topics in Laboratory Animal Science 31(3), 10-12
"These two design modifications [PVC tunnels and stainless steel tunnels connecting two adjacent cages] allow us to inexpensively modify existing caging to meet the USDA regulations of social grouping."

Bernstein IS 1989. Breeding colonies and psychological well-being. American Journal of Primatology 19(Supplement 1), 31-36
Valuable 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 1), 93-99
"These observations suggest that captive adult male chimpanzees have the potential to develop affiliative relationships with immature conspecifics. Housing adult males in groups along with infants 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 and violent injuries among behaviorally inhibited rhesus macaques. Health Psychology 17, 285-289
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 Proceedings of the Third International Conference on Environmental Enrichment Hare VJ, Worley E (eds), 209-217. The Shape of Enrichment, San Diego
"Enrichment often involves manipulation of animals' lives. However, non-interference in their social lives is an important form of environmental enrichment for chimpanzees." Rather than locking the chimpanzees "into their indoor cages every evening, an average of 17 hours a day" the animals were given "continuous access to their whole area and each other 24 hours a day, except for routine cleaning. ... Almost from the beginning [1991] the group changed. There appeared to be a calming effect with the group actually being unified. The males became more tolerant towards one another, and started to socialise as a unit. ... Far more normal behaviours are present and the afternoon tension for both animal and keeper has ceased."

Caws C, Aureli F 2001. Coping with short-tem space restriction in chimpanzees. Primate Eye 74, 9
"During the indoor period the chimpanzees showed no increase in aggression, grooming, and submissive greeting, nor changed their proximity to adult males. However, the percentage of aggressive events that involved more than 2 individuals was significantly lower during the indoor period. In addition, 36 dyads were identified as "highly aggressive" during the control period; aggression was reduced in these dyads during the indoor period. These results confirm previous evidence that chimpanzees do not increase aggression during space restriction. Furthermore, they seem to inhibit aggression by not joining ongoing conflicts and by selectively decreasing the targeting of common `victims'."

Dazey J, Kuyk K, Oswald M, Marenson J, Erwin J 1977. Effects of group composition on agonistic behavior of captive pigtailed macaques (Macaca nemestrina). American Journal of Physical Anthropology 46, 73-76
Females showed significantly less aggression in the presence of adult males [one male per group] 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
Crowding produced sharp increases in aggression, noticeable increase in tension and general activity. "Social disintegration [e.g., vicious aggression, social withdrawal accompanied by self-directed behaviors], 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 this group 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. In Captivity and Behavior Erwin J, Maple T, Mitchell G (eds), 139-171. Van Nostrand, New York
Providing a male-dominated group access to two rooms rather than one allowed some animals to be out of the dominant male's sight. Loss of the male's control over his group resulted in a dramatic 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 of a viable birth and increased gestation length and the need for clinical treatment of the dam, while increased group size decreased gestation length. Increased moves and group size may increase stress by continuously shuffling social relationships, keeping females from establishing social hierarchies, and reducing group stability. Low group stability may increase aggression by making females more likely to attack other females without knowing the opponent's social position or physical abilities."

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

Judge PG, de Waal BM, Paul KS, Gordon TP 1994. Removal of a trauma-inflicting alpha matriline from a group of rhesus macaques to control severe wounding. Laboratory Animal Science 44, 344-350
"Results identify an unusual outbreak of serious wounding by the alpha matriline of a large captive group [of rhesus macaques] and indicate that identification and removal of the animals responsible 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 hamadryas baboons (Papio hamadryas). American Journal of Primatology 54(Supplement 1), 68-69
Aggressive, submissive, affiliative and self-directed responses of the six adults - two males and four females - were recorded in their small indoor quarters versus large outdoor section of their enclosure. Agonistic behavior, and "scratching, an indicator of anxiety in primates, did not increase during crowding. .. Perhaps male hamadryas baboons exert such a controlling influence that conflict management among the other group members is unnecessary during 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 100 females per year] in a breeding colony of rhesus monkeys living in groups was an important management problem. It was found that the cause of the fighting was the social disruption resulting from a breeding protocol which required the 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 agonism in 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 of harem groups of 23 pig-tailed macaques] 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 and Aquarium Association (AZA) Regional Conference Proceedings, 323-325
"Installing an inexpensive electric net fencing system offered safe and innovative separation to two groups of monkeys in the field enclosure. Animals with incentive to transfer between areas successfully penetrated the electric net fence by leaping over it, or darting through the mesh openings 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. The socially 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 tension between 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 the St. Louis Zoological Park. American Zoo and Aquarium Association (AZA) Regional Conference Proceedings, 720-728
"Our experience suggests that a gorilla bachelor group is a viable and indeed a desirable alternative to solitary housing of 'emigrated' captive males."

Reinhardt V, Reinhardt A, Houser WD 1986. Hair pulling-and-eating in captive rhesus monkeys. Folia Primatologica 47, 158-164
It was concluded that hair pulling and eating is an aggressive behavioral 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 disturbance 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 carefully supervised removal of these individuals brought harmony back into the group."

Reinhardt V 1990. Catching Individual Rhesus Monkeys Living in Captive Groups (Videotape). Available on loan from Animal Care Audio-Visual Materials, WRPRC, 1220 Capitol Court, Madison, WI 53715
A simple capture-chute design is demonstrated. Using vocal commands, a single person swiftly catches all members of a trained rhesus breeding group one-by-one in a transport box without causing any disturbance.

Reinhardt V 1993. Nonspecific diarrhea in the alpha-male of a breeding troop: A case report. Laboratory Primate Newsletter 32(1), 4
"Bob's prompt recovery from intractable diarrhea upon being removed from his troop suggests that asserting his role as alpha-animal constituted a chronic social challenge that may have altered his resistance to facultative pathogens and/or autonomic neural tone, to produce diarrhea."

Rolland RM 1991. A prescription for psychological well-being. In Through the Looking Glass. Issues of Psychological Well-being in Captive Nonhuman Primates Novak 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 trauma sustained by macaques in group-housing situations."

White G, Hill W, Speigel G, Valentine B, Weigant J, Wallis J 2000. Conversion of canine runs to group social housing for juvenile baboons. AALAS 51st National Meeting Official Program, 126
"Our Division recently converted two rooms equipped with 10 stainless steel, elevated floor canine runs into rooms providing social housing for young baboons. The detachable walls were removed to create larger primary enclosures and tops were fitted with stainless steel panels to provide complete containment. ... Our group has trained the juvenile baboons [6 months to two years of age] to enter squeeze cages through guillotine openings available in the front door of the primary enclosures."

Wolfensohn S, Peters A 2005. Refinement of neuroscience procedures using non human primates. Animal Technology and Welfare 4, 49-50
It is demonstrated that long-tailed macaques with cranial implants can be group-housed without undue risk. "Contrary to initial expectations we have not found any increased incidence in infection due 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, Eley RM 1986. Enclosure design and reproductive success of baboons 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 placement with females. Eight animals were removed within the first month due to fight wounds and general incompatibility."

Wallis J, Hartley D 2001. Comparing two methods of forming large social groups of captive baboons (Papio spp.). American Journal of Primatology 54(Supplement 1), 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 pathology in Cebus apella. Laboratory Primate Newsletter 30(2), 9-12
No 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 males into a group of tufted capuchin monkeys (Cebus apella). American Journal of Primatology 42, 10
"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 settled quickly, the social integration of male capuchins was a gradual process."

Fragaszy D, Baer J, Adams-Curtis L 1994. Introduction and integration of strangers into captive groups 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 resident group's two-room cage, while the resident group remained in the other room. Following the acclimation 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 months following. Introductions of adult females can be carried out with acceptable risk to the newcomers provided that careful monitoring occurs, so that the onset of severe aggression instigated by resident females toward new females can be avoided [by temporarily dividing the group for a few days]; juveniles can be introduced with minimal risk, and adult males can be introduced 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), 36-39
Five 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.)

Bloomsmith MA, Lambeth SP 1996. Managing aggression in multi-male, multi-female chimpanzee groups. American Zoo and Aquarium Association (AZA) Regional Conference Proceedings, 449-452
"We found that wounding aggression was minimal during introductions of females to males or other females, and during male-male introductions of formerly single-caged adolescent and young adult males having long-term prior visual familiarity. Serious wounding occurred during male-male introductions, particularly when there were major discrepancies in their ages and social 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
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 groups were successful.

Fritz J, Howell S 2001. Captive chimpanzee social group formation. In Special Topics in Primatology Volume 2 - 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 requires appropriate facilities, a knowledgeable staff, planning, and careful observations." A well-tested socialization system is reviewed which "includes a gradual acclimation of unfamiliar chimpanzees and introductions in a controlled setting. The process has been used to form hundreds of different social groups without serious injuries.... Most of our 35 males live in one of seven all-male groups. While there is considerable potential for male-male aggression among adults, we have found males to be quite social and, in most cases, able to live compatibly with other males. We developed this social group strategy to provide males with increased opportunities to form strong social bonds with other males as is common among wild chimpanzees and as a management technique to prevent pregnancy." The authors share extremely valuable first-hand experiences and outline practical recommendations for the careful establishment of new social units without undue risk of stress, distress and injury.

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

McDonald S 1994. The Detroit Zoo Chimpanzees Pan troglodytes: exhibit design, group composition 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 all physical introductions, the chimpanzees involved were fed double their normal morning rations and then fed a single ration ten minutes prior to the start of the introduction. Play items were scattered throughout the day room. These strategies were employed in an attempt to reduce tension further and provide distractions. Following the dyadic/triadic introductions, an adult female group was formed and the [two] males were added later. All 11 Chimpanzees were successfully integrated into one social group. The mesh and physical introductions only produced five visible wounds, all minor and not requiring veterinary attention."

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

Pazol K, McDonald S, Baker K, Smuts B 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 socially experienced adult females can facilitate the integration of hand-reared infants 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 to a group of two adult females and one adult male gorilla is described in detail.

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

Downman M 1998. The formation 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 lowland gorillas: Implications regarding kin selection and zoo management. Zoo Biology 18, 53-62
"Infants may be introduced into non-natal groups without being attacked or physically harmed by 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), 5-6
A well-tested introduction protocol is outlined step-by-step.

Johnstone-Scott R 1992. The integration of Julia. International Zoo News 39(6), 18-26
Successful integration procedure 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 of Western Lowland gorillas after the introduction of five hand-reared infants. Zoo Biology 18, 261-278
The integration of five hand-reared infants into a group of 5 females and 1 male was successful and without incident. "Findings lend strong support to the importance of peer groups [security/companionship] and the presence of a silverback male for facilitating the integration of hand-reared infants into established groups."

Meder A 1985. Integration of hand-reared gorilla infants in a group. Zoo Biology 4, 1-12
Zoo-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 adult females in a small cage until strong social relations are formed leads to a smoother social integration in the whole group afterward and takes less time than socializing the infants to juveniles. Allowing the infants to explore the group's main enclosure alone and before they join the group permanently leads to better spacial orientation for them and helps to lessen their uneasiness in the new social situation. Providing the infants with a shelter within the group's enclosure, which gives them access to the group but is inaccessible to the adults, reduces tension and thus aggression toward them."

Winslow S, Ogden J. J., Maple TL 1990. Socialization of an adult male lowland gorilla (Gorilla gorilla gorilla). Proceedings: Columbus Zoo Gorilla Workshop , 195-204
Successful group formation process of an adult male, an adult female, 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 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
"In our experience, the simultaneous release of all animals has proven to produce the fewest injuries and the most rapid social integration. The addition of individuals to such a colony results in the mobbing of adults, often with severe consequences. Once a group is established, one should avoid adding animals no matter how desirable this might appear. If new groups are to be established, it is far less damaging to the stability of the colony to divide a group along matrilineal lines than to remove any particular age class."

Clarke AS, Czekala NM, Lindburg DG 1995. Behavioral and adrenocortical responses of male cynomolgus 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 pairwise combinations, and then formed into conspecific groups [of 3 animals each]. Following group formation [urinary] cortisol values showed a decreasing trend in the cynomolgus, but not in the lion-tails. The cynomolgus rapidly adapted to group living and relations between them were primarily 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."

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

Good GP, Sassenrath EN 1980. Persistent adrenocortical activation in female rhesus monkeys after new breeding group formation. Journal of Medical Primatology 9, 325-334
"Persistent elevated adrenocortical responsiveness to ACTH has been demonstrated in female rhesus 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. Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems. Brain, Behavior, and Immunity 5, 296-307
Eight females were introduced into an enclosure. "Dominance rank was established within 48 h by noncontact threats and chases and was unchanged throughout the study. Only two minor wounds were recorded." The animals showed physiological stress responses during the first 9 weeks after group formation.

Jensen GD, Blanton FL, Gribble DH 1980. Older monkeys' (Macaca radiata) response to new group 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. Management of a harem breeding colony of rhesus monkeys to reduce trauma-related morbidity and mortality. Journal of Medical Primatology 13, 91-98
Mortality rates per year were reduced from 13.4% to 3.5% "when monkeys were maintained in permanent harems to which returning females were reintroduced compared to new social groups formed from aggregates of unfamiliar animals."

Line SW, Morgan KN, Roberts JA, Markowitz H 1990. Preliminary comments on resocialization of aged macaques. Laboratory Primate Newsletter 29(1), 8-12
Each rhesus monkey [6 males and 7 females] was introduced to group members in a series of brief 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), 5-9
"Starting with submissive animals, individuals from the first group [2 females and 1 male] were introduced step by step to the second [resident] group [3 females and 1 male]. A new group was successfully formed without severe fighting. There were practically no aggressive acts."

Reinhardt V 1991. Group formation of previously single-caged adult rhesus macaques for the purpose of environmental enrichment. Journal of Experimental Animal Science 34, 110-115
"Future group members [of the same sex, 6 females and 6 males] were given ample opportunity to physically interact with each other on a one-to-one basis and were considered ready for group formation only when they had demonstrated compatibility and clear-cut dominance-subordination relationships." Persistent aggressive interactions made it imperative to disband both groups shortly after group formation.

Rhine RJ, Cox RL 1989 How not to enlarge a stable group of stumptailed macaques (Macaca arctoides). In Housing, Care and Psychological Well-being of Captive and Laboratory Primates Segal EF (ed), 255-269. Noyes Publications, Park Ridge
"The best advice, based on our experience with established groups of stumptails, 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. Behavioral management of specific pathogen-free rhesus macaques: Group formation, reproduction, and parental competence. Laboratory Animal Science 44, 229-234
Initial group formation was amicable. "However, during the first breeding season, there were outbreaks of 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 lion-tailed macaques (Macaca silenus). Primate Report 59, 93-108
"The [6 adult (5 years and older)] individuals were brought together simultaneously. .. .. The individuals showed no fights or other serious aggression during the first encounter on the first day. Aggression rates were high only during the first hour after introduction of the animals. Afterwards, the aggression level remained within a similar low level during the whole observation period. .. The development of the social relationships within the first days suggests that there is 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 conspicious aggressive behaviour but it was thought that he was not compatible with the other animals in the group. Four weeks after the group 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 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 specific pathogen free (SPF) colony. American Journal of Primatology 49, 339-347
Initially small groups were formed consisting of one male and up to eight females. Subsequently larger groups [about 3 males and 21 females] were formed by releasing group members simultaneously or incrementally" When forming rhesus macaque breeding groups from partial groups and strangers, a staged group formation method leads to lower traumatic wounding rates than does a rapid formation method in which all individuals are put together at once. When forming new rhesus macaque breeding groups, divided corrals that provide for social and visual separation 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 established family group. International Zoo Yearbook 27, 273-278
Successful re-introduction of two hand reared young orangutans into a family group is described.

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

Squirrel monkeys (Saimiri spp.)

King JE, Norwood VR 1989. Free-environment rooms as alternative housing for squirrel monkeys. In Housing, Care and Psychological Well-being of Captive and Laboratory Primates Segal 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 the establishment of these two free-environment rooms, a few monkeys incurred sprains and broken teeth, probably resulting from falls. ... Two deaths resulted from attacks by other monkeys."

Mendoza SP 1991. Sociophysiology of well-being in nonhuman primates. Laboratory Animal Science 41, 344-349
The formation of same-sex groups of squirrel monkeys is rarely accompanied by injurious aggression. Once unisexual groups have stabilized, formation of larger heterosexual groups generally proceeds smoothly.

Vermeer J 1997. The formation of a captive squirrel monkey group. International Zoo 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 from the same natal group. The introduction of unfamiliar females to a small group with several females can result in much aggression with severe injury." The minimum number of breeding females in a group should be five to seven. A maximum of two adult males should be added to these females. Groups of up to ten males can be formed without many problems.

Williams LE, Abee CR 1988. Aggression with mixed age-sex groups of Bolivian squirrel monkeys 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 unfamiliar with one another so as not to form competing 'teams'. Additions to groups should include enough animals so that aggression from the resident group will be diffused, not concentrated on one or two animals." New groups should be followed for a number of hours, even after an initial decline in total agonistic interactions.

Vervet monkeys (Cercopithecus aethiops)

Else JG 1985. Captive propagation of vervet monkeys (Cercopithecus aethiops) in harems. Laboratory Animal Science 35, 373-375
Animals were placed randomly in ten single-male harem groups with 5-10 females per enclosure. This "resulted in considerable fighting among the females. Each group was gradually reduced over a one year period to 2-4 females with their young. Three adult females died during the [three year] study. All had been under fairly 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 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 the presence of a privacy divider. Monkeys spent significantly more time in the same half of the pair-cage when the divider was in place. Subjects were fifty adult rhesus macaque monkeys aged between 5 and 13 years, housed in socially compatible pairs consisting of 18 male/male pairs, 2 female/female pairs, and 5 male/female pairs. We conclude that the increase in proximity associated with the presence of the privacy dividers reflects an increase in social tolerance and/or attraction. A privacy divider may provide a safe haven and give monkeys the ability to diffuse hostile situations before they escalate."

Baker 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). American Journal of Primatology 66(Supplement), 180 (Abstract)
"Baseline behavioral data were collected on 20 singly-housed adult rhesus macaques, 6 males and 14 females, all mother reared. Isosexual pairs were then formed, and pairs were housed in three form 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 forms of pair housing increased affiliative behavior, levels were lower in the protected contact than full contact or intermittent contact housing condition. Levels of inactivity and anxiety-related behaviors were higher in the protected than in the full contact or intermittent contact condition, and full contact reduced anxiety-related behaviors from baseline. Full contact and intermittent contact decreased inactivity and increased aggression which occurred at higher level in the intermittent than in the partial contact housing condition. Abnormal behavior was affected only in females, with a decrease from baseline only in the intermittent, and higher levels in the partial than in the full contact condition. "Results suggest that periodic separation may not detract from the benefits of pair housing for rhesus macaques, but protected contact housing may, balanced only by decreased aggression."

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 5.1. Pair Formation and Pair-Housing of Monkeys. Washington, DC: Animal Welfare Institute
"The PI who does research with our pair-housed rhesus insists that cage companions be separated during the night and on weekends, so that they cannot fight and injure each other while nobody is around. I would love to keep the animals together also during the night, but cannot argue with the PI because I really don't know if that would jeopardize the safety of the animals.
In our facility, compatible companions are allowed to remain together also during the night, on weekends and holidays. This applies for both female and male pairs, as well as for all animals who have head cap implants. It has never happened that we found paired animals injured or bruised when entering their room in the early morning. I think there is no special risk when pairs spend the night together without being supervised.
We also keep our male and female rhesus pairs together 24/7 and encounter no problems related to aggression during the night.
At our facility, after pairs have been established, they are housed together uninterruptedly. This includes male and female isosexual pairs, and each species housed here, including rhesus, pigtails, sooty mangabeys, squirrel monkeys, chimps, and cynos. We have not noticed that paired companions fight during the night, on weekends and holidays when nobody is around."


*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 5.3.1. Post-Operative Care. Washington, DC: Animal Welfare Institute
"It is my experience with rhesus macaques that it is advisable to pair-house an animal after surgery as soon as possible with his or her compatible companion. We do this especially with pairs, after one of them had cranial implant surgery. It is the investigator's and my own impression that the animals recover better from the surgery stress when their familiar companion is with them than when they are alone.
Close to 95 percent of our cyno population is pair-housed. The animals are subjected to a lot of orthopedic procedures. There have never been problems with the re-pairing of the animals after surgery. We partition the pairs cage with a transparent panel, which we remove after the treated companion has fully recovered from anesthetic effects (usually 24 hours). It has never happened that animals who had no surgery showed any negative behavioral reactions toward their temporarily probably weaker cage mates."

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, 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 Institute
"Our university tries to pair all rhesus macaques regardless of cranial implants. Normally the pairs are established before they have undergone surgery for head caps, but we have successfully paired primates after surgery as well. Over a period of ten years, we have had no incidents 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. The animals were 3 to 6 years old at the time of pair formation. They are presently approximately 10 years old. Some of them had head caps before they were paired, others got them afterwards. It didn't seem to matter. In my experience, pair-housing does not create a risk factor when the animals have head cap implants. In all the time I've been working with these monkeys, they've never 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
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 percent of the observation time within arm's reach, engaging in mutual grooming or passive body contact."

Coe CL, Franklin D, Smith ER, Levine S 1982. Hormonal responses accompanying fear and agitation in the squirrel monkey. Physiology and Behavior 29, 1051-1057
Dominant 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 Nature - Environmental Enrichment for Captive Animals Shepherdson DH, Mellen JD, Hutchins M (eds), 129-152. Smithsonian Institution Press, Washington
"Adult female long-tailed macaques benefit from social enrichment through pairing with other females. Adult males also have social needs, although they are more likely to express them toward females. Many males ignore or behave aggressively toward other males, although some male pairs are highly compatible. Housing longtailed macaque males in paired caging with widely spaced grooming-contact bars prevents aggressive pursuits and increases the success rate of male pairing."

Eaton GG, Kelley ST, Axthelm MK, Iliff-Sizemore SA, Shiigi SM 1994. Psychological well-being in paired adult female rhesus (Macaca mulatta). American Journal of Primatology 33, 89-99
Paired females spend in close proximity approximately 80% of the 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 differ between dominant, subordinate, and single-housed females. Paired females spend less time engaged in abnormal behavior than single-housed females."

Gonzalez CA, Coe CL, Levine S 1982. Cortisol responses under different housing conditions in female squirrel monkeys. Psychoneuroendocrinology 7, 209-216
Dominant 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 pairs among squirrel monkeys. Contemporary Topics in Laboratory Animal Science 35(4), 61
"Pair housing the animals has not interfered with research. During nine treatments with an identical test compound, singly housed animals lost significantly more weight on average than did pair housed animals."

Hotchkiss CE, Paule MG 2003. Effect of pair housing on operant behavior task performance by rhesus monkeys. Contemporary Topics in Laboratory Animal Science 42(4), 38-40
"In conclusion, pair-housing monkeys is feasible for studies involving operant behavior testing as a model for a variety of complex brain functions. However, housing condition may affect some test parameters, and this effect must be taken into consideration during experimental design."

Jackson MJ 2001. Environmental enrichment and husbandry of the MPTP-treated common marmoset. Animal Technology (21-28)
"One disadvantage of isosexual pairing that we have encountered is that temporary separation of the pair (e.g. for behavioural monitoring) can precipitate fighting on re-introduction. If this occurs we have found that a gradual re-association process, utilising adjacent cages to permit visual and audio contact, and supervised free running together, facilitates re-pairing."

McDonald KM, Ratajeski MA 2005. Pair-housing of monkeys on behavioral studies. AALAS [American Association for Laboratory Animal Science] 56th National Meeting Official Program , 133 (Abstract)
"After periods of separation, we did not observe the animals to act aggressively towards one other when re-paired, and injury to head holder implants was never observed."

Murray L, Hartner M, Clark LP 2002. Enhancing postsurgical recovery of pair-housed nonhuman primates (M. fascicularis). Contemporary Topics in Laboratory Animal Science 41(4), 112-113
"In many facilities, postsurgical protocol in the nonhuman primate requires individual housing for a period of 2-10 days. ... Our goal was to allow [15 adult females] same-day return of the postoperative [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 of these 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 be successfully employed, and it is a "best practice" when working with these laboratory animals."

Majolo B, Buchanan-Smith H 2001. Psychological wellbeing of common marmoset (Callithrix jacchus) females living in same-sex pairs. Primate Eye 74, 9-10
The behaviour of female pairs of common marmosets resembles that of females living in family groups suggesting that this method of housing does not compromise their welfare."

Reinhardt V, Cowley D, Eisele S, Vertein R, Houser WD 1988. Pairing compatible female rhesus monkeys for the purpose of cage enrichment has no negative impact on body weight. Laboratory Primate Newsletter 27(1), 13-15
"Keeping singly housed adult female rhesus monkeys in compatible pairs for the purpose of cage enrichment does not affect the animals' general health status as reflected in body weight."

Reinhardt V, Dodsworth R 1989. Facilitated Socialization of Previously Single Caged Adult Rhesus Macaques (videotape with accompanying text). Wisconsin Regional Primate Research Center, Madison
Thirty 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 combinations and research situations are shown: adult male/male, adult female/female, adult male/juvenile male, adult female/juvenile female; experiments requiring headcap implants, tethering, or in-home cage blood collection. Presenting for in-homecage injection. Paired companions interact with 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 every-changing, yet predictable stimulus, a compatible companion does not lose its boredom-reducing value over time."

Reinhardt V, Houser WD, Eisele S 1989. Pairing previously singly caged rhesus monkeys does not interfere with common research protocols. Laboratory Animal Science 39, 73-74
"Our experiences indicate that facilitated socialization of previously singly caged rhesus monkeys offers an inexpensive method of environmental enrichment that is practicable under common management situations and numerous research conditions."

Reinhardt V 1990. Time budget of caged rhesus monkeys exposed to a companion, a PVC perch and a piece of wood for an extended time. American Journal of Primatology 20, 51-56
After 1.5 years paired partners spent an average of 23.5% of the time interacting with the companion. Females were socially more active than males.

Reinhardt V, Cowley D, Scheffler J, Vertein R 1990. Living continuously with a compatible companion is not a distressing experience for rhesus monkeys. Laboratory Primate Newsletter 29(2), 16-17
Paired 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 their subordinate companions, indicating that neither dominant nor subordinate partners experienced social distress."

Reinhardt V 1991. Social enrichment for aged rhesus monkeys that have lived singly for many years. Animal Technology 43, 173-177
"There is widespread concern that aged rhesus monkeys who have been housed singly for a long time would do better living alone than sharing a cage with a companion. Ten female and five male rhesus monkeys, 22 to 33 years old and deprived of physical contact with any other conspecific for more than 10 years, were socialized with weaned infants or with each other using two standard methods of pairing. Pairs were compatible in every case throughout a one year follow-up period."

Reinhardt V, Pape R, Zweifel D 1991. Multifunctional cage for macaques housed in pairs or in small groups. American Ass for Lab Animal Science Bulletin [Contemp Topics in Laboratory Animal Science] 30(5), 14-15
Double-cage units were modified to provide optimal housing conditions for pair-housed macaques. Perch installation allows normal operation of the squeeze-back; a privacy panel offers optional visual seclusion.

Reinhardt V, Reinhardt A 1991. Impact of a privacy panel on the behavior of caged female rhesus monkeys living in pairs. Journal of Experimental Animal Science 34, 55-58
"Paired partners spent significantly more time in close proximity when the privacy panel was provided. At the same time, they were more engaged in affiliative interactions while the incidence of agonistic interactions tended to decrease."

Reinhardt V, Hurwitz S 1993. Evaluation of social enrichment for aged rhesus macaques. Animal Technology 44, 53-57
The 31-36 years old "subjects preferred to stay in close proximity with their companion even though this reduced their available cage space. They spent on average 21% of the time interacting with the companion. Sharing a cage with a compatible conspecific did not jeopardize the subjects' general health, as reflected in their body weight development."

Reinhardt V 1994. Social enrichment for previously single-caged stumptail macaques. Animal Technology 5, 37-41
Female pairs and male pairs engaged in non-injurious species-typical activities 25% and 17% of the time.

Reinhardt V 1994. Continuous pair-housing of caged Macaca mulatta: Risk evaluation. Laboratory Primate Newsletter 33(1), 1-4
"Pairs were compatible in 88% of cases during the follow-up period of 1 to 6.3 years. There were no indications that long-term compatibility of male pairs was less than that of female pairs."

Reinhardt V 1994. Pair-housing rather than single-housing for laboratory rhesus macaques. Journal of Medical Primatology 23, 426-431
First-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 female-infant pairs. The incidence of serious injury was 0.7% (2/272) during the first year after pair formation.

Reinhardt V 1996. Frequently asked questions about safe pair-housing of macaques. Animal Welfare Information Center (AWIC) Newsletter 7(1), 11
Nine frequently asked questions regarding safe pair-housing protocols for macaques are addressed.

Reinhardt V, Reinhardt V 2000. Meeting the "social space" requirements of pair-housed primates. Laboratory Primate Newsletter 39(1), 7
"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 animals should 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. Laboratory Primate Newsletter 41(3), 7-10
"The present paper summarizes the author's experiences transferring a colony of rhesus macaques (Macaca mulatta) from individual- to pair-caging. ... The implementation of pair-housing as standard caging at Wisconsin RPRC was not excessively expensive in terms of work time 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 pairs were formed involving 817 different animals, yet no indication was found that this rendered research data collected from them useless due to confounding variables such as stress or disease."

Roberts SJ, Platt ML 2005. Effects of isosexual pair-housing on biomedical implants and study participation 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 physical health of captive primates, and this factor has led to United States Department of Agriculture guidelines requiring facilities to address the social needs of primate species known to live socially in nature as long as doing so does not endanger the animals or interfere with research goals. Although pair-housing is the best way to provide social enrichment, many researchers and facilities are hesitant to implement it, particularly in biomedical research contexts where implanted devices or behavioral performance might be compromised. In order to study the effects of pair-housing on biomedical implants and study participation, we collected data from a group of isosexually pair-housed male macaques (adult and subadult) with 1) cranial and eye implants and 2) controlled access to water as means of motivating subjects to participate in psychophysical studies. Implants, study participation, and weight gain were not adversely affected by pair-housing. Our results support the use of pair-housing as social enrichment for macaques with biomedical implants and controlled access to water." Consistent directional dominance 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 was ascertained over a period of 0.8 - 3.3 years." One monkey, however, occasionally exhibited noninjurious self-biting when someone other than his usual handler took him out of his cage, and two other monkeys occasionally placed in their cages when agitated."

Schapiro SJ, Bloomsmith MA, Kessel AL, Shively CA 1993. Effects of enrichment and housing on 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 rhesus monkeys successively housed singly, in pairs, and in groups. Applied Animal Behaviour Science 48, 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 the presence of a social partner(s) led to more beneficial changes in behavior than did the provision of inanimate enhancements."

Sheehan J, Ziegelhofer T, Henn S, Miyamoto M, Vanterpool I 2005. A novel caging method for collecting telemetry data from pair-housed monkeys. AALAS [American Association for Laboratory Animal Science] 56th National Meeting Official Program , 117 (Abstract)
Caging method is described that allows telemetric measurements [ECG and blood pressure] of long-tailed macaques housed in pairs. "The first method consisted of modifying the current cages to add a wire mesh tunnel constructed above the two adjacent cages, with sliding doors on either end so the monkeys could be intermittently paired. The second method for improvement with these modified cages was to compare results if we permanently placed a telemetered and a non-telemetered pair of monkeys in the cages and collected data using the distributed receiver array which allows for two receivers to be configured to one animal." No differences were noted in the data collected nore were any artifacts created by application of the second uninterrupted pair-housing method.

Shively CA 2001. Psychological well-being of laboratory primates at Oregon Regional Primate Research Center. Web sit link in Willamette Week (Portland), March 21, 2001
"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 virus load. Animals on timed mating protocol do not need to be housed alone. Animals in protocols requiring food restriction can be pair housed and separated from cagemates for 8 hrs during the day when food is accessible. They can be socially housed the other 16 hrs/day. ... The IACUC should use its authority to decline approval of protocols that do not demonstrate a detailed defense of single caging."

Yanagihara Y, Matsubayashi K, Matsuzawa T 1994. Environmental enrichment in Japanese monkeys: 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 from each other in the different units during feeding time.

(2,2,b) Pair-housing: Pair formation

Baboons (Papio spp.)

Bourgeois SR, Brent L 2005. Modifying the behaviour of singly caged baboons: evaluating the effectiveness of four enrichment techniques. Animal Welfare 14, 71-81
Seven singly caged adolescent [mean age: 4.2 years] male baboons were studied. Pairs were formed by introducing sedated partners in the same cage. "Pairing was successful for all seven individuals, with no serious injuries or overt aggression observed."

Jerome CP, Szostak L 1987. Environmental enrichment for adult, female baboons (Papio anubis). Laboratory Animal Science 37, 508-509
"Each baboon was placed in a cage with another baboon for 3-4 hours, two or three times per week. The same pairs consistently visited each other in either animal's cage. No significant aggression 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
"Even though the silverback Colossus had not had an opportunity to interact with any other gorilla since infancy, his introduction to the adult female conspecific Muke was very successful." The careful pair formation procedure is described.

Macaques (Macaca spp.)

Abney 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 were socialized in different age combinations, consisting of adult/adult, adult/sub-adult, and adult/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 temprarily separated partners A discussion on the Laboratory Animal Refinement & Enrichment Forum. Laboratory Primate Newsletter 1, 11-12
"To sum up, it seems advisable to monitor the reintroduction of temporarily separated partners very carefully, and if possible, to allow the animals to first recognize each other before they are reunited as a pair. There is no good reason to believe that male cynos are less suitable for isosexual pair-housing than rhesus. If and how experimentally-induced pathophysiological processes affect the compatibility of pairs needs to be explored."

Byrum R, St. Claire M 1998. Pairing female Macaca nemestrina. Laboratory Primate Newsletter 37(4), 1
Twenty-four adult pig-tailed macaques were successfully transferred from single- to pair-housing arrangements following the establishment of rank relationships during a semi-contact familiarization 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
"As usually occurs when unfamiliar males first meet, agonisitc behaviors related to the establishment of dominance relations occurred at pair formation. The aggressive incidents were limited, usually involving threats and pursuit behavior. .. More typically, one animal submitted and indicated his subordinate status through communicative gestures. In the first week following pair formation, the occurrence of aggressive behavior subsided almost entirely."

Crockett CM, Bowers CL, Bowden DM, Sackett GP 1994. Sex differences in compatibility of pair-housed adult longtailed macaques. American Journal of Primatology 32, 73-94
Prefamiliarized partners were paired without ascertaining that they had established their dominance-subordination relationship. Newly formed pairs were separated for 17 hours and subsequently reintroduced daily during a study period of 23 days. Under these circumstances, no female pair but seven [47% of 15] male pairs were separated because of fighting and wounding.

Crockett CM, Lee GH, Thom JP, Bentson KL 2005. Does temperament similarity predict compatibility 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 introduction on adult male rhesus macaques. American Journal of Primatology 70, 1-9
Potential partners of four adult rhesus macaque pairs were first familiarized in cages in which partners were separated by a panel consisting of bars spaced 2 cm apart. The eight males were all implanted with biotelemetry devices for remote heart rate monitoring. After 24 hours, as neither persistent aggression nor wounding was observed, each pre-familiarized pair was introduced into full contact by removing the barred panel. All four introductions were successful and subjects showed no physiological (fecal cortisol concentration and heart rate) or behavioral signs (pathological behavior) of stress, or psychological indices of distress (depressive/anxiety-related behavior) not only during the introduction process but also over a follow-up period of 18 months. No overt aggression was displayed at all during the first two hours following pair formation. Aggressive interactions were minimal thereafter. Only one bite laceration was incurred 14 weeks after pair formation. The partners of this pair were maintained in the home cage with the barred panel to allow wound healing; they were subsequently placed again into full contact with no further complications. "The results of this study may be of practical use for designing and monitoring social introductions and suggest that managers should not dismiss the feasibility of successful pairing of adult male rhesus macaques."

Eaton GG, Kelley ST, Axthelm MK, Iliff-Sizemore SA, Shiigi SM 1994. Psychological well-being in paired adult female rhesus (Macaca mulatta). American Journal of Primatology 33, 89-99
Partners were paired after a noncontact familiarization period. Pairs were compatible in 86% of 21 cases.

Line SW, Morgan KN, Markowitz H, Roberts J, Riddell M 1990. Behavioral responses of female long-tailed macaques (Macaca fascicularis) to pair formation. Laboratory Primate Newsletter 29(4), 1-5
Potential partners were familiarized in a noncontact situation prior to pairing. Five of six pairs tested were compatible during a five to six months study period.

McLean M, Morris J, Watson E, Gavetti D, Marshall S 2006. Retrospective evaluation of pair-housing juvenile and adult cynomolgus macaques in a pharmaceutical environment. AALAS [American Association for Laboratory Animal Science] 57th National Meeting Official Program , 148 (Abstract)
"Our experience and data suggest that pair formation in juvenile and adult cynomolgus male and female macaques has been successful and as allowed us to provide social housing in a pharmaceutical environment."

McMillan J, Maier A, Tully L, Coleman K 2003. The effects of temperament on pairing success in female rhesus macaques. American Journal of Primatology 60(Supplement), 95
http://www.asp.org/asp2003/abstractDisplay.cfm?abstractID=576&confEventID=554
“We assessed temperament in these monkeys, along with their two partners, by measuring their reaction to novel objects (e.g., a brightly colored novel toy) presented to them in their home cages. 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 partner than their unsuccessful partner. These results suggest that assessing temperament with a simple testing paradigm may be useful in forming successful pairs.“

Niemeyer C, Eaton, GG, Kelley ST1998. Practical aspects of the program to promote psychological well-being in nonhuman primates at the Oregon RPRC. In Proceedings of the Third International Conference on Environmental Enrichment Hare VJ, Worley E (eds), 345-354. The Shape of Enrichment
"New pairs are formed by moving both [pre-familiarized] individuals to a new location because monkeys 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 have been no serious injuries. We later reproduced these results with our vervet colony and after the quarantine process with all new arrivals.".

Reinhardt V, Houser WD, Eisele S, Champoux M 1987. Social enrichment with infants of the environment for singly caged adult rhesus monkeys. Zoo Biology 6, 365-371
"Twenty-nine weaned rhesus monkey infants were removed from breeding troops to avoid overcrowding and were placed with unfamiliar singly caged adults" without prior familiarization. "Adult-infant pairs were compatible in 90% of cases. Compatibility depended neither on the sex, age, and origin of the adult nor on the sex of the infant."

Reinhardt V 1989. Behavioral responses of unrelated adult male rhesus monkeys familiarized and 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 relationships during a 5-day period of noncontact familiarization. Only then were they paired in a different double cage. Rank relationships were confirmed within the first 6 minutes after pairing without the occurrence of any biting and fighting. It stands to reason that the risk of injury, intrinsically associated with pairing, can be minimized if only those dyads are selected whose partners show unequivocal signs of an established rank relationship during a period of noncontact familiarization."

Reinhardt V 1991. Agonistic behavior responses of socially experienced, unfamiliar adult male rhesus monkeys (Macaca mulatta) to pairing. Laboratory Primate Newsletter 30(1), 5-7
"The present data demonstrate that unfamiliar adult male rhesus monkeys may generally be paired directly with each other without undue risk provided partners have previously lived with another male companion. This is congruent with the findings made with adult females."

Reinhardt V 1994. Social enrichment for previously single-caged stumptail macaques. Animal Technology 5, 37-41
10 females and 6 males were isosexually introduced following the establishment of rank relationships during a three-day non-contact familiarization period. "Pair formations did not entail serious antagonism; instead companions engaged in conciliatory interactions."

Watson LM 2002. A successful program for same- and cross-age pair-housing adult and subadult male Macaca fascicularis. Laboratory Primate Newsletter 41(2), 6-9
Isosexual pairs of adult males, adult male/juvenile male and adult females were established and pair compatibility ascertained throughout follow-up periods of 1 month to 3 years. Partners were introduced after a carefully supervised noncontact familiarization period in a specific pair formation cage placed in an location other than the animals' homeroom. Of 31 adult male pairs tested, 29 [94%] were compatible; two pairs had to be separated because "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 of unfamiliar common marmoset (Callithrix jacchus) females. Primate Eye 73, 12-13
"Data on the formation of 46 common marmoset (Callithrix jacchus) female pairs in a laboratory were analysed. The success rate was 83%. The age of the females appears to be a critical factor in success rate, and aggression is lower if one member of the pair is not yet sexually mature (i.e. < 12 months). The results of this study show that pairing unfamiliar common marmoset females can be accomplished safely to avoid single housing when natural social grouping is not feasible."

Squirrel monkeys (Saimiri spp.)

Gwinn LA 1996. A method for using a pole housing apparatus to establish compatible pairs among squirrel monkeys. Contemporary Topics in Laboratory Animal Science 35(4), 61
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 primate enrichment. American Association for Laboratory Animal Science 55th National Meeting Official Program, 129
“Selected pairs are housed with plexi-panels between them for at least one week. At the end of this adaptive periods, pairs are allowed access to each other by removal of the grated panels separating them for a supervised period of one hour. The daily amount of time monkeys access each other is increased gradually until transition to pair-housing is complete.”

Gerald MS, Weiss A, Ayala JE 2006. Artificial colour treatment mediates aggression among unfamiliar vervet monkeys (Cercopithecus aethiops): a model for introducing primates with colourful sexual skin. Animal Welfare 15(4), 363-369
"Painting the scrotum dark led to more aggression when these males were paired with dark coloured 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 of aggression when introducing new animals."

(2,3) Grooming-Contact Caging

Crockett CM, Bellanca RU, Bowers CL, Bowden DM 1997. Grooming-contact bars provide social contact for individually caged laboratory macaques. Contemporary Topics in Laboratory Animal Science , 53-60
Pair formation of adult long-tailed macaques was accomplished by using widely spaced, vertical grooming-contact bars that allow physical contact [but no copulation] but prevent pursuit by one animal into the other's cage. Pair compatibility was 100% in all cases except unfamiliar male pairs (86%).

Crockett CM, Koberstein D, Heffernan KS 2001. Compatibility of laboratory monkeys housed in grooming-contact cages varies by species and sex. American Journal of Primatology 54(Supplement 1), 51-52
"At the Washington Regional Primate Research Center, we promote grooming-contact caging as a means to provide laboratory monkeys with tactile social contact while maintaining research access to animals housed individually. Grooming contact is achieved through widely spaced vertical bars that permit grooming but not aggressive pursuit." The following pair compatibility was found:
Macaca fascicularis male-female 97%,
Macaca fascicularis female-female 89%,
Macaca fascicularis male-male 63%,
Papio cynocephalus male-female 88%,
Papio cynocephalus female-female 57%,
M. nemestrina male-female 78%,
M. nemestrina male-male 57%%,
M. nemestrina female-female 53%,
M. mulatta male-male 45%.
"The majority of male-male pairs involved juveniles, so MM compatibility percentages may overestimate compatibility of adult male pairs."
 
*Crockett CM, Lee GH, Thom JP 2006. Sex and age predictors of compatibility in grooming-contact caging vary by species of laboratory monkey. International Journal of Primatology 27(Supplement), 417
Adult rhesus pairs were significantly less likely to be fully compatible (16%) than adult baboon pairs (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 the Refinement and Enrichment Forum. Animal Technology and Welfare 5(2), 95-98
"I think an affectionate human-animal relationship makes a huge difference for the animals because it helps them overcome anxiety and fear in disturbing or distressing situations." "The stress resulting from a neutral or negative relationship between investigator/technician and animal is bound to affect the research data collected from the animal subject, but the research industry is not yet taking this methodological flaw seriously."

Anonymous 2006. Primate passion An interview with Karen MacLeod, RVT, AALAS Northern California Branch Technologist of the Year 2006. Lab Animal 35(9), 6
When asked how she deals with attatchment to animals in her care: "Its hard because I am passionate about what I do and because our animals are long-term. It is important to be attached and there are certainly days when I am in tears, but I think if I ever felt unaffected by euthanizing our animals, it would be time for me to leave. As hard as it is to be passionate about what 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), 14-15
"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 more about what the procedures mean to the animals. You will get more creative in finding animal friendly alternatives for the procedures you need to do on the animals. You will thus increase the well-being of your animals and, by doing so, make better research subjects and increase the validity of the test results. .. There was a consensus that the emotional attachment provides an assurance that the animals receive optimal care, both physically and behaviorally. .. Concern was expressed that establishing an affectionate relationship with experimental subjects and knowing them as individuals would hamper ones impartiality and capacity to be objective when observing and registering their behavior. A caregiver strongly objected: It seems to me that we get hung up on trying to divorce our emotions from what we hope to be our objectivity. I do not think that any normally functioning human being in the world does anything for any reason other than emotional. Sure, research is done to answer questions, but isn't the premise of all research to make human (or animal) lives better? If you want to make lives better, it's because of emotion, not because you are logically attached to life."

Baker KC 1997. Human interaction as enrichment for captive chimpanzees: A preliminary report. American Journal of Primatology 42, 92
Simple, unstructured affiliation between humans and chimpanzees has a powerful impact on well-being, promoting activity and relaxed conspecific interactions and ameliorating behavioral disorders.

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 2.3.1. Affection for Animals. Washington, DC: Animal Welfare Institute
"Animal care personnel and researchers should be encouraged to develop affectionate relationships with their animals. Having such a relationship assures that you regard the animals as living beings, rather than biological test tubes. As such, you will be more careful and more patient. You will think more about what the experimental procedure implies to the animals. You will get more creative in refining procedures that are normally stressful or distressing to the animals. You will thus enhance their well-being and, by doing so, you will increase the scientific validity of the research results.
If you are not kind to your animals, make no attempt to enrich their boring, often depressing living quarters by addressing species-typical behavioral and social needs, and never show any kind of affection towards them (for example by offering them food treats from time to time), 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, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 2.3.2. Giving Animals Names. Washington, DC: Animal Welfare Institute
"Naming the animals helps me realize that I am working with sentient beings who deserve my consideration of their well-being. I guess, we can all relate much better to names than to numbers, and we tend to treat named versus numbered animals accordingly. The naming of animals 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 research protocol. The PI is afraid that, when bonding with her research subjects, we add a variable that is detrimental to performing research. Our staff feels that this is an antiquated mentality and we are all standing strong in our position of naming all animals in our charge!"

Bayne K 2002. Development of the human-research animal bond and its impact on animal well-being. ILAR [Institute for Laboratory Animal Research] Journal 43(1), 4-9
The 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 as people who care about their animals are committed to promoting and ensuring the well-being of those animals."

Bayne K, Dexter SL, Strange GM 1993. The effects of food treat provisioning and human interaction on the behavioral well-being of rhesus monkeys (Macaca mulatta). Contemp Topics in Laborat Anim Sci 32(2), 6-9
"The effects of human interaction and food supplementation appear to be protracted, resulting in a reduction of pathology [behavioral disorders] even after the enrichment is removed."

Bennett BT 1990. Alternative methodologies. In Essentials for Animal Research: A Primer for Research Personnel Bennett BT, Brown MJ, Schofield JC (eds), 13-25. USDA, National Agricultural Library, Beltsville
"Almost every animal commonly used in the laboratory responds positively to a little tender loving care. It's inexpensive, readily portable, safe even at the highest doses and spreads rapidly through the staff."

Boccia ML, Broussard C, Scanlan J, Laudenslager ML 1992 Practice makes predictable. In The Inevitable Bond: Examining Scientist-Animal Interactions Davis H, Balfour AD (eds), 153-170. Cambridge University Press, Cambridge
"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 eliminating confounding handling effects. The results presented here, however, suggest that it may be necessary 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 single-housed animals received more attention from the attending personnel.

European Economic Community 1986. Council Directive 86/609, Annex II Guidelines for Accommodation and Care of Animals. Official Journal of the European Communities L358 , 7-28
"The performance of an animal during an experiment depends very much on its confidence in man, something which has to be developed. It is therefore recommended that frequent contact should 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 Housing and Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London
"Where appropriate, time should be set aside for handling and grooming. All staff, both scientific and technical, should be sympathetic, gentle and firm when dealing with the animals."

Jensvold ML 2007. Promoting positive interactions between chimpanzees (Pan troglodytes) and caregivers. Laboratory Primate Newsletter 46(1), 1-4
"We tested our contention that when caregivers use chimpanzee behavior, more positive interactions 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 of empathy with the right encouragement, without destroying the primary research goals. In my experience [as attending veterinarian] it is utterly impossible, however, to make an uncaring person caring. Such people are not suited for this line of work (p. 35). .. There should be no sharp demarcation between 'good guys' and 'bad guys.' All employees, to some extent must share the work. Nonhuman primates are quick to forget, or perhaps forgive, the momentary fear or resentment they feel towards a human being who has just subjected them to an unpleasant experience 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, Page C, Sharman I, Verschoyle R, Westall L, Wilson AB 2001. Refining procedures for the administration of substances. Laboratory Animals 35, 1-41
"Where substances are administered infrequently but on a long-term basis handling the animals during routine daily husbandry will help reduce stress when subsequently dosing them. In general, staff should be encouraged to handle animals as much as possible."

National Research Council 1996. Guide for the Care and Use of Laboratory Animals. National Academy Press, Washington
"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 of enrichment should be provided to compensate for the absence of other animals, such as safe and positive interaction with the care staff."

Reinhardt V 2003. Compassion for animals in the laboratory: Impairment or refinement of research methodology. Journal of Applied Animal Welfare Science 6, 123-130
http://www.awionline.org/Lab_animals/biblio/jaaws10.html
“Compassion for animals used in research, testing and teaching should not be regarded as subjective but as a sound methodological base for scientifically valid animal research.”

Reese EP 1991. The role of husbandry in promoting the welfare of laboratory animals. In Animals in Biomedical Research Hendriksen CFM, Koeter HBWM (eds), 155-192. Elsevier, Amsterdam
"An important, and often neglected, source of social enrichment, especially when animals must be isolated from conspecifics, is attention from caretakers and technicians. That many scientists lack detailed information about their animals, especially their behavior, is distressing and reflects a serious disregard for the single most important element of their research. The animal is the key to the entire experiment. ... The proper handling of laboratory animals is as essential to the collection of valid data as it is to the animals' comfort and well-being. The more the animal is handled properly, the more docile it becomes, especially if handling begins at an early age. Conversely, the more an animal is mishandled, the more difficult, frightened, and aggressive it is likely to become ... Successful shaping requires the right attitude, a thorough understanding of the individual animal and of the task to be performed, and clinical skills. There is only one 'right' attitude, and that is respect for the individual animal. ... My students must name their animals, and I do not let them put an animal in the apparatus until they show me it will eat from their hands."

Russow L-M 2002. Ethical implications of the human-animal bond. ILAR [Institute for Laboratory Animal Research] Journal 43(1), 33-37
"Researchers must continue to question the barriers that have traditionally been errected against forming HABs in the name of objectivity and to investigate seriously the ways in which fostering the formation of HABs can promote animal welfare without compromising the scientific respectability of research."

Sokol KA 1993. Commentary: Thinking like a monkey - "primatomorphizing" an environmental enrichment program. Lab Animal 22(5), 40-45
"We encouraged animal caretakers to visit the animals at times other than their normal routines to reinforce positive interactions and associations. Instead of identifying the monkeys by just a tattoo number, we gave them names. Thus, we could refer to them as individuals and better identify them for health considerations."

Southey ER, Baldwin CM 2006. Socialisation of rhesus macaques at CFM. Animal Technology and Welfare 5(2), 119-122
The Centre for macaques in England is an example of best practice in the care and welfare of old world primates in addition to an evolving centre for the education and training of people working in the area of primate research. Husbandry techniques and socialisation of the macaques are described. Socialisation comprises of hand feeding through cage room and lobby bars, going into the playpen to hand out food and sitting in with the animals and interacting on a closer basis.

Wolfle TL 1987. Control of stress using non-drug approaches. Journal of the American Veterinary Medical Association 191, 1219-1221
"Human interaction with monkeys and apes is essential for the well-being of the animal, data validity, and ease of handling." The 'social bond' with the animal "conveys to the animal a quiet sense of assurance on which coping strategies can be developed for dealing with other stressful aspects of the laboratory."

Wolfle TL 2002. Introduction. ILAR [Institute for Laboratory Animal Research] Journal 43(1), 1-3
"I was encouraged not to assign names to the many rhesus monkeys in my charge. I was admonished that the animals are research subjects, not pets. The concern was that having names for the animals might blur this distinction between a research subject and a pet. .. It did not seem possible to remain distant - emotionally isolated - from the animals. In fact, the inevitable closeness that resulted from those intimate interactions was precisely what made us capable of doing what we were asked to do. ... Eventually, we all came to know that F49 was Sam, A12 was Rosie, and Z13 was Curious. ... Such attachments are the results of compassionate people doing their job right."

(3) Promoting Intelligent Behavior: Positive Reinforcement Training

Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housing and Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London
"The least distressing method of handling is to train the animal to co-operate in routine procedures. 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's attempt to achieve appropriate social balance. The Physiologist 29, 1&19-21
"Physical restraint procedures should be used on awake animals only after alternative procedures have been considered and found to be inadequate. If a restraint will be utilized the animal should be trained or conditioned to the restraining device, using positive reinforcement, prior to the beginning of the experiment"

(3,1) Basic Recommendations

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 7.2. Injection and Blood CollectionHow to minimize Stress Reactions. Washington, DC: Animal Welfare Institute
"If the animals are under stress while you are working with them, there is a great risk that they show aggressive reactions to you, in an attempt to get away from the stressful situation. One of the conditions of successful and safe positive reinforcement training is a stress-free work environment, both for the animal and for you. This means, neither the animal nor you should be under the emotional influence of fear, apprehension or frustration. These emotions are dangerous 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 work with him or her. This does not mean that you should not be alert, but any traces of mistrust and fear puts you into a seriously dangerous position. Do not work with an animal, unless you have trust in him or her! For your additional safety, you will always have to make sure that your interaction with the trainee will not be disturbed or disrupted by any unexpected event, such as personnel 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
Very helpful outline of what has to be taken into consideration when training animals to cooperate during handling procedures. "Non-human primates, particularly the larger macaques, vervets, baboons and apes, are readily trained to cooperate in procedures such as presenting an arm for blood collection."

Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housing and Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London
" The least distressing method of handling is to train the animal to co-operate in routine procedures. 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
"The importance of training and adaptation cannot be overemphasized. This not only reduces stress to the animal but promotes safety and quality data collection."

Laule GE, Desmond T 1998. Positive reinforcement training as an enrichment strategy. In Second Nature - Environmental Enrichment for Captive Animals Shepherdson DH, Mellen JD, Hutchins M (eds), 302-313. Smithsonian Institution Press, Washington
Principles 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 negative reinforcement is used." Punishment "is only appropriate in a situation that is life threatening for person 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 Animal Welfare] Handbook on the Care and Management of Laboratory Animals Seventh Edition Poole T, English P (eds ), 21-27. Blackwell Science, Oxford
Very 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 is significantly enhanced while providing better (less stressed) research models for the biomedical community."

T-W-Fiennes RN 1972. Primates - General. In The UFAW Handbook on the Care and Management of Laboratory Animals Fourth Edition UFAW [Universities Federation for Animal Welfare] (ed), 374-375. Churchill Livingstone, London
"The higher primates, such as chimpanzees and baboons, are intelligent and sensitive. If handled with sympathy and understanding they can become more than research tools - even cooperative partners in experimentation. To achieve this, a little time, often time well spent, must be spent on conditioning the animals. A chimpanzee, 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 and the results of the experiment may be vitiated for this reason."

(3,2) Species-specific Recommendations

Baboons (Papio spp.)

Levison PK, Fester CB, Nieman WH, Findley JD 1964. A method for training unrestrained primates to receive drug injection. Journal of the Experimental Analysis of Behavior 7, 253-254
Training technique by which an adult, single-housed male baboon learned to offer his arm through a pothole and accept intramuscular injection in this home cage is described and the result demonstrated with a photo. Injection was reliably obtained after approximately nine one-hour training sessions.

Turkkan JS, Ator NA, et al 1989. Beyond chronic catheterization in laboratory primates. In Housing, Care and Psychological Well-being of Captive and Laboratory Primates Segal EF (ed), 305-322. Noyes Pub, Park Ridge
Training protocols are described to ensure cooperation of single-housed baboons during blood pressure measurement and during oral drug dosing in the homecage.

Chimpanzees (Pan troglodytes)

Bloomsmith MA, Laule GE, Alford PL, Thurston RH 1994. Using training to moderate chimpanzee aggression during feeding. Zoo Biology 13, 557-566
"Positive reinforcement training techniques were applied to reduce a dominant male chimpanzee's aggression and chasing during meals. Verbal commands and food reinforcers were used to train him to sit and remain seated while other group members received and ate their share of produce."

Bloomsmith MA, Stone AM, Laule GE 1998. Positive reinforcement training to enhance the voluntary movement of group-housed chimpanzees within their enclosure. Zoo Biology 17, 333-341
"Positive reinforcement techniques were applied to train groups of chimpanzees to move voluntarily into the indoor portions of their enclosures at the request of trainers and to be briefly restricted to those areas."

Kessel-Davenport AL, Gutierrez T 1994. Training captive chimpanzees for movement in a transport box. The Newsletter 6(2), 1-2
Training technique is described. "Thirty-seven [group-housed] captive chimpanzees were trained using operant conditioning to enter a transfer box." [Age and sex of subjects is not provided.]

Lambeth SP, Perlman JE, Schapiro SJ 2000. Positive reinforcement training paired with videotape exposure decreases training time investment for a complicated task in female chimpanzees. American Journal of Primatology 51(Supplement 1), 79-80
"Five females were exposed to a 10-minute videotape of female chimpanzees being positively reinforced for successfully urinating into a cup. Immediately following videotape exposure, these subjects participated in a training session." On average experimental and control subjects received 56 minutes of training. "Subjects with videotape exposure successfully responded to the command to urinate in significantly less time than did controls."

Laule GE, Thurston RH, Alford PL, Bloomsmith MA 1996. Training to reliably obtain blood and urine samples from a diabetic chimpanzee (Pan troglodytes). Zoo Biology 15, 587-591
Training techniques are described to gain the cooperation of a 3-year old female chimpanzee in obtaining blood and urine samples. "The first blood draw occurred during the 18th training session, with a total of 275 minutes invested prior to that. The first successful [urine] collection occurred 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 Handbook on the Care and Management of Laboratory Animals Seventh Edition Poole T, English P (eds ), 21-27. Blackwell Science, Oxford
Very 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 is significantly enhanced while providing better (less stressed) research models for the biomedical community."

Perlman JE, Thiele E, Whittaker MA, Lambeth SP, Schapiro SJ 2004. Training chimpanzees to accept subcutaneous injections using positive reinforcement training techniques. American Journal of Primatology 62(Supplement), 96
”Positive reinforcement training techniques were used to train four socially-housed, adult chimpanzees to present their abdomen for a subcutaneous injection. .. Subjects had been previously trained to present body parts for inspection, including the abdomen. For the present study, subjects were trained to 1) present the abdomen, 2) tolerate a pinch of the skin, 3) accept the subcutaneous insertion of a needle, and 4) remain stationary while the contents of the syringe were injected. Three of the four chimpanzees were reliably trained to voluntarily accept the subcutaneous injection. A mean of 98 minutes of training time was required for the animals to reliably accept penetration and injection of up to 10 cc through a 25-gauge needle. Training sessions lasted 5 to 8 minutes and 13 - 20 sessions (mean = 17) were required to achieve reliable performance.“

Russell JL, Taglialatela JP, Hopkins WD 2006. The use of positive reinforcement training in chimpanzees (Pan troglodytes) for voluntary presentation for IM injections. American Journal of Primatology 68(Supplement ), 122 (Abstract)
"Positive reinforcement has been used to gain the cooperation of captive primates for research and management needs. In this study, ten chimpanzees .. were trained to present for intramuscular (IM) injections. Clicker training was used to teach subjects to present their leg and accept an injection. .. Subjects reached criterion for presenting for a touch from a needle in 7 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 research protocol requiring multiple accesses."

Schapiro SJ, Perlman JE, Thiele E, Lambeth S 2005. Training nonhuman primates to perform behaviors useful in biomedical research. Lab Animal 34(5), 37-42
Training protocols are described and the time investments to achieve cooperation for semen collection [7 subjects: 29-453 minutes], subcutaneous [2 subjects: 90-104 minutes; 1 subject could not be trained] and intramuscular injection [39 subjects: 0.1-396 minutes; 43 subjects could not be trained] are presented.

Spragg SDS 1940. Morphine addiction in chimpanzees. Comparative Psychology Monographs 15, 1-132
Author provides formal description of training four unrestrained chimpanzees to approach an investigator and accept an injection of physiological saline solution. The training comprised a combination of adaptation, desensitization, and shaping, with fruit, praise, and patting as reinforcers. "It is the writer's contention that this preliminary adaptation to the injection situation was an important factor for the experiment; it obviated many undesirable aspects which 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 captive chimpanzees to cooperate for an anesthetic injection. Lab Animal 34(5), 43-48
Training protocol is described in detail and the time investment presented.

Videan EN, Fritz J, Murphy J, Howell S, Heward CB 2005. Does training chimpanzees to present for injection lead to reduced stress? Laboratory Primate Newsletter 44(3), 1-2
"Subjects were 17 captive chimpanzees living at the Primate Foundation of Arizona, aged 10.6 to 34.5 years at the time of the study. The sample included 8 males and 9 females. Eleven of the subjects 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 anesthetic injection, using the verbal cues "arm" and "leg". Training procedures were transferred from the trainer to either the colony manager or the assistant colony manager, after behaviors were under 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<0.010, Table 1)."

Drills (Mandrillus spp.)

Priest GM 1991. Loon, the Diabetic Drill (Videotape) Mac & Mutley, San Francisco
Training technique for in-homecage blood collection of an adult male drill is clearly demonstrated.

Priest GM 1991. The methodology for developing animal behavior management programs at the San Diego Zoo and Wild Animal Park. American Zoo and Aquarium Association (AZA) Annual Conference Proceedings, 553-562
"Within a few weeks, Loon was voluntarily allowing the veterinarians to draw blood from his forearm. Loon has voluntarily accepted his daily insulin injections and blood withdrawals for over two years."

Gorillas (Gorilla spp.)

Bettinger T, Kuhar C, Sironen A, Laudenslager M 1998. Behavior and salivary cortisol in gorillas housed in an all male group. American Zoo and Aquarium Association (AZA) Annual Conference Proceedings, 242-246
Gorillas were successfully trained to voluntarily chew on the cotton plugs then return them to the caretaker.

Bond M 1991. How to collect urine from a gorilla. Gorilla Gazette 5(3), 12-13
Training technique is clearly described. Mandara "not only urinates on demand but has been known 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 food treats. Collection of the first semen sample [from single-housed subjects] varied from 5-14 months after the initiation of training, with collections occurring earliest on the animal that appeared to have the best relationship with the trainer."

Brown CS 1998 A Training Program for Semen Collection in Gorillas (Videotape). Henry Doorly Zoo, Ohama
Training technique to ensure cooperation of single-housed adult male gorillas during physical examination, injection, semen collection are described and very clearly demonstrated.

Segerson L, Laule GE 1995. Initiating a training program with gorillas at the North Carolina Zoological Park. American Zoo and Aquarium Association (AZA) Annual Conference Proceedings, 488-489
Technique is clearly described to facilitate wound treatment of an unrestrained, single-housed female gorilla.

Macaques (Macaca spp.)

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 7.2. Injection and Blood Collection--How to minimize Stress Reactions. Washington, DC: Animal Welfare Institute
"With positive reinforcement, I have trained adult female cynos to cooperate during intramuscular injection in home cages that are not equipped with squeeze-backs. When they can trust you, they readily learn to cooperate during this common procedure. These animals work with rather than against me, which automatically implies that they show no fear or stress reactions during the procedure."

Bunyak SC, Harvey NC, Rhine Rj, Wilson MI 1982. Venipuncture and vaginal swabbing in an enclosure occupied by a mixed-sex group of stumptailed macaques (Macaca arctoides). American Journal of Primatology 2, 201-204
By 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 for vaginal swabbing."

Clarke MR, Phillippi KM, Falkenstein JA, Moran EA, Suomi SJ 1990. Training Corral-living Rhesus Monkeys for Fecal and Blood Sample Collection (Videotape). Delta Primate Research Center, Covington
Training technique is explained and the animals' reactions demonstrated.

Down N, Skoumbourdis E, Walsh M, Francis R, Buckmaster C, Reinhardt V 2005. Pole-and-collar training: A disucssion by the Laboratory Animal Refinement and Enrichment Forum. Animal Technology and Welfare 4, 157-161
Experiences with the pole-and-collar training training are shared. "Yes, most monkeys can be trained but some cannot, or let's say they should not be trained because their personality hich is presumably conditioned through negative experiences with people is very difficult to deal 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. AALAS [American Association for Laboratory Animal Science] 54th National Meeting Official Program, 101
"Animals that adapted to wearing jackets were surgically implanted with a biliary diversion cannula system, a venous cannula and three subcutaneous access ports. .. The animals [three females and nine male rhesus] were trained to present the pouch and to remain stationary while the catheters were accessed. The length of time required for training was variable between individuals, 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 during sample collection. Instead, positive reinforcement was used to reward the animals with food for their cooperation during sample collection. This has also increased the efficiency of conducing metabolic studies and minimized the potential stress of sample collection for both the personnel and animals."

Goodwin J 1997. The application, use, and effects of training and enrichment variables with Japanese snow macaques (Macaca fuscata) at the Central Park Wildlife Center. American Zoo and Aquarium Association (AZA) Regional Conference Proceedings, 510-515
Training protocol is briefly described which allows the keepers through vocal and visual cues to herd the animals to a holding area.

Heath M 1989. The training of cynomolgus monkeys and how the human/animal relationship improves with environmental and mental enrichment. Animal Technology 40(1), 11-22
"A relatively short, but predictable, course of routine handling and feeding enabled the monkeys to co-operate with their handlers and made working practices a lot easier, quicker and safer for both the animals and technicians."

Luttrell L, Acker L, Urben M, Reinhardt V 1994. Training a large troop of rhesus macaques to cooperate during catching: Analysis of the time investment. Animal Welfare 3, 135-140
"Using a simple chute system and applying a training technique based on patience, all 45 troop members were successfully conditioned in less then 15 work-hours to voluntarily enter a transport cage one by one."

Phillippi-Falkenstein K, Clarke MR 1992. Procedure for training corral-living rhesus monkeys for fecal and blood-sample collection. Laboratory Animal Science 42, 83-85
Clear 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 rhesus monkeys. Lab Animal 19(6), 52-53
Training technique is described. "We have successfully trained two heterogeneous rhesus troops of 28 and 33 members. The catching procedure has become a routine that is no longer associated with excitation and distress. It is now possible for one experienced person to catch animals at any given time without extra help."

Reinhardt V 1990. Catching Individual Rhesus Monkeys Living in Captive Groups (Videotape). Available on loan from Animal Care Audio-Visual Materials, WRPRC, 1220 Capitol Court, Madison, WI 53715
Using vocal commands, a single person swiftly catches all members of a trained rhesus breeding group 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), 32-35
A training technique is described for ensuring the active cooperation of pair-housed/single-housed adult male and female rhesus and stump-tailed macaques during in-homecage venipuncture. 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-homecage treatment. Laboratory Primate Newsletter 29(4), 9-10
One to 14 training sessions, each lasting for 1-5 minutes, were required to train adult, pair-housed and single-housed stump-tailed macaques of both sexes to cooperate during topical treatment in the homecage.

*Skoumbourdis EK 2008. Pole-and-collar-and-chair training. Laboratory Animal Refinement & Enrichment Forum (electronic discussion group) , January 24, 2008
http://groups.yahoo.com/group/LAREF/members
"All the monkeys I have pole/collar/chair trained have gone through an initial phase of resistance both when the pole was being attached to the collar, and when they were first put into the chair, but for the most part they finally did settle down and cooperate. All it takes is patience 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 and even rewarding for them to cooperate with you rather than resist. A successfully trained monkey will have developed so much trust in you that he/she will never fight against you when you pole and chair him/her.
To pole-collar-chair train a monkey can be a very rewarding process that is not necessarily 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 adult male cynomolgus.
My quickest subject took just five days of training to reliably cooperate (I should mention that he was two years old and an angel!), while other animals have taken me well over a month to 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 reality that both you and the investigators must acknowledge. You cannot force a monkey to cooperate and 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 undisturbed marmoset families. American Journal of Primatology 31, 223-230
"An apparatus and a method are described, which allow simultaneous urine collection from all individual members of undisturbed marmoset families. By the end of the third week of training, it was 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 time investment. Journal of Applied Animal Welfare Science 6, 209-220
Behaviours taught were target training to allow in homecage weighing and providing urine samples from 12 pairs of marmosets. "Between 2 to 13, 10-minute training sessions established desired behaviors. .. Trained animals proved extremely reliable, and data collection using trained animals was considerably faster than collection using current laboratory techniques."

Smith TE, McCallister JM, Gordon SJ, Whittikar M. 2004. Quantitative data on training new world primates to urinate. American Journal of Primatology 64(1), 83-93
"This study assessed the effectiveness of operant conditioning in training three species of captive callitrichid primates (Leontopithecus rosalia, Callithrix geoffroyi, and Saguinus imperator) to urinate on demand...Training sessions (30 min each) were conducted at dawn thrice weekly during five consecutive phases: habituation, control, training (animals were rewarded for urinating), maintenance (animals had reached a defined training criteria and continued 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 sessions required 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 significantly greater during the training, maintenance, and collection phases compared to the control phase... The entry of the trainer into the cage to collect the urine sample did not appear to alter urination behavior. We demonstrate that operant conditioning techniques, which typically incur minimal cost, time investment, and disturbance, can be used to increase the quantity of urine samples collected for physiological analysis, the proportion of animals that urinate, 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
Training technique is clearly described and demonstrated to ensure cooperation of two pair-housed female/male orangutans during daily insulin injection.

Moore BA, Suedmeyer K 1997. Blood sampling in 0.2 Bornean orangutans at the Kansas City Zoological Gardens. Animal Keepers' Forum 24, 537-540
Training technique is clearly described to ensure cooperation during in-homecage blood collection of adult, pair-housed female orangutans.

Sakis (Pithecia spp.)

Shideler SE, Savage A, Ortuño AM, Moorman EA, Lasley BL 1994. Monitoring female reproductive function by measurement of fecal estrogen and progesterone metabolites in the white-faced saki (Pithecia pithecia). American Journal of Primatology 32, 95-108
"Fist morning void urine was collected directly in a polypropylene container hand-held under the female subject. A second container was held under the female to collect fecal material. [The group-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 goeffroyi)

Hernándes-López L, Mayagoitia L, Esquivel-Lacroix C, Rojas-Maya S, Mondragón-Ceballos R 1998. The menstrual cycle of the spider monkey (Ateles geoffroyi). American Journal of Primatology 44, 183-195
Four of the five females were trained to enter a small cage attached to the door of their enclosure and to "allow a cotton swab to be introduced in the vagina. This procedure was slightly modified [not described], and the animals were trained to be injected with ketamine" for subsequent blood collection.

Squirrel monkeys (Saimiri spp.)

Panneton M, Alleyn S, Kelly N 2001. Chair restraint for squirrel monkeys. 2001 AALAS [American Association for Laboratory Animal Science] Official Program, 92
"Commonly used procedures include moveable-back cages, manual restraint and the use of restraint chairs. Such procedures have the potential to cause emotional distress to the animals due to adverse conditioning. ... Our facility has trained squirrel monkeys to cooperate during various procedures such as capture from their homecage and chair restraint for periods not exceeding 1 h. ... Each squirrel monkey [in the chair] is constantly supervised and given positive reinforcement during and after the training sessions. ... The initial training [habituation] period starts at 5-10 min three times a week. Additional training sessions of 5-20 min are added until 1 h of chair restraint is achieved. At this time, training is reduced to twice a week for 1 h and then once a week for maintenance. ... Concerns such as weight loss, chair abrasions and hypglycemia are among some of the obstacles to overcome."

Tamarins (Saguinus spp.)

Snowdon CT, Savage A, McConnell PB 1985. A breeding colony of cotton-top tamarins (Saguinus oedipus). Laboratory Animal Science 35, 477-480
Group-housed females were conditioned to urinate into containers each morning in return for a food reward.

Smith TE, McCallister JM, Gordon SJ, Whittikar M. 2004. Quantitative data on training new world primates to urinate. American Journal of Primatology 64(1), 83-93
"This study assessed the effectiveness of operant conditioning in training three species of captive callitrichid primates (Leontopithecus rosalia, Callithrix geoffroyi, and Saguinus imperator) to urinate on demand...Training sessions (30 min each) were conducted at dawn thrice weekly during five consecutive phases: habituation, control, training (animals were rewarded for urinating), maintenance (animals had reached a defined training criteria and continued 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 sessions required 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 significantly greater during the training, maintenance, and collection phases compared to the control phase... The entry of the trainer into the cage to collect the urine sample did not appear to alter urination behavior. We demonstrate that operant conditioning techniques, which typically incur minimal cost, time investment, and disturbance, can be used to increase the quantity of urine samples collected for physiological analysis, the proportion of animals that urinate, and the speed of sample collection."

Vervet monkeys (Cercopithecus aethiops)

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 7.3. Oral Drug Administration. How to minimize Stress Reactions. Washington, DC: Animal Welfare Institute
"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 dry ingredients are blended with water and form a stiff putty-like paste, which is an ideal vehicle for mixing 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 the compound in about a third of the morning feed. The bulk of the food is offered after this portion has 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 very successfully. Over a time period of 20 years, we have not had to deal with any substance that we could not feed to the vervets, including bitter herbal mixtures in fairly high concentrations."

Kelley TM, Bramblett CA 1981. Urine collection from vervet monkeys by instrumental conditioning. American Journal of Primatology 1, 95-97
Training technique is described. Six of eight group-housed males reliably produced clean urine samples after a two-month period of training.

Woolly monkeys (Lagothrix spp.)

Logsdon S 1995. Use of operant conditioning to assist in the medical management of hypertension in woolly monkeys. American Zoo and Aquarium Association (AZA) Regional Conference Proceedings, 96-102
Training 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

 

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