Maladaptation Chamove et al examined eight rhesus infants raised without a mother and demonstrated that allowing them to interact with only each other precludes normal social behaviour development. Familiar peers exhibited a preponderance of mutual clinging because they had no opportunity to develop affectional ties with any other conspecifics Chamove Ruppenthal et al tested infant pig-tailed macaques during play sessions scheduled throughout the first eight postnatal months. Play groups consisted each of two females and two males: four pair-housed versus four individually housed subjects.
The animals had been separated from their mothers shortly after birth. They were artificially reared during days and subsequently assigned to the experimental protocol. During the play sessions, pair-housed infants tried to maintain physical contact with their partners by clinging to each other. Individually housed infants spent significantly less time clinging to playmates and were less afraid to examine them.
No significant difference in social play was found between rearing conditions. At the end of the study, all animals were placed in cages with seven to eight other monkeys. Informal observations suggested that the pair-reared subjects fared poorly in this social housing situation: they were submissive and appeared depressed.
Nursery Rearing Methods for Rhesus Macaques
These reactions were not seen in the individually reared subjects. The authors concluded that pair rearing yields abnormal social development in pig-tailed macaques. Unlike motherless peer rearing, mother rearing and subsequent pair housing with another peer is unlikely to produce developmental disorders. Schapiro et al separated 24 mother-reared rhesus infants from their natal group when they were a little over one-year-old and placed them in single cages for one year. The animals were subsequently paired with another similarly reared peer of the opposite sex.
When they were three-years-old, subjects were placed into groups of six to eight other monkeys. The authors did not observe any social integration problems on these occasions.
Nursery Care Of Nonhuman Primates 1979
Discussion The present review leads to the conclusion that arguments justifying individual caging of laboratory non-human primates may often be based on assumptions rather than on facts. Rhesus macaques for example, are commonly single-housed because it is generally believed that the species is particularly aggressive and hence unsuitable for social housing. Disregarding this conventional wisdom, adult rhesus macaques of both sexes assigned to research, were successfully transferred from single housing to permanent isosexual pair housing with each other pairs or to pair housing with infants 91 pairs.
The available information indicates that transferring single-caged macaques to group housing is likely to be associated with a relatively high risk. The inherent socio-ethological advantages of group living, however, warrants carefully controlled and monitored attempts to provide compatible group housing, especially for young animals. Scientific findings show that pair formation and subsequent permanent pair housing offers a safe alternative to unsuccessful group housing attempts. Future studies will also have to examine if adult-infant pairing is equally successful in other macaque species as it is in rhesus macaques.
The information regarding the impact of social housing on morbidity is limited, but strongly suggests that the health risks associated with group living can effectively be minimized or even neutralized when non-human primates are housed in compatible pairs. The literature reviewed offers no evidence that compatible social housing causes more distress than single housing. This does not imply that single housing is stressful.
Compatible companionship, however, unlike solitary confinement, functions as a buffer against stress during fear-inducing events associated with routine management practices and experimental procedures. Housing gregarious non-human primates in compatible social conditions is also a safeguard against the pathological condition of behavioural disorders so commonly seen in single-caged subjects cf Erwin et al Goosen et al recommend therefore that individual housing should be used only when strictly necessary for the well-being of the animals, eg during recovery from surgery.
To make social housing a successful management improvement: a partner compatibility must be ascertained on a daily basis cf US Department of Agriculture Socially housed animals can readily be conditioned to allow capture in transport boxes Smith ; Boccia et al ; Reinhardt b; Luttrell et al The normal social adjustability by pair-housed macaque infants that were naturally raised by their mothers, as opposed to the relatively poor social adjustment of pair-housed infants that were artificially reared without mother contact, endorses natural rather than artificial rearing conditions for non-human primates.
The unnatural attachment of a mother-deprived infant to another infant inhibits rather than facilitates the devolvement of normal peer-peer interaction Chamove et al The cause of this behavioural problem is obviously not the social peer-housing condition but the absence of the biological mother cf Mason This notion is supported by findings of Alexander who reared infant rhesus macaques from birth for eight months with only their mothers.
These animals did not show the typical together-together syndrome when separated from their mothers, and socialized with peers. The present survey of the literature supports the regulatory recommendations of housing gregarious non-human primates, such as macaques, in an environment that allows them to express their social disposition. Keeping macaques under social rather than single housing conditions provides a simple way of approximating conditions that are normal.
It makes the animals more valuable for unbiased scientific research because they are now truly what they are supposed to be: social animals. Pair housing is likely to be one of the least expensive and most effective alternatives for improving the welfare of macaques inresearch facilities Line et al b. It would defeat the purpose of the regulations to stubbornly force laboratory macaques to live together and possibly kill each other. Given the complexity of non-human primates and the inherent dynamics of their social relationships, it would be unrealistic to expect unvarying compatibility Reinhardt b.
No strict rule can therefore be set which will guarantee successful social housing in all instances. Attempts to transfer single-caged animals to compatible permanent group or pair housing have to be based on ethological principles Table 2 , common sense, some expertise, and also on good will in order to take variables into account that may directly affect the outcome. The published data show that previously single-caged macaques can be transferred to social housing adequate for the species group housing for juveniles, pair housing for adults without undue risks to individual animals.
Techniques that are currently applied successfully with macaques should be attempted with other appropriate species and modified if necessary.
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The work described in this review presents a justifiable plan of action to provide social non-human primates with a social rather than solitary housing environment. Animal welfare implications Scientific evidence shows that laboratory macaques can be perrnanently housed in a compatible social environment without unduly jeopardizing their safety. Providing them with a social rather than the traditional solitary environment, fosters their well-being by offering them means to satisfy their need for social interaction and social contact.
Acknowledgements We are thankful to Mollie Bloomsmith, Gray Eaton, Catherine Reinhardt and Annie Reinhardt for reading the first draft of this manuscript and offering constructive criticism. The manuscript also benefited from very helpful suggestions of three anonymous referees.
References Alexander B K The effects of early peer-deprivation on juvenile behaviour of rhesus monkeys. Folia Primatologica Bernstein I S Social housing of monkeys and apes: group formations. A pilot study. Psychosomatic Medicine Coe C L Is social housing of primates always the optimal choice? Januar International Journal of Primatology 7: Epley S W Reduction of the behavioral effects of aversive stimulation by the presence of companions.
Psychological Bulletin Erwin J Factors influencing aggressive behavior and risk of trauma in pigtail macaque Macaca nemestrina. Laboratory Animal Science Erwin J Aggression in captive macaques: interaction of social and spatial factors.
Nursery Rearing of Nonhuman Primates in the 21st Century
Physiology and Behavior Gunnar M R, Gonzalez C A and Levine S The role of peers on modifying behavioral distress and pituitary-adrenal response to a novel environment in year-old rhesus monkeys. Proceedings of the National Academy of Science Hennessy M B Presence of companion moderates arousal of monkeys with restricted social experience. Physiology and Behavior Holm R A Effect of parental risk and prenatal stress on pregnancy outcome. Physiology and Behavior Mason W A Effects of social interaction on well-being: development aspects.
Laboratory Animal Science Maxim P E An interval scale for studying and quantifying social relations in pairs of rhesus monkeys. Laboratory Animal. Physiology and Behavior Mitchell G and Gomber J Moving laboratory rhesus monkeys Macaca mulatta to unfamiliar home cages. Office of Animal Care and Use. Primates O'Neill P L A room with a view for captive primates: issues, goals, related research and strategies. Laboratory Primate Newsletter 33 3 : Phillippi-Falkenstein K and Clarke M R Procedure for training corral-living rhesus monkeys for fecal and blood-sample collection.
Primates Ranheim S and Reinhardt V Compatible rhesus monkeys provide long-term stimulation for each other. American Journal of Psychiatry Redican W and Mitchell G The social behavior of adult male-infant pairs of rhesus macaques in a laboratory environment. American Journal of Physical Anthropology Reinhardt V Advantages of housing rhesus monkeys in compatible pairs.
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References | The Psychological Well-Being of Nonhuman Primates | The National Academies Press
See any care plans, options and policies that may be associated with this product. Email address. Please enter a valid email address. Comparative Medicine, 66 2 : Rearing environment and hypothalamic-pituitary-adrenal regulation in young rhesus monkeys Macaca mulatta.
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Developmental Psychobiology. Cognitive style: problem solving by rhesus macaques Macaca mulatta reared with living or inanimate substitute mothers. Journal of Comparative Psycholoty. Monkeys Macaca mulatta raised only with peers. A pilot study. Animal Behavior, 21 2 Early rearing conditions alter immune responses in the developing infant primate.
Pediatrics Surrogate mobility and orientation affect the early neurobehavioral development of infant rhesus macaques Macaca mulatta.
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