Animal Welfare Information Center Newsletter, Spring 1995, Vol. 6 No. 1

Arguments for Single-Caging of Rhesus Macaques: Are They Justified?

To: References

Human primates are social by nature and strive best in the supportive environment of compatible conspecifics. Being forcefully deprived of companionship is therefore one of the most dreaded punishments. Nonhuman primates share the same basic "social needs" (36) as human primates do, and sociality is central to their very survival (2). Like human primates, nonhuman primates may become mentally disturbed when chronically kept in social isolation, and they often express their distress in abnormal behavior patterns (cf. 6).

Despite the inherent ethical problems related to social deprivation, social housing of nonhuman primates is seen as a husbandry priority only by a minority of primatological investigators (14). Thus, single-caging is still the prevailing housing condition for laboratory primates (13, 30). The regulatory "safeguard" (15) prescribing social housing (36) is apparently not very effective. The following arguments are often brought forward in justification of the traditional single-caging:

1. The animals are too aggressive to be socialized with each other.

2. Socially housed animals are at greater health risk than individually housed animals. They suffer distress from being constantly exposed to companionship. Subordinate animals become undernourished because of food competition.

3. Pair-housed animals become bored of one another.

4. Social housing interferes with research protocols.

The present paper examines the justification of these notions as they pertain to the most common laboratory nonhuman primates, i.e., rhesus macaques (Macaca mulatta).

Numerous studies have indeed shown that unlike in other nonhuman primate species (e.g., Pan troglodytes, 7; Cebus apella, 1; Saimiri sciureus, 12) group formation and subsequent group housing of rhesus macaques are likely to be associated with serious problems related to aggressive intolerance (e.g., 5, 10). Alternative pair formation and subsequent pairhousing techniques have therefore been developed for rhesus macaques (17, 18, 21, 4) in order to avoid the risk attendant on group housing. How successful are these techniques?

• No noteworthy aggression was observed when either 64 or 104 juveniles were transferred from single-caging to heterosexual and isosexual pair-housing conditions for 1 year (33, 31).

• Transferring 65 adult females and 13 adult males from single- to pair-housing arrangements with infants for 1 year was successful in 93 percent of cases (94 percent of female/infant pairs, 92 percent of male/infant pairs). Pairs were split due to aggression in 3 percent of cases. Inadequate food sharing and "teasing" accounted for the other 4 percent of pair incompatibility (31).

• Transferring 154 adult females and 40 adult males from single-caging to continuous isosexual pair-housing conditions with each other for 1 year was successful in 87 percent of cases (88 percent of female pairs, 80 percent of male pairs). Partners were separated in 6 percent of cases because one of them seriously aggressed the other. Inadequate food sharing or depression accounted for the remaining 7 percent of partner incompatibility (31).

• Transferring 24 previously single-caged adults of both sexes to uninterrupted isosexual pair-housing conditions for 3 to 7 years was associated with pair incompatibility in 12 percent of cases, with serious aggression accounting for 3 percent. There were no indications that long-term compatibility of male pairs was less than that of female pairs, that partners did not readily adjust to new companions, or that the presence of offspring jeopardized the compatibility of companions (32).

These findings indicate that "the conventional wisdom that unfamiliar adult macaques are more likely to fight than to coexist peacefully" (11) does not hold true for the most common and, supposedly, most aggressive species, i.e., Macaca mulatta. The published information available provides evidence that no unreasonable risk of aggressive intolerance accrue when previously single-caged individuals are subjected to careful pair formation and subsequent permanent pair-housing protocols (c.f. 27). Pair housing effectively avoids the typical aggression problems of group housing.

The health risk associated with pair housing as compared to conventional single housing was assessed in three independent studies. In no case was clinical morbidity, as measured in the rate of veterinary treatment, higher in pair-housed than in single-housed subjects (23, 4, 35). In a study of 96 monkeys transferred from single- to compatible pair-housing conditions, subjects required veterinary treatment once every 909 days while singly caged, versus once every 2,104 days while pair housed (35). This suggests that pair housing may be an effective housing strategy not only from the behavioral but also from the veterinary point of view (35).

Three separate investigations examined the stress status of compatible pair-housed versus single-housed animals. Serum cortisol concentrations (26, 33) and immune stress response (4) of subjects did not differ in both housing conditions. Stress indices of subordinate animals were not higher than those of their dominant partners (26, 4).

Rather than being a source of distress, the compatible companion may function as a source of security (e.g., 8). This is particularly relevant for the experimental context in which the presence of a familiar conspecific functions as a buffer against environmental stress that the single-caged individual is lacking (21). Needless to say that scientific data collected from such a "stress-protected" subject are less confounded than data collected from a socially deprived research subject (cf. 3). The comforting rather than distressing effect of companionship can also be inferred from the fact that individuals afflicted with gross behavioral disorders often abandon their neurotic activities after being provided with a compatible cage mate (18, 19, 11).

Three independent studies failed to find a negative impact of pair housing on body weight development (20, 29, 4). There was also no evidence found of dominant animals gaining more body weight than their subordinate partners (20, 4). This is not surprising because adequate food sharing is an important condition to qualify a pair as compatible and allow partners to stay together (22).

The stimulatory effect of a cage mate has been evaluated in animals that have lived together as pairs for 1 year or longer. Five investigations have shown that paired companions spend approximately the same amount of time interacting with each other in species-typical ways (figure 1) as do wild animals living in troops (16, 24, 29, 4, 34). This suggests that a compatible cage mate-- unlike inanimate toys--maintains its stimulatory effect over time, probably because of its inherent ever-changing nature.

It has been documented that the following research-related procedures can readily be accomplished in pair-housed rhesus macaques:

• capture from cage (28);
• blood collection in the subject's home cage (25);
• tethering (25); and
• headcap implantation (22, 25).

Procedures such as controlled food intake and urine and fecal sampling require the temporary separation of partners with transparent cage-dividing panels, allowing uninterrupted visual, olfactory, and auditory contact.

The findings presented in this report indicate that common arguments in justification of the traditional single-caging of rhesus macaques are often based on subjective assumptions rather than on scientific facts. Providing the animals a social environment in the form of compatible pair-housing arrangements does not unduly jeopardize their safety (no conspicuous aggression problems), health (no conspicuous veterinary problems), physical well-being (no signs of distress), behavioral well-being (species-typical expression of social needs; amelioration of behavioral disorders) and adequate food intake, nor does it interfere with common research procedures. Professional standards stipulate that "unless absolutely essential, primates should not be housed alone in a cage on a long-term basis" (9). The question of what makes it "absolutely essential" to deprive the majority of research rhesus macaques of social contact and social interaction by housing them permanently alone in single cages remains to be answered.

References

1. Bayne, K., S.L. Dexter, and S. Suomi (1991). Social housing ameliorates behavioral pathology in Cebus apella. Laboratory Primate Newsletter 30(2): 9-12.

2. Bernstein, I.S. (1991). Social housing of monkeys and apes: group formations. Laboratory Animal Science 41: 329-333.

3. Coelho, A.M., K.D. Carey, and R.E. Shade (1991). Assessing the effects of social environment on blood pressure and heart rates of baboons. American Journal of Primatology 23: 257-267.

4. Eaton, G.G., S.T. Kelley, M.K. Axthelm, S.A. Iliff-Sizemore, and S.M. Shiigi (1994). Psychological well-being in paired adult female rhesus (Macaca mulatta). American Journal of Primatology 33: 89-99.

5. Ehardt, C.A. and I.S. Bernstein (1986). Matrilinear overthrows in rhesus monkey groups. International Journal of Primatology 7: 157-181.

6. Erwin, J., G. Mitchell, and T. Maple (1973). Abnormal behavior in non-isolate-reared rhesus monkeys. Psychological Reports 33: 515-523.

7. Fritz, J. (1989). Resocialization of captive chimpanzees: an amelioration procedure. American Journal of Primatology Supplement 1: 79-86.

8. Gust, D.A., T.P. Gordon, M.K. Hamabrigh, and M.E. Wilson (1994). Relationships between social factors and pituitary-adrenocortical activity in female rhesus monkeys. Hormones and Behavior 27: 318-331.

9. International Primatological Society (1993). International guidelines, code of practice: 1. housing and environmental enrichment. Primate Report 35: 7-16.

10. Kessler, M.J., W.T. London, R.G. Rawlins, J.Gonzales, H.S. Martines, and J. Sanches (1985). Management of a harem breeding colony of rhesus monkeys to reduce trauma-related morbidity and mortality. Journal of Medical Primatology 14: 91-98.

11. Line, S.W., K.N. Morgan, H. Markowitz, J.A. Roberts, and M. Riddell (1990). Behavioral responses of female long-tailed macaques (Macaca fascicularis) to pair formation. Laboratory Primate Newsletter 29(4): 1-4.

12. Mendoza, S.P. (1991). Sociophysiology of well-being in nonhuman primates. Laboratory Animal Science 41: 344-349.

13. National Institutes of Health Nonhuman Primate Management Plan (1991). Office of Animal Care and Use, NIH: Bethesda, MD.

14. Petto, A.J. (1994). Response to survey on ethical principles in primatology. Laboratory Primate Newsletter 33(3): 3-7.

15. Public Health Service Statement (1994). The importance of animals in biomedical and behavioral research. Animal Welfare Information Center Newsletter 5(2): 13.

16. Ranheim, S. and V. Reinhardt (1989). Compatible rhesus monkeys provide long-term stimulation for each other. Laboratory Primate Newsletter 28(3): 1-2.

17. Reinhardt, V., D. Cowley, S. Eisele, R. Vertein, and D. Houser (1987). Preliminary comments on pairing unfamiliar adult female rhesus monkeys for the purpose of environmental enrichment. Laboratory Primate Newsletter 26(2): 5-8.

18. Reinhardt, V., W.D. Houser, S.G. Eisele, and M. Champoux (1987). Social enrichment of the environment with infants for singly caged adult rhesus monkeys. Zoo Biology 6(4): 365-371.

19. Reinhardt, V., W.D. Houser, S. Eisele, D. Cowley, and R. Vertein (1988). Behavioral responses of unrelated rhesus monkey females paired for the purpose of environmental enrichment. American Journal of Primatology 14: 135-140.

20. Reinhardt, V., D. Cowley, S. Eisele, R. Vertein, and D. Houser (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.

21. 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.

22. Reinhardt, V., D. Houser, D. Cowley, S. Eisele, and R. Vertein (1989). Alternatives to single caging of rhesus monkeys (Macaca mulatta) used in research. Zeitschrift für Versuchsteirkunde 32: 275-279.

23. Reinhardt, V. (1990). Social enrichment for laboratory primates: a critical review. Laboratory Primate Newsletter 29(3): 7-11.

24. 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.

25. Reinhardt, V. (1991). An environmental enrichment program for caged rhesus monkeys at the Wisconsin Regional Primate Research Center. In: Through the Looking Glass. Issues of Psychological Well-being in Captive Nonhuman Primates, M.A. and A.J. Petto, eds., American Psychological Association: Washington, DC, pp.149-159.

26. Reinhardt, V., D. Cowley, and S. Eisele (1991). Serum cortisol concentrations of single-housed and isosexually pair-housed adult rhesus macaques. Journal of Experimental Animal Science 34: 73-76.

27. Reinhardt, V. (1992). Avoiding aggression during and after pair formation of adult rhesus macaques. Laboratory Primate Newsletter 31(3): 10-11.

28. Reinhardt, V. (1992). Transport-cage training of caged rhesus macaques. Animal Technology 43: 57-61.

29. Reinhardt, V. and S. Hurwitz (1993). Evaluation of social enrichment for aged rhesus macaques. Animal Technology 44: 53-57.

30. Reinhardt, V. (1994). Survey of environmental enrichment for research macaques. Laboratory Primate Newsletter 33(3): 1-2.

31. Reinhardt, V. (1994). Pair-housing rather than single-housing for laboratory rhesus macaques. Journal of Medical Primatology 23(8): 426-431.

32. Reinhardt, V. (1994). Continuous pair-housing of caged Macaca mulatta: risk evaluation. Laboratory Primate Newsletter 33(1): 1-4.

33. Schapiro, S.J., M.A. Bloomsmith, A.L. Kessel, and C.A. Shively (1993). Effects of enrichment and housing on cortisol response in juvenile rhesus monkeys. Applied Animal Behaviour Science 37: 251-261.

34. Schapiro, S.J. and M.A. Bloomsmith (1994). Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys. American Journal of Primatology 32: 159-170.

35. Schapiro, S.J. and D. Bushong (1994). Effects of enrichment on veterinary treatment of laboratory rhesus macaques. (Macaca mulatta). Animal Welfare 3: 25-36.

36. U.S. Department of Agriculture (1991). 9 CFR, Part 3: Animal Welfare; Standards; Final Rule. Federal Register 56: 6426-6505.

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