Animal Welfare Information Center Newsletter, Spring 1995, Vol. 6 No. 1
Viktor Reinhardt, D.V.M., Ph.D., Animal Welfare Institute,
Washington, DC 20007
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
- The animals are too aggressive to be socialized with each other.
- 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.
- Pair-housed animals become bored of one another.
- 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
- 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
- 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
- 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
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
- 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.
- Bayne, K., S.L. Dexter, and S. Suomi (1991). Social
housing ameliorates behavioral pathology in Cebus apella.
Laboratory Primate Newsletter 30(2): 9-12.
- Bernstein, I.S. (1991). Social housing of monkeys and
apes: group formations. Laboratory Animal Science 41: 329-333.
- 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:
- 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.
- Ehardt, C.A. and I.S. Bernstein (1986). Matrilinear
overthrows in rhesus monkey groups. International Journal
of Primatology 7: 157-181.
- Erwin, J., G. Mitchell, and T. Maple (1973). Abnormal
behavior in non-isolate-reared rhesus monkeys.
Psychological Reports 33: 515-523.
- Fritz, J. (1989). Resocialization of captive chimpanzees:
an amelioration procedure. American Journal of Primatology
Supplement 1: 79-86.
- 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.
- International Primatological Society (1993). International
guidelines, code of practice: 1. housing and environmental enrichment. Primate Report 35: 7-16.
- 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.
- 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.
- Mendoza, S.P. (1991). Sociophysiology of well-being in
nonhuman primates. Laboratory Animal Science 41: 344-349.
- National Institutes of Health Nonhuman Primate
Management Plan (1991). Office of Animal Care and Use, NIH: Bethesda, MD.
- Petto, A.J. (1994). Response to survey on ethical
principles in primatology. Laboratory Primate Newsletter 33(3): 3-7.
- Public Health Service Statement (1994). The importance of
animals in biomedical and behavioral research. Animal Welfare Information Center Newsletter 5(2): 13.
- Ranheim, S. and V. Reinhardt (1989). Compatible rhesus
monkeys provide long-term stimulation for each other.
Laboratory Primate Newsletter 28(3): 1-2.
- 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.
- 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.
- 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:
- 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.
- 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.
- 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.
- Reinhardt, V. (1990). Social enrichment for laboratory
primates: a critical review. Laboratory Primate
Newsletter 29(3): 7-11.
- 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.
- 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.
- 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.
- Reinhardt, V. (1992). Avoiding aggression during and
after pair formation of adult rhesus macaques. Laboratory
Primate Newsletter 31(3): 10-11.
- Reinhardt, V. (1992). Transport-cage training of caged
rhesus macaques. Animal Technology 43: 57-61.
- Reinhardt, V. and S. Hurwitz (1993). Evaluation of social
enrichment for aged rhesus macaques. Animal Technology
- Reinhardt, V. (1994). Survey of environmental enrichment
for research macaques. Laboratory Primate Newsletter 33(3): 1-2.
- Reinhardt, V. (1994). Pair-housing rather than
single-housing for laboratory rhesus macaques. Journal of
Medical Primatology 23(8): 426-431.
- Reinhardt, V. (1994). Continuous pair-housing of caged
Macaca mulatta: risk evaluation. Laboratory
Primate Newsletter 33(1): 1-4.
- 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.
- 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.
- Schapiro, S.J. and D. Bushong (1994). Effects of
enrichment on veterinary treatment of laboratory rhesus macaques. (Macaca mulatta). Animal Welfare 3: 25-36.
- U.S. Department of Agriculture (1991). 9 CFR, Part 3:
Animal Welfare; Standards; Final Rule. Federal Register 56: 6426-6505.
This article appeared in the Animal Welfare Information Center
Newsletter, Volume 6, Number 1, Spring 1995
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