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Social Housing of Previously Singly-Caged Macaques

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						 SOCIAL HOUSING OF PREVIOUSLY SINGLE-CAGED 
						   MACAQUES: WHAT ARE THE OPTIONS AND THE 
										   RISKS? 
			
							 V Reinhardt, C Liss and C Stevens 
			 
			  Animal Welfare Institute, PO Box 3650, Washington, DC 20007, USA 
			Contact for correspondence and requests for reprints: 4605 Crescent
			Road, Madison WI 53711, USA 
			 
			Abstract                             Animal Welfare 1995, 4: 307-328 
			 
			A review of the scientif c literature gives evidence that transferring
			previously single-caged adult macaques to permanent compatible
			pair-housing arrangements (isosexual pairs, adult/infant pairs) is
			associated with less risk of injury and morbidity than transferring
			them to permanent group-housing arrangements. Juvenile animals can
			readily be transferred to permanent group-housing situations without
			undue risks. Safe pairformation and subsequent pair-housing techniques
			have been developed for female and male rhesus (Macaca mulatta), 
			stump-tailed (M. arctoides) and pig-tailed macaques (M. nemestrina) as
			well as for female long-tailed macaques (M. fascicularis). Pair housing
			does not jeopardize the animals' physical health but it increases their
			behavioural health by providing them with an adequate environment to
			satisfy their need for social contact and social interaction. 
			 
			Keywords: aggression, animal welfare, behavioural health,
			compatibility, dlstress, morbidity, primates, psychological well-being,
			social housing, undernourishment 
			 
			Introduction 
			 
			The housing of non-human laboratory primates is a controversial issue.
			While the public argues that individual housing is not species-adequate
			and hence ethically not justifiable, some members of the primatological
			research community are reluctant to give up a housing system that is
			seemingly serving their scientific enterprise so well. A recent survey
			of North American primatological institutions showed that the most
			common laboratory primates, ie rhesus macaques (Macaca mulatta),
			long-tailed macaques (M. fascicularis), pig-tailed macaques (M.
			nemestrina), and stump-tailed macaques (M. arctoides), are being housed
			in appropriate social environments on average in only 38 per cent of
			cases (Reinhardt 1994a) despite the fact that published scientific
			information strongly supports guides and rules prescribing housing
			conditions that address the animals' social disposition. 
			 
			   The United States' Guide for the Care and Use of Laboratory Animals
			(National Institutes of Health 1985) states that group housing should
			be considered for communal animals. The British Code of Practice for
			the Housing and Care of Animals Used in Scientific Procedures 
			(Home Office 1989) recommends that non-human primates be so housed that
			they have an opportunity for social interactions. The US Animal Welfare
			Act (US Department of Agriculture 1991) requires that institutions
			address the 'social needs' of social non-human primates. An animal may
			be exempt from social housing for health reasons and approved
			scientific research reasons. The Swiss Animal Protection Law (Der
			Schweizerische Bundesrat 1981) explicitly restricts such exemptions for
			health reasons. The Canadian Guide to the Care and Use of Experimental
			Animals (Canadian Council on Animal Care 1993) stipulates that
			non-human primates should be provided with a social environment
			conducive to their well-being. The International Primatological
			Society's Guidelines (International Primatological Society 1993)
			propose that unless absolutely essential, primates should not be housed
			alone in a cage on a long-term basis, because a compatible conspecific
			probably provides more appropriate stimulation to a captive primate
			than any other potential environmental enrichment factor. 
			 
			   The intent of the guides and rules reflects frequently published
			notions of primatologists. Chance et al (1983) argue that except for
			some specialized cases the accepted practice of housing monkeys singly
			is completely unjustified, since primatologists are fully aware that
			monkeys are social animals and require companions for a healthy life.
			With sociality so central to the very survival of primates (Bernstein
			1991), Bramblett (1989) points out that the most stimulating, diverse
			and biologically important addition to the welfare of a captive primate
			is a social companion (cf Bennett & Davis 1989; Fouts et al 1989;
			Pereira et al 1989; Segal 1989; Rumpler 1992). Social deprivation
			should not be considered any more normal than water or food deprivation
			(de Waal 1991). The assumption that non-human primates have social
			needs (US Department of Agriculture 1991) is echoed by Novak and 
			Suomi (1991) who stated that social interaction is crucial for normal
			development in most primate species, and that having access to one or
			more companions may be the most effective way to foster their
			psychological well-being (cf Novak & Drewsen 1989). 
			 
			   Some primatologists warn against social housing, underscoring an
			increased potential for the transmission of contagious diseases, for
			wounding and for undernourishment (Novak & Suomi 1988; cf Vandenbergh
			1989; Woolverton et al 1989). The concern for wounding has been
			expressed most strongly by Line (1987) arguing that any plan to
			increase social interaction also increases the risk of injury and
			death. Unless they have grown up in the same social group, primates are
			not likely to tolerate each other when placed together as adults (cf
			Line et al 1989a). The fear of risking injury is shared by Coe (1991)
			cautioning that especially when new pairs are formed 'veterinarians
			will be kept quite busy suturing wounds'. Novak and Suomi (1988)
			underscored that stress may be increased in pairs as a result of
			incompatibility or excessive aggression by the dominant member of the
			pair. Ruppenthal et al (1991) pointed out that pair rearing may lead
			to behavioural maladaptation. 
			 
			   Taking both, the social disposition of primates and the potential
			risk of social housing into account, the Association of Primate
			Veterinarians strongly recommends that a programme of social
			interaction be adopted by each institution (Keeling 1990). Contrary to
			this veterinary recommendation, only 12 per cent of primatologists (n
			= 105 respondents) indicated that if non-human primates should have
			rights, the provision of an appropriate social situation should be one
			of them (Petto 1994). Investigators at the National Institutes of
			Health suggest social housing of caged research primates less
			frequently (7.7%) as a modification of the cage environment, than
			provision of inanimate enrichment objects (27.8%) such as toys, swings,
			perches and shelves (National Institutes of Health 1991). Woolverton
			et al (1989) echoes this attitude by expecting only 'marginal benefits'
			of social housing for laboratory non-human primates. 
			
			   The conflicting opinions of professionals working with laboratory
			primates warrant an evaluation of possible arguments used to justify
			individual housing (cf Visalberghi & Anderson 1993). The present review
			focuses on studies conducted in macaques (Macaca spp.), because
			comprehensive published information is available only for this genus. 
			
			Aggression 
			 
			Group housing 
			
			Group housing is probably the biologically most appropriate housing
			condition for macaques (cf Bernstein 1991; Rolland 1991). Aggressive
			intolerance of strange conspecifics, however, distinguishes adult
			macaques; and the artificial formation of groups or the introduction
			of strangers into established groups is associated with considerable
			risks of trauma and death (rhesus macaques: Bernstein & Mason 1963;
			Southwick 1967; Bernstein et al 1974; Fairbanks et al 1977, pig-tailed
			macaques: Bernstein 1969; Tokuda & Jensen 1969; Erwin 1979, long-tailed
			macaques: Dollinger 1971, stump-tailed macaques: Rhine & Cox 1989). 
			Kessler et al (1985), for example, routinely formed single male harems
			of 15-25 rhesus macaques and reported a 13 per cent trauma mortality
			rate per year. 
			 
			   Line et al (199Oa) tried to circumvent the consequences of
			xenophobia in rhesus macaques. Future group members were therefore
			familiarized by placing two monkeys in wire-mesh cages at 7cm distance
			for 15 minutes. Fights were common during the first day of group
			formation. By day four, one male was depressed and withdrawn, and was
			regularly harassed by two of the other males. The victim was
			permanently removed for treatment of several bite wounds. Four days
			later, the top-ranking female was found dead in the cage from trauma.
			Within less than a month 77 per cent of the animals (10/13) had
			sustained injuries. 
			
			   Assuming that adequate familiarization of potential group members
			cannot be achieved in the course of brief non-contact encounters,
			Reinhardt (199la) formed two isosexual groups of six adult rhesus
			macaques each, after group members had been given the opportunity to
			physically interact with each other on a one-to-one basis for one week.
			In both instances, group incompatibility was heralded by certain
			subjects challenging other individuals to whom they had originally been
			subordinate. Aggressive harassment was intensive and persistent, but
			victims showed no resistance. Both groups were split up within less
			than one hour to avoid similar consequences as those described by Line
			et al (199Oa). 
			
			   Unlike adults, socially experienced juvenile and subadult macaques
			can readily be transferred from single-housing to group-housing
			arrangements with other peers. Bernstein and Draper (1964) released
			eight female and three male juvenile rhesus macaques into a compound
			and observed that the animals formed an organized social group without
			resorting to serious aggression. Schapiro et al (1994) reported no
			problems associated with aggression when moving 19 juvenile rhesus
			macaques from single cages into heterosexual peer groups and
			maintaining group membership until the animals reached sexual maturity.
			Wolff and Ruppert (1991) encountered no aggression-related problem when
			forming a heterosexual group of six formerly single-caged subadult
			rhesus macaques. Group members were compatible and showed no serious
			aggression during a nine-week follow-up period. 
			
			   Vicious fighting among adult macaques is a frustrating management
			problem not only when groups are artificially formed, but also when
			excessive aggression develops spontaneously in well-established troops
			(Chance et al 1977; Ehardt & Bernstein 1986 Samuels & Henrickson 1983;
			Reinhardt et al 1987a; Rolland 1991) and is likely to flare up in
			association with sexual competition (Judge et al 1994; Schapiro et al
			1994) and whenever changes are being made in the troop's composition
			(Erwin 1977; Fairbanks et al 1978- Kaplan et al 1980; Kessler et al
			1985; Rolland 1991). 
			 
			Pair housing 
			
			Pair-housing techniques have been developed to avoid the risk of injury
			attendant on group housing. Reinhardt et al (1988a) and Eaton et al
			(1994) tested pairs of previously single-caged adult female rhesus
			macaques. Partners were first familiarized with each other in double
			cages with transparent barriers. Subsequent pair formation was
			successful in 89 per cent (16/18) and 90 per cent (19/21) of cases. In
			both studies two pairs were separated because of fighting. Eaton et al
			(1994) as well as Reinhardt et al (1988a) ascertained partner
			compatibility (cf Table 2) in 83 per cent of cases for 36 and 4 months
			respectively (Table 1). 
			   In an attempt to minimize the typical fighting during the initial
			introduction of partners (cf Maxim 1976), Reinhardt (1989) paired adult
			male rhesus macaques after it was verified that partners had
			established clear dominance-subordination relationships during a
			five-day period of non-contact familiarization. It was hypothesized
			that the establishment of such rank relationships would make aggressive
			disputes rather unnecessary during pair formation (cf Bernstein &
			Gordon 1974), because partners would respect their relative dominance-
			subordination relationships. In order to form five pairs with clear
			relationships, seven different dyads had to be screened. No rank
			decisive interactions (cf Table 2) could be observed in two dyads. The
			partners of the other five dyads established rank relationships within
			the first day of familiarization. When those males were paired in a
			different double cage (a precaution against possible territorial
			antagonism: Reinhardt et al 1988a; Line et al l990a) they confirmed
			their rank relationships within the first six minutes. No fighting, no
			biting and no signs of aggressive harassment or depression were
			observed during a five-day follow-up period. The males were strictly
			housed in male-only areas to exclude the risk of sexual competition
			possibly triggered by the sight of females (cf Coe & Rosenblum 1984;
			Coe 1991). Reinhardt (1994c, d) tested this technique again in other
			rhesus as well as in stump-tailed macaques of both sexes with the
			following results: 
			 
			1 Male rhesus pairs were compatible in 80 per cent of cases throughout
			  follow-up periods of one to five years (Table 1). 
			 
			2 Female rhesus pairs were compatible in 88 per cent of cases during
			  follow-up periods of one to seven years (Table 1). 
			 
			3 All stump-tailed pairs were compatible during pair formation and
			during a six-month follow-up period (Table 1). 
			 
			Crockett et al (1994) formed isosexual pairs of adult long-tailed
			macaques. Potential partners were also pre-familiarized, but no attempt
			was made to ascertain that they had established clear dominance-
			subordination relationships before introduction. During pair formation
			13 per cent of the female pairs, and 67 per cent of the male pairs
			engaged in fighting. Two male dyads were split due to serious injuries.
			Unlike the above mentioned studies, all newly paired subjects of the
			study by Crockett et al (1994) were separated after 90 minutes and
			reunited on the following day. On days 2-13 each pair was separated
			daily for 17 hours and re-introduced thereafter. All female pairs but
			only 40 per cent of the male pairs were compatible throughout the
			two-week study period (Table 1). Clarke et al (1986) also forrned pairs
			of male long-tailed macaques, but allowed partners to continuously stay
			together as long as they did not fight excessively. Pairs were
			compatible in 58 per cent of cases for an eight-month follow-up period.
			Unfortunately, the authors did not elaborate on how partners were
			initially introduced to each other. 
			 
			Table 1     Success rates of pairing techniques for previously
			single-caged adult  macaques. 
			
			Pairing technique/Compatibility/Follow-up/ Subject Macaca/  Reference
			
			 
			prefamiliarization 83% (15/18)  4-6 mths  female mulaffa    Reinhardt
																		et al 1988a
							   92% (11/12)  36 mths   female mulaffa    Eaton et 
																		al 1994 
							   75% (3/4)    5-6 mths  female fascicul   Line et al
																		1990a 
							   100% (15/15) 2 weeks   female fascicul   Crockett
																		et al 1994 
							   40% (6/15)   2 weeks   male fascicularis Crockett
																		et al 1994 
			unknown            58% (7/12)   8 mths    male fascicularis Clarke et
																		al 1986 
			 
			rank-
			relationships      100% (5/5)   5 days    male mulaffa      Reinhardt
																		1989 
			established during 80% (16/20)  1-5 yrs   male mulatta      Reinhardt
																		1994d 
			prefamiliarization 88% (68/77)  1-7 years female mulaffa    Reinhardt
																		1994d 
							   100% (5/5)   6 months  female arctoides  Reinhardt
																		1994c 
							   100% (3/3)   6 months  male arctoides    Reinhardt
																		1994c 
			 
			no familiarization 94% (16/17)  7-11 mths female/infant     Reinhardt
													  mulatta           et al 1987b
			
							   94% (61/65)  1-8 years female/infant     Reinhardt
													  mulatta           1994d 
							   92% (11/12)  7-11 mths male/infant       Reinhardt 
													  mulatta           et al 1987b
			
							   92% (12/13)  1-4 year  male/infant       Reinhardt
													  mulatta           1994d 
			
			Successful isosexual pair formation has been reported for male and for
			female pig-tailed macaques but the actual technique of partner
			introduction has not been published (Reinhardt 1994a) . 
			 
			   As an alternative to adult-adult pairings, Reinhardt et al (1987b)
			socialized previously single-caged rhesus macaques with 1-1.5 year-old,
			naturally weaned infants from breeding troops. It was hypothesized that
			infants of this age would trigger parental responses rather than overt
			aggression in the adults (cf Lorenz 1971; Redican & Mitchell1973;
			Gibber & Goy 1985; Schwind et al 1992). Infants were therefore directly
			placed into the cages of adults of both sexes. Pairs were compatible
			in 90 per cent of cases, with the adult subject huddling with the
			introduced infant, and the latter showing no signs of injury or
			depression. Compatibility was 94 per cent for female-infant pairs, 83
			per cent for male-infant pairs (Table 1). 
			
			   Adult males were as affectionate with juvenile companions as adult
			females (Figure 1). Pair incompatibility was due to non-injurious
			aggression in two cases, a non-bleeding injury in one case. In another
			study, Reinhardt (1994d) ascertained one to eight-year compatibility
			in 94 per cent of female-infant pairs, one to four-year compatibility
			in 92 per cent of male-infant pairs (Table 1). 
			 
			   There is little information about the risk of forrning pairs of
			unfarniliar young macaques. Brandt and Mitchell (1973) paired eight
			pre-adolescent rhesus macaques with eight infants in isosexual and
			heterosexual dyads without encountering aggression related problems
			during a three-week follow-up period. Schapiro et al (1993) transferred
			64 unfamiliarized juvenile rhesus macaques from single-housing to
			heterosexual pair-housing conditions for one year without noteworthy
			problems associated with aggression (cf Schapiro et al 1991; Schapiro
			& Bushong 1994). Weaned rhesus infants have been housed in isosexual
			pairs routinely at the Wisconsin Primate Research Center
			without any aggression related problems. When this manuscript was
			written, the Center had 12 female and 4 male pairs. Partners had 
			been directly introduced to each other with no incidence of serious
			aggression (cf Reinhardt 1994d), and they had lived together as
			compatible companions for up to three years (Figure 2). 
			
			Morbidity 
			
			Schapiro and Bushong (1994) assessed the rates of veterinary treatment
			in 98 rhesus macaques under the conditions of single, pair and group
			housing. Daily treatment per monkey was highest in the group condition,
			lowest in the pair condition, intermediate in the single condition. The
			authors underlined that there was relatively little intervention needed
			for pair-housed animals due to less diarrhoea and little trauma.
			Reinhardt (199Oa) compared rates of veterinary treatment per year of
			237 individually-housed with that of 382 pair-housed rhesus macaques
			that were kept in the same facility. Treatment was required by 23 per
			cent (54/237) of the single-housed, but only by 10 per cent (38/382)
			of the pair-housed subjects. Eaton et al (1994) found no significant
			difference in rates of clinical morbidity in 12 single-housed and 24
			pair-housed female rhesus macaques. 
			
			Distress 
			
			There is no scientific evidence demonstrating that living in a group
			per se causes more distress than living alone. Living with
			conspecifics, however, may provide a buffer against environmental
			stress that the singly caged subject is lacking (cf Bovard 1959; Rowell
			& Hinde 1963; Epley 1974; Cubicciotti & Mason 1975; Cobb 1976; Arnone
			& Dantzer 1980; Gunnar et al 1980; Taylor 1981; Coe et al 1982;
			Gonzalez et al 1982; Hennessy 1984; Stanton et al 1985; Mendoza & Mason
			1986; Lyons et al 1988; de Monte et al 1992). Gust et al (1994), for
			example, removed seven adult female rhesus macaques from their home 
			group and housed them in a novel environment both alone or with a
			member of the group. Subjects experienced measurable distress (elevated
			cortisol concentrations and decrease in absolute number of Iymphocyte
			subsets) in both conditions, but recovered from it significantly
			quicker in the presence of the companion. Shively et al (1989) noted
			in adult female long-tailed macaques that single housing may be a
			greater risk factor for atherogenesis than group housing. Thirty
			individually caged subjects had significantly more extensive
			atherosclerosis in the coronary arteries than 47 group-housed subjects.
			Atherosclerosis extent was four times greater in animals that were kept
			alone than in those that were living in groups. Coelho et al (1991)
			assessed the effect of companionship in four baboons (Papio spp.)
			during a distressing restraint situation. The animals were tested under
			traditional single housing, and under experimental social housing which
			implied that subjects had visual, tactile and auditory contact with
			compatible conspecifics. Being restrained in company with familiar
			social partners resulted in significantly lower resting blood pressure
			and lower heart rates than when being restrained alone, suggesting that
			familiar companionship ameliorated physiological stress responses. 
			 
			   Eaton et al (1994), Crockett et al (1994) and Reinhardt (1994c)
			emphasized that grooming is the salient social behaviour of compatible
			macaque pairs, and that companions show agonistic interactions only
			rarely but have a strong preference to stay in close proximity to 
			one another (cf Washburn et al 1994). These observations indicate that
			compatible companionship is a source of comfort rather than distress.
			
			   Schapiro et al (1993) were unable to detect significant differences
			in cortisol response to single versus pair housing in 64 juvenile
			rhesus macaques. This finding supports results of Reinhardt et al
			(1991) who examined serum cortisol concentrations of single-housed and 
			compatible pair-housed adult rhesus macaques. In both sexes, cortisol
			concentrations of isosexually paired animals (ten females, ten males)
			showed no significant differences with those of single animals (five
			females, five males). Both in female and in male pairs, dominant
			partners had cortisol concentrations that were equivalent to those of
			their subordinate counterparts (females: 19.5 yg dl-' vs 19.4 ,ug dl-';
			males: 17.5 ,ug dl-' vs 17.2 ,ug dl-'). These data corroborate those
			of Crockett et al (1994) who found no evidence of elevated levels of
			urinary cortisol in response to compatible pair housing versus single
			housing in ten adult female long-tailed macaques. 
			
			   Eaton et al (1994) assessed immune stress responses in adult female
			rhesus macaques when being single-housed (n = 45) versus pair-housed
			(n = 24) with a compatible partner. Lymphocyte proliferation response
			did not decline after pairing and showed no difference between dominant
			and subordinate members of pairs. The analysis of behavioural profiles
			complemented this finding, suggesting that subordinates were not
			stressed by the experience of pairing. Coe (1991) reported a decrease
			in Iymphocyte proliferation response in old rhesus macaques when being
			transferred from single housing to pair or group housing with
			juveniles. These physiological observations are in line with
			ethological records by Reinhardt and Hurwitz (1993) showing that
			pair-housed aged rhesus macaques have to discipline their sometimes all
			too frisky young companions. The authors therefore recommended that
			pairs should be split in the event of excessive disturbance of the aged
			subjects by their young cagemates. 
			
			   Taking the expression of gross behavioural disorders as signs of
			distress, compatible companionship may have a therapeutic effect
			(Harlow & Suomi 1971; Brandt & Mitchell 1973; Bushong et al 1992). Line
			et al (199Ob) observed self-abusive behaviours in five female
			long-tailed macaques and noted cessation of this disorder in all cases
			after the animals had been transferred to compatible pair housing for
			five to six months. Reinhardt et al (1987b) noted bizarre stereotypical
			behaviour patterns in three singly-housed adult female rhesus macaques.
			All three animals were paired with infants and gradually abandoned
			their peculiar habits within four months of social housing. Bloomsmith
			and Schapiro (1994 personal communication) noted that pair housing
			previously single-caged juvenile rhesus macaques, significantly reduced
			the percentage of time that was spent by the subjects engaged in
			self-aggressive activities. Ruppenthal et al (1991)observed
			stereotypies in individually caged but not in pair-housed pig-tailed
			infants. 
			
			   Social housing need not be distressing for laboratory non-human
			primates, however, involuntary separation from familiar companions for
			routine management or experimental reasons may be a disturbing
			experience (Redican & Mitchell 1973; Willott & McDaniel 1974; Suomi et
			al 1975; Reite et al 1981; Rasmussen & Reite 1982; Coe 1991; Mendoza 
			1991; Gordon et Ql 1992), as is the involuntary removal from the
			familiar home-cage (Mitchell & Gomber 1976; Holm 1979; Line et al
			1989b; Line et al 1991). Allowing partners continually to keep visual
			and/or auditory contact during physical separation is likely to
			minimize their stress response (cf Gust et al 1994; Table 2). 
			
			Table 2    Ethological guidelines to avoid aggression during and after
					   pair formation of previously single-caged adult macaques of
					   the same sex. 
			 
			1    Allow potential panners to establish clear dominance-          
			subordination relationships during a non-contact familiarization     
			period. This is a basic condition so that the animals will be able   
			  to live together in harmony. 
			 
			2    Check for signs of an established rank relationship, such as    
			 unidirectional fear-grinning, withdrawing, looking away,     
			threatening-away and absence of reciprocal threatening. 
			 
			3    Pair panners only after they have established their rank     
			relationship. This will give them no reason to fiRht over      
			dominance. 
			 
			4    Pair partners in a different double cage. This avoids possible  
			   territorial antagonism. 
			 
			5    Do not force animals to live together when they are incompatible.
				 Signs of incompatibility are serious injury, persistent fighting,
				 aggressive harassment, depression and inadequate food sharing. 
			 
			6    Keep male pairs in male-only areas. This avoids sexual     
			competition possibly triggered by the sight of females. 
			 
			7    Let a new pair live together continuously for at least one month.
				 This allows them to establish a stable social relationship. 
			 
			8    If partners have to be physically separated thereafter, allow   
			  them to keep continual visual and auditory contact. This minimizes
				 the possible stress associated with separation. 
			 
			9    If partners have to be housed in different rooms for more than  
			   one week, do not simply re-unite them in their home-cage     
			thereafter, but give them the opportunity to briefly recognize     
			each other across a temporary transparent cage divider. This is 
				 a safeguard that the animals will not treat each other as     
			strangers, ready to fight over dominance. 
			 
			10   Never threaten or scare the animals. This could excite them so  
			   much that they redirect the triggered aggressive tension toward   
			  each other. 
			
			Undernourishment 
			
			Eaton et al (1994) compared body weight developments of adult female
			rhesus macaques and found no differences between single-housed (n = 12)
			versus pair-housed subjects (n = 24), nor between dominant and
			subordinate partners of compatible pairs. Reinhardt et al (1988b)
			assessed body weight developments of 28 adult female rhesus macaques
			in the month before pairing, and in the first two months after
			formation of 14 compatible pairs. Compared with the pre-pairing
			situation, dominant partners showed no significant change in body
			weight during the first two months, while subordinates exhibited a
			significant increase in weight in the second month. Reinhardt and
			Hurwitz (1993) recorded body weights of eight aged rhesus macaques (six
			females, two males) one year prior to being paired with compatible 
			companions, at the day of pairing, and again one year after pairing.
			The aged animals were so old (31-36 years) that they experienced a
			gradual loss in body weight. Living with a companion did not accelerate
			this biological process: average yearly body weight balances were -4.4
			per cent in the year prior to pairing, -4.2 per cent in the year after
			pairing. Reinhardt et al (1987b, 1989) include food sharing between
			partners as one criterion of pair compatibility to guarantee that
			subjects obtain their adequate shares of the daily food ration (cf
			Table 2). 
			 
			Maladaptation 
			 
			Chamove et al (1973) 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 1973). Ruppenthal et al (1991) 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 14-28 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. Unlike single subjects, paired subjects exhibited no 
			rock/huddle/self clasp and stereotypic behaviour patterns, but instead
			spent significantly more time playing with toys. 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. 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 (1994) 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. 
			
			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, 295 adult rhesus
			macaques of both sexes assigned to research, were successfully
			transferred from single housing to permanent isosexual pair housing
			with each other (102 pairs) or to pair housing with infants (91 pairs).
			This socialization programme was associated with serious, yet not life
			threatening wounding in only less than 1 per cent (3/386) of animals
			(Reinhardt 1991b). 
			 
			   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. The relatively high degree of aggressive
			incompatibility found in male long-tailed macaques (Crockett et al
			1994; cf Goosen et al 1984; Whitney & Wickings 1987) could probably be
			attenuated as in rhesus and stump-tailed males (Reinhardt 1994c,d), if
			partners were allowed: a) to establish rank relationships during
			prefamiliarization, and b) to stay together continuously rather than
			intermittently thereafter. 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 1973) . Goosen et al (1984)
			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 1991). 
			b) animals should not be forced to live with each other if observable
			   and/or measurable evidence indicates that they are incompatible (cf
			   US Department of Agriculture 1991). 
			c) companions should have the option of moving into temporary visual
			   seclusion (Goosen et al 1984; Whitney & Wickings 1987; O'Neill 1989;
			   Taff & Dolhinow 1989; Reinhardt & Reinhardt 1991). 
			d) male companions should be housed in male-only areas to prevent   
			sexual competition (Reinhardt 1992a). 
			e) social relationships should not be disrupted to avoid possible   
			distress triggered by involuntary separation from familiar   
			conspecifics (cf Gordon et al 1992). 
			 
			It has been shown that groups/pairs can be successfully trained to
			voluntarily separate for common procedures such as blood collection
			(Bunyak et al 1982; Vertein & Reinhardt 1989; Clarke et al 1990;
			Reinhardt & Cowley 1992), faeces collection (Phillippi-Falkenstein &
			Clarke 1992), systemic drug administration (Reinhardt 1992c), topical
			drug application (Reinhardt & Cowley 1990), vaginal swabbing (Bunyak
			et al 1982), tethering (Reinhardt 1991b), and headcap implantation
			(Reinhardt 1991b). Socially housed animals can readily be conditioned
			to allow capture in transport boxes (Smith 1981; Boccia et al 1992;
			Reinhardt 1992b; Luttrell et al 1994). If an animal has to be kept
			singly for a limited time period (ie metabolic studies, feeding
			studies, urine collection, post-operative recovery, experiments
			involving chair restraint) a compatible companion can be kept close by
			behind a transparent barrier allowing visual and/or acoustic social
			contact (cf Reinhardt et al 1989; Coelho et al 1991). 
			   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 1973). The cause of this behavioural problem is obviously not 
			the social peer-housing condition but the absence of the biological
			mother (cf Mason 1991). This notion is supported by findings of
			Alexander (1966) 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. Partners of compatible macaque pairs spend
			approximately 1/5 of their time interacting with each other in
			affiliative ways typical for the species (Ranheim & Reinhardt 1989;
			Reinhardt 1990b; Line et al 1990a; Reinhardt & Hurwitz 1993; Crockett
			et al 1994; Eaton et al 1994; Reinhardt 1994c; Schapiro & Bloomsmith
			1994). This is compatible with the situation in groups containing
			animals of both sexes and different ages (Rhine & Kronwetter 1972; Post
			& Baulu 1978; Bernstein 1980; Teas et al 1980; O'Keeffe & Lifshitz
			1985; Chopra et al 1992; Leon et al 1993), and suggests that being
			transferred from single to pair housing improves theanimals'
			behavioural health by providing them with an appropriate environment
			for the expression of their social disposition (Reinhardt 1987). 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 1990b). 
			 
			   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 1994b). 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. Such
			variables are: technique of partner introduction, sex, age, rearing
			history, social experience, health status, research protocol, animal
			caregiver/technician, feeding regime and physical environment. 
			
			   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. 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. 
			 
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