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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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