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Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys.

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American Journal of Primatology 3215S170 (1994)
RESEARCH ARTICLES
Behavioral Effects of Enrichment on Pair-Housed
Juvenile Rhesus Monkeys
STEVEN J. SCHAPIRO AND MOLLIE A. BLOOMSMITH
University of Texas M . D. Anderson Cancer Center, Science Park, Department of Veterinary
Resources, Bastrop, Texas
Among captive primates, inanimate environmental enrichment can lead
to measurable changes in behavior indicative of an improvement in psychological well-being. Although this has been demonstrated repeatedly for
singly caged primates, the relationship is not as well studied for pairhoused animals. Study of the pair-housed setting has become increasingly
relevant because of the social housing mandate of the Animal Welfare Act
regulations. We therefore observed 68 juvenile rhesus monkeys born in
1988 and 1989 and living in mixed-sex pairs from the ages of 2 to 3 years.
All pairs were compatible. Half of the pairs received two types of enrichment, while the remaining pairs served as controls. Enriched and control
juvenile subjects differed in the amount of time that they spent being
inactive, playing, and drinking, but did not differ in the amount of time
they spent interacting with their partner. Grooming and play were the two
most common socially directed activities in both groups, a species-appropriate pattern. Males played more and vocalized less than did females.
Overall, enriched and control subjects spent equivalent amounts of time
located within a social distance of one another, but there was some difference between groups in allocation of behaviors while near the pairmate.
Environmental enhancers were frequently utilized, and led t o relatively
small changes in behavior between control and enriched subjects, suggesting that the presence of a partner for juvenile rhesus monkeys acts as a
form of enrichment that may dilute the effects of inanimate environmental
enhancements. o 1994 Wiley-Liss, Inc.
Key words: environmental enrichment, pair-housing, rhesus monkeys,
psychological well-being
INTRODUCTION
Recent legislation mandating the enhancement of captive primates’ environments raises an important question: Which enhancements are most effective, not
only in terms of the primates’ psychological well-being but also in terms of cost?
Cost-effectivenessis not the primary concern, but ineffective measures are a waste
of scarce resources and should be replaced with measures that more effectively
enhance the social, physical, and occupational needs of captive primates. It is
Received for publication October 30, 1992; revision accepted July 27, 1993.
Address reprint requests to Steven J. Sehapiro, Ph.D., University of Texas M.D. Anderson Cancer Center, Science Park, Department of Veterinary Resources, Route 2, Box 151-B1, Bastrop, TX 78602.
0 1994 Wiley-Liss,Inc.
160 / Schapiro and Bloomsmith
therefore imperative that the effects of various environmental enhancements be
studied in detail. Although many such studies have already been conducted [e.g.,
Bayne et al., 1991; Bloomsmith et al., 1988; Line & Morgan, 19911 and reviewed
[Fajzi et al., 19891, one area that has yet to receive adequate attention is that of
pair-housed primates. Few studies have reported on environmentally enriched
pairs nor have many discussed comparisons of social and nonsocial enrichment for
the same animals [except see Reinhardt, 19901. Our study therefore focused on two
factors: nonsocial enrichment and pair housing.
Nonsocial, or “inanimate,” enrichment often takes the form of providing primates with inanimate objects that encourage species-typical behavior. Many studies of inanimate enrichment have shown behavioral changes indicative of improved
psychological well-being as defined by increases in species-typical behavior [e.g.,
Bayne et al., 1991; Bloomsmith et al., 1990; Bryant et al., 1988; Novak & Drewsen,
1989; ONeill et al., 19911. It has been argued that increases in species-typical
behaviors and decreases in atypical behaviors are indicators of improved psychological well-being [Line, 1987; Novak & Suomi, 19881.Therefore, if the behavior of
captive primates can be affected to more closely approximate the behavioral patterns of their free-ranging counterparts, these changes will be judged as evidence
of improved psychological health. Particularly in situations of social restriction,
physical, feeding, and occupational enhancement procedures have been shown to
increase the amount of species-typical behavior andlor decrease the amount of
abnormal behavior displayed by primates [e.g., Bayne et al., 1991; Bloomsmith et
al., 1990; Bryant et al., 1988; Fajzi et al., 19893. Even among primates housed in
social groups, inanimate enrichment has produced similar beneficial changes
[Bloomsmith et al., 1988; Byrne & Suomi, 1991; Chamove et al., 19821.
Housing primates in pairs is not new [Brandt & Mitchell, 1973;Chamove, 1973;
Harlow, 19631, but the current climate emphasizes pair housing as a potential
improvement over single housing, since pair housing provides opportunities for
social interaction. Although many attempts to pair monkeys have worked out quite
well [Crockett et al., 1991; Eaton et al., 1991, 1992; Line et al., 1990; Reinhardt et
al., 1988;Reinhardt, 19891,others have not been as successful [Chamoveet al., 1973;
Ruppenthal et al., 19911. The clear message is that a universal enrichment procedure of pairing primates will not be appropriate across all ages, all species, or in all
settings. In general, pairs of animals in which both members are not infants [Brandt
& Mitchell, 1973; Crockett et al., 1991; Eaton et al., 1991; Line et al., 1990;
Reinhardt, 19891are likely to be more successfulthan pairs formed with two infants
[Chamove et al., 1973; Ruppenthal et al., 19911. From a management point of view,
then, there will be situations in which it is appropriate to house animals in pairs
because it improves psychological well-being, and there will be situations in which
pairing will actually diminish psychological well-being. This caution does not necessarily preclude a pairing that is an atypical social grouping for a particular species
(e.g., adult male-infant pairs, adult female-adult female pairs, etc.).
In the present investigation, we sought to determine whether physical and
feeding enrichment of pair-housed juvenile rhesus monkeys was effective, and
whether it was necessary to provide subjects with both social and inanimate enrichment, using enriched and control pairs of subjects.
MATERIALS AND METHODS
Specific Pathogen-Free (SPF) Breeding Program
This study was conducted on juvenile rhesus monkeys that were part of the
SPF breeding program at The University of Texas M. D. Anderson Cancer Center,
Science Park. Using a progressive program of social and housing manipulations,
Enrichment and Pair-Housed Juveniles / 161
the traditional breeding colony is being converted into a colony that is free of
Herpesvirus simiae, SIV, SRV, and STLV [Voss et al., 19911. Infants were left in
their natal groups for 1 year, were then housed in single cages for a year, which
was followed by a year of housing in mixed-sex pairs. The final step in the derivation strategy was to form unimale breeding groups at 3 years of age from the
formerly paired animals. The process of socialization (first year), followed by restriction (second year), followed by gradual resocialization (third year), prior t o full
social integration (fourth year) was specifically designed to minimize both viral
transmission and long-term behavioral disturbance. The goal was to build an SPF
colony with good reproductive abilities.
Subjects and Housing
Two groups of rhesus monkeys (Macaca mulattu) served as subjects. Group 1
consisted of 34 juveniles (18 males, 16 females) born in 1988 and Group 2 comprised another 34 juveniles (17 males, 17 females) born in 1989. All lived in ageand sex-matched pairs for the entire year of the study and all pairs formed were
compatible. For each group, half of the animals received an environmental enrichment program, and half served as controls, receiving no environmental enrichment. Although control subjects could see the enrichment devices when they were
brought to the experimental subjects, most had only limited sensory access to
subjects actually using enrichment. All subjects were provided with monkey biscuits twice daily, were given half of an orange three times per week, and had water
available ad libitum. Subjects were housed in rack-mounted Harford stainless steel
cages (88%had 8.2 square feet of floor space; the remainder had 6.2 square feet)
with sensory access to similarly housed subjects. They lived in an outdoor building
with sensory access to group-housed as well as pair-housed conspecifics and were
exposed to natural variation in environmental conditions.
Enrichment
Enriched subjects simultaneously received physical and feeding enrichers.
Physical enrichment consisted of the continuous availability of two chain perches,
one with an attached plastic rattle, a hard toy and a chewable toy, and a piece of
fleece. The goal of these enhancements was to provide the subjects with objects
that might stimulate species-typical behavior related to manipulating, climbing,
and playing. Feeding enrichment consisted of five different enhancements presented throughout each workday, with the order of presentation of enhancements
rotated daily. Three enrichment devices used were an astroturf foraging mat [similar to Bayne et al., 19921,a polyvinyl chloride (PVC) foraging tree [Schapiro et al.,
19911, and an acrylic food puzzle [Schapiro et al., 19911, each filled with 20 g of
popcorn, peanuts, sunflower seeds, or corn. The two other feeding enhancements
were a 100-ml cup of frozen juice and 125 g of fresh produce (50 g of vegetable and
75 g of fruit). The flavor of the juice and the specific produce items were changed
weekly. Two devices or two portions of each feeding enhancer were presented a t a
time to every pair, except in the case of the PVC foraging tree. On weekends and
holidays, an abbreviated enrichment routine was followed in which pairs received
only one set of enrichment devices (either the PVC trees, acrylic puzzles, or most
frequently, the astroturf mats) and the regular orange supplement. The goal of
giving these enhancements was to provide situations that required the animals to
work to obtain food and to supply novel foods that required time to process and
consume.
162 / Schapiro and Bloomsmith
Data Collection
Fifteen-minute focal animal observations [Altmann, 19741were conducted on
all subjects from ages 2 to 3 years. Four hundred and sixty hours of observations
were conducted on Group 1 between May 1990 and May 1991, and 465 hours of
observations were conducted on Group 2 between May 1991 and May 1992. Data
were collected using a Tandyo 102 portable computer and The Observer@[Noldus,
19911, an observational software package. Data were collected between 0830 and
1730 h throughout the year, were balanced for time of day, and included periods
during which feeding enrichments were “full,” “partially full,” and “empty.” Abnormal and social behaviors were emphasized on the ethogram of mutually exclusive behaviors (see Table I). Interobserver reliability for cumulative durations of
behaviors within observation sessions was measured monthly for a total of four
observers and the Kappa coefficient [Martin & Bateson, 1986; Hollenbeck, 19781
averaged 230.
In addition to recording the behavior of the subjects, the following measures
were recorded simultaneously: location in relation to the pairmate (social location),
whether the behavior was directed a t the cagemate (social direction), and whether
enrichment was being used (enrichment use). Operational definitions of these conditions appear in Table I. Interobserver reliability as measured by the Kappa
coefficient averaged 234, .83, and 3 0 for social location, social direction, and enrichment use, respectively. The Observer program allows for analyses of combinations of behaviors and conditions (e.g., socially located, socially directed grooming;
or nonsocially located, self-directed play, etc.) and thus social location, social direction of behaviors, and enrichment use included occurrences of more than one of
the previously mentioned, mutually exclusive behavior categories.
Data were analyzed using multivariate analysis of variance (MANOVA)techniques within the Systat@statistical package. Individual behaviors from the ethogram were grouped into the categories of activity outlined in Table I. The dependent measures used in the analysis were the cumulative durations of each activity
category for each subject during the entire year of pair housing, resulting in a total
of 68 data points per activity (35 enriched subjects, 33 controls). The two extra
enriched animals resulted from the replacement of an enriched pair with a new
pair midway through the study.
A 2 x 2 x 2 MANOVA examining group (1 or 2), treatment (enriched or
control), and sex (male or female) effects on the mutually exclusive categories of
activity was performed. In addition, separate 2 x 2 x 2 ANOVAs were conducted
for the same effects on social location and on social direction of behavior. Separate
ANOVAs were necessary to prevent skewing of the main analysis since these
conditions represented combinations of the mutually exclusive behavior categories.
RESULTS
The overall multivariate test was significant [Pillais = .47; P 5 .0011, and
comparison of enriched subjects to controls showed a significant difference based
on the experimental treatment [F(9,52) = 5.0, P 5 .0011. Subsequent univariate
tests indicated that enriched subjects spent significantly more time being inactive
[F(1,60) = 9.5, P 5 .011, more time playing [F(1,60) = 7.6, P 5 .011, and less time
drinking [F(1,60) = 8.0, P 5 .01] than did controls (see Table 11). Control and
enriched subjects did not differ in durations spent in any other activities, nor did
they differ in time spent located near or interacting with their partner. Abnormal
behavior was infrequent in all groups. Group 1and Group 2 animals did not differ
Enrichment and Pair-Housed Juveniles I 163
in any activities. Male subjects played significantly more than did females [F(1,60)
= 5.2, P 5 .05] and vocalized significantly less [F(1,60) = 20.8, P 5 .001]. There
were no significant two-way or three-way interaction effects.
The specific activities that comprised the categories of socially directed behavior and socially located activity were identified. Table I11 contains the mean
amount of time spent in each category and the distribution of some behaviors
within these categories.
Enrichment items were used frequently (mean use was 24.0 min per h),
whereas slightly less time was spent near a partner (mean of 22.8 min per h for all
subjects) or interacting with the partner (mean of 12.5 min per h for all subjects).
For both control and enriched subjects, feeding was rarely, but inactivity was
frequently, engaged in within a social distance of the cagemate. All subjects spent
less than one-fifth of their feeding time within 8 cm of their partner, and enriched
subjects spent about 1min less per h feeding near the partner than did controls.
DISCUSSION
The combination of feeding and physical enhancements provided to enriched
subjects affected their behavior when compared to the control subjects, but the
effects were neither as widespread nor as large as enrichment effects have been for
singly caged rhesus [Bayne et al., 1991; Bryant et al., 19881.Although these effects
were statistically significant, whether they are of practical significance is a question. It may be possible t o address the issue of practical significance by examining
how subjects choose to alter their behavior in response to enrichment. Age-related
influences on the effects of enrichment [O’Neill et al., 19901 have been documented, thus these findings apply most specifically to rhesus monkeys between the
ages of 2 and 3 years.
Enriched subjects played for durations approaching those typical of rhesus
juveniles in the wild [Lindburg, 19711. Enrichment successfully promoted play
among these juvenile subjects, and this change was of a desirable behavior in a
species-typical direction, and therefore indicated an improvement in psychological
well-being [Line, 1987;Novak & Suomi, 19881. Control and enriched subjects spent
similar amounts of time feeding, a finding inconsistent with previous feeding enrichment studies for singly or group-housed subjects [Bayne et al., 1991; Bloomsmith et al., 1988; Byrne & Suomi, 1991; Chamove et al., 19821. Many of these
studies used subjects as their own controls, increasing the likelihood of post-test
behavioral changes in response to the removal of enrichment (the rebound effect
discussed by Bayne & Dexter [ 19921). Additionally, many were considerably
shorter in duration than the present investigation, providing less opportunity for
the attractiveness of feeding enhancement to diminish. Enriched subjects in the
present investigation were presented with five feeding enhancements every workday for a year, and each contained only a limited quantity of food. The long duration and the cumulative frequency with which the enhancements were encountered may account in part for not achieving the major goal of increasing time spent
feeding.
The discrepancy between control and enriched groups in the amount of time
they spent feeding within a social distance of their partner is evidence for competition between pairmates for enrichment foods. Dominant control monkeys attempted to get as many orange pieces as possible, and when the subordinate was
able to get some orange, it would often move away to eat alone. This pattern of
competitive, solitary eating of a desirable food, supplied in limited quantity, was
more frequent among enriched subjects, who were provided with numerous treats
each day. Despite this pattern of feeding alone, enriched subjects spent as much
164 I Schapiro and Bloomsmith
TABLE I. Categories of Behaviors Analyzed, Behaviors Recorded, and
Operational Definitions
Mutually exclusive categories of behavior
Inactivity
Sitting with no discernible focus of attention
Sit
Sitting or lying down with eyes closed
Sleep
Sexual
Abnormal sexual behavior Sexual behavior that is improperly conducted
Oral or manual manipulation of the genitals
Masturbate
A male mounting a partner with a properly oriented
Normal sexual behavior
double-foot-clasp mount; the female equivalent of normal
(given)
sexual behavior given would be “present”
A female being properly mounted by a male
Normal sexual behavior
(received)
Drinking
Ingestion of water
Drink
Grooming
Normal care behaviors of the animal’s body surface
Groom (self)
Normal care of another animal’s body surface by the focal
Groom (given)
animal
Receipt by the focal animal of normal care of the body surface
Groom (received)
by the pairmate
Feeding
Ingestion of food items, including chewing
Eat
Manual manipulation of food items or food sources not directly
Forage
related to putting food in the mouth
Playing
Includes some or all of the following: swinging by all or a few
Play
limbs, rolling around, shaking, jumping, and/or gymnastics;
when enrichment devices are involved (toys, etc.), play
includes behaviors other than manipulating or directed
locomotion with the device; when a social partner is involved,
play includes chasing, wrestling, play fighting, etc.
Abnormal behaviors
The ingestion of urine from hands, cage structures, or directly
Urophagy
Focal animal performs extremely directed pulling out of own or
Pick (given)
partner’s hair or skin
Self-explanatory
Suck digit
Raising and pressing hand to the eye on the same side of the
Salute
head
Undirected, repetitive locomotor activity
Pace
Exaggerated throwing of the head when encountering a
Head toss
barrier, such as a cage wall
Ingestion of feces or materials picked from feces
Coprophagy
Self-directed “ h a r d biting or hitting
Aggression (self)
A catch-all category to record all other types of abnormal
Abnormal (other)
behavior, including bowing, crouching locomotion, bizarre
postures, etc.
Explore
Snifling a n object or pairmate
Olfactory explore
Visual exploration of the inside of the cage and/or its contents,
Investigate
including the pairmate
Visual exploration of the environment outside of the cage
Look
Vocalization
Self-explanatory, analyzed by frequency
Vocalize
(Continued)
Enrichment and Pair-Housed Juveniles I 165
TABLE I. Categories of Behaviors Analyzed, Behaviors Recorded, and
Operational Definitions (Continued)
Simultaneously recorded information
Enrichment use includes whenever the focal subject is in
Enrichment use
contact with or has its attention focused on a n enrichment
item
Socially directed behavior
All behaviors that are directed at a pairmate or directed a t
Socially directed
the focal subject by a pairmate
All behaviors that are not directed at the pairmate
(Nonsocially directed)
Socially located
When the focal subject is less than 8 cm from the pairmate
Social location
TABLE 11. Mean Durations Spent in Selected Activities, Comparing Enriched to
Control Subjects Across G r o u p s (in minutes/observation hour)+
Group 1
Activity
Inactivity
Sexual behavior
Drinking
Grooming
Feeding
Playing
Abnormal behavior
Exploration
Vocalization
Enrichment use
Socially directed behavior
Socially located
Group 2
Average
Control
Enriched
Control
Enriched
Control
Enriched
2.67
0.31
2.56
10.00
19.71
2.83
2.26
9.87
20.42
0.00
11.85
22.01
3.70
0.72
2.20
9.95
16.77
3.28
1.89
8.66
17.52
26.78
12.55
21.63
2.70
0.46
2.95
12.93
16.52
2.37
2.06
9.63
21.22
0.00
13.23
23.90
4.82
0.38
1.85
10.14
16.35
3.51
1.87
9.16
19.79
21.31
12.46
23.55
2.67*
0.38
2.75*
11.42
18.17
2.61*
2.16
9.75
20.80
0.00
12.52
22.90
4.27
0.55
2.02
10.04
16.56
3.40
1.88
8.92
18.69
23.97
12.50
22.62
+Activity will not sum to 60 min.
*Frequency of occurrence.
*P 5 0.01 for comparison of enriched to control
time as controls within a social distance of, and interacting with, their partner,
thus they seemed to compensate for eating alone by spending more time near each
other during nonfeeding activities. Feeding enrichment programs have been
shown to decrease levels of some positive social interactions [Bloomsmith et al.,
19881 (social play and social grooming specifically [Byrne & Suomi, 19911).Therefore, feeding enrichment may not be effective for achieving goals of increased
levels of social interactions, which are sometimes used as indicators of improved
psychological well-being.
The enrichment program did not affect the amount of time that subjects spent
near their pairmate, but it did influence the allocation of socially located activities
across treatment conditions. Enriched subjects actively altered their patterns of
social location as their own behavior changed. Enriched subjects spent significantly more time being inactive (sitting and sleeping) than did controls, yet the
implications for psychological well-being of increased inactivity are not clear.
Rhesus monkeys in natural conditions spend time being inactive [Lindburg, 19711,
and many enrichment programs strive to emulate natural behavior patterns, yet
few enrichment programs aim to increase inactivity (nor do they aim to increase
166 / Schapiro and Bloomsmith
TABLE 111. Partial Breakdown of Socially Directed Behavior
and Behaviors Performed While Socially Located (in
minutes/observationhour)
Socially directed behavior
Total
Social grooming
Social play
Other
Socially located behavior
Total
Feeding
Inactivity
Other
Control
Enriched
12.52
6.70
2.38
3.44
12.50
7.08
2.72
2.70
22.90
3.16
2.52
17.22
22.62
2.24
4.06
16.32
aggression or other natural, but undesirable, activities in the captive setting).
Since most of the inactive time was also spent near the partner (over 94% for all
pairs), enriched subjects spent an additional 1.5 min per h being inactive but near
their partner to compensate for the extra 1min per h they spent eating alone. Even
though the number of minutes of behavioral change was not large, this evidence
for behavioral compensation suggests that these changes were functionally significant to the subjects.
Enriched subjects spent significantly less time drinking than did control subjects. Again the implications for such a behavioral change in relation to psychological well-being are unclear. It is possible that the extra produce and frozen juice
that enriched subjects were given decreased their requirement for water.
The enrichment program did not influence the amount of time that subjects
spent interacting with one another. This is contrary to several other studies that
have reported changes in social interactions for socially housed primates as a
function of feeding enrichment in designs where subjects served as their own
controls [Bloomsmith et al., 1988; Byrne & Suomi, 19911. Studies using separate
control groups eliminate the possibility of behavioral changes in response to the
discontinuation of enrichment (rebound effects [Bayne & Dexter, 19921).The constant availability of both the same partner and inanimate enhancements over a
1-year period may account for the lack of an observed effect on social interactions.
Social grooming and social play accounted for over 80% of all socially directed
behaviors for all groups, a pattern that is typical of juvenile rhesus monkeys living
in other settings [Caine & Mitchell, 1979; Lindburg, 1971; Sade, 19721.
The findings of more play behavior and less frequent vocalizations for male
subjects than for females were compatible with previous examinations of sex differences in young rhesus. These studies examined subjects with rearing histories
that varied from social isolation to natural conditions [Baysinger et al., 1972;
Hinde & Spencer-Booth, 1967; Lindburg, 1971; Mitchell, 19791, a range that would
cover the present subjects who were reared socially, later socially restricted, and
then gradually resocialized. The SPF derivation program does not appear to prevent the development of normal sex differences in behavior.
There were several factors that contributed to the success of the pairing phase
of this derivation program. All pairs were compatible, there was little abnormal
behavior, and there were fewer injuries or health problems among pairs than
among singly or group-housed subjects [Schapiro & Bushong, in press]. The social
restriction for 1 year that preceded pair housing may have increased the subjects’
probability of interacting amicably with a peer. Two other possible influences were
Enrichment and Pair-Housed Juveniles / 167
the age of the subjects (about 2 years at initial pairing) and their early social
experience during the first year in the natal group. Studies have documented that
social groups of rhesus monkeys are easier to form with young animals and those
that are already socially experienced [Bernstein, 1991; Bernstein & Draper, 1964;
Bernstein et al., 19741. Infants, although young, may not have the requisite social
experience to be successfully paired with one another [Chamove et al., 1973; Ruppenthal et al., 19911. Our findings suggest that 2- to 3-year-old rhesus with some
social experience could be easily pair housed in many laboratory settings. Several
other laboratories have demonstrated that rhesus monkeys in various age-sex
combinations can be successfully pair housed [Brandt & Mitchell, 1973; Eaton et
al., 1991, 1992; Reinhardt, 1989; Reinhardt et al., 19881.
Although inanimate environmental enrichment had some beneficial effects for
pair-housed juveniles, the magnitude of behavioral changes observed was less than
usually seen in studies of enrichment involving singly-housed animals [Bayne et
al., 1991; Bryant et al., 19881, and more specifically, abnormal behavior was not
affected by enrichment. Even though subjects had been socially restricted during
the preceding year, abnormal behavior was still infrequent. Most behavior categorized as abnormal was pacing, although some animals maintained infrequent
and idiosyncratic stereotyped behavior that developed while singly caged. The
presence of the pairmate may have diluted the effects on behavior of the perches,
food puzzles, etc. Social enrichment is generally considered to be the most beneficial [but see Coe, 1991 and Ruppenthal et al., 19911 enrichment option [Bayne,
1991; Bramblett, 19891, because species-typical behaviors are expressed to the
greatest extent when conspecifics are available. Socially directed activities were
expressed by paired monkeys at levels typical for rhesus juveniles [Lindburg,
19711, even among control subjects in unenhanced cages. Except for an increase in
play as a function of the inanimate enrichment program, there were few behavioral changes measured that could easily be interpreted as influencing psychological well-being.
Line and Morgan [1991] suggest that measuring the effect of enrichment on
psychological well-being is better served by analyses of behavioral change than by
simple analyses of enrichment use. While this is reasonable, the current study
provides an interesting counterpoint; enrichment was used during 40% of observation time yet did not lead to large-scale behavioral changes. Pair-housed subjects
actually spent more time near their enrichment than they did near or interacting
with their partners, emphasizing the attractiveness of the enhancements employed. Inanimate enrichment may not alter behavioral durations for paired primates as it does for those that are singly-housed, but it still can provide important
behavioral options for laboratory monkeys, and cost-effective enhancements
should be implemented.
CONCLUSIONS
1. A combination of physical and feeding enrichment increased the time spent
playing and being inactive, decreased the amount of time spent drinking, but did
not affect durations spent feeding in juvenile pair-housed rhesus monkeys.
2. Male subjects housed in pairs spent more time playing and vocalized less
frequently than did female subjects.
3. Time spent interacting with or near the partner did not differ across treatment conditions, but enriched subjects compensated for time spent eating enrichment foods alone by spending more time inactive near the partner than did controls.
168 / Schapiro and Bloomsmith
4. Inanimate enrichment was well-used and potentially beneficial in the
paired captive setting, but was not as effective at improving psychological wellbeing as inanimate enrichment has been for socially restricted subjects.
ACKNOWLEDGMENTS
We thank A. Kessel, D. Bushong, and D. Oubari for their dedicated collection
of data, K. Vela and D. Glasgow for their data management efforts, and J. McMahan and M. Smith for providing the enrichment. This work would not have been
possible without the support of M.E. Keeling, D.V.M., and the primate section
staff. Thanks also to K. Flynn a t Scientific Publications, M. D. Anderson Cancer
Center, for editing advice. Animals are maintained in facilities approved by the
American Association for Accreditation of Laboratory Animal Care and in accordance with current United States Department of Agriculture, Department of
Health and Human Services, and National Institutes of Health regulations and
standards. Financial support for this project came from the National Institutes of
HealthiNCRR grants U42-RRO5080 and R01-RR05092.
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