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Effects of woodchips and buried food on behavior patterns and psychological well-being of captive rhesus monkeys.

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American Journal of Primatology 23:141-151 (1991)
RESEARCH ARTICLES
Effects of Woodchips and Buried Food on Behavior
Patterns and Psychological Well-Being of Captive
Rhesus Monkeys
GAYLE DIGREGORIO BYRNE AND STEPHEN J. SUOMI
Laboratory of Comparative Ethology, NICHD, Bethesda, Maryland
The effects of adding woodchip litter to bare-floored pens, burying monkey
chow in the woodchips, and scattering sunflower seeds in woodchips was
studied in 2 stable social groups of rhesus macaques (Macaca mulatta) to
ascertain the effects of these manipulations on levels of foraging, exploration, abnormal behavior, social interactions, and urinary cortisol levels.
The addition of woodchips increased exploration and feeding levels and
decreased social interactions. Burial of regular monkey chow in woodchips
had little effect on behavior beyond that of the woodchips alone, increasing
exploration and decreasing passivity. The addition of sunflower seeds to
the woodchips encouraged increased feeding and exploration and led to
decreases in passivity and social interaction. There was little discernible
effect of woodchip enrichment on urinary cortisol values. In contrast to
some previous studies, there was no effect of wood &ips or sunflower seeds
on the occurrence of agonistic interactions, play, or abnormal behavior
patterns.
Key words: rhesus, enrichment, behavior, foraging, cortisol
INTRODUCTION
There is currently a growing interest in the “enrichment” of captive environments and the influence of environmental variables on captive animals. The revised Animal Welfare Act of 1985 mandates a “physical environment adequate to
promote the psychological well-being of primates”; the debate continues in the
research community on the necessary and sufficient conditions t o provide such a n
environment.
One approach to a definition of psychological well-being makes the assumption
that well-being is enhanced by providing animals with opportunities to perform
the full range of behaviors seen in wild populations, at species-normative levels.
Captivity alone increases the frequency of some social interactions in many species
over levels seen in the wild [Rowell, 19671, as does provisioning of wild animals
[Southwick, 1969; Marriott, 19881. Behavior patterns that have become labeled
“abnormal” are also artifacts of captivity [Erwin & Deni, 19791. There have been
many recent efforts to promote behavior patterns in captive nonhuman primates
Received for publication February 14,1990; revision accepted October 17, 1990.
Address reprint requests to Gayle Byme, NIH Animal Center, Building 112, Poolesville, MD 20837.
0 1991 Wiley-Liss, Inc.
142 / Byrne and Suomi
that are characteristic of wild populations by enrichment of the physical environment. Some of these efforts have involved stimulation of behavior by providing a
suitable substrate in which to forage [Chamove & Anderson, 1979; Chamove et al.,
1982; Anderson & Chamove, 1983; Tripp, 1985; Westergaard & Fragaszy, 1985;
Maple & Finlay, 1986; Kleiman et al., 1986; Bloomsmith et al., 1988, Boccia, 19881.
Most of these studies have reported changes that are commonly regarded as beneficial to well-being, such as increases in activity and exploration, decreases in
abnormal behavior, increases in play, and decreases in aggression. Thus, the imposition of a foraging requirement in some studies seems to negate some of the
artificial effects of captivity and can be hypothesized to enhance psychological
well-being.
Wild environments are not without their own stresses; e.g., from predation,
fluctuations in food availability, and intraspecific aggression. A limit must be
imposed on approximations to wild patterns by balancing psychological well-being
with physical well-being. Another approach to the assessment of well-being lies in
monitoring behavioral and psychological correlates of stress. While it is recognized
that many physiological systems respond to stress [e.g., Mason, 19741, one of the
most widely studied is the pituitary-adrenocortical system. Emotionally arousing
stimuli that result in some degree of novelty or uncertainty are potent activators
of the adrenocortical system [Henry & Stephens, 1977; Hennessy et al., 1979;
Sassenrath, 1983; Levine, 19851. Feeding is a vital activity in any animal’s life,
and a challenge to expectancies concerning the procurement of food can be expected to affect emotional and physiological responses, including adrenocortical
activity. There have been few studies to relate changes in environmental enrichment or foraging opportunities to cortisol levels in nonhuman primates [see Line
et al., 1987; Novak & Drewsen, 1989, for exceptions].
The present study was designed to investigate the effects of woodchips and
foraging on behavior patterns and cortisol secretion in captive, stable groups of
rhesus macaques. The effects of physical enrichment of the environment were
tested by adding woodchips to the bare floors of animals’ pens. The effects of
foraging enrichment were investigated by burying monkey chow in the woodchips.
Foraging demand was manipulated further by scattering sunflower seeds in the
woodchips. Finally, in one group, the regular ration of monkey chow was increased
to test the effects of a change in food availability. Changes in activity levels,
affiliative and agonistic patterns, abnormal behaviors, and urinary levels of cortisol were all monitored with changes in environmental conditions.
MATERIALS AND METHODS
Subjects
Two groups of rhesus macaques (Macaca mulatta) were used in this study.
Group 1consisted of an adult male, 3 adult females, 5 juvenile offspring (2-3 years
old), and a 4 year-old male adopted into the group at 5 months of age. One infant
was born to group 1 during week 12 of the study. Data involving interactions with
this infant were excluded from analysis. Group 2 consisted of an adult male, 2
adult females and 3 offspring (2-4 years old). The adults in this study had been
raised in 2 peer groups from the age of 1 month, and these groups had been
together for 9 years at the time the study began.
Each group was housed in an indoor-outdoor pen with bare floors of tile (inside) and concrete (outside). The indoor pen measured 2.4 x 3.0 x 2.2 m and
contained 3 resting shelves; the outdoor pen measured 2.5 x 3.0 x 2.5 m and
contained a single isolation cage which was used to collect urine samples. The
animals were maintained on a 12L:12D light schedule indoors, and were fed mon-
Effects of Woodchips on Behavior I 143
TABLE I. Schedule of
Experimental Conditions*
Group
1
2
Experimental
Condition
B
W
F
F'
W'
F'
B'
INC
S
B
w1
F
w2
W'
F'
B'
S
Week
1-10
11-14
15-17
18-22
23-21
28-31
32-35
36-37
38-39
1-8
9-12
13-16
17
18-25
26-29
30-33
34-37
"B = bare floors, regular feeding (B' = fed 2 x /day);
W = woodchips, regular feeding (W' = fed 2 x /day);
F = woodchips, buried food (F' = fed 2 x /day);
S = woodchips, regular feeding (2 x /day), sunflower
seeds scattered in bedding;
INC = woodchips, regular feeding (2 x /day), increased
food ration.
key chow either once or twice a day (see below). Water was available ad libitum
through automatic watering spouts in the indoor pen. For the first 5 months of the
study (June to November) the animals had access to the indoor and outdoor pens
both day and night. During the winter months (November to March) animals were
locked inside overnight, and were occasionally kept locked in on extremely cold
days. Indoor and outdoor pens were cleaned every morning in the bare-floored
condition. During the conditions in which woodchips were added to the indoor pens,
the woodchips were replaced and the pens were cleaned once a week.
Procedure
This study employed a within-subjects reversal design under three main environmental conditions: 1)Baseline (B)-bare floors, food thrown in pen and scattered on bare floor; 2) Woodchips (W)-5 cm layer of woodchips on floor of indoor
pen, food thrown on top of woodchips; 3) Foraging (F)-woodchips on floor, food
buried beneath woodchips. Each of these conditions was presented under two different feeding regimes: 1)food given primarily once a day, in the afternoon, and 2)
food given both in the morning (0700) and in the afternoon (1400-1500). This
change was brought about at the reversal point of the study when a change in
animal care personnel a t the NIH Animal Center inadvertently resulted in a
change in feeding schedule and a small increase (10%) in total food ration. The
schedule of conditions for each group is shown in Table I.
The order of conditions was the same for both groups, but presentation of
conditions t o one group was staggered 2 weeks behind the other group. Thus, as
each group entered a new condition the other group was still in a prior condition
144 I Byrne and Suomi
under identical variables of day length, temperature, etc. Wherever possible, these
conditions were presented in 4-week blocks. However, the unplanned change in
feeding schedule at week 19 cut short the conditions in effect a t that time and
necessitated the extension of the succeeding conditions i n order to get back on a
staggered schedule.
After the replications of the three main experimental conditions were completed, two shorter conditions were added. After the last bare-floored baseline
condition, the woodchips were reinstated and, in addition to the regular food ration
placed on top of the chips, sunflower seeds were scattered every morning to further
induce foraging. This condition is identified as “S” in Table I, and was the final
condition under which observations were performed for both groups. In group 1one
other condition preceded the S condition. In this condition (INC) the woodchips
were reinstated and the total daily ration of food was increased approximately 25%
and placed on top of the woodchips. This group was almost twice the size of group
2, and this manipulation was intended to offset the increased competition for food
in the larger group. The increased food ration was kept in effect during the S
condition which followed.
Observational scoring. Within each environmental condition each animal
was observed for 10 minutes twice each week, once from 0900 to 1000 and once
from 1300 to 1400 hours. Within each 10 minute focal animal sample, 10-second
point samples of a number of behaviors were recorded (Table I1 lists the behaviors
that were scored). Order of observation of animals was randomized prior to the
session.
Urine sampling. A single isolation cage was installed in each group’s outdoor
pen. The animals were trained to urinate either inside or on top of the cage by
reinforcement with preferred foods (raisins, grapes, etc.). The urine was then aspirated with a syringe and plastic collection tube from the metal pan underneath
the cage and frozen to -20°C.
Attempts were made to obtain samples from both groups two to three times
during each observation day, at regular times between 0900 and 1200. A subset of
all the samples was selected such that there was a maximum of four samples for
any one subject in any one condition. The urine samples were analyzed for excreted
levels of cortisol by radioimmunoassay (Ciba Corning Magic‘@”Cortisol radioimmunoassay). Samples were also analyzed for creatinine in order to correct for
variables such as body weight and dilution of the urine. Creatinine values were
determined via kinetic alkaline picrate assay. Cortisol values were divided by
their corresponding creatinine values to give an index of cortisol excretion.
Data analysis. Behavioral scoring data were analyzed using repeated measures ANOVAs, with environmental conditions as the within-subject factor. Tukey
HSD tests were used to identify significant differences among means when the
overall F was significant at the .05 level. Data from the two groups were analyzed
separately, as the differences in size and composition of the groups precluded any
between-groups comparisons.
The behavioral categories listed above (Social, Abnormal, Agonistic, Active,
Feeding, and Passive) served as the behavioral measures used i n analyses. Means
of each subject’s scores in each category were calculated for each environmental
condition. Post hoc tests first compared the levels of behavior in the replications of
each experimental condition, to test for effects of changes in season and indooroutdoor access and to ascertain if the unplanned difference in feeding schedule
significantly affected behavior (e.g., B was compared to B’, W to W‘, and F to F’).
If there were no significant differences between the replications they were combined to yield a mean value for each condition, and ANOVAs were performed
Effects of Woodchips on Behavior I 145
TABLE 11. Behavioral Categories and Definitions
Social
Contact-in physical contact with another animal, not engaged in any other scored social
behavior with that animal
Proximity-within 30 cm of another animal, not touching or engaged in any other scored
social behavior with that animal
Grooming-one animal pickinglbrushing through the fur of another animal-may be scored
either as “groom” or “groom receive”, according to the focal animal’s role
Play-animated chasing, wrestling, sham-biting, may be accompanied by open-mouth play
face
Sex-either male or female sexual postures-includes mounting, thrusting, presenting
Abnormal
Abnormal-includes stereotypic pacing (repeated at least three cycles) and other repetitive
abnormal behavior patterns, e.g., self-biting or mouthing, “saluting”, etc.
Abnormal sex-masturbation by self-stimulation of genitals, either manually, orally, or
through disoriented mounts of other animals.
Agonistic
Withdraw-deliberately move out of the path of a n approaching animal
Aggression-includes noncontact open-mouth threat and/or stare, grabbing, biting, chasing
of another animal (not in play), bouncing display
Submission-includes fear grimace, lipsmacking, crouching, screeching, screaming, flight
from a threatening or attacking animal
Active
Locomotion-moving verticaly or horizontally at least 15 cm, not engaged in any social
behavior or self-play
Explore environment-oral, olfactory, or tactile manipulation or investigation of a nonfood
object or structure-includes exploration of woodchips but excludes searching through
woodchips for food, excludes manipulation of object while engaged in social or self-play
Self-play
Feeding
Forage-search for and/or handle food item, includes searching through woodchips for food,
picking up and investigating food item.
Eat-put food item in mouth and chew, also includes transfer of food from cheek pouches to
mouth
Drink-take i n water in any way
Passive
Sitting, standing, or lying alone, not engaged in any other scored behavior
across the main conditions. If significant differences were revealed between the
replications, additional ANOVAs were performed which included the differing
replications a s separate conditions. Differences in relative cortisol levels over the
experimental conditions were also tested in ANOVAs.
RESULTS
Focal Animal Samples
ANOVAs were first carried out across all of the environmental conditions. An
alpha level of .05 was adopted for all analyses. Post hoc tests were used to compare
146 / Byrne and Suomi
Baseline (B), Woodchips (W), and Foraging (F) conditions both before and after the
midpoint in the study.
In most cases the levels of behavior seen within the replications of the three
main conditions were not significantly different. There were two exceptions, however. In group l,the level of Active in the first F' condition was significantly lower
than that in the preceding condition F (F(8,72) = 18.00). When the first F' was
considered separately from the other combined F conditions, it was revealed that
Active levels in that phase were significantly lower than in the combined W, F, or
(A) SOCI,4L
(A)
FEEDING
401
m
2
in
rn
m
0
z
m
0
15
z
a
W
4
=
B
0
(B)
Ln
Y
a
a
W
F
INC
S
41
3
n
15
W
F
INC
F
INC
ACTIVE
45
30
m
m
0
0
5
z
15
4
W
W
=
0
B
(C)
W
F
INC
S
S
6o
0
10
m
I
B
0
v)
in
4
2oL
i
(El)
!n
0
2
I
10
ABNORMAL
20
!n
y
W
30
o
1
S
B
W
AGONlSTlC
in
2
B
W
F
INC
S
B
W
F
INC
S
Fig. 1. Mean occurrence of social, abnormal, and agonistic in the focal samples over the main experimental
conditions. Open bars = p o u p 1;Hatched bars = group 2. Vertical bars denote standard errors.
Fig. 2. Mean occurrence of feeding, active, and passive in the focal samples over the main experimental
conditions. Open bars = group 1;Hatched bars = group 2. Vertical bars denote standard error.
Effects of Woodchips on Behavior I 147
S conditions, and significantly higher than those in INC (F(5,45) = 22.82). In
group 2, Feeding levels in the first two presentations of the woodchip conditions
significantly differed from each other-Feeding in W2 was much lower than in W 1
(F(7,35) = 8.30). Examination of the data revealed a Feeding level of zero during
W2; none of the animals in this group were ever observed eating, foraging, or
drinking during this condition.
The replications of the main conditions were then combined, and behavior
scores across the main conditions were examined (Figs. 1, 2).
Social. The number of samples in which Social was scored was significantly
lower in S than in B, F, or INC in group 1 (F(4,36) = 8.04), and lower in S than in
all other conditions in group 2 (F(3,15) = 7.70 (Fig. 1A)). In addition, Social levels
in group 1 were significantly lower in W than in B. Further analyses examined the
levels of the behaviors comprising the Social category. Changes in Social were due
to changes in contact, proximity, and grooming; there were no significant differences in levels of play or sex among any of the experimental conditions.
Abnormal. There were no significant changes across conditions in Abnormal
behavior in either group (group 1-F(4,36) = 0.22; group 2-F(3,15) = 2.27; Fig.
1B).
Agonistic. There were no significant changes across conditions in Agonistic
behavior in either group (group 1-F(4,36) = 0.89; group 2-F(3,15) = 1.70; Fig.
1C).
Feeding. The number of samples in which animals were observed Feeding in
group 1 increased significantly in INC and S from those seen in B, W, or F (F(4,36)
= 13.27; Fig. 2A). Feeding in group 2 was significantly higher in S than in B
(F(3,15) = 4.40) and higher in W than in B when W2 was excluded from the W
condition (see above).
Active. In group 1 levels of Active in W, F, and S were greater than those in
B. Active in INC was less than in F and S (F(4,36) = 29.41; Fig. 2B). In group 2
scores for Active were greater in the S condition than in any of the other conditions
(F(3,15) = 15.13). In addition, analysis of environmental exploration (the main
component of Active scores) revealed that the level of this behavior was greater in
F than in B (F(3,15) = 15.60). (Significant changes in Active scores were always
due to changes in environmental exploration; no significant changes in locomotion
or self-play were observed.)
Passive. The number of samples in which Passive was scored was significantly lower in S than in B and W for both groups (group 1-44,36) = 9.19; group
2-F(3,15) = 6.25; Fig. 2C). In group 1 levels of Passive in F and INC were also
lower than those seen in Baseline.
Cortisol Values
An ANOVA based on data from 6 subjects in group 1 for the replications of the
main conditions revealed that cortisol levels in the second F’ condition were significantly higher than those in B, W, or F (F(6,30) = 2.75). There were no significant differences within replications for group 2 in the 3 subjects with adequate
samples (F(6,12) = 0.47). An analysis which combined replications of the three
main conditions for all subjects revealed no significant differences among the combined B, W, or F conditions in either group. There were not enough samples from
conditions INC or S to include in most of the statistical analyses. When the INC
condition was included for 3 subjects in group 1 with adequate samples, cortisol
levels in INC were significantly lower than in B or F (F(3,6) = 6.31).
148 I Byrne and Suomi
DISCUSSION
The results of this study with rhesus macaques were, to some extent, in agreement with those of previous studies with other species, but several discrepancies
emerged a s well. Enrichment with woodchips increased activity and led to decreases in social interactions, echoing results from Chamove and Anderson [19791,
Chamove et al. r19821, and Westergaard and Fragaszy 119851. Burying food in
woodchips had little effect on behavior beyond that of the woodchips alone; the
addition of buried food was associated in both groups with increased environmental exploration, and, in group 1,with decreased levels of Passive in comparison to
Baseline levels. The burial of food in the F condition was intended to affect the
amount of effort required to find food. In reality, however, simply burying food in
5 cm of woodchips did not constitute a particularly difficult foraging task. The
large pieces of monkey chow were easily uncovered, either deliberately or by accident, and were often examined and discarded, leaving a n assortment of unburied
food available for other animals.
Sunflower seeds scattered in the woodchips led to even greater changes in
behavior, with increases in activity and foraging and decreases in passivity and
social interaction. These findings again concur with Chamove’s studies as well as
with later studies by Bloomsmith et al. 119881 and Boccia [1988].
If approximation to patterns of behavior seen in the wild is indicative of
psychological well-being, then the S condition i n the present study came closest
to fulfilling this criterion. Captive rhesus may often spend less than 20% of their
time feeding [Bernstein, 1971; Post & Baulu, 19781, whereas percentages are
typically higher for wild, unprovisioned animals [Malik, 1986; Seth & Seth,
19861. In the present study, the percent of samples in which eating and foraging
occurred was small, ranging from 1 to 7 i n the combined B, W, or F conditions.
During the S condition this figure increased to 35% in group 1 (which also had
a n increased food ration) and 13% in group 2. Social behavior levels, which may be
artificially increased by captivity, were lowered in the S condition; nonsocial
exploration and activity increased as the incentive to attend to the physical
aspects of the environment increased. These changes resulted in a time budget
more characteristic of natural populations without compromising animals’
physical well-being.
In contrast to previous studies with other species [e.g., Chamove & Anderson,
19791, there were no changes i n abnormal behavior associated with any of the
environmental manipulations i n the present study. Abnormal behavior was relatively infrequent to begin with, occurring i n less than 10% of the samples, and
was most often exhibited by the adults, who had been raised from infancy in peer
groups. It has been suggested that peer-reared rhesus macaques are more reactive
to stress throughout their lives than mother-reared ones [e.g., Suomi & Harlow,
19753; the enrichment i n the present study may simply not have been sufficient to
reduce the incidence of abnormal behavior patterns in these animals.
The lack of effect of environment on levels of agonistic behavior or play was
probably due to the long-term stability and structure of the subject groups. The
importance of social enrichment, as contrasted with physical enrichment, has
been well recognized [Reinhardt, 1988; DeWaal, 19891. The nature of the social
groups in the present study was a comparatively enriched one; there were plenty
of opportunities for play t h a t were intrinsic to the social environment. Conversely,
levels of agonistic behavior were relatively low and were probably affected more
by the nature and stability of the social environment than the physical one.
Effects of Woodchips on Behavior / 149
Urinary Cortisol
There were few significant changes in cortisol values throughout the study. In
group 1 there was an increase in cortisol over several days during the second F’
condition, but it is difficult to account for this increase. This period occurred in late
December, after the groups had begun to be locked in overnight due to cold. This
restriction of freedom of movement may have been related to the increase in cortisol levels. However, there was no increase at that time of cortisol levels in the
other group, or in any other phase during the winter months.
In general, cortisol values gave little reliable indication of animals’ emotional
reactions to experimental manipulations of the housing environment, in contrast
to earlier work using 24 hour urine samples [e.g., Mason et al., 1957; Mason, 19591.
It may be that single urine samples, even taken repeatedly, are not as effective as
24 hour aggregate collections in detecting changes in overall cortisol excretion,
although Novak and Drewsen [1989], using single samples, did find changes in
urinary cortisol levels with changes in home cage lighting conditions in rhesus
macaques. It is also possible that the present environmental manipulations simply
did not affect cortisol levels in the long term. Under more controlled conditions of
sample collection, animal care, feeding, and indoor-outdoor access more conclusions might be drawn as to the utility of these values.
Implications for Psychological Well-Being
The use of woodchip litter and the addition of sunflower seeds is a promising
strategy for enhancing psychological well-being in social groups of rhesus
macaques, as has been suggested in studies with other macaque species. The fact
that behaviors such as aggression and play showed no change in the present study
emphasizes the importance of a stable social environment in interpreting levels of
social behavior. Psychological well-being is encouraged above all by access to conspecifics; new animal welfare regulations call for increased use of social groupings
of nonhuman primates. It must be recognized, however, that there may be increased risk to well-being when social groups are newly formed or if the composition of groups is constantly changing t o meet experimental requirements.
Proposed regulations for nonhuman primates which call for varied types of
food and methods of feeding recognize the potential for enrichment that these
techniques afford. Beneficial effects may be obtained solely with supplemental
foraging tasks, (e.g., sunflower seeds), and it may not be necessary or advantageous to require animals to forage for their full ration. Indeed, some of Rosenblum’s studies in bonnet macaques [e.g., Rosenblum & Sunderland, 1982; Rosenblum and Paully, 19841 have shown that such demanding requirements may be
detrimental to group relations and infant development. In addition, extreme variation in feeding schedules or methods may impart an atmosphere of unpredictability or uncontrollability which may affect group social relations and physiological
stress responses, and may actually be counterproductive.
CONCLUSIONS
1. Enrichment of rhesus macaques’ bare-floored pens with woodchips led to
increases in environmental exploration and feeding and decreases in social interactions, echoing results of studies with other species of nonhuman primates.
2. Burying chow in woodchips had little effect on behavior beyond that of the
woodchips alone; buried food was associated with increased environmental exploration, and decreased passivity.
150 I Byrne and Suomi
3. Sunflower seeds scattered in the woodchips led t o e v e n greater changes in
behavior, w i t h f u r t h e r increases in activity and feeding and decreases in passivity
and social interaction.
4. There w a s little systematic c h a n g e in urinary cortisol values w i t h different
environmental conditions. The l a c k of significant variation in cortisol m a y represent a failure of adequate sample collection and experimental control. It is also
possible that the environmental m a n i p u l a t i o n s did n o t affect cortisol levels in the
long term.
5 . There were n o c h a n g e s in levels of agonistic behavior, play, or a b n o r m a l
behavior in this study. The stability and composition of the social group m a y
influence these behaviors more than do aspects of the physical environment.
ACKNOWLEDGMENTS
The authors w i s h to acknowledge the contributions of E v a n B y r n e and Charles
Snowdon for editorial comments and statistical consultation, and Bob Brown for
technical expertise. T h i s research w a s conducted as part of the Intramural Res e a r c h P r o g r a m , Laboratory of Comparative Ethology, NICHD, Bethesda, MD, and
constituted part of the first author’s doctoral dissertation at the University of
Wisconsin-Madison. Data on u r i n a r y cortisol values in this study m a y be obtained
from the first a u t h o r .
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