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Enclosure environment affects the activity budgets of captive Japanese macaques (Macaca fuscata).

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American Journal of Primatology 70:1133–1144 (2008)
RESEARCH ARTICLE
Enclosure Environment Affects the Activity Budgets of Captive Japanese
Macaques (Macaca fuscata)
M. FIROJ JAMAN1,2 AND MICHAEL A. HUFFMAN1
1
Department of Ecology and Social Behavior, Primate Research Institute, Kyoto University, Inuyama, Japan
2
Wildlife Biology and Management Section, Department of Zoology, University of Dhaka, Dhaka, Bangladesh
Individuals adapt to changes in their environment, such as food availability and temperature, by
adjusting the amount of time spent in different behavioral activities. These adjustments in behavior
should vary across age–sex class according to specific physiological and social needs. We studied the
activity budgets of three social Japanese macaque groups inhabiting either vegetated or nonvegetated
enclosures in order to compare the effects of access with vegetation, as both food and substrate on
resting, feeding, grooming and moving activities over a 12-month period. Daily access to natural foods
for monkeys in the vegetated enclosure seems to be largely responsible for the differences in daily time
budgets of these three groups. Resting time in all three groups was longer than the time devoted to
other activities. Resting and moving time in the two nonvegetated enclosures was significantly longer
than in the vegetated enclosure. In contrast, feeding and grooming time was significantly longer in the
vegetated enclosure. Seasonal variation in time spent feeding, resting and grooming was significantly
effected by enclosure type. In all three enclosures, immatures, particularly females, spent more time
feeding and moving, whereas adults spent more time resting. Significant monthly variation in time
spent by age–sex class was noted only for feeding and resting. Interestingly, in the vegetated enclosure,
time spent feeding on natural vegetation was equal to the amount of time spent feeding on provisioned
food. This suggests that factors other than energetic and nutritional needs may be important
determinants of the activity budget of the species. These results have important implications for the
enrichment of captive primates and our understanding of the maintenance of activity patterns by
primates in the wild. Am. J. Primatol. 70:1133–1144, 2008.
r 2008 Wiley-Liss, Inc.
Key words: enrichment; captivity; seasonality; age–sex differences; activity budget;
Macaca fuscata; vegetated enclosure
INTRODUCTION
The allocation of time for multiple activities has
significant effects on the survival of primates. For
example, in winter months Japanese macaques
(Macaca fuscata) undergo an energy crisis, and
seasonal changes in their daily activities correspond
to the seasonal fluctuation of food supply and
atmospheric temperature [Nakayama et al., 1999;
Yotsumoto, 1976]. Seasonality of time budgets can be
affected by seasonal changes in food availability
[O’Brien & Kinnaird, 1997; Overdorff, 1996; Strier,
1987; Sussman, 1974]. Thus, the activity budgets of
primates can be highly flexible in response to
seasonal variation [Vasey, 2005].
Activity budgets are related to important physiological and environmental factors such as energy
balance, body size and food availability [CluttonBrock, 1974; Coelho, 1986; Harrison, 1985; Kurup &
Kumar, 1993; Li, 1992; Marsh, 1981; Menon &
Poirier, 1996; Watanuki & Nakayama, 1993]. Diet
and habitat structure are known to affect time spent
in activities because of trade-offs between obtaining
r 2008 Wiley-Liss, Inc.
food and the costs in energy of doing so [Altmann,
1974b; Oates, 1987; Post, 1981]. Habitat quality
affects food availability and primates respond variably to changes in food availability [Defler, 1995; Li
& Rogers, 2004]. In the wild, Japanese macaques
decrease traveling and feeding time when temperature decreases, but when food is abundant, food
distribution and feeding speed increase while time
spent feeding and traveling decreases [Hanya, 2004].
Feeding is considered to have priority over all
Contract grant sponsor: Graduate Studies Scholarship ‘‘Monbukagakusho’’ (Ministry of Education, Culture, Sports, Science
and Technology, Japan).
Correspondence to: Michael A. Huffman, Department of
Ecology and Social Behavior, Primate Research Institute, Kyoto
University, 41-2 Kanrin, Inuyama 484-8506, Japan. E-mail:
huffman@pri.kyoto-u.ac.jp
Received 22 February 2008; revised 11 August 2008; revision
accepted 12 August 2008
DOI 10.1002/ajp.20612
Published online 10 September 2008 in Wiley InterScience (www.
interscience.wiley.com).
1134 / Jaman and Huffman
nonessential activities. Studies predict that food
distribution and food quality determine activity
budgets [Agetsuma, 1995; Nakagawa, 1989a; Suzuki,
1965; Watanuki & Nakayama, 1993].
Temperature influences a plant’s rate of growth
and its nutritional content. This has both direct and
indirect effects on the seasonality of the activity
budget of species dependant upon plants for food
[Dunbar, 1992]. Activity budgets in wild Japanese
macaques can be affected by seasonal changes in
temperature and this can vary with age and sex
[Agetsuma, 1995; Jaman, 2007; Maruhashi, 1981;
Nakagawa, 1989b; Watanuki & Nakayama, 1993]. It
is expected therefore that age–sex class activity
patterns should be different. Immatures spend more
time feeding and playing [Hanya, 2003; Watanuki &
Nakayama, 1993], as well as moving [Maruhashi,
1981], than other age–sex classes throughout the
year. Furthermore, females spend more time engaged in social grooming and feeding, and are much
more active than males. However, we still do not
understand the relationship between behavioral
activities and how such factors as age class, sex and
environment influence the behavior of captive
macaques.
Our understanding about the dynamics of
Japanese macaques’ activity budgets comes from
free-ranging provisioned and nonprovisioned populations [Hanya, 2004; Maruhashi, 1981; Watanuki &
Nakayama, 1993]. Controlled experiments (or manipulations) are an ideal method for deciphering how
specific mechanisms affect behavior, but rigorous
controls are often impossible under natural conditions. Thus, captive populations provide an opportunity to more closely monitor behavioral variations in
response to factors such as food availability and
climate. However, one criticism might be that
enclosure conditions are too artificial. One possible
solution is to use captive populations housed in seminatural, vegetated enclosures that closely or partially
mimic natural conditions. Unfortunately, we do not
know to what degree environmental enrichment
benefits captive Japanese macaques or whether their
behaviors approach those of wild populations in
response to enrichment. Although both captive
rearing and enrichment of Japanese macaques have
received considerable attention, few studies have
compared activity budgets of monkeys inhabiting
different captive environments [Boinski et al., 1999;
Kerridge, 2005]. These comparisons are important
for our understanding of inter- and intra-specific
behavioral variations, could be helpful in devising
enrichment strategies, and may illuminate the
adaptive nature of variability in temporal activity
patterns in primates in general [Kinnaird, 1990;
Robinson, 1986; Terborgh, 1983]. In this light it can
be argued that studying the activity budgets of
captive monkeys, especially those in semi-naturally
vegetated enclosures, is important in understanding
Am. J. Primatol.
how captive macaques use both provisioned and
natural foods, when both are available, and how this
affects age–sex class at different times of the year.
The main objectives of our research are to
provide baseline data on the factors influencing
variations in activity budgets between captive populations of Japanese macaques in outdoor nonvegetated and semi-natural, vegetated enclosures. We
compare the results of this study with known
behavioral patterns from wild populations. Here we
test the following predictions based on the assumption that time spent in each behavioral activity varies
according to enclosure type, age–sex class, and
season: (1) the relative proportion of time spent in
various activities should vary according to enclosure
type; (2) in general, captive monkeys should spend
less time feeding and more time resting because they
have to work less to obtain abundant, high-energy
food than do their wild counterparts; (3) the presence
of natural vegetation in an enclosure should increase
the amount of time spent feeding; (4) time spent
feeding and resting should vary seasonally according
to food availability to meet nutritional and energy
demands; and (5) immatures should spent more time
feeding and less time resting than adults in order to
obtain sufficient amounts of nutrition for maturation
and high-energy demands.
METHODS AND MATERIALS
Study Subjects and Facilities
We observed three socially living groups of
Japanese monkeys at the Primate Research Institute
(PRI), Kyoto University, Japan. Two of these groups
(Takahama and Wakasa-3) were kept in nonvegetated enclosures. Takahama troop (48–53 individuals
during this study) lives in a 960 m2 outdoor enclosure
with metal climbing structures, one open-side 12 m2
wooden-roofed shelter and two metal shelter boxes
with an entrance from the floor for protection from
adverse weather. Wakasa-3 troop (20–22 individuals)
is kept in a 496 m2 outdoor enclosure with an 8 m
high climbing structure located in the middle of the
enclosure. The structure consists of two stories with
platforms and a smaller-roofed shelter on top. There
is also a 15 m long artificial stream with a small pond
and a small patch of grass on the ground. The
Wakasa-5 troop (32–41 individuals) is kept in a
6400 m2 naturally vegetated enclosure with three
wooden platforms, 2–3 m off the ground that monkeys daily climb up and rest on. Flora in the
vegetated enclosure consists of over 60 species of
trees, shrubs, grasses and climbers. The four most
common tree species are Eurya japonica (53.88% of
total treesZ1.5 m high in the enclosure), Cleyera
japonica (12.97%), Quercus glauca (10.13%) and
Photinia glabra (9.18%). Combined they account
for over 86% of the individual trees in the enclosure.
Enclosure Environment and Activity Budgets / 1135
All study groups are provisioned daily by
husbandry staff with commercial monkey chow
(AS, Oriental Yeast Co. Ltd., Tokyo, Japan) to meet
basic developmental and reproductive requirements.
The main difference between these groups was that
monkeys in Wakasa-5 enclosure are able to supplement their diet freely with natural vegetation. The
other two groups are dependent almost entirely upon
the commercial diet. Provisioning occurred once a
day between 9:00 and 11:00. Infrequently, they were
provisioned for a second time in the afternoon, and
this occurred often in Wakasa-3. As a result, food
remained on the ground until the latter part of the
day, allowing this group to feed on provisioned food
until sunset. Food was evenly dispersed in the
enclosure to avoid food competition. During the
study period, subjects were provisioned with monkey
chow, sweet potatoes, wheat, and occasionally cucumber and bamboo shoots. This research was
conducted in accordance with all national and
institutional guidelines for the care and management
of primates established by PRI.
Temperature Data Collection
Temperature was recorded automatically every
10 min throughout the year using PRI’s weather
recording device placed in a central location near the
enclosures. From these data, average daily and
monthly temperatures were calculated for the daily
study period between 7:00 and 17:00 hr. Temperature data collected from the summer months of two
different years (2005 and 2006) were compared in
order to see whether the maximum, average and
minimum temperatures of June, July and August
were similar. There was similarity in temperatures
between the two years and we therefore combined
the behavioral data of these two different years into
one ‘‘summer season’’ for the analysis of behavioral
correlates.
Observations and Behavioral Data Collection
Data collection began in August 2005 and
continued through July 2006. From a total of 816
observation hours, we collected 3,264 focal sessions
from 34 focal subjects on ten behavioral activities.
Before this, six months were spent habituating the
monkeys in each troop to our presence, establishing
individual identification of each monkey and to
identify and catalogue plants in the vegetated
enclosure. In both the nonvegetated enclosures
observations were made from both inside and outside. In the vegetated enclosure however observations could only be made from inside owing to the
larger size of the enclosure and abundant vegetation
that reduced visibility. All focal individuals were
identified using a tattoo number and/or individually
distinct morphological characteristic. Data were
collected by M. F. J. in the form of 15 min continuous
focal animal samples [Altmann, 1974a; Martin &
Bateson, 1993]. We classified all focal subjects into
one of two age classes: immature (male: r4 years
and female: Z3 years) and adult (male: 45 years and
female: 44 years). Three focal subjects were selected
from each of the four age–sex classes for every group
except Wakasa-3, where only one adult male was
present, for a total of 34 individuals. Focal subjects
were chosen for similarity of age across groups.
Observations were made in four different time
periods; early morning (EM: 7:00–9:30), late morning
(LM: 9:30–12:00), early afternoon (EA: 12:00–14:30)
and late afternoon (LA: 14:30–17:00). An equal
number of samples were collected in each timeperiod of the day for each focal subject in each troop
per week to facilitate monthly, seasonal and group
wise comparisons of behavioral data. Two focal
samples per week were collected for each subject
totaling 68 samples/week for 34 focal individuals.
We constructed and employed an ethogram
during observations, which included feeding, foraging, moving, resting, grooming, aggression and
submission, object manipulation, play, vigilance and
object licking. Closely related behaviors were later
combined and arranged to make seven behavioral
categories (dominance interactions, feeding, grooming, moving, object manipulation and play, resting,
vigilance) for easier comparisons. Eating, foraging
and licking were combined into feeding behavior.
‘‘Eating’’ is defined as the intake of solid food or
water into the mouth, followed by chewing and/or
swallowing. ‘‘Foraging’’ is uninterrupted search for
food items on the ground or in vegetation where food
is typically found, often but not always, ended by
ingestion of food or water. ‘‘Licking’’ is defined as
licking any object or surface. ‘‘Moving’’ is defined as
terrestrial or arboreal locomotion, lasting a minimum of 5 sec, from one place to another, except when
searching for food or another animal. ‘‘Resting’’
starts when no other behavior occurs regardless of
posture. ‘‘Grooming’’ is defined as the act of picking
out, scratching or removing debris, ectoparasites or
other objects from the hair or skin, regardless of
whether the focal subject is grooming itself, another
individual or being groomed. ‘‘Aggression’’ and
‘‘submission’’ are combined into ‘‘dominance interaction.’’ ‘‘Aggression’’ is defined as any aggressive
physical contact, gesture or vocalization (supplanting, grabbing, hitting, chasing, biting, stare threat,
head bobbing, threat bark, etc.) typically directed
toward a subordinate individual. ‘‘Submission’’ includes any submissive behavior, gesture or vocalization (retreat, avoidance of eye contact, crouching,
grimace, cry, etc.) in responses to aggressive behaviors received from a more dominant individual.
‘‘Object manipulating’’ is a behavior in which
monkeys pick up objects such as stones, sticks, tree
branches, etc. and manipulate them with their
hands. ‘‘Playing’’ is defined as jumping, running,
Am. J. Primatol.
1136 / Jaman and Huffman
hanging on, mounting on the back of mother or
another individual or grasping others in a nonthreatening context. ‘‘Vigilance’’ is defined as watching
something for more than 10 sec while not engaged in
other actions.
and tests were done using SYSTAT 11 and SPSS
[version 13.0].
RESULTS
Data Analysis
General Differences in Activity Between
Groups
Normality and equal variance tests on the data
failed and therefore analyses were done using
square-root n10.5 transformed data [Sokal & Rohlf,
1969]. We analyzed the duration (time in seconds) of
behavioral category (see description above) with
multivariate analysis of variance (MANOVA) using
age–sex class (adult male, adult female, immature
male and immature female), month (12 months),
enclosure (Takahama, Wakasa-3 and Wakasa-5) and
their interaction as explanatory variables. Post hoc
pair wise contrasts were then used to compare the
average time spent on each behavioral category
between enclosures using the MANOVA main model
error term as there were no significant differences in
the variance between the enclosure populations. For
the four most frequent behaviors (feeding, resting
grooming and moving), post hoc pair wise contrasts
were also used to compare time spent for each
behavior across age–sex class in each group. We
examined the relation between daily temperatures
and time spent on each activity per group and per
age–sex class using a Pearson correlation. Finally, we
analyzed time spent feeding using analysis of
variance (ANOVA) with enclosure type (vegetated,
nonvegetated) and food type (provisioned, natural
food) as explanatory variables. Post hoc pair wise
contrasts were used to compare the average time
spent feeding on provisioned and natural foods
within and between enclosure types. Statistical
significance for all analyses was set at Po0.05,
There were significant differences in the average
time spent between the seven behavioral activities
regardless of the month in the year of the study
(F6, 1848 5 1777.54, Po0.0001), and there was a
significant interaction between behavioral activity
and group (F12, 1848 5 43.29, Po0.0001) (Table I and
Fig. 1). Post hoc pair wise contrasts show that there
was no significant difference between each group
regarding time spent in dominance interactions or
vigilance activity. In addition, there were no significant differences in time spent grooming and
object manipulation and play between the two
groups in nonvegetated enclosures. However, for
each of these behavioral categories, there were
significant differences between each of the two
nonvegetated enclosure groups and the vegetated
enclosure group (grooming: Takahama vs. Wakasa-5,
F1,1848 5 7.99, P 5 0.005; Wakasa-3 vs. Wakasa-5,
F1,1848 5 13.58, P 5 0.0002; Object manipulation and
play: Takahama vs. Wakasa-5, F1,1848 5 11.29,
P 5 0.001; Wakasa-3 vs. Wakasa-5, F1,1848 5 12.81,
P 5 0.005; Resting: Takahama vs. Wakasa-5,
F1,1848 5 59.94, Po0.0001; Takahama vs. Wakasa-3,
F1,1848 5 10.75, P 5 0.001; Wakasa-3 vs. Wakasa-5,
F1,1848 5 104.11, Po0.0001). Time spent feeding
was significantly different between all three groups
(Takahama vs. Wakasa-3: F1,1848 5 12.48, Po0.0003;
Takahama vs. Wakasa-5: F1,1848 5 275.12, Po0.0001;
Wakasa-3 vs. Wakasa-5: F1,1848 5 126.56, Po0.0001),
but the two nonvegetated groups spent less time
TABLE I. MANOVA Result for the Effect of Group Type, Month and Age–Sex Class on Activity Budgets (Time
Spent in Seconds by Focal Animal)
Factor
Activity
Group
Month
Age–sex
Groupactivity
Monthactivity
Age–sexactivity
Monthtroop
Age–sextroop
Monthage–sex
Monthtroopactivity
Monthage–sexactivity
Age–sextroopactivity
Age–sextroopmonth
Monthtroopage–sexactivity
Error
Statistically significant P values appear in bold.
Am. J. Primatol.
DF
MS
F
P
6
2
11
3
12
66
18
22
6
33
132
198
36
66
396
1,848
101,502
13.02
245.19
2,028.93
2,472.47
421.55
4,266.08
20.21
79.27
23.06
132.89
83.23
358.43
19.56
67.62
57.1
1,777.54
0.23
4.29
35.53
43.29
7.38
74.71
0.35
1.39
0.4
2.33
1.46
6.28
0.34
1.18
o0.0001
0.79
o0.0001
o0.0001
o0.0001
o0.0001
o0.0001
0.99
0.21
0.99
o0.0001
o0.0001
o0.0001
1.0
0.01
Enclosure Environment and Activity Budgets / 1137
Fig. 1. Comparison of time spent for seven behavioral activities between Takahama, Wakasa-3 and Wakasa-5 enclosure monkeys. Bars
with different letters represent significant differences in pair wise comparisons, Po0.05. Comparisons were done for each behavior
separately.
feeding than the vegetated group (Fig. 1). Wakasa-3
may have spent more time feeding than Takahama,
the other nonvegetated group, most likely owing to
the seasonal presence of a small patch of grass that
grows inside the enclosure in spring and summer.
Takahama spent more time moving than either
Wakasa-3 or Wakasa-5 (F1,1848 5 42.6, Po0.0001;
F1,1848 5 64.07, Po0.0001, for each comparison,
respectively). But no significant variation for moving
was found between Wakasa-5 and Wakasa-3 groups
(P 5 0.53). In Takahama the movement of one group
of individuals sometimes resulted in the supplanting
of lower ranking family groups, which led to a chain
reaction of many individuals moving around the
periphery of the enclosure. In Wakasa-3, individuals
or family groups were able to avoid each other by
resting and interacting on different levels of the
stratified climbing platform. Likewise in Wakasa-5,
the dense vegetation and several wooden platforms
scattered throughout the enclosure provided the
opportunity for individuals to avoid such interactions.
Time spent feeding, resting and moving was the
only behavioral activities that varied significantly
between the two nonvegetated groups. Nonetheless,
the remaining analyses in this article are directed at
generally comparing vegetated (Wakasa-5) vs. nonvegetated (Takahama and Wakasa-3) enclosure types
to elucidate the influence of natural vegetation on
the activity patterns of captive primates.
Differences between Vegetated and
Nonvegetated Enclosures
Time spent resting in both vegetated and
nonvegetated enclosures was longer than the time
devoted for other activities (Fig. 2). Feeding, resting,
grooming and moving accounted for approximately
90% of the activity budget of either enclosure type
(Fig. 2). We focused on comparing these four most
frequently observed activities between ‘‘semi-naturally’’ vegetated and nonvegetated enclosures to
assess whether access to vegetation as food and as
substrate affects the overall activity budget of
primates housed in these conditions. The effects of
group, month and age-class on the time spent on
behavioral activity are summarized in Table I.
Effect of group
Whether the enclosure was vegetated or not
significantly affects the time spent for different
activities
by
each
group
(F12,1848 5 43.29,
Po0.0001) (Table I). The time spent resting and
moving by groups in nonvegetated enclosures (Takahama and Wakasa-3) was longer than the group in
the vegetated enclosure (Wakasa-5) (Fig. 2). Conversely, time spent feeding and grooming was longer
in the vegetated enclosure (Fig. 2).
Effect of month
Regardless of group, monthly variation of time
spent in all activities varied significantly
(F66,1848 5 7.38, Po0.0001) (Table I). Monthly variation of time spent and time spent by groups did not
interact significantly (F22,1848 5 0.35, P 5 0.99)
(Table I). In the vegetated enclosure, monkeys spent
more time feeding in the spring (March–May),
resting in summer (June–August), grooming in
summer and moving in autumn (September–November) (Fig. 3). In spring, new leaves and grasses
appeared. In the nonvegetated enclosures, feeding
time peaked in winter (December–February), resting
peaked in summer and moving peaked in autumn
(Fig. 3).
Am. J. Primatol.
1138 / Jaman and Huffman
Effect of age– sex class
Regardless of group, all behavioral categories
showed significant age–sex class differences in time
spent (F18,1848 5 74.71, Po0.0001) (Table I). Age–sex
class and enclosure type significantly affect activities
(F36,1848 5 6.28, Po0.0001). Post hoc pair wise con-
trasts showed the significant variation of time spent
feeding in all age–sex classes except between adults
and immatures of both sexes in Takahama and adult
males vs. adult females in Wakasa-5 group (Table II).
Time spent resting in all age–sex classes also varied
significantly in all groups except adult males vs.
adult females in both nonvegetated enclosure groups
and immature males vs. immature females in the
Wakasa-3 group. In all groups, immatures of both
sexes spent significantly more time feeding and less
time resting, whereas adults spent significantly less
time feeding and more time resting (Table II and Fig.
4). Time spent moving varied significantly only
between adult females and immature females in
the vegetated enclosure (Wakasa-5) and in one
nonvegetated
enclosure
(Wakasa-3
group)
(Table II). Time spent moving did not vary in any
of the age–sex classes in Takahama group (nonvegetated). In the nonvegetated enclosures, however,
females spent more time feeding and less time
resting and moving than males (Fig. 4). Time spent
grooming did not vary significantly by groups
according to their enclosure type for all age–sex
classes (Fig. 4), except between adult males and adult
females in Takahama and Wakasa-3 (both nonvegetated) groups, between immature males and immature females in Takahama group and between adult
females and immature females in Wakasa-3
(Table II). In Wakasa-5 group, grooming was only
significantly different between adult males and
immature males (Table II).
Relation between Temperature and Activity
Fig. 2. Distribution of diurnal behavioral activities of monkeys
living in vegetated (Wakasa-5) and nonvegetated captive
enclosures (Takahama and Wakasa-3).
In the vegetated enclosure group (Wakasa-5), we
found a negative correlation between time spent
feeding and temperature (Pearson correlation,
r 5 0.228, Po0.05, N 5 101). Resting time was not
correlated with temperature in this enclosure. However, regarding the two nonvegetated enclosures, in
Wakasa-3 only the time spent resting was positively
correlated with temperature (r 5 0.420, Po0.001,
N 5 50), whereas in Takahama no significant corre-
Fig. 3. Comparison of monthly average time spent for diurnal activity budgets between vegetated and nonvegetated captive monkeys.
Am. J. Primatol.
Enclosure Environment and Activity Budgets / 1139
TABLE II. MANOVA Post Hoc Results for the Comparison of Time Spent in Activities Across Age–Sex Class
Within Three Groups
Takahama
Activity
Age–sex
Feeding
Adult~–adult #
Adult~–immature~
Adult#–immature#
Immature~–immature#
Adult~–adult #
Adult~–immature~
Adult#–immature#
Immature~–immature#
Adult~–adult #
Adult~–immature~
Adult#–immature#
Immature~–immature#
Adult~–adult #
Adult~–immature~
Adult#–immature#
Immature~–immature#
Resting
Grooming
Moving
F1,
P
1848
17.33
29.56
102.6
35.34
5.91
16.61
4.11
Wakasa-3
F1,
0.87
o0.0001
o0.0001
0.2
0.08
o0.0001
o0.0001
0.01
o0.0001
0.3
0.3
0.004
0.9
0.07
0.7
0.2
1848
17.14
33.18
32.55
12.58
31.02
22.77
6.89
31.95
12.66
Wakasa-5
P
o0.0001
o0.0001
o0.0001
o0.0001
0.06
o0.0001
o0.0001
0.12
0.008
o0.0001
0.09
0.6
0.5
0.004
0.17
0.5
F1,
P
1848
147.5
52.33
12.26
6.74
238.07
48.16
34.73
12.1
6.13
o0.0001
o0.0001
0.0005
0.009
o0.0001
o0.0001
o0.0001
0.39
0.2
0.0005
0.2
0.9
0.01
0.3
0.14
Statistically significant P values appear in bold.
lations were found between time spent in any
activities and temperature.
Regardless of group, overall time spent feeding
and resting was significantly correlated with temperature only in adult females (Table III). Time
spent moving was only significantly correlated with
temperature in immature females, whereas grooming in immature males was negatively correlated
with temperature (Table III). Moreover, in the
vegetated enclosure, time spent feeding, grooming
and moving was significantly correlated with temperature only in adult females (r 5 0.291, Po0.01,
N 5 96; r 5 0.316, Po0.01, N 5 96 and r 5 0.235,
Po0.05, N 5 96, respectively).
Between the two nonvegetated enclosures, time
spent grooming was significantly correlated with
temperature only in Takahama and only for immature males (r 5 0.251, Po0.05, N 5 96). In
Wakasa-3, time spent feeding and resting was
significantly correlated with temperature only in
adult females (r 5 0.329, Po0.05, N 5 50 and
r 5 0.595, Po0.001, N 5 50 respectively). Also in this
group, time spent resting was significantly correlated
with temperature only in adult males (r 5 0.437,
Po0.01, N 5 50). No other activities were significantly correlated with temperature in any age–sex
class.
Inter- and Intra-Group Comparison of Feeding
on Provisioned and Natural Foods
The overall time spent feeding on provisioned
food did not differ significantly by enclosure type
(vegetated, nonvegetated) (ANOVA: F(1, 64) 5 0.123,
P 5 0.727). The Takahama group spent a nearly
equal amount of time feeding on natural foods as was
spent feeding on provisioned foods (6.2, 6.3 min/hr,
respectively). However, in the nonvegetated enclosure groups, considerably more time was spent
feeding on provisioned foods than on natural
vegetation (Takahama: 5.1, 0.6 min/hr; Wakasa-3:
7.2, 1.5 min/hr, respectively), as natural food was not
available to the extent that it was in the vegetated
enclosure. Taking the average amount of time spent
feeding on natural and provisioned foods by the two
groups in nonvegetated enclosures, (Takahama,
Wakasa-3), the amount of time spent feeding on
provisioned foods was highly significant (F(1,
64) 5 84.81, Po0.001).
DISCUSSION
Variation in the structure of activity budgets
(feeding, resting, moving, socializing, etc.) is attributed to fluctuating conditions of the environment in
which an animal lives. It is assumed that individuals
adjust their behavior in response to these conditions
based on a combination of age- and sex-specific
physiological factors. Naturally, an increase in one
behavior necessitates decreases in others. Kurup and
Kumar [1993] found that time devoted to feeding is
inversely related to that of resting. Temporal variations in temperature, especially high midday temperatures during the summer or dry season, may
cause an increase in time spent resting and a
decrease in social behavior [O’Brien & Kinnaird,
1997; Post, 1981; Robinson, 1986]. Activity budgets
are directly related to metabolism and reproduction,
and thus vary as energy requirements change across
the seasons [Halle & Stenseth, 2000].
We analyzed these relationships in three captive
Japanese macaque groups living in differing outdoor
Am. J. Primatol.
1140 / Jaman and Huffman
Fig. 4. Age–sex class variation of feeding, resting, grooming and moving in the vegetated and nonvegetated enclosures (M—Male,
F—Female).
TABLE III. Correlation Between Daily Average Temperature and Daily Activity (Sec.) Budgets Across Age–Sex
Classes (all Groups)
Age–sex
Adult male
Adult female
Immature male
Immature female
Activity
Feeding
Resting
Grooming
Moving
Feeding
Resting
Grooming
Moving
Feeding
Resting
Grooming
Moving
Feeding
Resting
Grooming
Moving
Statistically significant P values appear in bold.
Am. J. Primatol.
Correlation (r 5 )
0.111
0.044
0.062
0.018
0.248
0.156
0.065
0.059
0.019
0.035
0.156
0.025
0.069
0.006
0.111
0.141
Significance level (P 5 )
Sample size (N 5 obs. days)
0.085
0.492
0.335
0.784
o 0.000
0.015
0.313
0.358
0.767
0.584
0.015
0.697
0.288
0.927
0.084
0.028
243
243
243
243
243
243
243
243
243
243
243
243
243
243
243
243
Enclosure Environment and Activity Budgets / 1141
enclosure types (vegetated and nonvegetated) and
compared trends with the existing primate literature, in particular that of wild Japanese macaques on
the sub-tropical island of Yakushima [Hanya, 2004;
Marushashi, 1981]. Prediction 1 was supported by
our results. As summarized in Figure 5, we found
that the relative proportion of time spent in the four
major activities—resting, grooming, feeding and
moving—varied according to groups living in different enclosure types, reflecting differences and similarities in their respective behavioral modifications
in relation to their living conditions.
In both vegetated (Wakasa-5) and nonvegetated
(Takahama and Wakasa-3) enclosures, monkeys
spent more time resting compared with other
activities. This was greater than the time spent
resting by wild Yakushima macaques [Hanya, 2004;
Maruhashi, 1981]. In contrast, the proportion of time
spent resting by the vegetated group was similar to
that of a group of wild lion-tailed macaques (33% of
the day time) in the highlands of southern India
[Kurup & Kumar, 1993].
In all activities but moving, the activity budget
for the vegetated group was closer than the nonvegetated group to that of wild Yakushima macaques. Surprisingly, although the time spent moving
by Yakushima macaques was expected to be higher,
the nonvegetated groups actually spent a relatively
similar proportion of time moving, and spent more
time moving particularly, by Takahama group, than
the vegetated group (Wakasa-5) (Fig. 5). This may be
partly explained by the observation that in Takahama group the movement of dominant individuals
sometimes resulted in the supplanting of lower
ranking family groups, which led to a chain reaction
of many individuals moving around the periphery of
the enclosure. In the other two groups (Wakasa-3
and Wakasa-5), the structural or natural vegetative
Fig. 5. Relative proportion of time spent in resting, grooming,
feeding and moving in PRI captive groups and wild Yakushima
Japanese macaques. The values for Yakushima monkeys are the
mean values derived from Maruhashi [1981] and Hanya [2004].
enrichment provided individuals with the opportunity to avoid such types of interactions, limiting this
kind of movement.
Maruhashi [1981] found that the time devoted to
social grooming (27.9%) by Yakushima macaques is
exceptionally high in relation to other activities
when compared with other primates. Time devoted
to this activity was even higher than the PRI captive
groups reported here (nonvegetated, 13.2% and
vegetated, 16.1%).
Prediction 2 was supported by our results.
Monkeys in all enclosures spent more time resting
than feeding (Fig. 1). Furthermore, it was found that
monkeys in the two nonvegetated enclosures spent
more time resting than feeding (Fig. 2). This may be
a behavioral modification on their part to conserve
needed energy brought about by access to provisioned foods only.
Prediction 3 was supported by important differences in the amount of time spent feeding between
the vegetated and nonvegetated enclosure groups.
That is, monkeys in the two nonvegetated enclosures
spent less time feeding than monkeys in the
vegetated enclosure (Fig. 2). Agetsuma and Nakagawa [1998] predicted that when food availability
increases, monkeys increase feeding time. We found
that the presence of natural food in the vegetated
enclosure resulted in the monkeys spending more
time feeding. Interestingly, the amount of time spent
feeding by the vegetated group (27.1%) was intermediate to that of two troops on Yakushima (23.5
and 38%, Maruhashi, 1981; Hanya, 2004, respectively, see Fig. 5).
In the vegetated enclosure time spent feeding on
natural food was equal to the amount of time spent
feeding on provisioned food, and overall they spent
twice as much time feeding as did monkeys in the
nonvegetated enclosures. In spite of the fact that the
provisioned diet is supposed to adequately provide for
basic growth and reproduction, vegetated monkeys
devoted more time to feeding. The motivation to feed
more may be based on factors other than nutritional
or energetic deficit alone. Three possible explanations
are proposed for this difference; (1) regardless of
nutritional or energetic needs, when given the
opportunity to feed more, captive primates continue
to do so until satiated, (2) monkeys prefer a greater
diversity in their diet than that available from
provisioned foods alone, or (3) other nonnutritive
elements missing in the provisioned diet are available
in natural vegetation, and when given the opportunity, monkeys seek to fulfill these needs. Analysis of
the diet’s chemical and nutritional content is needed
to further evaluate these possibilities.
Feeding and moving are energy-consuming
activities [Coelho et al., 1976]. Food availability is
expected to fluctuate seasonally as energy expenditures are expected to fluctuate with changes in
temperature [Halle & Stenseth, 2000]. Japanese
Am. J. Primatol.
1142 / Jaman and Huffman
macaques living in the high-altitude region of
Yakushima decreased time spent moving and feeding
with decreasing temperature [Hanya, 2004]. At
temperate Takagoyama, the time spent feeding and
resting fluctuated seasonally [Yotsumoto, 1976]. In
winter, when the least amount of food was available,
time spent feeding dropped to its lowest levels of the
year [Yotsumoto, 1976]. For Japanese macaques
living in the lowland sub-tropical areas of Yakushima, time spent feeding and resting is constant
between months, whereas time spent grooming
increases from October to –December and moving
decreases toward winter [Maruhashi, 1981]. Vasey
[2005] noted that for red-ruffed lemurs in the
lowland coastal rain forest of Madagascar, time
allotted to feeding and resting mainly depended on
food availability. In Geoffroy’s marmosets, time
spent resting and foraging showed a significant
difference between the dry and wet seasons and is
related to the availability of food, i.e. insects
[Passamani, 1998]. Hill [1997] also noted seasonal
trends for Japanese macaques on Yakushima related
to the availability of plant and insect foods.
Therefore, according to Prediction 4, we expect
that time spent feeding and resting should vary
seasonally according to food availability to meet
nutritional and energetic demands. Prediction 4 was
supported by our results. We found that the time
spent feeding was significantly correlated with
temperature in the vegetated enclosure (Wakasa-5).
However, between the two nonvegetated enclosures,
time spent resting was significantly correlated with
temperature only in the Wakasa-3 group. This is
likely owing to the availability of more shaded
resting places provided by the multi-floored tower,
not found in Takahama group enclosure, allowing
them to rest for longer duration during hot periods of
the year. Time spent resting was greatest in summer
and shortest in autumn (Fig. 3). In the vegetated
enclosure, monkeys spent more time feeding in
spring, when low quality foods such as young leaves
and grasses were most abundant; presumably eating
more to satisfy nutritional needs from available
sources. In autumn, the vegetated group (Wakasa5) spent relatively less time feeding than other
seasons (Fig. 3). Autumn is a period when availability of nutrition-rich foods in the vegetated
enclosure increases, in particular a variety of fruits
and nuts became available, e.g. C. japonica,
E. japonica, P. glabra, Q. glauca. In winter, monkeys
in all enclosures spent relatively more time feeding,
assumedly to maintain body heat, resulting in the
reduction in time spent in other activities, such as
resting and moving in winter months. Adult females
spent significantly more time feeding and less time
resting in colder temperatures, probably owing to
food availability in the vegetated enclosure and
perhaps, equally important, owing to the need to
accumulate fat during the early reproductive stage.
Am. J. Primatol.
Prediction 5 was supported by our results. We
found that immatures spent more time feeding year
round than did adults. This was more pronounced for
the vegetated enclosure, where monkeys have access
to both provisioned and natural foods at the same
time. Immatures of both sexes spent more time
feeding and less time resting than adults, particularly in the vegetated enclosure, throughout the year
(Fig. 4). Immature monkeys spent more time feeding
throughout the year, perhaps because they are more
active and need more nutrients for physical development and maturation [Watanuki & Nakayama,
1993]. Juvenile Yakushima macaques spent more
time playing and moving whereas females spent
more time grooming and feeding, and were more
active than males [Maruhashi, 1981]. Immatures
may be accumulating more energy reserves for
sexual maturation by spending more time feeding
and less time resting, regardless of season. In the
vegetated enclosure, unlike provisioned food, natural
food items are small in size (fruits and flowers),
sometimes few in number, and not always easy to
process. Therefore, monkeys, and particularly immatures, eat constantly by extending their feeding
time to satisfy energy demands [Hanya, 2004;
Nakagawa, 1989b]. In the vegetated enclosure,
immature individuals, particularly females, spent
more time feeding on natural foods, partly because
they were often chased away by adults from the site
of provisioning when food was first given. Dominant
individuals tend to monopolize high-quality food
patches until they are satiated [Post et al., 1980].
Watanuki and Nakayama [1993] reported that
adult male Japanese macaques spent less time
grooming than adult females. Similar trends are
noted for males of other primate species [CluttonBrock, 1974; Smith, 1977; Waser, 1977]. The possible
reasons for this are: (1) they do not face the energy
costs of pregnancy and lactation; (2) in most primate
species, they are dominant to females and juveniles
and thus have access to the places of maximum food
availability; and (3) they tend to feed faster than
females and juveniles [Clutton-Brock, 1977]. In this
study, we found that adult males and females in
Wakasa-5 and Takahama groups spent more time in
social grooming than immatures of both sexes.
Young spent more time in feeding and engaged in
other social interactions, such as play.
In conclusion, the activity budgets of Japanese
macaques in ‘‘semi-naturally’’ vegetated and nonvegetated enclosures reflect adaptations related
mainly to food availability and seasonal changes of
temperature, largely by adjusting time spent feeding
and resting. Daily access to natural foods for
monkeys in the vegetated enclosure seems to be
largely responsible for the differences in daily time
budgets of the two enclosure types. Activity budgets
also varied across age–sex class. These data support
the idea that captive groups can be used to
Enclosure Environment and Activity Budgets / 1143
experimentally test behavioral adaptations to environmental conditions, and to evaluate species relevant food resources and provisioning schedules for
the betterment of their living conditions. One
approach, if the goal is to provide captive primates
with conditions as close to those in the wild as
possible, would be to experiment with the amount,
type and timing of provisioning across seasons.
Furthermore, we are currently investigating the
nutritional properties of plant foods selected by
different age–sex classes in the vegetated enclosure
to verify the nutritional and potential medicinal
effect of natural vegetation on the health of
individuals. This is needed to evaluate and compare
the differences between a traditionally provisioned
diet and the one enhanced by natural vegetation. For
primates in captivity, evaluating the benefits of this
type of environmental enrichment concerning the
physiological and mental well-being of the group is
an important and essential process in the formulation and refinement of management practices.
ACKNOWLEDGMENTS
We express our gratitude to the Center for
Human Evolution Modeling Research for maintaining the enclosure facilities and caring for the
monkeys, and to the ‘‘research and animal care’’
committee for permission to conduct our research in
the enclosures at PRI. We thank our colleagues Drs.
A. Mori, T. Furuichi, G. Hanya, H. Sugiura,
C. Hashimoto, H. Takemoto and others at PRI for
their valuable suggestions and comments during the
research period, oral presentations and manuscript
preparation. We thank Dr. K. Zamma and Dr. A.D.
Hernandez for their guidance in analyzing the data.
We thank A. D. Hernandez and A. MacIntosh for
reading and commenting on an earlier draft of the
manuscript. We are grateful to participants of the
annual conference of the Primate Society of Japan,
from whom we benefited in their many constructive
comments and advice. M. F. J. was supported by a
Graduate Studies Scholarship ‘‘Monbukagakusho’’
(Ministry of Education, Culture, Sports, Science and
Technology, Japan). Finally, we are grateful to
associate editor Dr. W. D. Hopkins and two anonymous reviewers for their helpful comments.
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