close

Вход

Забыли?

вход по аккаунту

?

Effects of caller activity and habitat visibility on contact call rate of wild Japanese macaques (Macaca fuscata).

код для вставкиСкачать
American Journal of Primatology 70:1055?1063 (2008)
RESEARCH ARTICLE
Effects of Caller Activity and Habitat Visibility on Contact Call Rate of Wild
Japanese Macaques (Macaca fuscata)
HIROKI KODA, YUKIKO SHIMOOKA, AND HIDEKI SUGIURA
Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
A major function of contact calls in nonhuman primates is to maintain spatial cohesion among
individuals in a group. The risks of spatial/visual separation from the group are likely to affect auditory
contact behavior, in particular by increasing the call rate. We tested whether the risk of separation
influences coo call emission by investigating the variation in call rate among behavioral contexts in two
wild populations of Japanese macaques (Macaca fuscata). We focused on caller activity and the degree
of visibility within the habitat as primary potential factors mediating call rate. We first estimated the
habitat visibility of the two research sites at Yakushima Island (YK) and Kinkazan Island (KZ), Japan.
The habitat visibility of YK was significantly more restricted than that of KZ. We then compared the
call rate of 20 adult and 12 juvenile female macaques between the two wild populations to examine the
potential effects of environmental differences. Both populations had a lower call rate during grooming
than during feeding and moving, which are behaviors associated to higher interindividual distances.
The call rate of YK adult females was significantly greater than that of both juveniles and KZ adult
females, independently of activity. The call rate increased as macaques matured in the YK population,
but not in the KZ population, suggesting that different developmental processes involved in contact
calling of the two populations. Our findings suggest that separation risk influences call rate, and also
imply a possibility of social influence that social structure change effects on the call rates. Am. J.
c 2008 Wiley-Liss, Inc.
Primatol. 70:1055?1063, 2008.
Key words: Japanese macaques; contact calls; habitat visibility; caller activity; call rate
INTRODUCTION
Contact calls are used by many social animals
[Bradbury & Vehrencamp, 1998]. Primates are
usually organized into a wide variety of social groups,
and their behaviors within a group are coordinated.
In nonhuman primate social groups, contact calls
serve to maintain interindividual spatial cohesion
more efficiently than by visual contact, i.e., monitoring of group members [Boinski & Garber, 2000].
Several studies have shown that adult monkeys
frequently produce contact calls to prevent separation from other group members [white-faced capuchins: Boinski, 1993; Boinski & Campbell, 1995;
squirrel monkeys: Boinski & Mitchell, 1992; chacma
baboons: Cheney et al., 1996; Rendall et al., 2000;
pygmy marmosets: Cleveland & Snowdon, 1982;
Japanese macaques: Itani, 1963; rhesus macaques:
Rendall et al., 1996], and that juvenile monkeys
frequently emit contact calls when they are separated from their mothers [white-faced capuchins:
Gros-Louis, 2002; chacma baboons: Rendall et al.,
2000]. Thus, one function of these calls is to prevent
separation. The degree of risk of separation primarily determines the style of auditory and visual
contact communication used for spatial cohesiveness.
r 2008 Wiley-Liss, Inc.
The behavioral context should have a primary
effect on contact calling, because the degree of
spacing among individuals varies broadly according
to context, such as activity levels [e.g., Stevenson,
1998]. Previous studies on the contact calls of whitefaced capuchins, i.e., trill calls, demonstrated that
trills were frequently produced while traveling or
during activities related to spatial separation in both
adults and juveniles [Boinski, 1993; Boinski &
Campbell, 1995; Gros-Louis, 2002], supporting the
effect of behavioral context on contact calling. Other
Contract grant sponsor: Grant-in-Aid for JSPS Fellows; Contract grant number: 15-5472; Contract grant sponsor: Grant-inAid for Young Scientists; Contract grant numbers: 19730461;
and 14740419; Contract grant sponsor: Grant for the Global
COE; Contract grant number: A6.
Correspondence to: Hiroki Koda, Department of Behavioral and
Brain Science, Primate Research Institute, Kyoto University,
Kanrin 41, Inuyama, Aichi 484-8506, Japan.
E-mail: koda@pri.kyoto-u.ac.jp
Received 6 March 2008; revised 23 June 2008; revision accepted
23 June 2008
DOI 10.1002/ajp.20597
Published online 21 July 2008 in Wiley InterScience (www.
interscience.wiley.com).
1056 / Koda et al.
primates [e.g., ring-tailed lemurs: Oda, 1996] have
shown similar patterns.
Forest habitat structure is also a significant
factor influencing contact calls. In natural habitats,
auditory signals are subject to temporal and spectral
degradation, as well as frequency-dependent
attenuation, when sounds travel through the environment [Wiley & Richards, 1978]. For example, birds
have clearly been shown to adjust their acoustics to
habitat [e.g., Brumm, 2004; Slabbekoorn & Smith,
2002]. The influence of forest habitat structure on
the acoustical call structure of several nonhuman
primate species has been reported [blue monkeys,
gray-cheeked mangabeys, vervet monkeys, and yellow baboons: Brown et al., 1995; pygmy marmosets:
de la Torre & Snowdon, 2002; Japanese macaques:
Sugiura et al., 2006; Tanaka et al., 2006; blue
monkeys: Waser & Brown, 1984, 1986]. Although
many studies have investigated the effects of forest
habitat on the acoustic features of contact calls, little
information is available on the effects of habitat on
call rates or patterns. An exception is a study by
Boinski and Campbell [1995], who compared the call
rates of several call types in white-faced capuchins
between a wet and dry forest, and found differences
in vocal usage patterns between the populations.
They also found that forest habitat structure, such as
visibility, affected the call rate and the emission
pattern.
In general, behavioral context and forest habitat
structure influence contact call behavior, because the
risk of spatial separation from a group varies broadly
according to behavior and habitat [Boinski & Garber,
2000]. We predicted that these two factors would
interact to lead to variation in the contact call rate.
Regarding behavioral context, activity type should
greatly impact call rate. Because individuals within a
group usually disperse during foraging or moving,
and show spatial cohesiveness during grooming, the
degree of separation risk likely differs among these
activities. Habitat visibility is a major environmental
factor mediating call rate. Because monkeys more
often become separated from the group in a habitat
with restricted visibility, they probably increase
their call rate to ensure spatial cohesiveness. However, few studies have investigated the interaction
between caller activity and habitat visibility. Therefore, we examined the effects of this interaction on
the contact call rates of wild Japanese macaques.
Japanese macaques are suitable models for this
examination for many reasons. Comparative ecological and sociological studies have been performed on
this species [e.g., Yamagiwa et al., 1998]; they are
widely distributed from warm- to cool-temperate
zones in Japan, and they inhabit forests from the
seashore to alpine regions [Agetsuma & Nakagawa,
1998]. Although habitat visibility has never before
been evaluated objectively, we predict different
degrees of visibility in their different habitats. In
Am. J. Primatol.
addition, Japanese macaques emit ??coo?? calls as
contact calls to maintain group cohesion. The coo call
is the most frequent call type of their vocal repertoire
and is uttered in a broad range of contexts [Green,
1975; Mitani, 1986; Okayasu, 1987; Sugiura, 2007b].
Several studies on wild populations have consistently
suggested that Japanese macaques adjust or modify
the acoustic structure of coo calls for the efficient
maintenance of spatial cohesion among individuals
[Koda, 2004, 2008; Sugiura, 1993, 1998, 2007a,b;
Sugiura et al., 2006; Tanaka et al., 2006].
We tested whether separation risk influenced
coo call emission by investigating the variation in call
rate according to caller activity and habitat structure. First, we directly evaluated the habitat visibility of the two study sites using a laser range finder.
We then compared the rates of coo calls of wild
Japanese macaques between two populations inhabiting forests with variable visibility as well as the
three major behavioral activities, i.e., feeding, moving, and grooming. Moreover, to better clarify the
effects of the interaction of caller activity and habitat
visibility, we also considered caller age differences.
Adult females normally remain in contact with other
adult females in the group, whereas juveniles
normally remain in close proximity to their mothers
in this species [e.g., Nakamichi, 1996], suggesting
that risk of separation varies according to age.
Therefore, contact call rates should be different
between adults and juveniles. This basic condition of
proximity should predict that the effects of the
interaction between activity and habitat on call rates
will differ between adult and juvenile monkeys.
METHODS
The research methodology complied with protocols approved by the guidelines (Guide for the Care
and Use of Laboratory Primates, Second Edition) of
the Primate Research Institute, Kyoto University,
Japan, and adhered to the legal requirements of
Japan.
Study Sites
We investigated two wild populations of Japanese macaque, one inhabiting Yakushima Island
(YK) in southern Japan (30.41N, 130.41E) and one
at Kinkazan Island (KZ) in northern Japan (38.11N,
141.31E). The total area of Yakushima Island is
approximately 503 km2, and the study site is located
on the northwest coast (0400 m above sea level). The
mean annual temperature is approximately 211C and
annual rainfall is approximately 2,600 mm. The site
is covered with warm-temperate, broad-leaved forest
species. The forest canopy consists mainly of Fagaceae and Lauraceae. Deciduous trees include several
species of Ficus. Thus, the diversity of plant species
is very high within the study area [Agetsuma &
Nakagawa, 1998]. The total area of Kinkazan Island
Activity and Visibility Effects on Calls / 1057
is approximately 10 km2, with a peak at 445 m above
sea level. The mean annual temperature is 111C and
annual rainfall is approximately 1,500 mm. The
island is covered with a mixed deciduous?coniferous
forest, which includes trees such as Fagus crenata,
Abies firma, and Pinus thunbergii. However, the
saplings of woody plant species rarely develop into
mature trees owing to high feeding pressure by Sika
deer, Cervus nippon; grasslands are widely spreading
in areas of the study site [Agetsuma & Nakagawa,
1998]. Both populations were equally habituated to
human observers [e.g., Yamagiwa et al., 1998].
d :
Evaluation of Environmental Characteristics
Among the several physical environmental characteristics that may affect macaque vocal behavior,
we focused on habitat visibility, i.e., the degree of
visual perspective in the forest. In other words, we
examined how far we could observe certain objects
(e.g., trees, rocks) from an arbitrary location in the
forest. We evaluated habitat visibility using the
procedures that follow.
We randomly chose 50 and 80 measuring
locations from the home range of the subject
macaque populations of YK and KZ, respectively.
The home ranges of YK and KZ were approximately
70 and 100 ha, respectively; therefore, one or two
measuring locations per 2 ha were carefully chosen to
avoid sampling bias.
We then measured the distance between the
observer and the farthest object on the ground using
a laser range finder (Laser Rangefinder Nikon Laser
800S, Nikon, Tokyo, Japan; measurement range 5 10?730 m; measurement accuracy 5 0.5 m; Fig.
1) at each measuring location. The observer used the
laser range finder at a height of 100 cm from the
ground. In the case of the farthest objects within
10 m, we directly measured the distance using a tape
measure. In our measurements, the target objects
were mostly stones or trees. If there were no
appropriate stones or trees in any direction, then
we measured the distance to the surface of the
ground. The distance was defined as the maximum
visible distance (MVD), and we recorded MVDs in
eight directions, i.e., 0, 45, 90, 135, 180, 225, 270, and
3151, determined using a magnetic compass at each
measuring location (Fig. 1). To reduce measuring
error, we measured each distance five times, and
adopted the average value for the MVD in that
direction. All measurements were taken on sunny
days from 17 May to 3 June 2005 at YK and from
18?23 July 2005 at KZ.
We defined the degree of visual perspective from
each measuring location. First, the visible area
from each location was calculated based on the
MVDs in eight directions. We estimated the area as
a polygon with eight vertices (Fig. 1). By denoting
the MVD at direction y as dy, we could calculate the
Fig. 1. Schematic representation of the MVDs in eight directions
(0, 45, 90, 135, 180, 225, 270, and 3151) and circle approximation.
The star represents the standing point of the observer for
measuring MVD using a laser range finder. The eight directions
were measured with a magnetic compass. The visible area of the
polygon (area within bold lines) and the estimated radius r were
used for the circle approximation. The area of the polygon
represents the S value, which is equal in size to the gray circle
with radius r. The estimated radius r was used for the
subsequent analysis. MVD, maximum visible distance.
area of the polygon as follows: S Ό π1=2ή sin πp=4ή
P
7
iΌ0 dπp=4ήi dπp=4ήπiώ1ή , where S is the polygon dimension, i is an integer, and d0 5 d2p. We calculated 50
and 80 visible areas for YK and KZ, respectively. We
then approximated the visible polygon using apcircle
?????????
of radius r and calculated r as S 5 pr2 or r Ό S=p.
The circle approximation allowed us to interpret the
result of the visible area more easily because r
represented the standardized distance based on the
visible area (Fig. 1). We could treat r as the degree of
visual perspective at the measuring location. The
distribution pattern of r values is likely to reflect the
specific features of environmental characteristics at
each site. We performed a Mann?Whitney test on the
r values to test which habitat had better visibility.
Behavioral Observations
Subject populations and animals
Field observations were carried out for three
groups of the YK population (Kw, Kw-A, and Kw-Z)
and one group of the KZ population (A) from 2002 to
2005 during the nonmating season. Kw, which was
the original group on Yakushima Island, split into
two groups (Kw-A and Kw-Z) between August 2003
and April 2004. In 2002 and 2003, the Kw Group was
composed of about 50 individuals (range: 48?56
individuals), including 21 adult females (Z4 years),
15 or more adult males (Z4 years), 4 juvenile females
(1?3 years), 4 juvenile males (1?3 years), and some
unidentified monkeys. After fissioning of the Kw
Group, there were 15 individuals (6 adult females,
Am. J. Primatol.
1058 / Koda et al.
2 adult males, 3 juvenile females, 2 juvenile males,
and 2 infants (o0 years)) in the Kw-A Group, and up
to 40 (14 adult females, Z11 adult males, 3 juvenile
females, and 4 juvenile males) in the Kw-Z Group in
2004 and 2005. In 2004, the Kinkazan-A Group was
composed of 39 monkeys (17 adult females, 5 adult
males, 5 juvenile females, 4 juvenile males, and 8
infants). We identified all subject macaques before
observations.
We focused on the coo calls of females. We
collected data on the frequency ratio of calls from 20
adult females and 12 juvenile females from the two
study areas. Juvenile macaques were defined as
being between the ages of 1 and 3 years, and adult
macaques were older than 6 years. The ages of all
subjects in the Kinkazan-A Group and those of all
juvenile subjects in the Yakushima Kw-A and Kw-Z
Groups were confirmed; however, the ages of all
adult female subjects in the Yakushima Groups were
estimated from their appearance, a technique that is
widely accepted [e.g., Yamagiwa et al., 1998]. We
chose six female macaques from Kw, three from KwA, four from Kw-Z, and seven from A as subjects.
Moreover, we chose six juveniles from both the Kw-Z
and A Groups. As the individual differences of call
rates are likely large, therefore we made a great
effort to collect data from a large number of female
macaques. The age and observational period of all
subjects are listed in Table I.
Data collection
We observed subject animals using the focal
animal sampling method, with a given observational
session lasting more than 30 min. Observations were
carried out by the three authors, with an agreement
of behavioral sampling definition before observation.
We performed observations so that the total observation time was more than 4 hr for each subject (for
total time per subject, see Table I). Observations
were during both morning and afternoon to avoid the
sampling bias for each subject. Vocalizations were
TABLE I. The Population, Group, Sex, Age, Age Class, and Total Observation Time of the 32 Subject Animals
Subject
Population
Age (years)a
Age class
Group
Total observation
time (min)
Kinako
Mao
Rabi
Shima
Nene
Otoha
Ibis
Haro
Kiki
Kurara
Shifu
Atena
Mariko
Bera
Chiro
Mari
Chiara
Neri
Julia
Jun
Anie
Blanche
Chocolat
Doris
Hanna
Miyo
Nobuko
Raffie
Sara
Anne
Fumiko
Zina
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Kinkazan
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
Yakushima
1
1
1
1
3
3
11
14
15
17
18
19
20
1
1
1
2
2
3
Middle
Middle
Middle
Middle
Middle
Middle
Middle
Middle
Middle
Middle
Old
Old
Old
Juvenile
Juvenile
Juvenile
Juvenile
Juvenile
Juvenile
Adult
Adult
Adult
Adult
Adult
Adult
Adult
Juvenile
Juvenile
Juvenile
Juvenile
Juvenile
Juvenile
Adult
Adult
Adult
Adult
Adult
Adult
Adult
Adult
Adult
Adult
Adult
Adult
Adult
A
A
A
A
A
A
A
A
A
A
A
A
A
Kw-Z
Kw-Z
Kw-Z
Kw-Z
Kw-Z
Kw-Z
Kw-Zb
Kw-A
Kw-Zb
Kw-Z
Kw-Zb
Kw-Zb
Kw-Z
Kw-Z
Kw-Z
Kw-Z
Kw-Ab
Kw-A
Kw-Zb
437
427
423
449
433
425
1,316
1,003
1,620
1,277
1,457
1,722
824
278
259
242
501
243
241
732
241
813
741
843
758
778
311
240
438
365
242
241
a
Observation period
2004
2005
2005
2004
2004
2004
2004
2004
2004
2004
2004
2004
2004
2005
2005
2005
2004
2004
2004
2003
2004
2003
2004
2003
2003
2004
2004
2004
2004
2002
2004
2003
July
July
July
July
July
July
July
July
July
July
July
July
July
May
May
May
April?May
April?May
April?May
July, 2005 May
August
July, 2005 May
August, 2005 May
July, 2005 May
July, 2005 May
April?May, 2004 August, 2005 May
April?May
August
August, 2005 May
July
August
July
The ages of all subjects in the Kinkazan-A Group and all juvenile subjects in Yakushima Kw-A and Kw-Z Groups were confirmed. However, the ages of all
adult female subjects in the Yakushima population were estimated.
This was the Kw Group during observations. After group fission between August 2003 and April 2004, the subjects belonged to Kw-A or Kw-Z as indicated.
b
Am. J. Primatol.
Activity and Visibility Effects on Calls / 1059
Data analysis
For each subject, the call rate during each
activity was calculated as a frequency ratio, which
was the number of calls (times) during each activity
per observation time of each activity (min). To
examine the habitat, age class, and activity effects
on the call rate, we performed a four-way mixedmodel analysis of variance (ANOVA) using the
general linear mixed-model (GLMM) procedure with
population (YK or KZ), age class (adult or juvenile),
and activity (feeding, moving, or grooming) as fixed
effects, and individuals as a random effect. Least
significant differences (LSDs) were calculated for
post hoc comparisons among the significant main
effects if interactions were not significant. Moreover,
post hoc comparisons were performed using the
simple main effect test if some interactions were
significant. Because the grooming activity of two
subjects (Kinako, a KZ juvenile, and Julia, a YK
juvenile) could not be observed, we treated these
data as missing values in the GLMM analysis.
All statistical procedures were performed using
SPSS 13.01. In all ANOVAs we used the type III
sums of squares for all main effects [Grafen & Hails,
2002]. The significance level was set at Po0.05.
RESULTS
Habitat Visibility
The medians of the estimated radius r in the YK
and KZ habitats were 20 and 42.5 m, respectively
(Fig. 2). A Mann?Whitney U-test showed significant
differences between the two sites, indicating better
visibility at KZ than at YK (U 5 40, N1 5 50, N2 5 80,
100
r (m)
150
Habitat visibilities
50
counted using continuous recording methods. We
recorded the types of activities in three main
categories, i.e., feeding, moving, and grooming, using
instantaneous sampling methods with 1-min intervals. Feeding included searching for, handling, and
processing food, and moving within a food patch.
Grooming comprised social grooming, self-grooming,
and other grooming activities before grooming such as
approaching a grooming partner or soliciting grooming. Functionally, self-grooming is not allo-grooming.
However, self-grooming also frequently occurred
when monkeys could not find a grooming partner.
They remained alone and allo-grooming during the
time that other members allo-groomed at a particular
grooming site. Therefore, self-grooming was treated
as grooming in the same way as allo-grooming was in
our current analysis. Moving indicated movement
between food patches and resting sites. Activities that
were not classified as above were treated as undefined
activities in the analysis. We excluded all vocalization
associated with agonistic interactions or aggressive
events, such as screaming, as well as controllable
sounds such as sneezing.
Yakushima
Kinkazan
Fig. 2. Estimated visible distance radius r of Japanese macaque
habitat in Yakushima and Kinkazan. Box plots represent the
medians (horizontal bold lines), 25th and 75th percentiles
(bottom and top of box), the 1.5 interquartile range
(whiskers), and outliers (circles).
Po0.0001; Fig. 2). The statistical results and the
distribution patterns of the radii of visibility
(r values) clearly showed two characteristic properties of habitat visibility in the YK and KZ forests.
First, the visual perspectives were extremely limited
throughout the YK forest. Visibility in YK had a
short perspective distance (median: 20 m) and small
range (25th?75th percentile: 16?22 m; Fig. 2). The
small range suggests poor visibility. These environmental properties likely restrict visual contact
among macaques to about 20 m throughout the YK
forest. In contrast, visibility in KZ had a longer
perspective distance (median: 42 m) and greater
range (25th?75th percentile: 35?56 m; Fig. 2). However, there were many positive outliers for habitat
visibility in KZ, suggesting extremely high visibility
at this location (Fig. 2). Therefore, both physical
characteristics (i.e., distance and range) implied
poorer habitat visibility in the YK forest than in
the KZ forest.
Call Rate
The mean (7SE) calling rates of all observation
times for the four subject groups (YK adult, YK
juvenile, KZ adult, and KZ juvenile) were 0.95 (0.11),
0.51 (0.069), 0.48 (0.059), and 0.37 (0.055) times per
minute, respectively. There were significant main
effects of population, age class, and activity on the
call rates of monkeys (Fig. 3, Table IIa). However,
there was a significant two-way interaction between
population and age class (Table IIa). No other
interactions were significant.
The lack of significant interactions involving
activity suggested that population levels and age
Am. J. Primatol.
1060 / Koda et al.
Fig. 3. Call rates of Japanese macaques for each activity. Mean values with standard errors represent averaged values among each
subject?s mean call rate. Closed circles represent the Yakushima population and open triangles represent the Kinkazan population.
TABLE II. (a) Summary of Mixed-Model ANOVA Results of the Effects of Population, Age Class, and Activity on
the Call Rate of Japanese Macaques Using the GLMM Procedure, (b) Summary of Post Hoc Least Significant
Differences for Pair-Wise Comparisons of the Effect of Activity on the Call Rate of Japanese Macaques Using the
GLMM Procedure, and (c) Summary of Tests of the Simple Main Effects of Population and Age Class on the Call
Rate of Japanese Macaques Using the GLMM Procedure
F
P
10.0
11.8
21.2
6.94
2.63
0.36
0.72
0.004
0.002
o0.0001
0.013
0.081
0.70
0.49
Mean difference
95% Confidence interval
df
P
Feeding vs. moving
Feeding vs. grooming
Moving vs. grooming
0.058
0.397
0.338
?0.067 to 0.184
0.266?0.527
0.208?0.468
54.5
55.7
55.7
0.356
o0.0001
o0.0001
(c)
Simple main effects
(specific level of the other factor)
df
F
P
Population (adult females)
Population (juveniles)
Age class (Yakushima population)
Age class (Kinkazan population)
1,
1,
1,
1,
21.6
0.12
20.9
0.29
o0.0001
0.74
o0.0001
0.59
Source
df
(a)
Population
Age class
Activity
Population Age class
Population Activity
Age class Activity
Population Age class Activity
1,
1,
2,
1,
2,
2,
2,
(b)
Pair-wise activities
28.8
28.8
55.3
28.8
55.3
55.3
55.3
27.9
29.4
28.9
28.7
ANOVA, analysis of variance; GLMM, general linear mixed model.
class did not influence the activity types differently.
We performed post hoc pair-wise comparisons to
calculate the LSDs among the three levels of activity.
The call rate was significantly lower during grooming than during feeding or moving (Fig. 3, Table IIb).
Because there were no significant interactions with
activity, the effects of population and age class did
not differ among the three levels of activity. In
Am. J. Primatol.
contrast, the significant interaction of population
and age class suggested that the effect of population
differed between the two levels of age class and vice
versa. Therefore, we performed subsequent simple
main effect tests for each level of population and age
class. There was a significant effect of population for
adult females and a significant effect of age class for
the YK population (Table IIc). The results of both
Activity and Visibility Effects on Calls / 1061
ANOVA and simple main effect tests showed a
higher call rate only by the YK adult female subjects.
DISCUSSION
Effects of Caller Activity on Call Rate
Caller activity is generally one of the primary
factors regulating the call rate in a wild social
group [Boinski, 1993; Boinski & Campbell, 1995;
Gros-Louis, 2002]. Call rate during grooming was
lower than that during feeding or moving. Because
macaques disperse more and range farther during
feeding and moving than during other activities, coo
calls probably become more important. In contrast,
macaques usually groom within close proximity to
each other at grooming sites [e.g., Kawai, 1969].
Because of lower separation risk, auditory contact
during grooming is less necessary than during
feeding and moving. These results are supported by
previous studies that also reported that wild Japanese
macaques emit coo calls more frequently when they
are moving and feeding than when they are grooming
[Itani, 1963; Okayasu, 1987; Sugiura, 2007b].
Of further importance is the nonsignificant
difference in call rate between feeding and moving.
This suggests that caller activity certainly influences
call rate, but also that the degree of spatial dispersion
in the group is the primary factor influencing call rate,
in agreement with previous studies [Boinski, 1987,
1991, 1993; Boinski & Campbell, 1995, 1996; Boinski &
Garber, 2000; Boinski & Mitchell, 1992; Boinski et al.,
1994]. The acoustic variation in the calls of wild
Japanese macaques also supports this idea; the
acoustic features of the coo call increase detectability
and locatability in accordance with proximity rather
than caller activity [Sugiura, 2007b]. The variation in
call rate by activity in this study likely reflects the
potential variation in spatial dispersion.
Habitat Visibility and Age Effects
The differences in call rate between the populations are primarily explained by the variation in
habitat visibility. Because visibility is restricted in
the YK forest compared with KZ, macaques are
probably exposed to higher risk of separation from
the group. To maintain group cohesion, they likely
emit coo calls more frequently than KZ. In the KZ
habitat, it is possible for macaques to remain in
contact both visually and by calling. Consequently,
the adult call rate was greater at YK than at KZ. The
difference in adult female call rates between the
populations is probably provoked by the difference in
habitat visibility. As visual contact is impeded among
macaques at YK, spatial cohesion is probably maintained to a large extent by auditory contact achieved
by exchanging coo calls among individuals.
Although call emissions by adult female macaques were affected by the environment, this phe-
nomenon was not observed in juvenile macaques,
likely because juveniles normally maintain close
proximity to their mothers [Nakamichi, 1996],
whereas adult female macaques maintain contact
with other adult females within the group [Mitani,
1986]. Because the distances between adult female
members are relatively greater than those between
juveniles and their mothers, adult female contact
with other members is more strongly influenced by
habitat visibility. Contrary to adult females, juveniles are usually near their mothers, and their
contact is not affected by habitat visibility. Thus,
their call rates did not significantly differ between
the two populations. These findings suggest that call
rate is generally affected by habitat visibility in wild
Japanese macaques.
Separation Risk as a Fundamental Cause of
the Underlying Variation in Call Rates
Our results consistently showed that wild
Japanese macaques increase their call rate when
they risk losing the group, suggesting their sensitivity to spatial separation. For spatial cohesion in
primate social groups, we propose a fundamental
cause, namely separation risk. Indeed, separation
risk could explain the variation. For example, visual
separation during group travel leads to an increase
in the call rate, and in several primate species, the
call rate increases as distance among group members
increases [Boinski, 1991, 1993; Boinski & Campbell,
1995; Boinski & Mitchell, 1992; Cheney et al., 1996;
Rendall et al., 2000; Snowdon & Hodun, 1981]. These
findings, along with our current results, suggest that
auditory contact effectively serves to maintain
spatial cohesion, especially to compensate for visual
contact under conditions of low visibility.
Our study indicates that Japanese macaques are
sensitive to spatial separation, which is reflected in
their calls, in particular in acoustic modifications of
their contact calls according to the degree of spatial
separation. In both naturalistic observations and
experimental settings, increasing the distance between caller and recipient(s) led to more detectable,
longer-lasting, and/or higher-pitched calls [Masataka
& Symmes, 1986; Oda, 1996; Snowdon & Hodun,
1981; Sugiura, 2007b]. These findings both indicate
sensitivity to separation risk. Boinski and Garber
[2000] proposed a similar idea that vocal communication by contact calling is primarily determined
by the ??motivation to coordinate troop travel.?? They
suggested that increased motivation to coordinate
troop travel leads to higher call rates, louder calls,
longer travel signals, more fluctuation and modulation of acoustic signals, and more exaggerated
movements and monitoring of recipient responses.
Motivation to coordinate troop travel could be
interpreted as sensitivity to separation risk. Such
internal motivation or sensitivity likely determines
Am. J. Primatol.
1062 / Koda et al.
the type of vocal communication used in wild
primate social groups.
Further Directions
Another important contribution of this study is
the first systematic evaluation of habitat visibility.
Our procedure successfully described the qualitative
differences in habitat visibility between the two
research sites, considering previous data on vegetation sampling [Maruhashi et al., 1998]. They carried
out vegetation sampling at YK and KZ Islands, and
found that the density of trees at YK was 13.4 times
that at KZ, and that the density of small trees was
particularly greater at YK, suggesting lower visibility
there. Furthermore, grasslands were spreading at
the KZ study site. The high density of trees
corresponds to our results for YK habitat visibility,
whereas the low density of trees and grasslands
corresponds to our results for KZ. The importance of
forest structure on contact calls has been strongly
suggested [Boinski & Garber, 2000], but habitat
visibility has never before been considered. Our
procedure could be applied together with geographic
information system techniques in future studies on
audiovisual contact communication in wild populations.
Finally, another factor that should not be overlooked is social influence or effect of individual life
histories on matrilineal society. The social framework influences intragroup vocal communication
[e.g., Snowdon & Hausberger, 1997]. For example,
call usage is developmentally acquired via social
learning from adults [e.g., Seyfarth & Cheney, 1986].
Social status also likely determines the pattern of
vocal communication. Adult male primates, including Japanese macaques, usually produce fewer
contact calls than adult females [Boinski, 1991;
Boinski & Garber, 2000; Mitani, 1986]. Such sex
differences in contact calls are no doubt provoked by
sex differences in social status or role for group
cohesiveness. We should extend our current findings
in future research by considering social status,
social life history, and social dynamic change. For
example, our data might have been affected by
variable social structures of the four subject
groups, as we can expect that the call rate can be
influenced by the numbers of potential partners
among a group. Increasing the call rate in YK adult
females might have been provoked by the social
structure of large Kw-Z Group. Although the juvenile
call rate is generally higher than that of the adult
females in other primate species [e.g., Boinski &
Campbell, 1995, 1996; Gros-Louis, 2002], our contrary result for YK might be explained by such a
social structure variation. To examine such social
influences on call rates, we have to investigate more
groups of a greater variety of compositions and sizes.
The comparison of call rates of troops at prefission
Am. J. Primatol.
and postfission is also appropriate. Although we
had insufficient data to address this factor, members
of the split group (Kw-A), which was smaller than
the original group (Kw), might have gradually
decreased their call rates because this split small
group also seems to have become more spatially
cohesive. Future research should consider other
factors such as social influences on vocal communication of wild populations.
ACKNOWLEDGMENTS
We appreciate helpful comments from Professor
Nobuo Masataka and Dr. Yasuyuki Muroyama
throughout the study, and we thank Professor Kosei
Izawa, Dr. Masaki Shimada, Dr. Yamato Tsuji, and
the researchers of Kinkazan Island for information on
the Kinkazan-A Group. We also thank the researchers
and residents of Yakushima Island for their help, the
Yakushima Environment Conservation Center for
permission to perform the research, and the field
research center of KUPRI for permission to stay at
the field station in Yakushima Island during the
research. The manuscript was considerably improved
thanks to Dr. M. A. Huffman and two anonymous
referees. The research methodology complied with
protocols approved by the guidelines (Guide for the
Care and Use of Laboratory Primates, Second Edition)
of the Primate Research Institute, Kyoto University,
Japan, and adhered to the legal requirements of
Japan. This work was supported by a Grant-in-Aid for
JSPS Fellows to H. K. (15-5472), a Grant-in-Aid for
Young Scientists (B) to H. K. (19730461) and H. S.
(14740419), and a Grant for the Global COE (A6) to
Kyoto University, MEXT, Japan.
REFERENCES
Agetsuma N, Nakagawa N. 1998. Effects of habitat differences
on feeding behaviors of Japanese monkeys: comparison
between Yakushima and Kinkazan. Primates 39:275?289.
Boinski S. 1987. Birth synchrony in squirrel monkeys (Saimiri
oerstedi)?a strategy to reduce neonatal predation. Behav
Ecol Sociobiol 21:393?400.
Boinski S. 1991. The coordination of spatial position?a field
study of the vocal behavior of adult female squirrel
monkeys. Anim Behav 41:89?102.
Boinski S. 1993. Vocal coordination of troop movement among
white-faced capuchin monkeys, Cebus capucinus. Am J
Primatol 30:85?100.
Boinski S, Campbell AF. 1995. Use of trill vocalizations to
coordinate troop movement among white-faced capuchins?
a 2nd field test. Behaviour 11?12:875?901.
Boinski S, Campbell AF. 1996. The huh vocalization of whitefaced capuchins: a spacing call disguised as a food call?
Ethology 102:826?840.
Boinski S, Garber P, editors. 2000. On the move: how and why
animals travel in groups. Chicago: The University of
Chicago Press.
Boinski S, Mitchell CL. 1992. Ecological and social factors
affecting the vocal behavior of adult female squirrel
monkeys. Ethology 92:316?330.
Boinski S, Moraes E, Kleiman DG, Dietz JM, Baker AJ. 1994.
Intragroup vocal behavior in wild golden lion tamarins,
Activity and Visibility Effects on Calls / 1063
Leontopithecus rosalia?honest communication of individual activity. Behaviour 1?2:53?75.
Bradbury JW, Vehrencamp SL. 1998. Principles of animal
communication. Sunderland, MA: Sinauer.
Brown CH, Gomez R, Waser PM. 1995. Old World monkey
vocalizations?adaptation to the local habitat. Anim Behav
50:945?961.
Brumm H. 2004. The impact of environmental noise on song
amplitude in a territorial bird. J Anim Ecol 73:434?440.
Cheney DL, Seyfarth RM, Palombit R. 1996. The function and
mechanisms underlying baboon ?contact? barks. Anim
Behav 52:507?518.
Cleveland J, Snowdon CT. 1982. The complex vocal repertoire
of the adult cotton-top tamarin (Saguinus oedipus oedipus).
Z Tierpsychol 58:231?270.
de la Torre S, Snowdon CT. 2002. Environmental correlates of
vocal communication of wild pygmy marmosets, Cebuella
pygmaea. Anim Behav 63:847?856.
Grafen A, Hails R. 2002. Modern statistics for the life sciences.
Oxford: Oxford University Press.
Green S. 1975. Variation of vocal pattern with social situation
in the Japanese monkey (Macaca fuscata): a field study. In:
Rosenblum LA, editor. Primate behavior. New York:
Academic Press. p 1?102.
Gros-Louis J. 2002. Contexts and behavioral correlates of trill
vocalizations in wild white-faced Capuchin monkeys (Cebus
capucinus). Am J Primatol 57:189?202.
Itani J. 1963. Vocal communication of the wild Japanese
monkey. Primates 4:11?66.
Kawai M. 1969. Ecology of Japanese monkeys (Nihonzaru no
seitai). Tokyo: Kawade Shobo (in Japanese).
Koda H. 2004. Flexibility and context-sensitivity during the
vocal exchange of coo calls in wild Japanese macaques
(Macaca fuscata yakui). Behaviour 141:1279?1296.
Koda H. 2008. Short-term acoustic modifications during
dynamic vocal interactions in nonhuman primates?implications for origins of motherese. In: Masataka N, editor. The
origins of language. Tokyo: Springer. p 59?73.
Maruhashi T, Saito C, Agetsuma N. 1998. Home range
structure and inter-group competition for land of Japanese
macaques in evergreen and deciduous forests. Primates
39:291?301.
Masataka N, Symmes D. 1986. Effect of separation distance on
isolation call structure in squirrel monkeys (Saimiri
sciureus). Am J Primatol 10:271?278.
Mitani M. 1986. Voiceprint identification and its application to
sociological studies of wild Japanese monkeys (Macaca
fuscata yakui). Primates 27:397?412.
Nakamichi M. 1996. Proximity relationships within a birth
cohort of immature Japanese monkeys (Macaca fuscata) in a
free-ranging group during the first four years of life. Am J
Primatol 40:315?325.
Oda R. 1996. Effects of contextual and social variables on
contact call production in free-ranging ringtailed lemurs
(Lemur catta). Int J Primatol 17:191?205.
Okayasu N. 1987. Coo sound communication. Quaternary
Anthropol 19:12?30 (in Japanese).
Rendall D, Rodman PS, Emond RE. 1996. Vocal recognition of
individuals and kin in free-ranging rhesus monkeys. Anim
Behav 51:1007?1015.
Rendall D, Cheney DL, Seyfarth RM. 2000. Proximate factors
mediating ??contact?? calls in adult female baboons (Papio
cynocephalus ursinus) and their infants. J Comp Psychol
114:36?46.
Seyfarth RM, Cheney DL. 1986. Vocal development in vervet
monkeys. Anim Behav 34:1640?1658.
Slabbekoorn H, Smith TB. 2002. Habitat-dependent song
divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals. Evolution
56:1849?1858.
Snowdon C, Hausberger M, editors. 1997. Social influences on
vocal development. New York: Cambridge University Press.
Snowdon CT, Hodun A. 1981. Acoustic adaptations in
pygmy marmoset contact calls?locational cues vary with
distances between conspecifics. Behav Ecol Sociobiol 9:
295?300.
Stevenson PR. 1998. Proximal spacing between individuals in
a group of woolly monkeys (Lagothrix lagotricha) in Tinigua
National Park, Colombia. Int J Primatol 19:299?311.
Sugiura H. 1993. Temporal and acoustic correlates in vocal
exchange of coo calls in Japanese macaques. Behaviour
124:207?225.
Sugiura H. 1998. Matching of acoustic features during the
vocal exchange of coo calls by Japanese macaques. Anim
Behav 55:673?687.
Sugiura H. 2007a. Adjustment of temporal call usage during
vocal exchange of coo calls in Japanese macaques. Ethology
113:528?533.
Sugiura H. 2007b. Effects of proximity and behavioral context
on acoustic variation in the coo calls of Japanese macaques.
Am J Primatol 69:1412?1424.
Sugiura H, Tanaka T, Masataka N. 2006. Sound transmission
in the habitats of Japanese macaques and its possible effect
on population differences in coo calls. Behaviour 143:
993?1012.
Tanaka T, Sugiura H, Masataka N. 2006. Cross-sectional and
longitudinal studies of the development of group differences
in acoustic features of coo calls in two groups of Japanese
macaques. Ethology 112:7?21.
Waser PM, Brown CH. 1984. Is there a sound window for
primate communication? Behav Ecol Sociobiol 15:73?76.
Waser PM, Brown CH. 1986. Habitat acoustics and primate
communication. Am J Primatol 10:135?154.
Wiley RH, Richards DG. 1978. Physical constraints on acoustic
communication in atmosphere?implications for evolution
of animal vocalizations. Behav Ecol Sociobiol 3:69?94.
Yamagiwa J, Izawa K, Maruhashi T. 1998. Long-term studies
on wild Japanese macaques in natural habitats at
Kinkazan and Yakushima: preface. Primates 39:
255?256.
Am. J. Primatol.
Документ
Категория
Без категории
Просмотров
6
Размер файла
136 Кб
Теги
habitat, macaque, fuscata, called, contact, rate, wild, effect, visibility, japanese, activity, call, macaca
1/--страниц
Пожаловаться на содержимое документа