Chapter 1: Research History of Japanese
Macaques in Japan
Juichi Yamagiwa

1.1

Scope of Japanese Primatology in the First Stage

Japanese primatology is characterized by a unique history among mammalian studies
in Japan. In general, mammalogists initiated their studies by collecting specimensfrom the point of view of systematics, morphology, and physiology, and theninvestigated the adaptive significance of these traits from the aspect of ecology. In
contrast, the Japanese primatologists initiated their studies with sociologicalperspectives. After World War II, Kinji Imanishi, based in the Department of
Zoology, Kyoto University, started his field studies on feral horses (Equus caballus)
at Cape Toimisaki in Miyazaki Prefecture. The aim of his study was to understandthe species society and to thus trace the evolution of human society (Asquith 1991,
2000; Takasaki 2000). The concept of species society had developed from his study
on mayflies skittering around the river in Kyoto and extended to all living things(Imanishi 1941). He began to consider the evolution of animal societies, and inparticular, the evolution of human society through comparisons with other animalsocieties (Imanishi 1951a).
During a survey on feral horses at Toimisaki in 1948, his students Jun’ichiro
Itani and Shunzo Kawamura encountered a group of wild Japanese macaques(Macaca fuscata fuscata; Fig. 1.1). Although it was very brief, they were impressedby this encounter and expected a more complex social structure to be present in
macaques than in horses. Thus, they decided to study Japanese macaques andformed the Primate Research Group in 1951. They searched extensively for goodstudy sites for Japanese macaques in their natural habitats in Japan. However, theJapanese macaques were very shy and were frightened away from encounters withhuman observers as a result of past hunting and chase pressures from the farmland

J. Yamagiwa (*)
Laboratory of Human Evolution Studies, Department of Zoology, Division of Biological
Sciences, Graduate School of Sciences, Kyoto University, Kitashirakawa-oiwakecho,
Sakyo, Kyoto 606-8502, Japane-mail: yamagiwa@jinrui.zool.kyoto-u.ac.jp
N. Nakagawa et al. (eds.), The Japanese Macaques,
DOI 10.1007/978-4-431-53886-8_1, © Springer 2010

3

4

J. Yamagiwa

Fig. 1.1 Pioneers of Japanese primatology at Cape Toimisaki in 1950. From left to right: Shunzo
Kawamura, Kinji Imanishi, Kisaburo Tokuda, and Jun’ichiro Itani. (From Itani Jun’ichiro Archiveof Primate Research Institute, Kyoto University)

inhabitants. Kawamura and Itani tried to habituate macaques by provisioning (feedingthem with sweet potatoes, wheat, or soybeans) and finally succeeded in provisioningat Koshima Islet (Miyazaki Prefecture) and Takasakiyama (Oita Prefecture) in 1952.
Imanishi conducted field studies on feral horses by identifying each individual
and naming it. He thought this method to be essential for illustrating social interactions among individual animals. The Japanese primatologists used this method tostudy Japanese macaques and, later on, other primate species. Individual identification by marking had previously been used by Clarence R. Carpenter for rhesus
macaques (Macaca mulatta) at Cayo Santiago Island. Instead of using artificial
marks, the Japanese primatologists identified each macaque by features and bodycharacteristics (shape, color, scars). The first generation of Japanese primatologists
thought that social structure was not merely a reflection of individual survival or
reproductive strategies but reflected a norm of species-specific sociality (Itani 1972,1985). To elucidate the social features of primates, Imanishi devised a guide to fieldstudies by (1) adopting methods of comparative sociology, (2) basing work on
individual identification, and (3) recording social interactions from prolonged continuous observations (Imanishi 1951b, 1957).
Daily observations on social interactions among Japanese macaques at the artificial
feeding sites produced many findings. The social structure of Japanese macaques is basedon multimale–multifemale group formation with linear dominance rank, a leadershipsystem, and matrilineal kin relationships (Itani 1954; Kawamura 1958; Kawai 1964).

Chapter 1: Research History of Japanese Macaques in Japan

5

Females acquire their dominance rank via two rules: (1) a daughter is dominant to all
females who are subordinate to her mother and (2) maturing daughters become dominant to their older sisters, a process termed youngest ascendancy (Kawamura 1958).
Correspondingly, females belonging to the same kin-group outrank females of otherkin-groups, and dominance rank among mature sisters correlates inversely with age.
Dominance relationships between individuals often reflect their affiliative relationships
to the third party who is dominant to both of them (Kawai 1958). After provisioning, thegroup size rapidly increased, and the large group consisting of more than 100 individuals split into several groups everywhere (Sugiyama 1960; Furuya 1960). The increased
conflicts between matrilineal kin-groups with increasing group size may have causedgroup fission, and after such separations males associated with kin-groups unrelated tothem (Koyama 1970).
Another important finding induced by provisioning was the “culture” ofJapanese macaques. A young female started to wash sandy potatoes with freshwaterin a stream near an artificial feeding site at Koshima a few years after provisioning.
Then, she began washing potatoes and wheat with seawater (Fig. 1.2). These newly
acquired techniques were transmitted to other group members. Kawamura (1959)
and Kawai (1965) called such sharing a subculture or preculture, and traced theprocess of transmitting such information. Other than feeding techniques, conspicuous
local variations were found in paternal care (Itani 1963a) and in some vocalizations

Fig. 1.2 Washing potatoes
with seawater at Koshima Islet.
(Photograph by Noritsugu
Yamaguchi)

6

J. Yamagiwa

in close proximity (Itani 1963b). Imanishi (1957) and Itani (1991) regarded suchvariations in subtle behavior as behavioral culture in Japanese macaques.
Detailed observations on social interactions among macaques led to various
findings of their complex social perceptions. Mori (1975) found local variations in
vocalizations emitted in grooming requests. Affiliative interactions among solitary
males and alliance formations in conflicts within groups have been reported (Sato
1977; Watanabe 1979; Sugawara 1980). Mother–son relationships, along with
development (Norikoshi 1974) and dominance relationships in extraordinary large
groups with provisioning (Mori 1977), have been described and analyzed from thepoint of view of social organization of Japanese macaques. Sociosexual behavior
and changes in sexual partnership through copulation were analyzed in relationshipto individual life history (Hanby et al. 1971; Hanby and Brown 1974; Enomoto
1974, 1978; Takahata 1980, 1982). These findings suggested that higher dominancerank did not always lead males to mating success, but that their past relationships
with females or their choice of females might affect their success. It was suspectedthat provisioning may have influenced such relationships and choices.

1.2

Field Studies of Japanese Macaquesin Their Natural Habitats

Provisioning Japanese macaques stimulated not only research interests but also thetourism industry in Japan. Oita City has conducted provisioning of Japanesemacaques with researchers from the beginning, and opened the Monkey Park at
Takasakiyama to attract tourists who could observe macaques at close range. Thisnew business was very successful. The Japanese macaques and their social life wereintroduced in newspapers, journals, films, and television programs, and many tourists visited Takasakiyama, paying the entrance fee for monkey watching. By 1977,
the number of monkey parks with provisioned Japanese macaques available fortourism had increased to 37 in Japan (Nihonzaru Editorial Committee 1977;
Fig. 1.3).
However, provisioning appeared to have a great influence on the life of Japanesemacaques. The annual rate of increase in group size at Takasakiyama after provisioning was 1.102, which meant that group size doubled every 7 years (Masui 1976).
Irrespective of location, without exception group size increased after provisioning,
and tended to exceed 100 individuals after prolonged provisioning (10–20 years)(Nihonzaru Editorial Committee 1977). Provisioning improved the nutritional condition of Japanese macaques and increased survival rates and birth rates, especiallyfor dominant-class females (Sugiyama and Ohsawa 1982). Daily travel distancedecreased, and the ranging of the macaques concentrated on the artificial feedingsites. Their activity time budget for feeding and moving decreased and that for resting
and for social interactions thus increased. Agonistic interactions may have increased
at the artificial feeding sites, and such situations may have reinforced dominancerelationships among group members (Wada 1979; Izawa 1982). Provisioning alsoChapter 1: Research History of Japanese Macaques in Japan

7

Fig. 1.3 Provisioning of Japanese macaques at Iwatayama Monkey Park in Arashiyama

affected unprovisioned groups by male movements. The larger groups produced byprovisioning stimulated more males to transfer into adjacent small groups andchanged intergroup relationships (Suzuki et al. 1975; Sugiyama and Ohsawa
1982).
These findings at the artificial feeding sites led the younger generation ofJapanese primatologists to study Japanese macaques in their natural habitats. From
single groups observed under isolated conditions at Takasakiyama, Koshima, andArashiyama (Kyoto Prefecture), Itani (1954) and Kawai (1964) concluded that all
males sought dominant social status within a group and that the losers left the group
to become solitary males. However, as observations on male immigration andemigration increased in various habitats where several groups overlapped theirranges, it became obvious that males usually leave their natal groups before maturity. They transfer into other groups and do not stay for a prolonged period, evenafter taking the highest rank (Sugiyama 1976). It began to appear likely that several
small multimale–multifemale groups in partly overlapping ranges might represent
the natural population structure (Kawanaka 1973). In 1952, just before provisioningat Koshima and Takasakiyama, Kawamura and Itani visited Yakushima Island,
Kagoshima Prefecture (the southern limit of distribution) and estimated such asocial structure as consisting of several groups for Japanese macaques (Macaca
fuscata yakui) from fragmentary observations and information from hunters (Itani
1952). However, because of the success of provisioning, Japanese primatologists
did not choose Yakushima as their study site. If they had continued their intensive
field studies at Yakushima, they could have easily found such social structure inwhich males frequently transferred between groups. It was only in the mid-1970s
that the younger generation of Japanese primatologists started to conduct field studies

8

J. Yamagiwa

Fig. 1.4 Japanese macaques in the warm-temperate forest at Yakushima Islandin the natural habitats of Japanese macaques everywhere in Japan without
provisioning.
However, it was difficult to habituate Japanese macaques in their natural habitats
because of their shyness and the dense undergrowth in deciduous forests.
Researchers started to follow the fresh trails of macaques on the snow. They could
observe macaques on the snow, but stayed at considerable distance, and observations were limited to winter. Only two places were found to satisfy the conditions
for observations. Subtropical and warm-temperate forest at the low altitude ofYakushima is characterized by poor undergrowth, and visibility is high (Fig. 1.4).
Their high density and small home ranges meant that it was easier to find themacaques there than in other areas. The western side of Yakushima was declared anational park in 1964, and it is not inhabited by local people. Young primatologists,
including high school teachers and university students, formed research groups andconducted a census voluntarily in the early 1970s (Iwano 1983). Tamaki Maruhashi
started habituation of a group of Japanese macaques without provisioning in 1975,
and I joined him to habituate three groups in 1977 (Maruhashi 1980; Yamagiwa
1985). Another good study site was Kinkazan Island (Miyagi Prefecture), which iscovered by cool-temperate forest. Dense undergrowth usually reduces the visibilityof macaques in the cool-temperate forest of Japan. However, because of the highdensity of sika deer (Cervus nippon) in Kinkazan, herbs and shrubs were overgrazed, and visibility was high. The small island allowed researchers to findmacaques again after losing them to sight. Similar to Yakushima, this island also
was not inhabited by local people, and Kosei Izawa started to conduct long-term
field studies on Japanese macaques without provisioning in 1982 (Izawa 1983).
Field studies on Japanese macaques in natural habitats had been conducted
mainly in snowy areas in the 1960s and 1970s. The habitats of Japanese macaquesconstitute the northern limit of living nonhuman primate distribution. Their morphological, physiological, and ecological features may reflect their past adaptations

Chapter 1: Research History of Japanese Macaques in Japan

9

Fig. 1.5 Japanese macaques in the snow at Shiga Heights

to the coldest climate in primate habitats. The foods, feeding behavior, and activity
budget of Japanese macaques were investigated during heavy snow in winter (Wadaand Tokida 1981; Izawa 1982; Fig. 1.5). Several general surveys including morphology, population genetics, physiology, and ecology were conducted in various
habitats, and the adaptive features of Japanese macaques to cold climates wereanalyzed. Uehara (1977) compared food composition of Japanese macaques among
different types of vegetation and found their most common foods occurred in the
cool-temperate and warm-temperate forests. He hypothesized that dietary featuresof Japanese macaques reflect those of their ancestors coming across the Korean
Peninsula. Nozawa et al. (1975) collected and analyzed blood samples from
macaques captured during the surveys and proposed the “stone-step hypothesis,”
meaning that gene flow occurred by male transfers between groups similar to skippingstones on the surface of the water when we throw them. Male Japanese macaques
usually leave their natal group and travel a long distance to join other groups(Hazama 1965; Nishida 1966). Nozawa et al. (1991) estimated that two local populations with an intervening distance of more than 100 km were geneticallyindependent.

1.3 Prolonged Socioecological Studies in Yakushima
and Kinkazan
Ecological studies on Japanese macaques were conducted in their natural habitats
in the 1970s. After preliminary studies on their dietary features, activities, and ranging
in snowy areas, their foraging strategies in relationship to environmental factors
were analyzed in various habitats. The marked seasonal changes were found in their

10

J. Yamagiwa

Fig. 1.6 An alpha-male of a small group in the lowland forest at Yakushima Island

daily activity rhythm (Yotsumoto 1976), and the relationship between nutritional
intake and energy expenditure in individual female macaques was analyzed fromthe bioenergetic point of view (Iwamoto 1974, 1982). A significant correlation was
found between food quality with group size, daily travel distance, and home range
size in both warm-temperate and cool-temperate forests (Ikeda 1982; Furuichi et al.
1982). Takasaki (1981) found a positive correlation between their group size andhome range size in both habitats, and that home range size was greater in the cooltemperate forest than in the warm-temperate forest for the same group size.
A highest density of Japanese macaques in their entire habitats was estimated at
the low elevations of Yakushima (Maruhashi 1982; Iwano 1983). A preliminary
survey conducted at higher altitudes found lesser density and larger ranges ofmacaques but a similar group size to macaques at lower altitudes (Azuma et al.
1984). As Itani had expected in 1952, we found that Yakushima macaques formed
smaller groups with a high socionomic sex ratio (SSR: the number of reproductive
males/the number of reproductive females within a group) and moved in smaller
ranges than did Japanese macaques in other habitats (Iwano 1983; Azuma et al.
1984; Fig. 1.6). Both ecological and social factors shaping these social features
were investigated and discussed (Maruhashi 1982; Furuichi 1983, 1984, 1985;
Yamagiwa 1985; Oi 1988).
Habituation and long-term research with individual identification of several
groups found that social features of Yakushima macaques differed from thoseof Japanese macaques in other habitats (Fig. 1.7a,b). In provisioned groups ofJapanese macaques at Takasakiyama, Gagyusan (Okayama Prefecture), andArashiyama, group fission occurred with large group size (more than 100 individuals),and several kin-groups of females associated with a few group males to create a
new group during the nonmating season (Furuya 1960; Sugiyama 1960; Koyama1970). At Yakushima, group fission occurred at a smaller group size, mainly by
nongroup males and estrous females with their kin-groups during the mating season(Maruhashi 1982; Yamagiwa 1985). A large number of males left their groups andChapter 1: Research History of Japanese Macaques in Japana11

Non-mating season
M

Join at bottom

M
M
Rank
M
M

Mating season
M

M
M
M

F-F-F-F-F

M

M
M
M
M

M
M

F-F-F-F-F-F

M
M

M
M
M

M

F-F-F

M
M
F-F-F

F-F-F

Non-mating seasonb

Group fission occurs
during the non-mating
seasonMating season
M

M

M
M

M

M
F-F-F-FM
F-F-F-F

M

M

M

TakeoverM

M

M
F-F-F-FM

M

F-F-F-F

Join at bottom

M

M

M
Group fission occurs
during the mating season

M

M

M
F-F-F

F-F-F

F-F-F

Fig. 1.7 Individual movements and group structure of Japanese macaques based on the studies ofprovisioned groups (a), and group fissions observed in a population of Yakushima (b). M and F
indicate adult male and female macaques, respectively. F An estrous female. Solid arrows, individual movements; dotted arrows, dominance ranks (from bottom to top rank)

visited other groups as nongroup males to solicit mating with estrous females during the mating season (Yamagiwa 1985; Sprague 1992). When group takeover
occurred by nongroup males, females extended their estrous periods and showedstrong proceptivity (Okayasu 2001). The youngest ascendancy in the dominancerelationships among sisters (Kawamura 1958) was not found in the Yakushimagroups (Hill and Okayasu 1995).

12

J. Yamagiwa

The population of Japanese macaques at Kinkazan was very small (a groupwith 60–70 individuals) when Izawa visited this island for the first time in 1962
(Izawa 1983). He found four groups with 250 individuals in 1982, when hestarted habituation of these macaques without provisioning. After a sudden dipof population size in 1984 as a result of poor climate and food conditions, thispopulation has recovered rapidly through two group fissions during 10 years(Izawa 2001). Since then, a population census has been conducted by Izawa andhis colleagues every year at Kinkazan. Feeding ecology was the main subject offield studies, and the optimal feeding strategy from the aspect of energetics wasinvestigated (Nakagawa 1989a, 1990a,b; Saito 1996). Individual feeding strategies during the period of food scarcity in winter were argued based on data from
Kinkazan and Shimokita Peninsula, Aomori Prefecture (Nakagawa 1989b, 1997;
Watanuki and Nakayama 1993; Nakayama et al. 1999). A strong gregariousness
among individuals during the cold weather, and differences in mating successbetween group and nongroup males, were investigated (Takahashi 1997, 2001).
Differences in the social structure of the Kinkazan population from those ofother populations have become apparent by these studies.
Various factors, such as climate, vegetation, provisioning, or isolated conditions, may shape the socioecological features of Japanese macaques (Yamagiwa
and Hill 1998). To identify such factors, we formed working groups to comparesocioecological features of Japanese macaques between Yakushima (warm-temperate forest) and Kinkazan (cool-temperate forest). Food abundance, food patch
density, daily travel distance, home range size, proportion of overlap between
ranges of neighboring groups, population density, group size, SSR, activity timebudget, reproductive parameters, frequency of intergroup encounters, antagonism
of intergroup encounters, dominance relationships between groups, male emigration and immigration, and mating patterns were compared, and relationships
between variables were discussed (Table 1.1). In summary, under the higherquality and more abundant food conditions (Agetsuma and Nakagawa 1998;
Maruhashi et al. 1998), the Yakushima macaques compete more severely forresources between groups than the Kinkazan macaques (Saito et al. 1998; Sugiura
et al. 2000). Such competition leads to strong intergroup antagonism, which poses
the risk of group extinction or a decreased birth rate of subordinate groups after a
bad fruiting season (Takahata et al. 1994a,b, 1998; Suzuki et al. 1998a; Sugiura
et al. 2002). Female macaques at Yakushima more positively solicit nongroup
Table 1.1 Ecological and social features of Japanese macaques at Kinkazan and Yakushima
KinkazanYakushima
Environmental conditions
Year of habituation
1982
1976
No. of study groups
4–6
2–5
Mean temperature
11
20
Annual rainfall (mm)
1,500
3,000
(continued)

Chapter 1: Research History of Japanese Macaques in Japan

13

Table 1.1 (continued)
KinkazanYakushima

Cool-temperate
32
180
94
39.6

Warm-temperate
62
2,417
1,802
12.4

151
1,878
221
53
12
30
0.6
48.7
0.34
54
34
12
10

70
1,464
90
63
23
80
4.2
27.1
0.87
31
45
21
32

35
7.1
2.4
Male < female
6–18
23

27
6.1
2.2
Male > female
5–14
25

0.012
15
16
Unclear

0.039
64
46
Large group >small group
Male > female
Males are moreaggressive

Forest typeNo. of species of trees (>5 cm in DBH)
Density of trees (no./ha)Density of food trees (no./ha)Mean diameter at breast height (DBH) (cm)
Ecological features
Distance between consecutive feeding patches (m)Daily travel distance (>10 h observation) (m)Annual home range (ha)Range overlap between neighboring groups (%)
Core area overlap between neighboring groups (%)
Population density (individuals/km2)
Group density (groups/km2)
Mean group size (individuals)
SSR (no. reproductive males/no. reproductive females)
Feeding time budget (%)
Moving and resting time budget (%)
Social grooming time budget (%)
Feeding on fruit in total feeding time (%)
Reproductive parameters
Birth rate (no. births/female/year) (%)
Age at first parturition (years)
Interbirth interval (years)
Survival ratio (1–3 years old)
Age to participate in reproduction (female) (years)
Infant mortality (within 1 year after birth) (%)
Social features
No. intergroup encounters (no./h)
Proportion of agonistic encounter (mating season) (%)
Proportion of agonistic encounter (nonmating season) (%)
Dominance relationships between groups
Sex differences in aggression
Aggression during mating season

Male > female
No difference

Male life history
Age at first emigration (years)
Mean length of stay after immigration (years)
Dominance rank at immigration
HighestMiddleLowestSolitary male
All-male group
Copulation by nongroup male (%)
Source: Primates (1998) Vol. 39(3), Sugiura et al. (2000)

4.7
2.9

5.3
2.8

1
2
6
Many
Many
41

13
1
14
Few
Few
41

14

J. Yamagiwa

males to associate with them during the mating season (Yamagiwa and Hill 1998;
Okayasu 2001). Such a tendency may promote frequent male movement between
groups and diverse entries, frequent group fissions by estrous females and nongroup males, and frequent nonagonistic interactions among males within a group(Sprague et al. 1998; Takahashi and Furuichi 1998). As socioecology predicts, thestrong intragroup competition may form female social bonds and nepotism inJapanese macaques (Nakagawa 1998).
However, although food quality and availability may explain female gregariousness and relationships, many aspects of male association and movements remain
unknown (Takahashi and Furuichi 1998; Horiuchi 2005, 2007). As suggested by the
recent arguments in primate socioecology (Janson 2000; Koenig 2002; Henzi andBarrett 2003), it is difficult to find clear relationships between environmental factors and social variation within primate species where the environment changes
rapidly. Adding to socioecological analyses, we should consider variation in socialfeatures of Japanese macaques in relationship to their community structure,including several groups and their life history in future studies (Yamagiwa 2008).

1.4

New Scope of Field Studies and Conservationof Japanese Macaques

Until the present, long-term studies on Japanese macaques with individual identification have been conducted for provisioned groups at various sites in Japan. Life
history parameters based on demographic data for more than 50 years have been
analyzed in both Koshima (Watanabe 2003) and Takasakiyama (Kurita et al. 2008).
Infant social development, parental behavior, and social relationships among adultmales and females have been analyzed from long-term observations at Katsuyama,
Okayama Prefecture (Itoigawa 1973, 2001; Nakamichi and Shizawa 2003;
Nakamichi and Yamada 2007; Nakamichi et al. 1995). At Arashiyama, long-term
behavioral observations and DNA analysis from hair and fecal samples found thatmale mating success relied heavily on female choice in relationship to the male’s
length of tenure (Huffman 1987; Takahata et al. 1999; Inoue and Takenaka 2008).
Stone handling behavior (Nahallage and Huffman 2008; Huffman et al. 2008)
and social object play (Shimada 2006) have also been analyzed in relationship toenvironmental and social factors at Arashiyama. Suckling behavior and nipple
preference have been analyzed in relationship to parity at Shiga Heights, Nagano
Prefecture (Tanaka 1989, 1992, 1997, 2004). Kutsukake and Hasegawa (2005)
reported the mutualism among males when a turnover occurred in a provisioned
group at Shiga Heights. Grooming interactions such as louse egg-handlingtechniques for hygienic purposes (Tanaka 1995; Zamma 2002) or as a reciprocal
strategy for association (Muroyama 1991, 1996) have been analyzed and consideredfrom observations at long-term study sites.
Intensive field studies with individual identification have also been conductedwithout provisioning at Yakushima and Kinkazan (Yamagiwa 2008; Izawa 2009).

Chapter 1: Research History of Japanese Macaques in Japan15

A census to estimate population size, group size, and group composition has been
made every year at Shimokita, Kinkazan, Hakusan (Ishikawa Prefecture), andYakushima. Yoshihiro et al. (1999) implemented a new method at higher elevationsof Yakushima, dividing each research area into grid squares of 500 × 500 m, withan observer positioned in each grid square at a fixed point. Three to six fixed
observers formed a party together with a leader who tracked the macaques.
This method adapted the conventional census method for unhabituated groups ofJapanese macaques so that nonprofessional fieldworkers could participate. These
censuses found that small groups inhabited the higher elevations with relatively
high density, in spite of the cold climate (Yoshihiro et al. 1999; Hanya et al. 2003).
Subsequent field studies made at higher altitudes suggest that total annual foodabundance, especially fruit, was the determinant factor of density, and mature
leaves constituting fallback foods may mitigate the severity of fruit scarcity (Hanya
2004a,b; Hanya et al. 2004). At Kinkazan, long-term monitoring of food resources
and feeding behavior found that Japanese macaques changed their choice of foods
according to large fluctuations in nut production (Tsuji et al. 2006).
The flexible feeding strategies of Yakusima macaques according to seasonalchanges in availability of high-quality foods (Agetsuma 1995a,b,c; Agetsuma
and Noma 1995; Maruhashi and Takasaki 1996), their feeding ecology in relationship to seed dispersal (Noma and Yumoto 1997; Yumoto et al. 1998; Otani
and Shibata 2000), and vocal and behavioral communication (Mitani 1986;
Tsukahara 1990; Sugiura 1993, 1998; Sugiura and Masataka 1995; Koda et al.
2008) were investigated and discussed. Based on identification of individual
macaques, female reproduction, mating strategies, intergroup male movements,and life history have been studied (Sprague et al. 1996; Thomsen 1997; Takahata
et al. 1998; Sprague 1998, 2004; Suzuki et al. 1998b; Soltis et al. 2001;
Matsubara and Sprague 2004; Thomsen and Soltis 2004; Soltis 2004; Thomsen
et al. 2006). These data on reproductive strategies of both female and male
Japanese macaques in natural habitats were comparable to those in provisioned
groups (Koyama et al. 1992; Itoigawa et al. 1992; Watanabe et al. 1992; Takahata
et al. 1994b, 1995).
Adding to these findings, the recent scope of field studies would focus more
attention on individual reproductive strategy using steroid hormones or DNA markers.
By measurement of urinary and fecal steroid metabolites during the ovulation
cycle, hormone profiles and reproductive features have been investigated both incaptivity and in the wild (Fujita et al. 2001, 2004). Microsatellite DNA analysis andpolymerase chain reaction (PCR) techniques have been used by collecting hair,fecal, or sperm samples for determination of paternity (Inoue et al. 1990, 1993;
Hayakawa and Takenaka 1999; Soltis 1999), and female and male reproductive
strategies have been discussed in relationship to ecological factors, group size,
dominance rank, tenure, or age (Takahata et al. 1999; Soltis et al. 2001; Soltis 2002;
Thomsen and Soltis 2004; Hayakawa 2008; Inoue and Takenaka 2008). DNA
markers have also been used for analysis of local genetic differentiation of Japanesemacaques (Hayaishi and Kawamoto 2006; Kawamoto et al. 2007a,b). Low genetic
diversity among populations of Japanese macaques suggests their recent dispersion

16

J. Yamagiwa

to the islands of Japan along with distribution of vegetation and ancient bottleneck
effects on some isolated populations (Kawamoto et al. 2007a,b, 2008). Morphologicalmethodologies based on skeletal and somatic specimens have been greatly improved
and used for analysis of local variations in the life history of Japanese macaques(Hamada et al. 1996, 2003).
These findings on the morphological, genetic, physiological, ecological, andsocial features of Japanese macaques have provided useful data for the conservation of wild populations and their habitats. However, these data have not been well
implemented into the policies of wildlife management by central and local governments. The main reasons were (1) a rapid increase of crop raiding by Japanesemacaques everywhere in Japan and (2) the difficulty of creating appropriate measures to control them because of their highly developed social and intellectual
activities. Although Japanese macaques had not been the main subject of hunting
so far, their ranging area had been limited to higher mountains until the 1960s.
They avoided contacts with humans, who actively chased them away from farmlands on the lower hills and plains. However, industrialization in the 1950s and1960s led to a decline of agriculture and to a rapid decrease in the population ofrural areas. Urbanization increased timber requirements for construction andaccelerated deforestation. Many roads were newly constructed in macaque habitats to transport commercial goods and people between prefectures. These humanactivities resulted in destruction of their natural habitats and increased theiraccess to farmlands. Wild macaques became accustomed to crops in the abandoned
farmlands and to humans using the newly constructed roads through contacts
with tourists, who fed them human foods. Capture of Japanese macaques tocontrol their raiding of crops gradually increased in the 1970s, exceeded 5,000
individuals, and reached 10,000 individuals at the end of the twentieth century(see Fig. 7.3 in Chap. 7).
Since the 1970s, Japanese primatologists have organized symposiums and workshops to discuss the recent changes in the number and range of Japanese macaques andappropriate measures to keep them away from farmlands without capturing them.
A number of surveys have been conducted to estimate the number of groups andtheir distribution (Yoshihiro et al. 1998; Watanabe 2000; Oi and Masui 2002).
Various measures have been designed and applied to decrease the raiding of crops
by wild macaques (Muroyama 2003; Izawa and Miyagi Research Group ofMonkeys 2005). Nevertheless, it is still difficult to establish the best methods tocontrol the macaque’s destructive activities, because there are numerous variationsin their behavior according to environmental conditions. Since the Primate Societyof Japan (PSJ) was established in 1985, Japanese primatologists have increased
their influential power on the policies and measures of the government. From the
beginning, PSJ has declared a high priority for conservation of the habitat ofYakushima macaques. Its continuous efforts obtained international support andresulted in inscription of the central part of Yakushima into the World Heritage List
in 1993 and in suspension of new road construction within the Heritage site atYakushima (Yamagiwa 2008). PSJ also declared that macaques captured for raiding
crops should not be provided for invasive experimental use and recommended that

Chapter 1: Research History of Japanese Macaques in Japan17

the Japanese government establish guidelines for experimental use of wild Japanesemacaques from the aspects of conservation and animal welfare in 2000 (Primate
Society of Japan 2000).
Since the 1980s, Taiwanese macaques, rhesus macaques, and long-tailed
macaques have dispersed into wild populations of Japanese macaques as a consequence of the closure of monkey gardens and inappropriate management of these
captive populations (Kawamoto et al. 2001, 2007a,b). These macaque species havea large influence on the wild population of Japanese macaques and on the ecosystems of their habitat. In Wakayama and Chiba Prefectures, these macaques started
interbreeding with Japanese macaques. PSJ proposed that these prefectures should
prevent interbreeding and has cooperated with them to capture these macaques until
now (Kawamoto 2005; Kawamoto et al. 2001, 2007a,b). The Japanese government
established a law for invasive alien species and included these macaques in the listin 2004. Decisions concerning capture of pest animals was transferred from theEnvironment Agency (currently Ministry of the Environment) of the Japanese
Government to city, town, and village mayors under the guidance of prefectural
governors in 1994. The Environment Agency established a new system for management and conservation of specific animals and ordered each prefecture to make aplan for its achievement in 1999. PSJ has cooperated with this action to provide amanual for prefectures.
Although we still have many problems in the conservation of Japanesemacaques, understanding of the importance of Japanese macaques as our nationaltreasure has become widespread in Japan. Ecotourism is one of the effective measures for primatologists to promote conservation of Japanese macaques and theirhabitats in cooperation with local people who are seeking harmonious development
in local economy and conservation. The monkey parks are now rising in popularity,especially among foreign tourists. In contrast to zoological parks or safari parks,
visitors can approach free-ranging macaques to enjoy direct observations of themin close proximity at the feeding sites. Feeding macaques by visitors is strictly
prohibited in most of the parks. Visitors are requested to follow the rules of observation and learn many things through careful observations. Watching the monkeys,
with naming of each individual, is our traditional way to understand their social
life. We need to maintain such field methods not only for research work but also forpromotion of ecotourism to combine with observations in their natural habitats. At
Yakushima, the number of tourists has greatly increased after the inscription ofWorld Heritage, and more than 180 professional guides take tourists for nature
walks every day. However, in addition to Japanese macaques, the number of sika
deer has prominently increased in the protected areas because of the prohibition of
hunting, and their damage of the undergrowth vegetation by feeding has brought
many endemic plant species to the danger of extinction (Yumoto and Matsuda
2006). Because of the lack of foods on the forest floor, deer follow macaques to eat
foods discarded by the macaques, even the macaques feces (Nishikawa andMochida, 2010). Management plans of wild populations of Japanese macaquesshould consider sympatric populations of other mammal species. Many tourists visit
natural forests and come in contact with wild macaques now, sometimes trying to18

J. Yamagiwa

feed them. The risk of disease transmission from human visitors and provisioning
by tourists is increasing and becoming a greater concern. To decrease such risks
and to promote conservation of Japanese macaques, cooperation with local nongovernmental organizations (NGOs) and local governments is particularly important.
None of the conservation measures will be successful without the interest andsupport of the local people.
Acknowledgments This study was financed in part by the Grants-in-Aid for Scientific Researchby the Ministry of Education, Culture, Sports, Science, and Technology, Japan (No. 19107007 to
J. Yamagiwa), and the Kyoto University Global COE Program “Formation of a Strategic Base for
Biodiversity and Evolutionary Research.”

References
Agetsuma N (1995a) Dietary selection by Yakushima macaques (Macaca fuscata yakui): theinfluence of food availability and temperature. Int J Primatol 16:611–627
Agetsuma N (1995b) Foraging strategies of Yakushima macaques (Macaca fuscata yakui). Int
J Primatol 16:595–609
Agetsuma N (1995c) Foraging synchrony in a group of Yakushima macaques (Macaca fuscata
yakui). Folia Primatol 64:167–179
Agetsuma N, Nakagawa N (1998) Effects of habitat differences on feeding behaviors of Japanesemonkeys: comparison between Yakushima and Kinkazan. Primates 39:275–291
Agetsuma N, Noma N (1995) Rapid shifting of foraging pattern by Yakushima macaques(Macaca fuscata yakui) in response to heavy fruiting of Myrica rubra. Int J Primatol
16:247–260
Asquith PJ (1991) Primate research groups in Japan: orientations and East-West differences.
In: Fedigan LM, Asquith PJ (eds) The monkeys of Arashiyama: thirty-five years of researchin Japan and the West. State University of New York Press, Albany, NY, pp 81–98
Asquith PJ (2000) Negotiating science: internationalization and Japanese primatology. In: Strum
SC, Fedigan LM (eds) Primate Encounters. The University of Chicago Press, Chicago andLondon, pp 165–183
Azuma S, Ohtake M, Yamagiwa J, Ashizawa S. Akaza H, Miyagawa T, Fujita T, Iwakawa T, Oi
T (1984) Ecological survey of the Yaku Japanese monkeys (Macaca fuscata yakui) in the
Yaku-shima Widerness Area, Yakushima Island. Conservation Reports of The Yaku-shima
Widerness Area, Kyushu, Japan, Nature Conservation Bureau, Environment Agency, Japan,
pp 517–568 (in Japanese with English summary)
Enomoto T (1974) The sexual behavior of Japanese monkeys. J Hum Evol 3:351–372
Enomoto T (1978) On the social preference in sexual behavior of Japanese monkeys (Macaca
fuscata). J Hum Evol 7:283–293
Fujita S, Mitsunaga F, Sugiura H, Shimizu K (2001) Measurement of urinary and fecal steroid
metabolites during the ovarian cycle in captive and wild Japanese macaques, Macaca fuscata.
Am J Primatol 43:167–176
Fujita S, Sugiura H, Mitsunaga F, Shimizu K (2004) Hormone profiles and reproductive charactersin wild female Japanese macaques (Macaca fuscata). Am J Primatol 64:367–375
Furuichi T (1983) Interindividual distance and influence of dominance on feeding in a natural
Japanese macaque troop. Primates 24:445–455
Furuichi T (1984) Symmetrical patterns in non-agonistic social interactions found in unprovisioned Japanese macaques. J Ethol 2:109–119

Chapter 1: Research History of Japanese Macaques in Japan

19

Furuichi T (1985) Inter-male associations in a wild Japanese macaque troop on Yakushima Island,
Japan. Primates 26:219–237
Furuichi T, Takasaki H, Sprague DS (1982) The winter range utilization of a Japanese macaquetroop in a snowy habitat. Folia Primatol 37:77–94
Furuya Y (1960) An example of fission of a natural troop of Japanese monkeys at the Mt.
Gagyusan. Primates 10:47–69
Hamada Y, Watanabe T, Iwamoto M (1996) Morphological variation among local populations of
the Japanese macaque (Macaca fuscata). In: Shotake T, Wada K (eds) Variations in the Asian
macaques. Tokai University Press, Tokyo, pp 97–115
Hamada Y, Hayakawa S, Suzuki J, Watanabe K, Ohkura S (2003) Seasonal variation in the bodyfat of Japanese macaques Macaca fuscata. Mamm Study 28:79–88
Hanby JP, Brown CE (1974) The development of socio-sexual behaviors in Japanese macaques
Macaca fuscata. Behaviour 49:152–196
Hanby JP, Robertson LT, Phoenix CH (1971) The sexual behavior of a confined troop of Japanesemacaques. Folia Primatol 16:123–143
Hanya G (2004a) Diet of a Japanese macaque troop in the coniferous forest of Yakushima. Int
J Primatol 25:55–80
Hanya G (2004b) Seasonal variations in the activity budget of Japanese macaques in the coniferous forest of Yakushima: effects of food and temperature. Am J Primatol 63:165–177
Hanya G, Yoshihiro S, Zamma K, Kubo R, Takahata Y (2003) New method to census primate groups:
estimating group density of Japanese macaques by point census. Am J Primatol 60:43–56
Hanya G, Yoshihiro S, Zamma K, Matsubara H, Ohtake M, Kubo R, Noma N, Agetsuma N,
Takahata Y (2004) Environmental determinants of altitudinal variations in relative group
densities of Japanese macaques on Yakushima. Ecol Res 19:485–493
Hayaishi S, Kawamoto Y (2006) Low genetic diversity and biased distribution of mitochondrial
DNA haplotypes in the Japanese macaque (Macaca fuscata yakui) on Yakushima Island.
Primates 47:158–164
Hayakawa S (2008) Male–female mating tactics and paternity of wild Japanese macaques(Macaca fuscata yakui). Am J Primatol 70:986–989
Hayakawa S, Takenaka O (1999) Urine as another potential source for template DNA in polymerase chain reaction (PCR). Am J Primatol 48:199–304
Hazama N (1965) Wild Japanese macaques at Mt. Hiei. In: Kawamura S, Itani J (eds) Monkeys:
sociological studies. Chuokoronsha, Tokyo, pp 375–401 (in Japanese)
Henzi P, Barrett L (2003) Evolutionary ecology, sexual conflict, and behavioral differentiation
among baboon populations. Evol Anthropol 12:217–230
Hill DA, Okayasu N (1995) Absence of ‘youngest ascendancy’ in the dominance relations ofsisters in wild Japanese macaques (Macaca fuscata yakui). Behaviour 132:267–279
Horiuchi S (2005) Affiliative relations among male Japanese macaques (Macaca fuscata yakui)
within and outside a troop on Yakushima Island. Primates 46:191–197
Horiuchi S (2007) Social relationships of male Japanese macaques (Macaca fuscata) in different
habitats: a comparison between Yakushima island and Shimokita peninsula population.
Anthropol Sci 115:63–65
Huffman MA (1987) Consort intrusion and female mate choice in Japanese macaques. Ethology
75:221–234
Huffman MA, Nahallage CAD, Leca JB (2008) Cultured monkeys: social learning cast in stones.
Curr Dir Psychol Sci 17:410–414
Ikeda H (1982) Population changes and ranging behavior of wild Japanese monkeys at Mt.
Kawaradake in Kyushu, Japan. Primates 23:338–347
Imanishi K (1941) The world of living things. Kobunsha, Tokyo (trans. Asquith PJ, Kawakatsu H,
Yagi S, Takasaki H (2002) Routledge, Curzon)
Imanishi K (1951a) Pre-human societies. Iwanami-shoten, Tokyo (in Japanese)
Imanishi K (1951b) Natural society of Japanese macaques. Shizen 6:76–79 (in Japanese)
Imanishi K (1957) Present situation and theme of studies on Japanese macaques. Primates 1:1–29(in Japanese)

20

J. Yamagiwa

Inoue E, Takenaka O (2008) The effect of male tenure and female mate choice on paternity infree-ranging Japanese macaques. Am J Primatol 70:62–68
Inoue M, Takenaka A, Tanaka S, Komiyama R, Takenaka O (1990) Paternity discrimination in a
Japanese macaque group by DNA fingerprinting. Primates 31:563–570
Inoue M, Mitsunaga F, Nozaki M, Ohsawa H, Takenaka A, Sugiyama Y, Shimizu K, Takenaka O(1993) Male dominance rank and reproductive success in an enclosed group of Japanesemacaques: with special reference to post-conception mating. Primates 34:503–511
Itani J (1952) Natural society of Yakushima macaques. Primate Research Group of Kyoto University(in Japanese)
Itani J (1954) The monkeys of Takasakiyama. Kobunsha, Tokyo (in Japanese)
Itani J (1963a) Paternal care in the wild Japanese monkeys, Macaca fuscata. In: Southwick CH(ed) Primate behavior. Van Nostrand, Princeton, pp 91–97
Itani J (1963b) Vocal communication of the wild Japanese monkey. Primates 4:11–66
Itani J (1972) Primate social structure. Kyoritsu-shuppan, Tokyo (in Japanese)
Itani J (1985) The evolution of primate social structure. Man 20:539–611
Itani J (1991) The concept of culture: after the identification theory. In: Nishida T, Izawa K, Kano
T (eds) Cultural history of monkeys. Heibonsha, Tokyo, pp 269–277 (in Japanese)
Itoigawa N (1973) Group organization of a natural troop of Japanese monkeys and mother–infantinteraction. In: Carpenter CR (ed) Behavioral regulators of behavior in primates. Bucknell
University Press, Lewisburg, pp 229–250
Itoigawa N (2001) The role of individuals in the history of a free-ranging group of Japanesemacaques: some thoughts on the relevance for human behavioral research. Int J Behav Dev
25:184–186
Itoigawa N, Tanaka T, Ukai N, Fujii H, Kurokawa T, Koyama T, Ando A, Watanabe Y, Imakawa
S (1992) Demography and reproductive parameters of a free-ranging group of Japanesemacaques (Macaca fuscata) at Katsuyama. Primates 33:49–68
Iwamoto T (1974) A bioeconomic study on a provisionized troop of Japanese monkeys (Macaca
fuscata fuscata) at Koshima Islet, Miyazaki. Primates 15:241–262
Iwamoto T (1982) Food and nutritional condition of free ranging Japanese monkeys on Koshima
Islet during winter. Primates 23:153–170
Iwano T (1983) Concluding remarks on the socio-ecological characteristics of the Yakushimazaru.
Nihonzaru 5:86–95 (in Japanese)
Izawa K (1982) Ecology of Japanese macaques. Dobutsusha, Tokyo (in Japanese)
Izawa K (1983) The ecological study of wild Japanese monkeys living in Kinkazan Island. Miyagi
prefecture: a preliminary report. Bull Miyagi Univ Educ 19:1–9 (in Japanese with English
summary)
Izawa K (2001) The ecological study of wild Japanese monkeys living in Kinkazan Island, Miyagi
prefecture: on the population change 1995–2000. Bull Miyagi Univ Educ 35:329–337 (inJapanese with English summary)
Izawa K (2009) Studies of wild Japanese macaques. Dobutsusha, Tokyo (in Japanese)
Izawa K, Miyagi Research Group of Monkeys (2005) The complete manual for crop-raiding bymonkeys. Dobutsusha, Tokyo (in Japanese)
Janson CH (2000) Primate socio-ecology: the end of a golden age. Evol Anthropol 9:73–86
Kawai M (1958) On the rank system in a natural group of Japanese monkey: (1) basic rank anddependent rank. Primates 1:111–130 (in Japanese)
Kawai M (1964) Ecology of Japanese macaques. Kawadeshobo, Tokyo (in Japanese)
Kawai M (1965) Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys
of Koshima Islet. Primates 6:1–30
Kawamoto Y (2005) NRAMP1 polymorphism in a hybrid population between Japanese andTaiwanese macaques in Wakayama, Japan. Primates 46:203–206
Kawamoto Y, Ohsawa H, Nigi H, Maruhashi T, Maekawa S, Shirai K, Araki S (2001) Genetic
assessment of a hybrid population between Japanese and Taiwan macaques in Wakayama
Prefecture. Primate Res 17:13–24 (in Japanese with English summary)Chapter 1: Research History of Japanese Macaques in Japan

21

Kawamoto Y, Kawamoto S, Kawai S, Sirai K, Toshida J, Ogiwara H, Shiratori D, Naoi Y (2007a)
Status report of hybridization in an introduced population of rhesus macaques (Macaca
mulatta) with native Japanese macaques (M. fuscata) in the Boso Peninsula, Chiba, Japan.
Primate Res 23:81–89 (in Japanese with English summary)
Kawamoto Y, Shotake T, Nozawa K, Kawamoto S, Tomari K, Kawai S, Shirai K, Morimitsu Y,
Takagi N, Akaza H, Fujii H, Hagihara K, Aizawa K, Akachi S, Oi T, Hayaishi S (2007b)
Postglacial population expansion of Japanese macaques (Macaca fuscata) inferred frommitochondrial DNA phylogeography. Primates 48:27–40
Kawamoto Y, Tomari K, Kawai S, Kawamoto S (2008) Genetics of the Shimokita macaquepopulation suggest an ancient bottleneck. Primates 49:32–40
Kawamura S (1958) The matriarchal social order in the Minoo-B group: a study on the rank system
of Japanese macaque. Primates 1:149–156 (in Japanese with English summary)
Kawamura S (1959) The process of sub-culture propagation among Japanese macaques. Primates
2:43–60
Kawanaka K (1973) Intertroop relationships among Japanese monkeys. Primates 14:113–159
Koda H, Shimooka Y, Sugiura H (2008) Effects of caller activity and habitat visibility on contact
call rate of wild Japanese macaques (Macaca fuscata). Am J Primatol 70:1055–1063
Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783
Koyama N (1970) Changes in dominance rank and division of a wild Japanese monkey troop in
Arashiyama. Primates 11:335–390
Koyama N, Takahata Y, Huffman MA, Norikoshi K, Suzuki H (1992) Reproductive parameters offemale Japanese macaques: thirty years data from the Arashiyama troops, Japan. Primates
33:33–47
Kurita H, Sugiyama Y, Ohsawa H, Hamada Y, Watanabe T (2008) Changes in demographic
parameters of Macaca fuscata at Takasakiyama in relation to decrease of provisioned foods.
Int J Primatol 29:1189–1202
Kutsukake N, Hasegawa T (2005) Dominance turnover between an alpha and a beta male anddynamics of social relationships in Japanese macaques. Int J Primatol 26:775–800
Maruhashi T (1980) Feeding behavior and diet of the Japanese monkey (Macaca fuscata yakui)
on Yakushima Island, Japan. Primates 21:141–160
Maruhashi T (1982) An ecological study of troop fission of Japanese monkeys (Macaca fuscata
yakui) on Yakushima Island, Japan. Primates 23:317–337
Maruhashi T, Takasaki H (1996) Socio-ecological dynamics of Japanese macaque troop. In: Fa JE,
Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press,
Cambridge, pp 146–159
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:
291–302
Masui K (1976) A record on group size and composition of Japanese macaques: reconsiderationon the knowledge of group size and population. Physiol Ecol 17:185–194 (in Japanese)
Matsubara M, Sprague DS (2004) Mating tactics in response to costs incurred by mating withmultiple males in wild female Japanese macaques. Int J Primatol 25:901–917
Mitani M (1986) Voiceprint identification and its application to sociological studies of wild
Japanese monkeys (Macaca fuscata yakui). Primates 27:397–412
Mori A (1975) Signals found in the grooming interactions of wild Japanese monkeys of the
Koshima troop. Primates 16:107–140
Mori A (1977) The social organization of the provisioned Japanese monkey troops which haveextraordinary large population sizes. J Anthropol Soc Nippon 84:325–345
Muroyama Y (1991) Mutual reciprocity of grooming in female Japanese macaques (Macaca
fuscata). Behaviour 119:161–170
Muroyama Y (1996) Decision making in grooming by Japanese macaques (Macaca fuscata). Int
J Primatol 17:817–830

22

J. Yamagiwa

Muroyama Y (2003) Getting along with monkeys around the village. Kyoto University Press,
Kyoto (in Japanese)
Nahallage CAD, Huffman MA (2008) Comparison of stone handling behavior in two macaquespecies: implications for the role of phylogeny and environment in primate cultural variation.
Am J Primatol 70:1124–1132
Nakagawa N (1989a) Feeding strategies of Japanese monkeys against deterioration of habitat
quality. Primates 30:1–16
Nakagawa N (1989b) Bioenergetics of Japanese monkeys (Macaca fuscata) on Kinkazan Island
in winter. Primates 30:441–460
Nakagawa N (1990a) Decision on time allocation to different food patches by Japanese monkeys(Macaca fuscata). Primates 31:459–469
Nakagawa N (1990b) Choice of food patches by Japanese monkeys (Macaca fuscata). Am
J Primatol 21:17–29
Nakagawa N (1997) Determinants of the dramatic seasonal changes in the intake of energy andprotein by Japanese monkeys in a cool temperate forest. Am J Primatol 41:267–288
Nakagawa N (1998) Ecological determinants of the behavior and social structure of Japanesemonkeys: a synthesis. Primates 39:375–383
Nakamichi M, Shizawa Y (2003) Distribution of grooming among adult females in a large, freeranging group of Japanese macaques. Int J Primatol 24:607–625
Nakamichi M, Yamada K (2007) Long-term grooming partnerships between unrelated adult females
in a free-ranging group of Japanese monkeys (Macaca fuscata). Am J Primatol 69:652–663
Nakamichi M, Itoigawa N, Imakawa S, Machida S (1995) Dominance relations among adultfemales in a free-ranging group of Japanese monkeys at Katsuyama. Am J Primatol
37:241–251
Nakayama Y, Matsuoka S, Watanuki Y (1999) Feeding rates and energy deficits of juvenile andadult Japanese monkeys in a cool temperate area with snow coverage. Ecol Res 14:291–301
Nihonzaru Editorial Committee (1977) Changes in population of Japanese macaques at monkey
parks in Japan. Nihonzaru 3:113–120 (in Japanese)
Nishida T (1966) A sociological study of solitary male monkeys. Primates 7:141–204
Nishikawa M, Mochida K (2010) Coprophagy-related interspecific nocturnal interactions between
Japanese macaques (Macaca fuscata yakui) and sika deer (Cervus nippon yakushimae).
Primates 51:95–99
Noma N, Yumoto T (1997) Fruiting phenology of animal-dispersed plants in response to wintermigration of frugivores in a warm temperate forest on Yakushima Island, Japan. Ecol Res
12:119–129
Norikoshi K (1974) Mother–son relationships in a natural troop of Japanese macaques.
Q Anthropol 5:39–62 (in Japanese)
Nozawa K, Shotake T, Ohkura Y, Kitajima M, Tanabe Y (1975) Genetic variations within andbetween troops of Macaca fuscata fuscata. In: Kondo S, Kawai M, Ehara A (eds) Contemporary
primatology: proceedings of 5th International Primatological Congress, Nagoya 1974. Karger,
Basel, pp 75–89
Nozawa K, Shotake T, Minezawa M, Kawamoto Y, Hayasaka K, Kawamoto S, Ito S (1991)
Population genetics of Japanese monkeys. III. Ancestry and differentiation of local populations. Primates 32:411–435
Oi T (1988) Sociological study on the troop fission of wild Japanese monkeys (Macaca fuscata
yakui) on Yakushima Island. Primates 29:1–19
Oi T, Masui K (eds) (2002) Natural history of Japanese macaques: their ecological varieties andconservation. Tokai University Press, Tokyo (in Japanese)
Okayasu N (2001) Contrast of estrus in accordance with social contexts between two troops ofwild Japanese macaques on Yakushima. Anthropol Sci 109:121–139
Otani T, Shibata E (2000) Seed dispersal and predation by Yakushima macaques, Macaca fuscata
yakui, in a warm temperate forest of Yakushima Island, southern Japan. Ecol Res 15:133–144
Primate Society of Japan (2000) Opinion about experimental use of wild-derived Japanesemacaques. Primate Res 16:309–310 (in Japanese)Chapter 1: Research History of Japanese Macaques in Japan

23

Saito C (1996) Dominance and feeding success in female Japanese macaques, Macaca fuscata:
effects of food patch size and inter-patch distance. Anim Behav 51:967–980
Saito C, Sato S, Suzuki S, Sugiura H, Agetsuma N, Takahata Y, Sasaki C, Takahashi H, Tanaka T,
Yamagiwa J (1998) Aggressive intergroup encounters in two populations of Japanesemacaques (Macaca fuscata). Primates 39:303–312
Sato S (1977) Lifestyle of male Japanese macaques: a case study on Kamuri-A troop at Hakusan.
In: Kato T, Nakao S, Umesao T (eds) Morphology, evolution and primates. Chuokoronsha,
Tokyo, pp 275–310 (in Japanese)
Shimada M (2006) Social object play among young Japanese macaques (Macaca fuscata) in
Arashiyama, Japan. Primates 47:342–349
Soltis J (1999) Measuring male–female relationships during the mating season in wild Japanesemacaques (Macaca fuscata yakui). Primates 40:453–467
Soltis J (2002) Do primate females gain nonreproductive benefits by mating with multiple males?
Theoretical and empirical considerations. Evol Anthropol 11:187–197
Soltis J (2004) Mating systems. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: amodel for the study of social organization. Cambridge University Press, New York, pp 135–151
Soltis J, Thomsen R, Takenaka O (2001) The interaction of male and female reproductive strategies and paternity in wild Japanese macaques, Macaca fuscata. Anim Behav 62:485–494
Sprague DS (1992) Life history and male intertroop mobility among Japanese macaques (Macaca
fuscata). Int J Primatol 13:437–454
Sprague DS (1998) Age, dominance rank, natal status, and tenure among male macaques. Am
J Phys Anthropol 105:511–521
Sprague DS (2004) Monkey lives, human lives: the biology of life plans. Kyoto University Press,
Kyoto (in Japanese)
Sprague DS, Suzuki S, Tsukahara T (1996) Variation in social mechanism by which males
attained the alpha rank among Japanese macaques. In: Fa JE, Lindburg DG (eds) Evolution
and ecology of macaque societies. Cambridge University Press, Cambridge, pp 444–458
Sprague DS, Suzuki S, Takahashi H, Sato S (1998) Male life history in natural populations ofJapanese macaques: migration, dominance rank, and troop participation of males in two habitats. Primates 39:351–364
Sugawara K (1980) Structure of encounters between solitary male Japanese macaques.
Q Anthropol 11:3–70 (in Japanese)
Sugiura H (1993) Temporal and acoustic correlates in vocal exchange of coo calls in Japanesemacaques. 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, Masataka N (1995) Temporal and acoustic flexibility in vocal exchanges of coo calls
in Japanese macaques (Macaca fuscata). In: Zimmermann E, Newman JD, Jürgens U (eds)
Current topics in primate vocal communication. Plenum Press, New York, pp 121–140
Sugiura H, Saito C, Sato S, Agetsuma N, Takahashi H, Tanaka T, Furuichi T, Takahata Y (2000)
Variation in intergroup encounters in two populations of Japanese macaques. Int J Primatol
21:519–535
Sugiura H, Agetsuma N, Suzuki S (2002) Troop extinction and female fusion in wild Japanesemacaques in Yakushima. Int J Primatol 23:69–84
Sugiyama Y (1960) On the division of a natural troop of Japanese monkeys at Takasakiyama.
Primates 2:109–148
Sugiyama Y (1976) Life history of male Japanese monkeys. Adv Stud Behav 7:255–284
Sugiyama Y, Ohsawa H (1982) Population dynamics of Japanese monkeys with special reference
to the effect of artificial feeding. Folia Primatol 39:238–263
Suzuki A, Wada K, Yoshihiro S, Tokita E, Hara S, Aburada Y (1975) Population dynamics andgroup movement of Japanese monkeys in Yokoigawa Valley, Shiga Heights. Physiol Ecol
16:15–23 (in Japanese)
Suzuki S, Noma N, Izawa K (1998a) Inter-annual variation of reproductive parameters and fruit
availability in two populations of Japanese macaques. Primates 39:313–324

24

J. Yamagiwa

Suzuki S, Hill DA, Sprague DS (1998b) Intertroop transfer and dominance rank structure of nonnatal male Japanese macaques in Yakushima, Japan. Int J Primatol 19:703–722
Takahashi H (1997) Huddling relationships in night sleeping groups among wild Japanesemacaques in Kinkazan Island during winter. Primates 38:57–68
Takahashi H (2001) Influence of fluctuation in the operational sex ratio to mating of troop andnon-troop male Japanese macaques for four years on Kinkazan Island, Japan. Primates
42:183–191
Takahashi H, Furuichi T (1998) Comparative study of grooming relationships among wild
Japanese macaques in Kinkazan A troop and Yakushima M troop. Primates 39:365–374
Takahata Y (1980) The reproductive biology of a free-ranging troop of Japanese monkeys.
Primates 21:303–329
Takahata Y (1982) The socio-sexual behavior of Japanese monkeys. Z Tierpsychol 59:89–108
Takahata Y, Suzuki S, Okayasu N, Hill D (1994a) Troop extinction and fusion in wild Japanesemacaques of Yakushima Island, Japan. Am J Primatol 33:317–322
Takahata Y, Sprague DS, Suzuki S, Okayasu N (1994b) Female competition, co-existence, andmating structure of wild Japanese macaques on Yakushima Island, Japan. In: Jarman PJ,
Rossister A (eds) Animal societies: Individuals, interaction and organization. Kyoto University
Press, Kyoto, pp 163–179
Takahata Y, Koyama N, Suzuki S (1995) Do old aged females experience a long post-reproductive
life span? The cases of Japanese macaques and chimpanzees. Primates 36:169–180
Takahata Y, Suzuki S, Agetsuma N, Okayasu N, Sugiura H, Takahashi H, Yamagiwa J, Izawa K,
Furuichi T, Hill DA, Maruhashi T, Saito C, Sato S, Sprague DS (1998) Reproduction of wild
Japanese macaque females of Yakushima and Kinkazan Islands: a preliminary report. Primates
39:339–350
Takahata Y, Huffman MA, Suzuki S, Koyama N, Yamagiwa J (1999) Why dominants do notconsistently attain high mating and reproductive success: a review of longitudinal Japanesemacaque studies. Primates 40:143–158
Takasaki H (1981) Troop size, habitat quality, and home range area in Japanese macaque. Behav
Ecol Sociobiol 9:277–281
Takasaki H (2000) Traditions of the Kyoto School of field primatology in Japan. In: Strum SC,
Fedigan LM (eds) Primate encounters. The University of Chicago Press, Chicago and London,
pp 151–164
Tanaka I (1989) Change of nipple preference between successive offspring in Japanese macaques.
Am J Primatol 18:321–325
Tanaka I (1992) Three phases of lactation in free-ranging Japanese macaques. Anim Behav
44:129–139
Tanaka I (1995) Matrilineal distribution of louse egg-handling techniques during grooming infree-ranging Japanese macaques. Am J Phys Anthropol 98:197–201
Tanaka I (1997) Parity-related differences in suckling behavior and nipple preference among freeranging Japanese macaques. Am J Primatol 42:331–339
Tanaka I (2004) Non-offspring nursing by a nulliparous pregnant female just before first parturition in free-ranging Japanese macaques. Primates 45:205–206
Thomsen R (1997) Observation of periparturitional behaviour in wild Yakushima macaques(Macaca fuscata yakui). Folia Primatol 68:338–341
Thomsen R, Soltis J (2004) Male masturbation in free-ranging Japanese macaques. Int J Primatol
25:1033–1041
Thomsen R, Soltis J, Matsubara M, Matsubayashi K, Onuma M, Takenaka O (2006) How costly
are ejaculates for Japanese macaques? Primates 47:272–274
Tsuji Y, Fujita S, Sugiura H, Saito C, Takatsuki S (2006) Long-term variation in fruiting and food
habits of wild Japanese macaques on Kinkazan Island, Northern Japan. Am J Primatol
68:1068–1080
Tsukahara T (1990) Initiation and solicitation in male–female grooming in a wild Japanesemacaque troop on Yakushima Island. Primates 31:147–156

Chapter 1: Research History of Japanese Macaques in Japan25

Uehara S (1977) Biogeographical studies of Japanese macaques from an analysis of their foods: atrial to reconstruct history of distribution of Japanese macaques. In: Kato T, Nakao S, Umesao T(eds) Morphology, evolution and primates. Chuokoronsha, Tokyo, pp 187–232 (in Japanese)
Wada K (1979) World of the wild Japanese macaques. Kodansha, Tokyo (in Japanese)
Wada K, Tokida E (1981) Habitat utilization by wintering Japanese monkeys (Macaca fuscata
fuscata) in the Shiga Heights. Primates 22:330–348
Watanabe K (1979) Alliance formation in a free-ranging troop of Japanese macaques. Primates
20:459–474
Watanabe K (2000) Crop-raiding by Japanese macaques and wildlife management. Tokai
University Press, Tokyo (in Japanese)
Watanabe K (2003) Japanese macaques at Koshima Islet: a family tree for 50 years. Ecosophya
12:15–19 (in Japanese)
Watanabe K, Mori A, Kawai M (1992) Characteristic features of the reproduction of Koshimamonkeys, Macaca fuscata fuscata: a summary of thirty-four years of observation. Primates
33:1–32
Watanuki Y, Nakayama Y (1993) Age difference in activity pattern of Japanese monkeys: effects
of temperature, snow, and diet. Primates 34:419–430
Yamagiwa J (1985) Socio-sexual factors of troop fission in wild Japanese monkeys (Macaca
fuscata yakui) on Yakushima Island, Japan. Primates 26:105–120
Yamagiwa J (2008) History and present scope of field studies on Macaca fuscata yakui atYakushima Island, Japan. Int J Primatol 29:49–64
Yamagiwa J, Hill DA (1998) Intra-specific variation in the social organization of Japanesemacaques: past and present scope of field studies in natural habitats. Primates 39:257–274
Yoshihiro S, Furuichi T, Manda M, Ohkubo N, Kinoshita M, Agetsuma N, Azuma S, Matsubara
H, Sugiura H, Hill DA, Kido E, Kubo R, Matsushima K, Nakajima K, Maruhashi T, Oi T,
Sprague DS, Tanaka T, Tsukahara T, Takahata Y (1998) The distribution of wild Yakushima
macaque (Macaca fuscata yakui) troops around the coast of Yakushima Island, Japan. Primate
Res 14:179–188
Yoshihiro S, Ohtake M, Matsubara H, Zamma K, Hanya G, Tanimura Y, Kubota H, Kubo R,
Arakane T, Hirata T, Furukawa M, Sato A, Takahata Y (1999) Vertical distribution of wild
Yakushima macaques (Macaca fuscata yakui) in the western area of Yakushima Island, Japan:
preliminary report. Primates 40:409–415
Yotsumoto N (1976) The daily activity rhythm in a troop of wild Japanese monkey. Primates
17:183–204
Yumoto T, Matsuda H (eds) (2006) Japanese deer feed on the World Heritage: ecology of deer andforest. Bunichisogo-shuppan (in Japanese)
Yumoto T, Noma N, Maruhashi T (1998) Cheek-pouch dispersal of seeds by Japanese monkeys(Macaca fuscata yakui) on Yakushima Island, Japan. Primates 39:325–338
Zamma K (2002) Grooming site preferences determined by lice infection among Japanesemacaques in Arashiyama. Primates 43:41–49

http://www.springer.com/978-4-431-53885-1