SOCIAL ORGANIZATION AND BEHAVIOR
Japanese macaque groups are
matrilineal groups (Fooden & Aimi 2005). Female Japanese macaques remain with their
groups for life while males emigrate before becoming sexually mature (Fukuda 2004). Groups are
typically multi-male and multi-female populated with several males which have immigrated from other
groups and females, still in their natal group (Fukuda 2004). Several, and often many, matrilines
can be present in a single Japanese macaque troop. In a troop it is possible to arrange kin groups
according to rank on a linear continuum (Koyama 1967). Thus, all of the members of a specific kin
group are higher ranked than all of the members of a lower-ranked kin group. Group composition
averages around 18% adult males, 32% adult females, 35% juveniles, and 15% infants
(Fooden & Aimi 2005). Males typically emigrate from their natal group between five or six years of
age and sometimes form temporary all male groups (Fukuda 2004). Males which have emigrated often
join and leave groups several times in their lives and may stay in a new troop for years
(Fukuda 1982 cited in Fukuda 2004). These new groups can be considerably far away from the male's
natal group, and in exceptional cases, involving travel surpassing 100km (62.14 mi) to reach
(Yoshimi & Takasaki 2003). In fact, many males spend a significant amount of their lives outside of
membership in any group (Sugiyama 1976).
Photo: Frans de Waal
There is a discrete hierarchy of rank in males within Japanese macaque groups and one individual
attains alpha status
dominant to, yet tolerant of, other males in the troop. There are several mechanisms by which male
alpha status is acquired, including the death or departure of a former alpha male, a loss of rank by
the former alpha male, the splitting of a troop such that there is a new alpha position, and a
non-group male aggressively appropriating the alpha male position (Sprague et al. 1996). In
general, succession by means of death or departure of the former alpha male is the typical method
by which dominant status changes (Sprague et al. 1996). The period of time a male has been in the
group often correlates with his status and the longer he has been a member of the troop, the higher
his status is likely to be (Takahashi 2002). The relationships dominant males have with dominant
females help reinforce male hierarchy and allow males to retain dominance where otherwise they would
not (Nakamichi et al. 1995). In fact, there is evidence that alpha males often are able to maintain
their position by relying on the alpha female, especially when the alpha male is old or infirm
(Nakamichi et al. 1995).
exists among females as well as among males (Koyama 1967). The ranking
hierarchy among females is stable and female offspring assume similar rank to that of their mothers.
Among female siblings, the younger usually has the highest rank although there are exceptions to
this rule (Koyama 1967; Takahata 1991). In addition, the ranking of an individual's matrilineal kin
group can affect the status of offspring and serve to help that monkey of the same matriline gain
hierarchical status (Koyama 1967). Finally, there is a higher level of social cohesion among
higher-ranking matrilines which serve to reinforce the troop cohesion as a whole (Koyama 2003).
When Japanese macaque groups encounter one another in the wild, the nature of their interactions
varies with the demographics of the groups involved, with reproductive seasonality and with group
identity (Saito et al. 1998). Among various troops, home ranges overlap 20% of the time, but
troops tend to avoid one another as they get closer (Kawanaka 1973). Aggressive behavior during
inter-group encounters between Japanese macaque troops serves several purposes including mate
guarding by males, food competition among females during non-mating season, and male investigative
behavior preceding potential emigration to another group (Saito et al 1998).
Photo: Frans de Waal
There are three different ways in which troops of Japanese macaques experience social change.
These are troop fission, or division; takeover of control by a new alpha-male; and extinction, in
which the troop ceases to exist (Maruhashi 1992). Most social changes within troops of Japanese
macaques occur as a result of interplay between the mating strategies of both male and female
members of the troop vying for reproductive advantage (Maruhashi 1992). Fission in groups helps to
control group size, maintain male hierarchies, and to possibly limit inbreeding
Grooming plays an important role in female social organization. In Japanese macaques, as in other
primates, grooming serves to reinforce social bonds and friendly social relationships between
individuals, in addition to serving hygienic purposes (Majolo et al. 2005). There is a strong
correlation in grooming between pairs who are matrilineally related as opposed to unrelated
individuals (Koyama 1991). However, grooming among individuals who are unrelated does occur and
serves to reinforce group cohesion as a whole as it strengthens bonds between different kin groups
within a troop (Nakamichi & Shizawa 2003). Females tend to groom only a small cohort of other
females, even if group size increases (Nakamichi & Shizawa 2003). Allogrooming of other
individuals by the Japanese macaque is independent of climate and season differences, which supports
the view that its function is primarily social (Ventura et al. 2005). When males are
groomed by females, it is likely for skin-care purposes but helps the females attract and retain
high-ranking males in the troop for reproductive purposes (Tsukahara 1990). Grooming techniques are
passed from mother to offspring, probably through social means and not genetically (Tanaka 1995).
Several provisioned Japanese macaques have been observed washing sand off sweet potatoes in water
and passing this behavior on to others. This behavior is described as being pre-cultural, having
been picked up and spread among a number of individuals within a troop (Kawai 1965). Macaques in
both wild and feral groups have also been known to construct snowballs, repetitively and
stereotypically manipulate stones, and to transmit these behaviors to other individuals
(Eaton 1972; Huffman & Quiatt 1986).
A key feature of the reproduction of the Japanese macaque is the
. This association
between a male and a female Japanese macaque is characterized by a pair mating, feeding, resting,
and traveling together, and lasts an average of 1.6 days during mating season (Huffman 1992). Over
the course of a mating season, Japanese macaque females were observed to enter consortships with
over 4 different males on average (Gouzoules & Goy 1983). Typically there is a correlation between
male rank and consort duration, with higher-ranking males remaining in consortships longer than
lower-ranking males (Huffman 1992). Higher-ranking males will interfere in the consortships of
lower-ranking males in an attempt to disrupt them (Perloe 1992).
Females attempt to mate with males of all ranks, but are more likely to actually mate with higher
ranking males due to their ability to mate-guard and aggressively prevent mating with lower-ranking
males (Soltis 1999). Ultimately, it is the female who makes the decision as to whether or not
mating will occur (Huffman 1991b). There is some ambiguity as to whether or not an ultimate
correlation exists between male dominance rank and ultimate reproductive success, but male dominance
rank does not ensure mating opportunities with receptive females (Fooden & Aimi
2005). In addition, females will typically mate with more than one male during an
(Matsubara & Sprague 2004). Finally, a significant number of copulations by females are with
non-troop males who enter the troop during mating season and then depart after the season (Sprague
Photo: Frans de Waal
Same-sex mounting is seen among female Japanese macaques. This behavior appears to be
hormone-linked and represents a greater number of mounting postures than seen in male mounting
behavior (O'Neill et al. 2004; Vasey et al. 2006). Both male and female autosexual behavior has
been observed (Fooden & Aimi 2005).
Presenting behavior can include several signals including looking backward over a shoulder,
remaining very still, or walking backwards towards the potential partner (Hanby & Brown 1974). The
most typical copulatory position is a posterior mount with both of the male's feet clasping the legs
of the female (Hanby et al. 1971). Copulation occurs both arboreally and terrestrially (Yotsumoto
1976). Two types of female reproductive vocalization are typical. The first is a "smooth-late-high
coo", or "squawk" or "squeak" uttered before copulation, possibly to solicit mating. The second is
an atonal "cackle" uttered during copulation. Male Japanese macaques do not emit copulatory
vocalizations (Oda & Masataka 1992).
Reproduction in Japanese macaques is seasonal, but its exact timing varies with locality and group.
Within each group of macaques however, the birth season is discrete and occurs between March and
September across the species' range (Kawai et al. 1967). The mating season lasts between four and
five months and ranges between September and April (Kawai et al. 1967). Differences in birth season
between different groups across the Japanese macaque range are correlated with the latitude of the
habitat (Kawai et
al. 1967). This does not mean, however, that nearby troops will exhibit the same birth season as
two troops located near to each other exhibited a two-month difference in average birth date
(Fooden & Aimi 2003).
In females, estrus usually is first seen around 3.5 years of age. Male mounting behavior can occur
as early as 1.5 years but ejaculation among males is first seen later, at 4.5 years of age
(Takahata 1980). Average age at male emigration from his natal troop is 5 years (Sprague et al.
1998). The female estrus cycle averages 27.1 days during the mating season but becomes irregular
or might not occur at all during the non-mating season (Nigi 1975; Fooden & Aimi 2005). Gestation
averages 5.64 months (171.7 days) (Fooden & Aimi 2005).
Discrete morphological color changes occur in both male and female Japanese macaques during mating
season. In the males, the face and genitalia turn deep red and the tail will stand erect, exposing
the bright genitals (Wolfe 1979). Female Japanese macaques exhibit similar morphological changes
during estrus with their faces and anogenital regions turning scarlet red (Wolfe 1979).
To give birth, a Japanese macaque mother will move to the periphery of the troop and to a private
spot (Fedigan & Zohar 1997). However, if the troop moves during birth, the mother will move to
remain with the group and will not allow herself to be separated from it (Nakamichi et al. 1992;
Thomsen 1997). Birth in the wild typically takes place on the ground (Fooden & Aimi 2005). Infant
mortality before one year averages 28.4% in wild groups of Japanese macaques (Fooden & Aimi 2005).
Weight at birth for Japanese macaque infants averages 546.8 g (1.21 lbs) for females and 538.7 g
(1.19 lbs) for males (Fooden & Aimi 2005). At birth, the fur of the infant Japanese macaque is very
dark brown and lightens progressively over the next six months while still remaining somewhat darker
than the coat of the adult during that time (Hiraiwa 1981). Solid food consumption by the infant is
first seen at 5 or 6 weeks of age followed by foraging independent of the mother at 7 weeks of age
(Hiraiwa 1981). From birth until 4 weeks, an infant is carried ventrally by the mother. After 4
weeks of age, dorsal carrying is observed in addition to ventral carrying. Carrying by the mother
can persist up to and past one year of age (Hiraiwa 1981).
Photo: Frans de Waal
There is experimental evidence in captivity that Japanese macaque mothers can pick out the whistle
and "coo" vocalizations of their own infant from those of other infants (Pereira 1986;
Shizawa 2005). In captivity,
during the first month of life, locomotor behaviors quickly evolve from crawling, toddling and
backward hunching, to more adult locomotion such as quadrupedal walking, running, climbing and jumping
(Negayama et al. 1983). Locomotor development in the infant Japanese macaque is completed by as
early as 3 to 4 months of age (Minami 1974). As the adolescent macaque ages, the amount of time
spent by the mother grooming it decreases and solicitation of grooming by the offspring increases.
However, Japanese macaque mothers groom their adult female offspring far more than they will groom
either sex of their adolescent offspring (Muroyama 1995).
Sex differences in infant behavior are evident in some populations. Male infants play in larger
groups and play in groups more often than females (Glick et al. 1986). Males also display more
mounting behavior than female infants. Female infants have more social contacts and groom more
often than male infant macaques (Glick et al. 1986). From the second year of life, males
preferentially associate with males of the same approximate age (Nakamichi 1989). Females
preferentially associate with other females of all age and sex classes as well as with infants and
adult males. Evidence points to the early development of sex-specific social roles during the
second year of life (Nakamichi 1989).
At seven months of age, the mother starts actively discouraging suckling of the infant with a peak
in active discouragement of suckling around 11 to 12 months of age (Hiraiwa 1981).
While it is possible for
weaning to be finished as early as six months of age, it often happens when the infant is older
and can sometimes occur later than 18 months of age
(Nigi 1982 cited in Ôta et al. 1991; Tanaka et al. 1993).
Among the troop, relationships between a mother and her infant and the rest of the troop are
described as cool and somewhat avoidant and the mother only slowly resumes her typical social
activities postpartum (Itani 1959; Bardi et al. 2001). There is some interaction allowed between
infant and others in the troop and allomothering is observed. Infant care by other females is most often seen among
females who have not yet borne their own infants and is not likely to be received from a female who
has had offspring (Hiraiwa 1981). Male care of infants is present in some troops, while in others
it is absent (Itani 1959; Gouzoules 1984). When present, this relationship entails an older
male protecting, grooming, and carrying of an infant typically in the same manner as would a female.
In addition, such behavior is typically of a finite duration and in the long term, bestows social
benefits on the young Japanese monkey (Itani 1959; Gouzoules 1984). In rare cases observed several
times only in the wild or free-ranging contexts, males will commit
possibly as a method for the male to increase
his chances of successfully mating with females (Yamada & Nakamichi 2006). Specific predatory
threats on Japanese macaque infants include the raccoon dog as well as feral dogs (Iwamoto 1974).
The Japanese macaque utters a number of vocalizations which can be roughly divided into six groups:
peaceful or soothing, defensive, aggressive, warning, female estrus, and infant vocalizations
(Itani 1963). Over half of the vocalizations uttered by the Japanese macaque are peaceful or calm
(Itani 1963). Often, during feeding or moving, Japanese macaques will utter a "coo" sound which
likely functions in group cohesion by allowing females to reinforce their social ties (Mitani 1986).
This "coo" sound is not typically heard in agonistic interactions, and when uttered, other Japanese macaques typically respond
in kind (Sugiura 2001).
Photo: Frans de Waal
The "coo" in conjunction with the "girney" is also uttered immediately before
grooming contact between individuals. Research on the "girney" call in grooming contexts
has shown that variants of a specific call have specific purposes and affect different outcomes
(Masataka 1989). The function of the "girney" is also supposed to be as a form of
appeasement between individuals and serves to
curtail interpersonal aggression (Blount 1985). Alarm calls and estrous calls in the Japanese
macaque are quite similar in sound yet serve two discrete purposes and have different motivations.
Alarm calls serve to warn the troop of danger while the similar estrous call serves to advertise the
reproductive state of a specific monkey (Yoshida 1988a cited in Yoshida 1988b). Threat calls are a
type of aggressive Japanese macaque vocalization. This type of vocalization is uttered most often
by supporters of those involved in agonistic interactions and is used to show support of others.
In this context, a threat call serves to advertise that the individual being supported will support
the caller in the future. In this way, a threat call helps fend off future attacks (Machida 1990).
The Japanese macaque also uses facial expressions to communicate between those of its species. In
captivity, threatening facial expressions include "ear-flattening,"
"brow-raising," "ear-erecting" and "mouth-opening." Subordinate
behavior includes "grimacing." Other captive physical communicatory clues include
lipsmacking, presenting and hindquarters displays and "gaze-avoidance"
(Masataka & Fujii 1980).
Display behavior is also an important aspect of Japanese macaque communication. Display behavior
is seen in several postures in Japanese monkeys including shaking, kicking, and leaping. Such
displays serve as a method by which a male advertises himself to potential mates. An increase in
display postures is seen during the breeding season in males, but not in females. Compound
displays with more than one individual participating were observed in an introduced troop in
Oregon. Only a small proportion of female individuals perform displays and this small proportion
is typically high-ranking within a troop. All adult males within a troop perform displays (Wolfe
Content last modified: April 26, 2007
Written by Kurt Gron. Reviewed by Sarah Turner.
Cite this page as:
Gron KJ. 2007 April 26. Primate Factsheets: Japanese macaque (Macaca fuscata) Behavior . <http://pin.primate.wisc.edu/factsheets/entry/japanese_macaque/behav>. Accessed 2014 April 23.