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Japanese macaque
Macaca fuscata

SOCIAL ORGANIZATION AND BEHAVIOR

Japanese macaque groups are matrilineal groups (Fooden & Aimi 2005). Female Japanese macaques remain with their natal 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).

Macaca fuscata
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).

Dominance hierarchy 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).

Macaca fuscata
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 (Furuya 1969).

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).

REPRODUCTION

A key feature of the reproduction of the Japanese macaque is the consortship . 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 estrus season (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 1991).

Macaca fuscata
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).

PARENTAL CARE

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).

Macaca fuscata
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 the 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 infanticide, 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).

COMMUNICATION

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).

Macaca fuscata
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 1981).

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 September 22.