Several different reproductive strategies occur simultaneously
in a troop of macaques. Among the males, the dominant animals monopolize
most
of the mating opportunities, and high-ranking males guard the females
to prevent other males from mating with them. Because only a few females
display mating behavior during a single day, it is not incredibly difficult
for high-ranking males to monopolize mating opportunities. However, lower
ranking males attempt "sneak copulations" when no other males
are in the area, in order to avoid direct competition with higher-ranking
males. Occasionally, non-troop males will come into a troop's area and
mate with the females in that troop as well (Soltis 2001).
Associations between central males and adult females during non-mating season are usually continuations of associations established during the mating season. Thus, sexual relations play an important role in breaking old bonds and forming new ones during the mating season that will shape the troop’s social relations during the subsequent non-mating season (Grewal 1980). Such bonds are especially important for maintaining the concentric social organization of the troop (Kawai 1969 as cited in Enomoto 1981).
During the non-mating season, dominant males chased females most frequently out of all the males. During the mating season, however, the link between dominance rank and chasing behavior is not strong. Females in estrus search for potential sexual partners separately from their female kin, and they do not follow the higher-ranked males as they do during non-mating season. This weakening in male-female and female-female bonds causes the concentric social organization of the troop to disappear during mating season because the peripheral males come into the central part of the troop to chase or display to a female, and females also travel into the periphery of the troop in search of males (Enomoto 1981).
During the mating season, frequencies of copulation, male chasing, and vocalizations associated with tree-shaking increase. However, studies conflict on the presence or absence of correlation between male dominance rank and frequency of copulation. This conflict could indicate that the frequency of copulation is dependent on more factors than simply male dominance rank (ie- social, behavioral, and physiological factors) (Enomoto 1981).
Japanese macaques engage in very little sexually related interaction during the non-mating season. However, when breeding season arrives, contact between males and females becomes much more important. The increased level of sexual activity during the mating season is accompanied by increased aggression, and males may injure females or other males while chasing or fighting with them. It is believed that increased levels of testosterone in males correlate with the increased level of aggressive activity during this time (Nigi 1980 as cited in Enomoto 1981). Because of this aggression, males must perform "appeasement behavior" (positive behavior) such as sitting with and grooming the female. This behavior serves to reduce the female’s fear of the male, which is necessary before she will mate with him. The higher ranking the male is, the more appeasement behavior he must perform toward a female, since higher-ranking males are generally the most intimidating. Males show positive behavior toward members of their own matrilineal group and to other females, but females never show positive behavior toward males in their matrilineal group, possibly as a psychological mechanism to avoid incest (Enomoto 1974). The daily frequencies of male chasing had a positive correlation with the number of females in estrus that day.
Another important incest avoidance mechanism
is male dispersal. Because male young have been observed to emigrate
to troops relatively close
to their natal troop, dispersal is not believed to be the result of a
male tendency to move far away from the natal troop (Enomoto 1974). In
rhesus monkeys (which are closely related to Japanese macaques), males'
dominance increased and their reproductive activity decreased with age
(Packer 1979 as cited in Enomoto 1981). Males then emigrated from their
natal troop because they were interested in females from other troops.
It is possible that sexual relations between male and female Japanese
macaques establish an affinitive bond between them that reduces the males'
subsequent sexual opportunities within the troop in a way similar to
that of close blood bonds. The males then emigrate to other troops to
increase their reproductive opportunities (Norikoshi 1975 as cited in
Enomoto 1981). By reducing the male's sexual opportunity within the troop
and causing the male to leave the troop, this mechanism prevents incestual
relations between that male and his daughters in the original troop (Enomoto
1981).
Each troop of macaques has a clear estrus season, but its timing varies between troops (Enomoto 1974). External signs of female estrus include increased redness of the face, swelling and redness of the sexual skin (which females display to males), and vaginal secretion. In males, non-behavioral signs of sexual activity include increased redness of the face and coloration of the scrotum, which they show to the females in a “hind-quarters display” (Enomoto 1974).
Males are larger (average 12 kg) than females (average 10 kg) and reach their full body size at 8 years of age, whereas females are not fully-grown until age 6 (Flannery 2002). A female's first estrus occurs at 3.5 years, but few become pregnant from their first mating attempt. Each female over 3.5 years comes into estrus and mates with males, regardless of whether she has an infant. If the infant dies, the mother will not come into estrus again until the next mating season. Males leave the troop between the ages of 3-6 years, but they do not fully develop their secondary sex characteristics (canine teeth and red scrotum) until 8 years of age (Hiraiwa 1980).
Japanese macaques engage in many different
sexual sign behaviors during the mating season. Sign behavior is defined
as a form of social communication in which the behavior of one individual
affects the behavior of others (Altmann 1967 as cited in Enomoto 1974).
Sexual sign
behavior seen most often in non-copulatory sequences include:
-tail raising –Tail raising exposes
the most colorful part of the male's body- the white sections near
the base of the tail, a red anus, and a pink, red, or purple scrotum.
Males raise their tails regardless of dominance rank, but females do
not raise their tails as often as males do.
-testes-lowering
-tree shaking
-vocalizations
-biting
-chasing –Estrus females are chased more frequently than non-estrus
females. Males usually chased females who were alone, though they occasionally
chased females who were sitting with another male. Most often, the male does
not catch the female. But when he does, he bites her all over her body. Sometimes,
following the biting, the pair copulates.
-muzzle-to-genitals—The male inspects and smells the
female's genitals, sometimes to determine whether or not she is in estrous.
-hindquarters display
-penile erection—Sometimes this behavior is not directed toward
another macaque.
Sexual sign behaviors most
often observed during copulatory sequences include:
-approach
-crouching
-kicking
-leading-and-following
-looking backwards
-attacking-the-third-monkey
-head-bobbing
-head-ducking
-nodding
-scratching the ground
-head-on-the-ground
-beating the ground
-lip smacking
-scanning
-walking-by
-hindquarters display—Following the male’s hindquarters
display, the female can accept or reject copulation attempts.
-walking over
-hand-on-back—This behavior is usually enacted by the male
right before a mounting series.
-sitting-with
-embracing
-standing-by-the-side-of-the-partner
-muzzle-to-partner
-grooming
-self-grooming
-presenting— Presenting is a female behavior resembling the male's
hindquarters display.
-hitting
-mounting— The male mounts the female several times, with resting intervals in between mountings, until he ejaculates. Ejaculation usually occurs with the last mount.
-pausing—Pausing occurs between mountings, when the male and female sit together quietly.
-spasmodic movement
-copulation with ventral-ventral posture— This behavior is observed mostly in pairs of juveniles. The male does not ejaculate in this sexual posture.
-pushing-male-onto-the-back
-yawning
Other types of sexual behavior include:
-a female mounting a male
-a male mounting a male
-a female mounting a female
-male masturbation
-female masturbation
None of the behaviors listed above have been highly correlated with dominance rank (Enomoto 1974).