My studies of primates: Sex, affinity, and competition.

In this essay, I summarize my research career, with reference to the early days of the Laboratory of Physical Anthropology (LPA) at Kyoto University led by Kinji Imanishi and Junichiro Itani. When I started conducting research on the sexual behavior of Japanese macaques in 1975, I made some unexpected observations. High-ranking males did not obtain high mating success. Estrous females often rejected the courtships of high-ranking males and chose to mate with lower-ranking males. Some male-female dyads exhibited long-lasting affinitive relations, but they avoided mating. Females frequently showed 'excessive' sexuality. Clear explanations for some of these observations do not exist. After that, I changed my study subjects several times from chimpanzees, Yakushima macaques (a subspecies of Japanese macaque), and ringtailed lemurs. It is difficult to summarize my findings into a consistent story. Instead, I review my research and experiences. Throughout my career, I kept two things in mind. The first was established by Imanishi at the Laboratory of Physical Anthropology at Kyoto University: to explore the evolution of human society. Second, I tried to understand seemingly incomprehensible phenomena using evolutionary theory. Despite adhering to these foundational concepts, things did not always work out as planned.

Process of Japanese macaque group fission at Arashiyama and the influences of maternal kin relations and social relations between adult males and females on it.

In 1986, the Japanese macaques of Arashiyama B group fissioned into Arashiyama E and F groups through the following process. In December 1985, the death of the beta male triggered aggressive interactions among the adult males of B group, leading to a decline in the ranks of two mid-ranked males. Several females started to gather around these two males, formed a stable subgroup (here called the female cluster), and spatially distanced themselves from other group members (main group). Some of these females had mating relations with these two males in previous mating seasons. After the end of the 1985-86 mating season, agonistic interactions occurred frequently between the female cluster and main group. Eventually, two independent groups were established. The females within the 4th degrees of matrilineal consanguinity tended to belong to the same group, but no such tendency occurred in those dyads separated by the 5th or more degrees. After the completion of group fission, mating occurred only a few times between E and F group members. In 1986, when the group fission was in progress, the birth rate of both branch groups declined, and infant mortality increased in E group. After 1987, the birth rate recovered in both branch groups although infant mortality remained high.

Ranging patterns of Japanese macaques in the coniferous forest of Yakushima: Home range shift and travel rate.

Ranging is one of the most important behavioral adaptations for coping with seasonally fluctuating food and thermal conditions. We studied the ranging patterns, in particular home range shift and travel rate of Japanese macaques (Macaca fuscata) in the coniferous forest of Yakushima by tracking a group for 17 months. We also supplemented our data with records collected every August over a 5-year annual census. The macaque group used the eastern part of their home range from May to September and the western part during the rest of the year. The eastern part of the home range was largely primary forest in the national park, and the altitude was higher than in the western part. When they used the western part, the macaques ate more herbs and fruits from small-sized trees, the availability of which was higher in the logged forest. This east-west home range shift occurred repeatedly over multiple years. A neighboring group occupied the western part of the focal group's home range in summer, which the focal group did not use in that season. Both temperature and diet affected seasonal changes in the monthly average travel rate. Animals need more energy for thermoregulation when the temperature is low, so the macaques decreased their ranging efforts to save energy at times of low temperature. They increased their ranging distance to eat fungi, since their encounters with this food would increase with the total distance walked. They also increased their travel rate when eating flowers, which had lower food patch (tree) density than other foods such as fruits. The data supported the hypothesis that the macaques capitalize on habitat heterogeneity in a seasonally fluctuating habitat by shifting their home range and modifying their travel rate.

Longitudinal changes in the targets of chimpanzee (Pan troglodytes) hunts at Mahale Mountains National Park: how and why did they begin to intensively hunt red colobus (Piliocolobus rufomitratus) in the 1980s?

The hunting activities of chimpanzees (Pan troglodytes) at Mahale Mountains National Park exhibited a significant change over a 46-year observation period, shifting from sporadic hunting for small ungulates and primates through seizure or chasing, to a specialized hunting habit for red colobus (Piliocolobus rufomitratus). By the early 1980s, a new hunting habit had developed through the following stages: (1) occasional single kills by mature/adolescent males, (2) multiple kills by mature/adolescent males, (3) participation of mature females in both multiple and single kills, and (4) increased frequencies of multiple kills and female participation in killing. Throughout the observation period, red colobus was the most frequently hunted species, accounting for 71.0% of all hunts, 68.1% of all kills, and 70.3% of the consumed prey. Adult/adolescent female chimpanzees accounted for 23.1% of all kills and 20.4% of red colobus kills, both of which are higher than proportions reported in other areas. There are several possible explanations for these changes: (1) improved observation conditions, including familiarization of the chimpanzees with human observers; (2) environmental changes such as forest and faunal recovery, particularly an increase in the red colobus population; (3) change(s) in observation methods; (4) a new invention or (5) reinvention by the Mimikire (M) group chimpanzees; and (6) the change in intergroup relationships between the M and Kajabala (K) groups.

Wild chimpanzees deprived a leopard of its kill: Implications for the origin of hominin confrontational scavenging.

This study reports the first observed case of wild chimpanzees (Pan troglodytes) obtaining animal prey freshly killed by a sympatric leopard (Panthera pardus) and scavenging it with the leopard still nearby. This observation has important implications for the emergence of confrontational scavenging, which may have played a significant role in human evolution. Many scholars agree that eating meat became important during human evolution, and hominins first obtained meat by scavenging. However, it is debatable whether scavenging behavior was "passive" or "confrontational (power)." The latter is more dangerous, as it requires facing the original predator, and it is thus considered to have been important for the evolution of several human traits, including cooperation and language. Chimpanzees do scavenge meat, although rarely, but no previous evidence of confrontational scavenging has hitherto emerged. Thus, it was assumed that they are averse to confrontation with even leopard-sized predators. However, in the observed case the chimpanzees frequently emitted waa barks, which indicated that they were aware of the leopard's presence but they nevertheless continued to eat the scavenged meat. In addition, we compiled and reviewed 49 cases of chimpanzee encounters with animal carcasses in the Mahale Mountains of Tanzania in 1980-2017. Chimpanzees scavenged meat in 36.7% of these cases, and tended to eat the meat when it was fresh or if the animal species was usually hunted by chimpanzees. However, no evidence indicated that carcasses were avoided when leopard involvement was likely. These results suggest that chimpanzee-sized hominins could potentially confront and deprive leopard-size carnivores of meat.

Hormonal contraceptive affects heterosexual but not homosexual behavior in free-ranging female Japanese macaques over 17 mating seasons.

We assessed the effect of a progestin-based contraceptive treatment (chlormadinone acetate) on female heterosexual and homosexual behaviors in a free-ranging group of Japanese macaques (Macaca fuscata) living at Arashiyama-Kyoto, Central Japan. The data included estimated intensity of fertility cues, sexual solicitations and mounting behaviors collected daily during 17 consecutive mating seasons (1995-2012) from 159 females. Females that were on contraception: (1) exhibited less intense cues of putative fertility and for shorter periods; (2) were solicited by fewer males, and those males that did solicit them did so less often (i.e., lower heterosexual attractivity); (3) solicited fewer males and when they did perform sexual solicitations they did so less often (i.e., lower heterosexual proceptivity); (4) engaged in shorter heterosexual consortships with fewer male partners (i.e., lower heterosexual receptivity), compared with females that were not on contraception. In contrast, contraceptive treatment had no significant effect on the prevalence, occurrence, frequency, or duration of female homosexual behaviors. Even though heterosexual and homosexual behaviors can both be considered sexual in character and under hormonal control, our results suggested they are, to some extent, dissociable. Because females engaging in homosexual interactions showed less intense cues of putative fertility than those engaging in heterosexual interactions, regardless of contraceptive treatment, we argued that the hormonal threshold required for the expression of heterosexual behavior by females was associated with elevated sex hormones levels compared to homosexual behavior. We discussed the hormonal correlates of sexual behavior and partner preferences in Japanese macaques.

Lifespan and Reproductive Senescence in a Free-Ranging Ring-Tailed Lemur (Lemur catta) Population at Berenty, Madagascar.

The lifespan and age-specific fecundity of female ring-tailed lemurs (Lemur catta) were estimated from a 24-year longitudinal dataset based on individual identification at Berenty Reserve, Madagascar. The mean lifespan of females in 10-year (1989-1998) birth cohorts was 4.9 ± 4.9 years (n = 77), and the longest recorded lifespan in the population was 20 years. The mortality rate of adult females increased to ≥20% at 10-11 years old and reached 33-50% at 12-15 years old. Although the birth rate of old females (12-17 years old) was 72.0%, slightly lower than that of prime adult females (4-11 years old), i.e. 80.2%, no significant difference was found between them. Half of the females who reached the age of 12 years gave birth in the last year of their life. The oldest mother to give birth was 17 years old. These results suggest that most females can maintain reproductive performance in their later life and that there is no evidence for a postreproductive lifespan in this species.

Isolation and characterization of microsatellite loci for the large-seeded tree Protorhus deflexa (Anacardiaceae).

PREMISE OF THE STUDY: Protorhus deflexa is an endemic large-seeded tree in Madagascar that depends heavily on insects for cross-pollination and on large-bodied frugivores for seed dispersal. Because such mutualistic relationships are vulnerable to human disturbance, the development of microsatellite markers will enhance analyses of gene flow in this tree species in degraded forests. • METHODS AND RESULTS: Nineteen microsatellite markers were developed for P. deflexa using 454 pyrosequencing. The number of alleles ranged from two to nine, and the ranges of observed and expected heterozygosities were 0.200-0.800 and 0.303-0.821, respectively. The parentage exclusion probability by the 19 loci reached 0.98583 for the first parent and 0.99971 for the second parent. • CONCLUSIONS: These markers will be useful for studying gene flow via pollination and seed dispersal by animals and the genetic structure of P. deflexa in protected and degraded forests in Madagascar.

The relationship between female rank and reproductive parameters of the ringtailed lemur: a preliminary analysis.

We used data from a 13-year field study of wild ringtailed lemurs to analyze the relationship between female rank and reproductive parameters. In medium and small groups there were no significant differences in birth rate, infant mortality rate, and the number of surviving infants between the female rank categories. On the other hand, in large sized groups low-ranked females had a smaller number of surviving infants than middle-ranked females. This suggests that in large sized groups, within-group competition lowered the values of reproductive parameters of low-ranked females. On the other hand, high and low-ranked females of small sized groups tended to have a smaller number of surviving infants than high-ranked females of medium sized groups and middle-ranked females of large sized groups. Between-group competition should lower the values of their reproductive parameters. In sum, these results fit the expectation from Wrangham's (1980) inter group feeding competition model.

Food conditions, competitive regime, and female social relationships in Japanese macaques: within-population variation on Yakushima.

Feeding conditions, competitive regime, and female social relationships of Japanese macaques (Macaca fuscata) on Yakushima were compared between the two habitats at two different altitudes (coniferous forest, 1,000-1,200 m and coastal forest, 0-200 m). Fruit availability was higher in the coastal forest. There was no consistent difference in the frequency of agonistic interactions within a group during feeding between the two habitats. The coastal forest evoked stronger inter-group contest competition compared to the coniferous forest as evidenced by a higher inter-group encounter rate and a higher proportion of aggressive encounters to non-aggressive ones. Birth rate was higher in larger groups compared to smaller ones in the coastal forest, but did not differ in the coniferous forest. In spite of these differences in competitive regime, no variation in female social relationships was observed, such as direction and concentration on particular individuals in grooming, linearity in dominance rank, counter-attack, and support of juvenile kin during agonistic interactions. The present results indicate that the female social relationships of Japanese macaques are robust and do not change according to changes in the current environment.

Body mass of wild ring-tailed lemurs in Berenty Reserve, Madagascar, with reference to tick infestation: a preliminary analysis.

In 1999, we measured the body mass of 101 wild ring-tailed lemurs (Lemur catta) inhabiting the Berenty Reserve, Madagascar. In addition, we counted the number of ticks [Haemaphysalis (Rhipistoma) lemuris Hoogstraal, 1953] infesting their facial skin and external auditory meatuses. For both males and females, the body mass appeared to increase until the age of 3 years. With the apparent exception of infants, there were no sexual differences in body mass. Within a group, higher-ranked adult males tended to be heavier than lower-ranked males. In contrast, there was no consistent correlation between the body mass of females and their ranks. Among the study groups, there was a small difference in body mass and significant difference in the number of ticks infesting the facial skin and external auditory meatuses. In particular, lemurs of a group who inhabited an area of gallery forest in the study area exhibited the smallest values of body mass and were severely infested with ticks. Such group variations were not consistently correlated with the reproductive parameters of the study groups. In three groups moderately infested with ticks, ticks infested adult males and subadults more heavily than adult females, juveniles, and infants.

Influence of group size on reproductive success of female ring-tailed lemurs: distinguishing between IGFC and PFC hypotheses.

Based on data obtained over a period of 11 years from female ring-tailed lemurs (Lemur catta), we analyzed the correlation between group size and female reproductive parameters. The birth rate and mean number of surviving infants 1 year after birth per adult female generated an inverted U-shaped curve when plotted against group size (although not significant) and number of adult female members. Infant mortality rate did not have a consistent correlation with group size and number of adult female members. Thus, our findings were similar to the predictions of Wrangham's inter-group feeding competition hypothesis.

Long-term changes in dominance ranks among ring-tailed lemurs at Berenty Reserve, Madagascar.

A study was conducted between 1989 and 2001 to monitor changes in the dominance ranks among adult ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. Adult females were observed to be dominant over adult males. Their rank fluctuated greatly. However, in some troops, female rank orders were fairly stable over a period of several years. In general, male ranks were more unstable than female ranks. Most young females aged 3 years occupied the lowest ranks among adult females. However, several were also observed to have attained relatively higher ranks, placing them right beneath their high-ranking mothers; this suggested the existence of "dependent ranks". Mothers were dominant over their daughters. Similarly, older sisters were usually dominant over younger sisters. The mean duration of alpha status for females was 1.95 years, although considerable variation was observed in the duration of the alpha status (1-5 or more years). Most young males aged 3 years initially occupied the lowest ranks in their natal troops, and then they migrated to non-natal troops around the age of 4 years. They ascended in rank between the ages of 4 and 6 years, although there was considerable variation in the acquirement of high rank. The mean duration of alpha status for males was 2.2 years. Larger males were observed to occupy higher ranks. Occasionally, both males and females showed intense aggression (i.e., targeting aggression) towards others.

Comparisons of food availability and group density of Japanese macaques in primary, naturally regenerated, and plantation forests.

We compared food availability and group density of Japanese macaques in Yakushima, southern Japan, among primary forest and two habitats that had been disturbed by logging and had different regeneration histories. The study was conducted in an undisturbed national park, forest that was logged 7-18 years ago and later naturally regenerated, and forest that was logged 19-27 years ago and later planted with Japanese cedar (Cryptomeria japonica) trees. The plantation forest was primarily composed of large Cryptomeria japonica trees at low stand density, while the naturally regenerated forest was composed of many small trees. The total basal area and number of trees in the primary forest were comparable to those in the plantation forest. Annual fruit production was greatest in the naturally regenerated forest, intermediate in the primary forest, and negligible in the plantation forest. Herb availability was high in the naturally regenerated forest, but low in the primary and plantation forests. The group density of Japanese macaques was high in the naturally regenerated forest, intermediate in the primary forest, and low in the plantation forest. Since group size in the naturally regenerated forest was small, individual density was almost the same as in the primary forest. These results suggest that the effects of regeneration on macaques vary between the two habitats. The plantation forest consisted mostly of Cryptomeria japonica, which supplies only flowers as food in a limited season, and had a lower density of macaques. On the other hand, in the naturally regenerated forest, fruit production and herb availability were high (probably because of the enhanced light conditions after logging), and the density of macaques was as high as in the primary forest.

New method to census primate groups: estimating group density of Japanese macaques by point census.

We devised a new method to estimate the density of primate groups in habitats that preclude the use of a line-transect census because the ground is too steep. We combined point census and group follows. From the number of groups counted at a fixed point for an hour, n, group density D was calculated: D = lambda n / pi. Lambda, the detectability constant, was a constant when distance-dependent detectability g(y) was regressed on a half-normal model: g(y) = e (-lambda y(2)) and can be estimated by combining the information of group follow and point census. Using this method, we estimated the group density of Japanese macaques in Yakushima. A census area of 7 km(2) was divided into 28 grid squares (500 m x 500 m). One observer was positioned at a point in each grid square, and those points were censused simultaneously for 4-6 days from 0600-0700 to 1500-1600 hr. Four troops were followed for 144 hr during the point census. Distance-dependent detectability closely correlated with the half-normal model. The detectability constant varied with the time of day, but it was not influenced by troop identity or topography. Group density was calculated to be 1.48 +/- 0.61 and 0.701 +/- 0.432 groups/km(2) in the disturbed and undisturbed areas, respectively (95% confidence limit). "True" group density estimated by home range data was within the confidence limit calculated by a point census in the home range of the troops for two troops, suggesting that this method was valid. This method is applicable to other species as long as at least one group can be followed, because it satisfies the fundamental assumptions of point census, and the detectability does not seem to be biased by troop or topography.

Population and social dynamics changes in ring-tailed lemur troops at Berenty, Madagascar between 1989 - 1999.

In the present study, we recorded all births, immigrations, deaths, and emigrations for a population of ring-tailed lemurs at Berenty Reserve, Madagascar, between September 1989 and August 1999. In September 1989, three troops (C, B, and T) inhabited the study area of 14.2 ha. During the 10-year period, eight troop divisions, six evictions of females, and three troop takeovers of ranges by other troops occurred in and around the study area. Consequently, in August 1999, the number of troops in the same area increased to six (CX, C1, C2A, C2B, T1, and T2). The number of lemurs aged > 1 year increased from 63 to 82, which resulted from 204 births, 58 immigrations, 125 deaths, and 118 emigrations. Of the 204 newborn lemurs during the study period, 103 died, 44 emigrated outside the study area, and 57 remained within the study area. The total number of lemurs that emigrated from natal troops was 69 (54 males and 15 females). Natal males left their troops around the age of 3. Non-natal males changed troops after a tenure varying from 1 to 7 years. Survival curves showed a fall in survival rates of both sexes to < 0.5 between the ages of 2 and 3. For females, the survival rate gradually decreased to < 0.2 at the age of 9. On the other hand, due to emigration, the survival rate of males could not be determined after the age of 5 yr. Since some males attained high-rank at the age of 6 - 10 yr, the prime age for male ring-tailed lemurs is thought to be around 7 - 10 yr. Ring-tailed lemurs are essentially female philopatric, because all cases of females leaving natal troops resulted from troop divisions or forced evictions. Such social changes may have resulted from competition among females. All cases of troop divisions or evictions occurred in larger troops consisting of >or=20 lemurs, and only a few females could rejoin their troops. When males joined such a female-group, a new troop was formed. Although promoted by an increase in population, frequent emigrations of females from original troops are the characteristics of ring-tailed lemurs at Berenty.

Troop extinction and fusion in wild Japanese macaques of Yakushima Island, Japan.

A wild Japanese macaque troop decreased in size because the birth rate dropped and infant mortality increased. In the 1989 mating season, the last male left the troop, and the remaining two females joined a neighboring troop. Thus, the troop ceased to exist as an independent troop. A lower limit to troop size may exist, below which a troop cannot effectively defend its range, forcing the females to join a larger troop. © 1994 Wiley-Liss, Inc.