The role of kinship in the formation of a primate multilevel society

A small number of mammalian species live in a modular or multilevel society in which several individual social/reproductive units called one-male units (OMUs) are embedded within a large cohesive band. Factors that affect band composition and stability are poorly understood. In this study we examined the role of kinship in the formation and maintenance of a multilevel society in an endangered population of golden snub-nosed monkeys (Rhinopithecus roxellana). From 2005 to 2011, we obtained genetic samples from 86 individuals (including 88.9% of leader males and 80.5% of adult females) living in a band of 8–10 OMUs. We used microsatellite genotyping to identify patterns of relatedness and individual transfer. We found that adult females residing in the same OMU were more closely related to each other than to a random set of females drawn from the band and that females tended to disperse into OMUs that contained female relatives. In addition, adult females who transferred were not more closely related to their previous leader male than to the leader male of their new OMU. These results support the contention that kin bonds contribute importantly to the formation and stability of this primate multilevel society by influencing a female's decision to remain in her current OMU, or during transfer, which new OMU to enter. Am J Phys Anthropol 156:606–613, 2015. © 2014 Wiley Periodicals, Inc.     

Group composition in wild and commensal hamadryas baboons: A comparative study in Saudi Arabia

Papio hamadryas was surveyed throughout its range in Saudi Arabia and was observed at altitudes ranging from 0 to 2300 m. Wild populations occur along the whole range of altitude, while commensal populations are only found above 850 m altitude. No variation in group size was found with altitude. Comparison of wild and commensal populations showed the following. (1) Their composition in terms of age and sex classes, overall adult sex ratios, and group size does not significantly differ. (2) Groups of both populations include, in similar proportions, three types of parties: one-male units (>70%), two-male units (>13%), and a few other units of variable composition. (3) The mean size of commensal parties is significantly larger than in the wild population; specifically one-male units are larger in the commensal population due to a larger number of females per male. Thus, female distribution in commensal groups is more inequitable than that in wild groups. (4) Finally, the number of females included in two-male units increases with altitude. These differences are discussed in terms of food availability and predator pressure and are compared with results obtained on other Arabian and Ethiopian populations.     

The influence of snowfall,temperature and social relationships on sleeping clusters of Japanese monkeys during winter in Shiga Heights

We studied Japanese monkeys (Macaca fuscata) of the Shiga A₁ troop at their sleeping sites in Shiga Heights, Japan, for 41 nights during 3 winters. Monkeys chose their sleeping sites in Japanese cedars and in deciduous broad-leaved forests on non-snowing nights and in Japanese cedar forests on snowing nights. We counted 399 sleeping clusters in which 2 or more monkeys remained in physical contact through the night and 43 solitary sleeping monkeys, though monkeys did not maintain physical contact with others in the daytime. We found 397 clusters on tree branches and 2 clusters on rocks. The mean size of huddling clusters was 3.06±1.22 SD. The cluster size (3.17±1.26 SD) at lower ambient temperatures between −7 and −4°C was larger than that at higher temperatures between −2 and 4°C (cluster size 2.88±1.13 SD). Most clusters were composed of kin. Females kept close to related females in the daytime and huddled with them at night. The highest-ranking male mainly huddled with his kin and his familiar females. Other males kept farther apart from each other in the daytime, probably to avoid social conflicts. Through cold winter nights, however, such males reduced inter-individual distances and huddled with other males. Japanese monkeys appear to recognize three types of inter-individual distances: an intimate distance less than 1 m, a personal distance of 1–3 m and a social distance of 3–20 m; they change their inter-individual distances according to social and ecological circumstances.     

A preliminary study of food transfer in Sichuan snub-nosed monkeys (Rhinopithecus roxellana)

Food transfer happens regularly in a few nonhuman primates species that are also characterized by remarkable social tolerance. Sichuan snub-nosed monkeys (Rhinopithecus roxellana), or golden monkeys, which exhibit high social tolerance in their social relationships are thus of interest to see whether tolerance would extend to food transfer. In this study, branch feeding activity was observed in a semi-captive group of Sichuan snub-nosed monkeys, which consisted of 10 subjects that included a one-male unit (OMU) and an all-male unit (AMU). We recorded 1,275 food interactions over 27 days, and 892 instances of food transfer. The most commonly observed types of food transfer behavior were co-feeding (62.1%) and relaxed claim (22.8%). Of 892 food transfers, 756 (84.8%) took place in the OMU, most of which were among adults (34.7%) and among juveniles (42.1%). The transfer success rate was high in both the cases (87.9% for adults and 78.9% for juveniles). Food transfer in the AMU took place less often than that among adults in the OMU though with similar high transfer success. Food transfer between the OMU and AMU was limited to juvenile males from the OMU and adults from the AMU. These results provide the first evidence of food transfer in golden monkeys and suggest that tolerant social relationships in golden monkeys make transfer possible.     

A study on the social structure and dispersal patterns of hamadryas baboons living in a commensal group at Taif,Saudi Arabia

Three levels of hamadryas social structure—the one male unit (OMU), the band, and the troop—have been observed at all sites studied, but a fourth—the clan—has been observed at only one site, Erer-Gota, Ethiopia, during a longitudinal check of the dispersion of identified individuals. The clan is important since it appears to provide the basis for male philopatry, although comparative data is needed from other sites to confirm this. We studied a huge commensal group of hamadryas baboons (over 600 animals) in Saudi Arabia. We put ear tags on baboons between 1998 and 2004 and analyzed social structure, relying on the interactions of these tagged animals by focusing especially on their dispersal patterns from OMUs. OMU membership tended to be looser than that of the Ethiopian hamadryas. Females tended to shift between OMUs on an individual basis in our study group, whereas the collapse of an OMU was a major occasion of adult female transfer in Ethiopia. We found neither stable bands (a “band” in our study group was defined as a regional assemblage of OMUs) nor clans that lasted for several years. Some OMUs moved and transferred into neighboring areas over both the short and long term. Further, some post-adolescent males appeared to move out of the study area. The ratio of adult females in an OMU in our study group was larger than for any other documented study site, and this may be the reason for enhanced female transfer between OMUs. A large proportion of the adolescent females showed no clear membership to OMUs, and no “initial units” (commonly observed in Ethiopia) were discernible. The ease with which young males acquired adult females at the study site must have disrupted the formation of a clan, a “male-bonded society.”     

Impact of male takeover on intra-unit sexual interactions and subsequent interbirth interval in wild Rhinopithecus roxellana

Data were collected on sexual interactions before and after a male takeover of a one-male unit (OMU) of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China. The original unit consisted of an adult male, 2 adult and 2 subadult females, 2 female juveniles and a single infant. Following the takeover, the new resident male copulated with 1 adult female, which was not lactating. Subsequent to the disappearance of her infant, the second (lactating female) entered breeding condition and began to solicit copulation with the new resident male. The subadult females also engaged in matings with the new male. The new resident male was observed mating, on 3 occasions, with females in 2 other OMUs. These are the first observations of sexual behaviour in free-ranging Sichuan snub-nosed monkeys after an OMU takeover. Sexual interactions play an important role in establishing relationships between the new male and resident females in the OMU.     

Copulation patterns in captive hamadryas baboons: a quantitative analysis

For primates, as for many other vertebrates, copulation which results in ejaculation is a prerequisite for reproduction. The probability of ejaculation is affected by various physiological and social factors, for example reproductive state of male and female and operational sex-ratio. In this paper, we present quantitative and qualitative data on patterns of sexual behaviour in a captive group of hamadryas baboons (Papio hamadryas), a species with a polygynous–monandric mating system. We observed more than 700 copulations and analysed factors that can affect the probability of ejaculation. Multilevel logistic regression analysis and Akaike’s information criterion (AIC) model selection procedures revealed that the probability of successful copulation increased as the size of female sexual swellings increased, indicating increased probability of ovulation, and as the number of females per one-male unit (OMU) decreased. In contrast, occurrence of female copulation calls, sex of the copulation initiator, and previous male aggression toward females did not affect the probability of ejaculation. Synchrony of oestrus cycles also had no effect (most likely because the sample size was too small). We also observed 29 extra-group copulations by two non-adult males. Our results indicate that male hamadryas baboons copulated more successfully around the time of ovulation and that males in large OMUs with many females may be confronted by time or energy-allocation problems.     

Social organization of black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Deqin, China

Data on social organization of two bands of black-and-white snub-nosed monkeys (Rhinopithecus bieti) were collected when the monkeys were crossing an open spot at Nanren and Bamei (northwest of Yunnan, China) using a sampling rule where individuals within one social unit are spatially closer to each other than individuals between social units. The typical pattern of social organization in this sample was multiple adult females (AFs) and their offspring with one adult male (AM) in a one-male unit (OMU), similar to that of many other colobines. In such units, on average one male is associated with 4.0 AFs and 2.5 of their offspring. Moreover, there are multimale/multifemale units and monogamous units besides OMUs. All bisexual units traveled together with at least one all-male unit as a cohesive band. In two bands of monkeys, 87% of AMs in bisexual units were within OMUs, 7.8% within monogamous units and 5.2% within multimale, multifemale units. In the Bamei band, 6.7% of AMs were in the all-male unit. The size of OMUs in the Nanren band was larger than that of the Bamei band, with more AFs and juveniles, which may be related to better conservation in the Nanren band's habitat. For the Nanren band, the average number of AFs in OMUs varied across time, increasing from 4.3 in 1994 to 5.1 in 2001, and then decreasing to 3.8 in 2005. This article suggests three possible explanations for this variation, but more data are needed for these hypotheses to be tested.     

Annual variation in reproductive parameters of Adélie penguins at Edmonson Point,Victoria Land,Antarctica

Annual egg and chick production and breeding success at the Adélie penguin (Pygoscelis adeliae) colony Edmonson Point (74°21′S–165°10′E), Victoria Land, is presented for eight breeding seasons between 1995 and 2005. During this period the colony consisted of 10–13 subcolonies and averaged 2098 ± 278 breeding pairs. A sample of over 100 nests (114–150), belonging to two subcolonies, was monitored each year. Some breeding parameters remained constant while others showed substantial annual variation. Laying date showed little variation, and laying was highly synchronous: 82.5% of clutches were initiated in a 10-day period, 9–18 November. In contrast, clutch size (1.77–1.97) and incubation period (34.4 ± 2.5) varied significantly. Variation among years was also recorded in hatching success (from 58 to 86%) and breeding success. This last parameter, measured as number of chicks reared to crèche per nest with eggs, varied between 0.34 and 0.97.     

Effects of Seasonal Folivory and Frugivory on Ranging Patterns in <Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>

The distribution of food resources in time and space may affect the diet, ranging pattern, and social organization of primates. We studied variation in ranging patterns in a group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) over winter and summer in response to variation in their diet in the Qingmuchuan Nature Reserve, China. There was a clear diet shift from highly folivorous in winter to highly frugivorous in summer. The home range was 8.09 km² in summer and 7.43 km² in winter, calculated via the 95% kernel method. Corresponding to the diet shift, the focal group traveled significantly longer distances in summer (mean 1020 ± 69 m/d) than in winter (mean 676 ± 53 m/d); the daily range was also significantly greater in summer (mean 0.27 ± 0.02 km²/d) than in winter (mean 0.21 ± 0.01 km²/d). There was no significant variation in home range size between winter and summer, and the monkeys did not use geographically distinct ranges in summer and winter. However, overlap in the actual activity area and core range between winter and summer was only 0.13 km², representing 4.4% of the summer core area and 5.3% of the winter core area. Differences were apparent between summer and winter ranging patterns: In summer, the group traveled repeatedly and uninterruptedly across its home range and made 3 circles of movement along a fixed route in 31 d; in winter, the activity area was composed of 3 disconnected patches, and the focal group stayed in each patch for an average of 8 successive days without traveling among patches. Winter range use was concentrated on mixed evergreen and deciduous forest patches where leaves and fruits were available, whereas the summer range pattern correlates significantly positively with the distribution of giant dogwood (Cornus controversa) fruits. Thus it appears that the diet shift of Sichuan snub-nosed monkeys between winter and summer caused the monkeys to use their home range in different ways, supporting the hypothesis that food resources determine primate ranging patterns.     

Vertical distribution of wild Yakushima macaques (Macaca fuscata yakui) in the western area of Yakushima Island, Japan: Preliminary report

A census of wild Yakushima macaques (Macaca fuscata yakui) was carried out in a 23-km² area of the western coast of Yakushima Island, Japan. We analyzed the census data to investigate changes in monkey distribution associated with the vertical distribution of vegetation. In the lowland coastal zone of 0–300 m above sea level (a.s.l.), 4.8 troops and 62.4–99.8 monkeys are estimated to have existed per km². In the mountainside zones of 300–900 m a.s.l., the troop density decreased to 1.3–1.6 troops/km². Since there was no difference in size between the coastal and mountainside troops, population density should decrease with altitude to about 30–36 monkeys per km². On the other hand, 2.4 troops and about 36 monkeys were estimated to have inhabited per km² in the mountain summit zone of 900–1,323 m a.s.l. Nature Conservation College     

Cerebrospinal Fluid Monoaminergic Metabolites in Wild Papio anubis and P. hamadryas are Concordant with Taxon-specific Behavioral Ontogeny

We used a cross-sectional sample to compare ontogenetic trajectories in the concentrations of monoamine neurotransmitter metabolites in cerebrospinal fluid of wild anubis (Papio anubis, n = 49) and hamadryas (P. hamadryas, n = 54) baboons to test the prediction that they would differ, especially in males, in association with their distinct behavioral ontogenies. Values of all 3 metabolites [3-methoxy-4-hydroxyphenylglycol (MHPG), the norepinephrine metabolite; 5-hydroxyindoleacetic acid (5-HIAA), the serotonin metabolite; and homovanillic acid (HVA), the dopamine metabolite] declined consistently with dentally-calibrated maturation, and few taxon-related differences were apparent among juveniles. Adult females were too few for adequate comparison, but a discriminant function suggested that they might differ by taxon. Adult males of the 2 species differed strikingly from juveniles and from each other. Contrary to our initial hypothesis, adult male anubis had significantly lower HVA and MHPG, and higher 5-HIAA levels, than predicted from the overall, age-related trend, and MHPG continued to decline with age among adults. As young adults, male hamadryas had low 5-HIAA and a high HVA/5-HIAA ratio, while older males [normatively one-male unit (OMU) leaders] showed a reversal in the trend, with 5-HIAA rising and the HVA/5-HIAA ratio tending to fall. We speculate that the results are related to the dispersing and philopatric ontogenies of anubis and hamadryas males, respectively. Adult male anubis, whose fitness depends on building social networks with nonkin, have high relative serotonin activity, commonly associated with greater social circumspection and skill. Young adult male hamadryas, living among agnatic kin and mating opportunistically, exhibit low 5-HIAA levels, generally associated with impulsivity and social irresponsibility. This reverses as a male approaches the age at which he is normatively the leader of a one-male unit (OMU), and his fitness depends on his maintaining stable relationships with other leaders and with females. An erratum to this article can be found at     

Ranging Behavior of Proboscis Monkeys (Nasalis larvatus) in the Lower Kinabatangan, Northern Borneo

I studied the ranging behavior of proboscis monkeys (Nasalis larvatus) at two sites in the Lower Kinabatangan Region of northern Borneo. I collected data on ranging behavior via scan sampling during group follows. Groups of Nasalis larvatus had ranges overlapping those of other groups in each area. I observed no territorial behavior. Groups of Nasalis larvatus occasionally swam across the Kinabatangan River, and frequently across its tributaries. The home range size of a focal one-male group (SU1) was 220.5 ha. The group traveled farther on days when the proportion of young leaves in the diet was higher. In addition, SU1 used particular areas when they fed on flowers and fruits. Apparently, rainfall and phenology did not influence ranging patterns.     

Growth and reproductive parameters of bonnet monkey (Macaca radiata)

The present paper summarizes some of the important biological and physiological data recorded over a 30-year period on the biology of bonnet monkeys in captivity. Data on sexual maturity, menstrual cyclicity, general behaviour, endocrine profile, reproductive physiology, gestation, parturition, postpartum amenorrhoea in the female, and sexual maturity, hormone profile, and seasonal variation in sperm count of the male monkeys are presented. In addition to the biological values, weights of selected organs, vertebral and dental pattern are also presented. Menarche occurred at an age of 36±4 months and the first conception in the colony occurred at an age of 54±4 months. The average menstrual cycle length was 28±4.3 days. Majority of monkeys did not cycle regularly during March–June during which the temperature reached a peak. The pregnancy index of the colony was 80% with controlled breeding. The gestation period was 166±5 days with 6–7 months postpartum amenorrhoea. Males attained sexual maturity by the age of 6–7 years and exhibited the characteristic nocturnal surge of serum testosterone at this age and sperm concentration ranged from 116–799 millions/ejaculate.     

Periovulatory time courses of plasma estradiol and progesterone in the Japanese monkey (Macaca fuscata)

Periovulatory time courses of plasma estradiol and progesterone were determined in 21 menstrual cycles of 20 Japanese monkeys. Both steroids were measured by radioimmunoassay. Ovulation was detected by serial laparoscopic observations of the ovaries. Three of the 21 cycles were anovulatory cycles. In the remaining 18 ovulatory cycles, a preovulatory estradiol peak occurred on day 12.2±1.4 (range 10–15) of the menstrual cycle. The estradiol concentration at the peak was 431±199 (range 210–930) pg/ml. The time interval between the estradiol peak and ovulation was within 48 hr; the shortest interval was 10–13 hr and the longest 32–48 hr. Although the progesterone levels began to increase slightly (0.6–1.4 ng/ml) before ovulation, they did not show a continuous increase but decreased once before ovulation. The increase in progesterone with development of the corpus luteum after ovulation was very gradual during the first 2 days after ovulation. Subsequently, in 13 of 18 ovulatory cycles the progesterone levels rose rapidly and reached a maximum, 4.0±1.2 (range 2.3–5.7) ng/ml, 4–8 days after ovulation. In 5 of the 18 cycles, the progesterone levels did not rise at all or did not exceed 2.0 ng/ml even if they showed more or less an increase. In the 5 cycles, the length of the luteal phase was 8.2±1.6 (range 6–10) days, which was significantly shorter than that of the former 13 cycles with 14.0±1.1 (range 13–16) days.     

神农架自然保护区川金丝猴投食群友好行为的初步观察

为探讨人工补食条件下川金丝猴(Rhinopithecus roxellana)的友好行为因补食产生的影响,2007年1～9月,采用行为取样法、扫描取样法和全事件记录法对湖北神农架自然保护区大龙潭投食猴群的友好行为进行了观察.共记录到11种友好行为,发生频次居前的是理毛、张嘴、拥抱、游戏、趋近.友好行为的发起者和承受者在性别间差异均不显著,但在年龄间差异均显著.在一雄多雌单元内发起者按次数多少为成年、少年、青年、亚成年猴,承受者的顺序亦如此.在全雄单元内发起者按次数多少为成年、少年、亚成年、青年猴,承受者的顺序亦如此.友好行为在单元内和单元间差异显著,单元内多于单元间.这在一定程度上说明川金丝猴社会单元内个体间的关系紧密,单元间的关系相对疏远.友好行为在繁殖和非繁殖季节差异不显著.     

The variable social organization of hanuman langurs(Presbytis entellus), infanticide,and the monopolization of females

Data from 24 wild populations of hanuman langurs (Presbytis entellus)in south Asia are used to test hypotheses seeking to explain variation in troop structure and the incidence of infanticide. The occurrence of infanticide is associated with a one-male troop structure and not with a high density. The density, predation, and economic-advantage hypotheses, as explanations for the occurrence of one-male and multimale troops, are not supported by the review. However, the monopolization hypothesis is not contradicted; the number of adult males per troop is significantly correlated with troop size and with the number of adult females per troop. Therefore it is suggested that a one-male troop structure will arise if a male is able to monopolize a group of females, a multimale troop if he cannot. One-male troops may predispose to infanticide because of high variance in male mating success and high intermale competition between groups rather than within troops. If female dispersion determines troop structure, it is speculated that females could manipulate males to form a multimale society if the advantages in terms of infant survival and intertroop conflict exceeded the costs in terms of not producing infanticidal “sexy sons.”     

The reconciliation behavior of golden monkeys (Rhinopithecus roxellanae roxellanae) in small breeding groups

Observations were made following 130 spontaneous aggressive incidents in two small breeding groups of captive golden monkeys (Rhinopithecus roxellanae roxellanae). Participants were observed both during the first 10 min following these incidents and during matched control observations. An increased contact rate was observed between opponents following the aggressive incident. Post-conflict contacts were characterized by a number of behavior patterns: open mouth, rapid grooming, embrace, and crouching. Adult males played an important role as mediator in agonistic disputes among females: males intervened in 93.6% of female fights. It is speculated that this intervention behavior is related to the species' organization into one-male units.     

Copulation behavior within one-male groups of wild <Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis> in the Qinling Mountains of China

This study was conducted using focal animal sampling on the west ridge group of the Sichuan snub-nosed monkey (Rhinopithecus roxellana) located in the Zhouzhi National Nature Reserve on the north slope of the Qinling Mountains, from 8 July 2003 to 24 May 2004. The difference in the average frequency of copulations for each focal male for each month was significant (F = 3.068, P = 0.016, one-way ANOVA test) with the majority of copulations occurring between September and November. Duration of intromission ranged from 2 to 39 s, with a mean of 16.0 ± 0.4 s. Females initiated 627 courtship attempts (96.2%), while males only initiated 3.8%. Both adult females (72.8%) and sub-adult females (27.2%) were involved in sexual interference acts. Females who gave birth in 2004 performed more sexual interference acts than would be expected by chance in the reproductive period of 2003 (X ² = 13.73 > X ² _0.005,2, df = 2, P < 0.005). Male response to female interference was equally divided into “solicitor mounting” and “interrupter mounting”. The resident males of one-male units were not observed to mount both the solicitor and the interrupter or mount neither following female solicitation interruptions. Three post-conception copulations were also observed in this study. These results suggest a skewed sexual competition, with multiple females competing for a single male, which was shown by courtship attempts and female interference.     

Field ecology and behaviour of the rhesus macaque (Macaca mulatta): I. Group composition,home range,roosting sites,and foraging routes in the Asarori Forest

The data presented here resulted from about 1,100 observation hours in a nine-month field study of rhesus monkey from January to October 1976 in the Asarori Forest, Dheradun. Six groups were studied, the group size varied from 6–90 individuals. With the exception of one group, all were of the bisexual multimale type. The number of adult males per group varied from two to seven, and of adult females from 4 to 27. The adult sex ratio was male 1 to females 2.2–3.7 (mean 1:2.7). The exceptional group originally consisted of five juveniles only (3 ♂, 2 ♀); later on an adult male joined the group. Home ranges varied from 1.3–13.4 km² and overlapped extensively with another. The area of home range showed straight line relationship with group size. Roosting sites were not fixed but changed from night to night. The straight line distance between one night to the next varied from 75–2,500 m. Foraging routes per day ranged from 1,050–3,500 m (mean 1,803.3±160.2). There is a significant relationship between the foraging route (L) and the straight line distance between roosting sites (D). The ratio D/L varies from 0.14–0.87.