Female choice impacts resident male takeover in golden snub-nosed monkeys(Rhinopithecus roxellana)

In primate species with social systems consisting of one-male breeding units(OMUs), resident male takeover represents a major challenge to individual reproductive success and mating strategies. The golden snub-nosed monkey(Rhinopithecus roxellana)is characterized by large multilevel societies(MLS)comprised of several OMUs and all-male units(AMUs);however, the factors and mechanisms associated with resident male takeover, which offer important insight into primate reproduction and social strategies, are still poorly understood. Based on 5-year monitoring data from a free-ranging herd of golden monkeys from the Qinling Mountains in China, we categorized three phases of an OMU, that is, a rising phase,developing phase, and declining phase. The rising and declining phases were unstable periods in which male takeover in an OMU might occur. Factors causing takeover, such as leader male rank, fighting ability, reproduction rate, and affiliation(proximity,allogrooming), were analyzed for males and females and for different OMUs. Results indicated that the new resident male's fighting ability was lower than that of the former resident male in 23 cases. After replacement, the rank order of the new resident male significantly declined. Females involved in a takeover increased their distance from the resident male and decreased mating frequency during the three months prior to takeover. Females with infants under one-year-old had a marked effect on the specific time of takeover occurrence. These results suggested that female choice was the main factor deciding whether a takeover attempt was successful. Furthermore, rather than male conflict, females more often initiated and affected takeover and outcome, implying that the social status and competitive ability of the males played lesser roles during takeover.     

Female social dynamics in a provisioned free-ranging band of the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in the Qinling Mountains, China

Little information is available on the social dynamics of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Here, we provide 5-year observational data on a provisioned free-ranging band in the Qinling Mountains, central China, from October 2001 to December 2005. The results of this study suggested that females place a high priority on maintaining long-term relationships with other female in their one-male units (OMUs). Females had more social interactions with unit members than with nonunit individuals. They showed relatively high rates of affiliation with their unit females, intermediate levels with the resident males, and low levels with individuals outside the unit. Females had few interactions with other resident males. Social interactions, especially affiliative interactions, were more symmetrical between focal females and their unit females than between focal females and the resident males. Thus female social interactions appeared to resemble those of other female-bonded primate societies. On the other hand, female transfers occurred sometimes. We recorded 11 cases of female immigration and 5 cases of female disappearance, 1 case of female intraband shift, and 2 cases of "merging of OMUs," which suggested that unit females might be loose-knit in this species. We discussed influencing factors on female Sichuan snub-nosed monkey social dynamics, by comparing them with those of Hamadryas and gelada baboons that also have multilevel societies.     

Social organization of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, Central China

Sichuan snub-nosed monkeys were observed for 197 days from 2000 to 2003 in the Qinling Mountains, Central China. The study group was provisioned in 2001 allowing detailed observations of social organization based on individual identification. The group was composed of 45–82 monkeys, all of which belonged to one of 6–8 one-male units (OMU) that foraged to form one big group. The average unit size was 9.0±2.3, 8±1.5 in the winter and 11.1±2.0 in the spring. Immigration or emigration of one-male units to or from the foraging group was observed, as was migration of individuals in and out of OMU, especially for by subadult females and juveniles. Group size therefore tended to fluctuate with the number of OMU and the number of young monkeys present in the group. The OMU in the study area were smaller than those in Shennongjia area. The factors influencing the size of these OMU and the entire group are discussed.     

Sexual interference in the Golden snub-nosed monkey (Rhinopithecus roxellana): a test of the sexual competition hypothesis in a polygynous species

Sexual interference (SI), which is defined as any disturbance directed to a mating pair by other individuals, has been reported in several primate species. It is widely suggested that successful harassers experience improved mating success by increasing their access to reproductive partners as well as by reducing the mating success of rivals. Although theories of primate sexual conflict highlight male intra-sexual mating competition, females also are reported to actively disrupt copulations between mating partners. In this study, we investigated SI in a multilevel troop of Golden snub-nosed monkeys (Rhinopithecus roxellana) inhabiting the Qinling Mountains, China. Behavioral observations of 11 one-male units (OMU) that comprised the multilevel troop were conducted from September 2007 to May 2008. During this period 17.1% of 652 documented intra-OMU sexual encounters were characterized either by mild or aggressive forms of harassment. Sexual harassment was typically performed by a single individual (91.9%), and in 75.7% of cases the harasser was an adult or sub-adult female. The frequency of female harassment was positively correlated with the number of adult and sub-adult females residing in an OMU, and resulted in a significant decrease in matings ending in ejaculation. We found that the amount of SI a female received was not a significant predictor of her reproductive success. However, females who conceived during the mating season directed higher levels of harassment at other females than females who did not conceive. We evaluate the strength of the sexual competition hypothesis and the hormonally modulated aggression hypothesis in explaining patterns of SI in female Golden snub-nosed monkeys.     

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.     

Evidence of allomaternal nursing across one-male units in the Yunnan snub-nosed monkey (Rhinopithecus Bieti)

Background

Allomaternal nursing, common in several species of social mammals, also has been reported in nonhuman primates. However, the function of this behavior in enhancing infant survivorship remains poorly understood.

Methodology and Principal Findings

The study was conducted on a free-ranging group of the Yunnan snub-nosed monkey (Rhinopithecus bieti) in the Baimaxueshan Natural Reserve. Direct observation and ad libitum sampling were used to record allocare behavior during a 20 month field study. R. bieti exhibits a multilevel social organization in which a large single troop, consisting of over 100 individuals, is divided into many one-male units (OMUs: 6∼41). These OMUs coordinate their daily activities, and feed, forage, travel, and rest together. Here we report on one case of infant temporary adoption in which an adult female from one OMU engaged in allomaternal nursing and cared for an infant from a different OMU of the same troop. This event began when the mother and her five-month-old infant were found to became separated accidentally. The victim infant was observed staying in another OMU. Over the next several days we observed a lactating female in the new OMU to care for and nurse both her infant and the immigrant infant, who also was tolerated by and cared for by the harem male.

Conclusions and Significance

Our findings suggest that lactating primate females are primed to care for young infants and, that the misdirected parental care hypothesis may offer the strongest explanation for allomaternal nursing in R. bieti.     

Dominance relationships among one-male units in a provisioned free-ranging band of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China

We studied the dominance relationships among one-male units (OMUs) in a provisioned free-ranging band of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of central China from 2001 to 2005. The band was composed of 6-8 OMUs that stayed in the band for several years. Linear dominance orders could be detected using displacement interactions with directional asymmetry among OMUs in 82.3+/-5% of interactions, and ambiguous and reversed interactions in 17.7+/-5%. The dominance rank of OMUs was positively related with the duration of their stay in the band, and this may be attributed to the association of the resident male with adult females, rather than the fighting ability of resident males, as males do not fight seriously with each other. Subordinate units were observed to merge with dominant units resulting in an elevation of their rank order. The linear dominance relationship among OMUs in the Sichuan snub-nosed monkeys may have evolved as a result of competition for preferred food trees.     

Social dynamics of the golden snub‐nosed monkey (Rhinopithecus roxellana): female transfer and one‐male unit succession

Among primates that form multilevel societies, understanding factors and mechanisms associated with the movement of individuals between groups, clans, and one‐male social units offers important insight into primate reproductive and social strategies. In this research we present data based on an 8‐year field study of a multilevel troop of Sichuan snub‐nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of China. Our study troop contained 78–126 individuals, and was usually organized into 6–8 one‐male units (OMU). The majority of OMUs were composed of networks of unrelated females and their offspring. We found that 59.7% (43/72) of subadult and adult females in our study troop transferred between OMUs (n=66) or disappeared (n=7) from the troop. In the majority of cases, two or more females transferred together into new OMUs or troops. In R. roxellana, new OMUs formed in several ways. During 2001–2008, 16 adult males appeared in the study troop. Over this period, we observed 13 different males who became harem leaders either by taking over an existing harem or by attracting females from other OMUs into their harem. We also observed four OMUs from a neighboring troop to successfully immigrate into the study troop. The number of individuals in these newly immigrated OMUs was significantly smaller than that number of individuals in resident OMUs. During harem formation, fighting between adult males was rarely observed, and female mate choice appeared to play a crucial role in harem male recruitment and replacement. These results suggest that golden snub‐nosed monkeys are organized in a nonmatrilineal social system. Female mate choice and possibly incest avoidance appear to play important roles in female transfer, male tenure, and OMU stability. Am. J. Primatol. 71:670–679, 2009. © 2009 Wiley‐Liss, Inc.     

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.     

Male Infanticide in the Golden Snub-Nosed Monkey (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>), a Seasonally Breeding Primate

In nonhuman primates, infanticide by adult males can occur when the leader male is ousted from a one-male, multifemale group, or when male dominance rank changes within a multimale, multifemale group. According to the sexual selection hypothesis, this behavior may be adaptive if perpetrators increase their reproductive success by killing unrelated, unweaned infants, thus shortening the interbirth interval of the mother, and then siring her next infant. Under an alternative hypothesis, infanticide is a byproduct of aggressive male–male competition and these predictions do not hold. Direct observations of the context surrounding infanticide in free-ranging primate populations that allow a test of these predictions are rare. Here, we document four cases of male infanticide and report paternity data for a group of golden snub-nosed monkeys (Rhinopithecus roxellana) at Shennongjia, China. Three cases of infanticide by new leader males supported the predictions of the sexual selection hypothesis, while another provides partial support for the sexual selection hypothesis, but can also be explained via a nonadaptive hypothesis. In this latter case, a male from an all-male group killed an infant during an aggressive episode that appeared to be accidental, as it took place 7 mo before a male takeover happened, and the perpetrator did not obtain any reproductive advantage. We conclude that most male infanticide events in golden snub-nosed monkeys are consistent with the adaptive selection sexual hypothesis.     

Evidence for sexually selected infanticide in captiveCercopithecus mitis,Cercocebus torquatus,andMandrillus leucophaeus

Adult resident males of one-male-multi-female primate groups housed at the Hannover Zoo exhibited aggression, when confronted with nonadult individuals, which were fathered by other males: (1) a new adult resident male in a group of blue monkeys killed a 5.8-month-old female infant: (2) a new adult resident male in a group of white collared mangabeys injured a 24.0-month-old female and an 18.9-month-old male severely; they would have died without veterinary care; and (3) the resident male of a group of drills threatened an 1.8-month-old foreign female infant seriously; efforts to introduce the infant were discontinued. Pathological explanations are unlikely because the adult males showed no aggression towards own nonadult offspring under the same captive conditions. By and large, the events support the theory that infanticide is the result of sexual selection among males.     

Female transfer between one-male groups of proboscis monkey (<Emphasis Type="Italic">Nasalis larvatus</Emphasis>)

Successful or unsuccessful female transfers were observed seven times during a 32-month field study of proboscis monkeys (Nasalis larvatus) inhabiting a riverine forest along a tributary of the Kinabatangan River, Sabah, Malaysia. In all cases, the females voluntarily left their own groups and immediately joined with another one. When adult females tried to shift to other groups, adult males called them back to their own groups, but appeared to be indifferent to subadult females. When the adult females returned, the males never attacked the females physically, but instead often emitted herding sounds to them. One subadult female was repelled by a resident adult female. When one adult female transferred into a new one-male group, she left her behind son in an all-male group. The number of females often fluctuated in most study groups, with this fluctuation being more prominent among subadult females than adult females. It is likely that female transfer in proboscis monkeys is not a rare occurrence and that it is especially common among sub-adult females.     

Male replacement and stability of territorial boundary in a group of agile gibbons (Hylobates agilis agilis) in West Sumatra, Indonesia

We report membership change in a group of wild agile gibbons, Hylobates agilis agilis, in West Sumatra, Indonesia. During 6-month observational periods, we focused on a particular unit of individuals known as the B group. We confirmed that the group consisted of five individuals: one adult female, one adult male, one subadult male, one subadult female, and one infant male. During our observations, the resident adult male and the two subadult individuals dispersed or disappeared, and a new adult male took over the group. We examined the effects of the male replacement on the territorial boundary, using the auditory census technique. The boundary was stable. We also documented the succession of the home range. Our results indicate a flexible social structure in this species and contribute some useful data to an ongoing debate on their social dynamics.     

Mate competition and reproductive correlates of female dispersal in a polygynous primate species (Rhinopithecus roxellana)

Different mating systems in group-living animals have characteristic behavioral correlates that are primarily related to mate competition. Mate competition may push individuals to selectively make dispersal decisions for the purpose of maximizing of opportunities for reproduction. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is a polygynous primate species endemic to China. We provide the first data on female dispersal in a free-ranging group of R. roxellana in the Zhouzhi National Nature Reserve, Qinling Mountains, China. Both adult and subadult female dispersal occurred. Immigration/emigration rates of adult females are higher than those of subadult females. Mate competition is one apparent driving force behind adult female dispersal, and inbreeding avoidance is the possible proximate factor influencing subadult female dispersal. Adult female R. roxellana employ various reproductive strategies related to dispersal, which may increase their reproductive success.     

Changes in female reproductive condition following male take-overs in a colony of hamadryas and hybrid baboons

This paper describes and discusses events observed in the Madrid colony of hamadryas and hybrid baboons, when a novel group of 3 adult males, 3 adult females and 1 unweaned infant was introduced to the resident colony comprising 12 adult females, 11 juveniles and 6 unweaned infants. Novel males took over resident adult females in any reproductive condition, and all acyclic females (i.e. lactating, pregnant and immature) exhibited a dramatic enhancement of sexual activity. Lactating females shortened their postpartum amenorrhoea periods and resumed oestrous cycles around day 14 following the introduction of the novel males, without infanticide occurring. Their return to breeding condition was not affected by the age of their current infant or the day they were taken over by the males. A female in an early stage of pregnancy aborted spontaneously and resumed oestrus on day 26. The other pregnant female significantly shortened her gestation time, delivered a viable infant on day 13, and resumed breeding activity 39 days post-partum (on day 52), while suckling her infant. A cycling female adopted and suckled a 74-day-old infant, continued showing oestrous cycles and conceived. Immature females reached menarche significantly earlier than expected and only then joined one of the newly established harem units. It is argued that the observed enhancement of sexual activity was not imposed by the males' aggressive behaviour but rather was a spontaneous female response to male novelty. This single causal factor was potent enough to override the role that nutrition and lactation normally play in the control of the females' reproductive activity. Differences in latency until the appearance of the response were probably due to the different constraints imposed by the female's current reproductive state. It was also hypothesized that when (a) sexual swellings are attractive to males, (b) novel males are especially active in the process of bonding with new females, and (c) males are important sources of coalitionary support, females might by developing sexual swellings compete more successfully against other females and attain a higher position in the female hierarchy of the newly established unit. This would have the ultimate effect of increasing their potential reproductive success. In several cases females did gain socially by coming into oestrus, but attained no immediate reproductive advantage.     

Aspects of Male Competition in <Emphasis Type="Italic">Colobus vellerosus</Emphasis>: Preliminary Data on Male and Female Loud Calling,and Infant Deaths After a Takeover

Male Colobus vellerosus are the main participants in intergroup encounters, and lead incursions in neighboring groups during which they attack infants. Extragroup copulations, all-male groups, and male takeover occur in the species. Here, we provide additional information on behaviors associated with male reproductive competition in Colobus vellerosus. We examined 1 resident male loud calling and participation in intergroup encounters in relation to a takeover. We also report a second case of takeover that led to the death of the former resident male and the death of 2 male infants, presumably as a result of aggression from the all-male group. The new resident male wounded the third infant of the group, which apparently died after its mother abandoned it. During the period characterized by the attacks on the infant and after its disappearance, females initiated and participated in loud call bouts with the new resident male. We examine the possible functions of female loud calling, and suggest that in this context, it might force the resident male to call along to indicate his presence.     

Female resistance to invading males increases infanticide in langurs

Background

Infanticide by adult male occurs in many mammalian species under natural conditions, and it is often assumed to be a goal-directed action and explained predominately by sexual selection. Motivation of this behavior in mammals is limitedly involved.

Methodology and Principal Findings

We used long-term reproductive records and direct observation in captivity and in the field of two snub-nosed langur species on the basis of individual identification to investigate how infanticide happened and to be avoided in nonhuman primates. Our observations suggested that infanticide by invading males might be more accidental than goal-directed. The invading male seemed to monopolize all the females including lactating mothers during takeovers. Multiparous mothers who accepted the invading male shortly after takeovers avoided infanticide in most cases. Our results conjectured primiparous mothers would decrease infanticidal possibility if they sexually accepted the invading male during or immediately after takeovers. In the studied langur species, voluntary abortion or mating with the invading male was evidently adopted by females to limit or avoid infanticide by takeover males.

Conclusions and Significance

The objective of the invading male was to monopolize all adult females after his takeover. It appeared that the mother''s resistance to accepting the new male as a mating partner was the primary incentive for infanticide. Motivation analysis might be helpful to further understand why infanticide occurs in primate species.     

Annual Reproductive Behavior of Rhinopithecus roxellana

Ren conducted year-round observations on sexual behaviors of Sichuan snub-nosed monkeys in Shanghai Wild Animal Park from May 2000 to May 2001, which confirmed quantitatively that the species is a rigorous seasonal breeder with a single birth season between late March and early June. Lactation continues until the infant reaches about 1.5 years or it dies. Accordingly, the interbirth interval is ca. 18–20 mo. The results also confirm that females regulate the timing of reproduction. To avoid mating competition their conception times differ from one another, and they conceive between October and December. Three focal females maintained proceptive activities with significant durations due to their different ages and mating choice. If new babies died in the same year the mothers resumed sexual activity on different days. Apart from female peak mating times there is no significant difference among them regarding the regularity of their sexual activities. Temporal differences in birth peaks at different locations might be due to latitude.     

Infanticide in black capuchin monkeys (Cebus apella nigritus) in Iguazú National Park, Argentina

We report here one observed and two potential cases of infanticide during a brief period of 1 month after a dominant male replacement in one group of black capuchin monkeys in Iguazú National Park, Argentina. We also compile infant disappearances and demographic data in seven groups followed from 1-14 years. Behavioral and molecular data showed that the probability that an infanticidal male would kill his own progeny is very low in this species. Females that lost infants less than 6 months old had shorter interbirth intervals than females whose infants survived (14.12 ± 5.32 months, n=17 vs. 20.42 ± 5.65 months, n=34). Females whose infants die shortly after takeovers mate with the presumed infanticidal male during the most fertile days of their subsequent estrous periods giving this male a high probability of siring the new progeny. We recorded 181 proceptive periods and 52 births from 18 adult females in two groups. Most proceptive periods were concentrated during a conception season, but there was an increase in sexual behavior after male takeovers. Seven females copulated while pregnant after the observed male takeover, an unusual behavior in this species in years of group stability. Of 24 infants born during takeover years, 62.5% did not survive the first year, whereas only 22.5% of 80 infants died in years without male replacements. We found a significant positive association between infant mortality and male takeovers, but not with food provisioning. The main cause of infant mortality in this population is associated with male takeovers. Our results suggest that infanticide can have an important effect on the behavior of this species, selecting for female behaviors that function to reduce infanticide risk.     

Reproductive strategies of the orang-utan: New data and a reconsideration of existing sociosexual models

Recent field data indicate that MacKinnon’s model of the orang-utan’s sexual and agonistic activity needs to be revised. In this model, male reproductive activity is concentrated in an extended phase of subadulthood and in early adulthood. According to this model, the role of older adult males is primarily that of range guardian, and in that role they would ensure that the offspring they had generated earlier would have safe access to food resources. This study presents cases suggesting that subadult males, even though sexually active, may have low reproductive success. In previous studies adult males were shown to display less sexual initiative than subadult males. In this study an adult male was at times involved infrequent mating activity in response to proceptive activity of females in the course of consortship. This adult male proved to be a successful breeder, thus refuting the hypothesis of adult male sterility. The female is most likely to conceive through cooperative mating in lengthy consortships with the dominant resident adult male. We hypothesize that the extended subadult phase represents a submissive strategy, allowing subadult males to remain in the home range of adult males but with minimal reproductive success.