Sexual Behavior of Immature Tibetan Macaques (Macaca thibetana)

Tibetan macaque sociosexual behavior begins in infancy, and comprises much of their initial interactions with other group members as infants. Tibetan macaques possess a large sociosexual behavioral repertoire, including a behavior called bridging, which involves infants and juveniles and is found in only four species. Immature macaques differ in the types, rate, and partner preferences across a variety of behaviors. This study compared rates of sexual behavior among four age and sex classes of 26 immature 12 Tibetan macaques at Mt. Huangshan, China. A total of 643 sexual behaviors were observed and evaluated for each class in five aspects: total sexual behavior rates, initiation rates, rates of different types of sexual behavior, partner preference, and rates within different social contexts. Nine types of sexual behaviors were observed with bridging being the most common (n = 179), and self-genital manipulation being the least common (n = 18). Sexual behavior occurred at the highest rate within spontaneous (2.9 sexual behaviors per hour) and play (2.2 sexual behaviors per hour) social contexts. Generally, younger males exhibited significantly higher rates of sexual behavior relative to other immature classes across all five aspects, and younger females exhibited significantly lower rates of sexual behavior relative to other immature classes across all five aspects. Older females and older males exhibited rates that were variably both higher and lower than other age classes across the five aspects. Introduction The complex social structures and hierarchies of primates require an aspect of social learning that is arguably unmatched in other mammal orders. The effects of age, sex, and rank are clearly influential in the expression and use of sexual behavior especially in species with social dominance hierarchies (Aureli, 1997; Cooper, Aureli, & Singh, 2007; Berman, Ionica, Dorner, & Li, 2006, Thierry, 2011). Non-conceptive sexual behaviors may be used as practice for reproduction, to confuse paternity, and to communicate in many social primates (Pan paniscus, Cebus capucinus, Manson, Perry, & Parish, 1997; Gorilla gorilla, Doran-Sheehy, Fernandez, & Borries, 2009; M. fuscata, Gunst, Leca, & Vasey, 2013). Same-sex mounts and presentations have been commonly 13 documented in many Old World anthropoids including macaques, mandrills, talapoins, mangabeys, red colobus, proboscis monkeys, patas monkeys, langur species and great apes (Dixson, 2012). Sociosexual behaviors are behaviors that are associated with sexual activity but are used socially to mediate fitness-enhancing goals (Lee, 2007). Despite possessing a unique affiliative sexual behavior first described by Ogawa in 1995 called “bridging,” in which two adults touch or lick the genitals of an infant while teeth chattering, few studies exist on the sexual behavior of Tibetan macaques (Jiang, Li, Sheeran, Sun, Xia, & Wang, 2013; Li, Yin & Zhou, 1996; Ogawa, 1995a; Zhao, 1993). Research on sexual behavior in primates including macaques has focused mainly on reproductive tactics of adults. Juvenile and infant behavior has been studied in macaques (M. radiata, Simonds, 1974; M. fuscata, Eaton, Modahl, & Johnson, 1981, Leca, Gunst, & Vasey, 2014, Gunst et al., 2013) but few of these studies examine sexual behavior. Much of what we know about primate sexual development has come from the experimental manipulation of hormones (Goy, 1988), social environment of rhesus macaques (M. mulatta, Harlow, Harlow, Hansen, & Suomi, 1972), and from observational studies of social development (Eaton, Johnson, Glick, & Worlein, 1986) and sexual development (Leca et al., 2014; Gunst et al., 2013) of Japanese macaques (M. fuscata). Even considering the complex social learning required for the acquisition of sexual behavior, few studies exist on the sexual behavior of immature wild macaques. The social learning component of sexual behavior makes the examination of these behaviors in immature individuals particularly interesting and necessary to understanding their functions. Many primates begin their lives learning about social relationships through play (M. fuscata, Gunst, et. al., 2013; Rhinopithecus roxellana, Li, Guo, Ji, He, 14 Wang & Li, 2011). This social context has been extremely important in shaping behaviors, including sexual behaviors, in young Rhesus macaques, as evidence by infants reared without peers their own age, which do not exhibit a full repertoire of social behaviors exhibited by adults raised with peers. (Champoux, Byrne, Delizio, & Suomi, 1992) Additionally, demographic differences have been documented in many non-human primates (P. paniscus, C. capucinus, Manson. et. al., 1997; M. fuscata, Tokuda, 1961; M. radiata, Simonds, 1974). In Japanese macaques, male and female differences in play and partner preference appear in the first and second years of life, respectively (Glick, Eaton, Johnson, & Worlein, 1986). Sex differences in behavior frequencies are apparent in juvenile Vervet monkeys and are not predictive of adult differences (Raleigh, Flannery, & Ervin, 1979). Immature Japanese macaques gradually acquire adult-like behavioral patterns and gradually lose less effective immature behavioral patterns as they age from juveniles to adults, with a major threshold in behavioral changes occurring at the age of 4 years for females (Leca et al., 2014), and the frequency of mounts directed towards adult females increasing around 2 to 3 years of age for males (Gunst et al., 2013). Although Tibetan macaques spend much of their time with their mothers as infants, they are particularly sought-after during the first year of life by other group members for their use in bridging (Ogawa, 1995b, 1995c). There is a significant sex difference between male and female infants in their involvement in bridges. Adults show a strong preference for male infants, using male infants in bridges 0.43 times per hour, while using female infants 0.04 times per hour (Ogawa, 1995a). Male and female infants experience differential treatment by their mothers and other group members. Female infants are groomed and carried more by their mothers than are male infants, while male infants play 15 more often and are cared for by other group members more often than female infants (Deng, 1993; Deng & Zhao 1991). Many developmental differences between male and female primates are attributable to their different life histories within their society (Wallen, Zehr, Herman, & Graves, 2003). In female philopatric species such as the Tibetan macaque (Berman, Ionica, & Li, 2004), immature males and females prepare to assume different roles as adults. Young males prepare for emigration and alliance formation while young females begin to establish themselves in the matriarchal community and to raise infants (Wallen, et. al., 2003). The onsets of physiological aspects that occur during puberty such as sperm viability and first ovulation/menses in Tibetan macaques are not well known, so visible markers of puberty have been used to distinguish developmental stages in the species. Physical development in Tibetan macaques separates sub-adult and young adult males based on canine eruption and wear, body weight, age, and behavior, including ability to ejaculate (Zhao, 1993). Estrus is marked by a slight swelling between the tail and anus in females, but is not reliably detectable (Zhao, 1993). Female Tibetan macaques’ first birth occurs around 5 years of age and has been used to determine the onset age of adulthood (Zhao & Deng, 1988). Methods Subjects and Study Site Immature individuals in a group of free-ranging, habituated Tibetan macaques at a tourist park in the Valley of the Wild Monkeys at Mt. Huangshan, China served as the subjects of this study. Monkeys at the site have been habituated to human presence since its establishment in 1986 and are provisioned dry corn 3-4 times a day by park staff. The 16 immature macaques in the group, designated YA1, served as the subjects of this study, which included 7 adult males, 9 adult females, 14 immature males, and 12 immature females. Video footage was recorded from 830h to 1700hr for forty days between August 7 and September 21, 2014. Preliminary observations were made before collecting data for familiarization with the group’s behaviors, and an intra-observer reliability rate of 1.0 was reached for behavior and individual identification from video footage before coding. For analysis, individuals were separated into four age and sex classes based on rates of copulation and ejaculation, which serve as biological markers of puberty for the species (Zhao, 1993; Zhao & Deng, 1988). Older males were characterized by the ability to copulate with observed ejaculation, distinct from younger males who were not observed to ejaculate; and older females were characterized by the observance of copulation involving intromission, distinct from younger females who were mounted with no intromission.