Reproductive tactics influence cortisol levels in individual male gray-cheeked mangabeys (Lophocebus albigena)

Concentration of the hormone cortisol is often used as an indicator of stress, and chronically high cortisol levels are often associated with poor health. Among group living animals that compete for resources, agonistic social interactions can be expected to contribute to variation in cortisol levels within and among individuals over time. Reproductive tactics of males can change with individual quality, relatedness, and social structure, and affect cortisol levels. In gray-cheeked mangabey (Lophocebus albigena) groups, male rank is an important factor in social interactions, and males also move between groups while actively competing for females or sneaking copulations. During a 20-month study we observed the social behavior and collected 461 fecal samples from 24 adult male gray-cheeked mangabeys from five groups in Kibale National Park, Uganda. Aggressive interactions and the presence of females at the peak of sexual swelling were associated with elevated cortisol concentrations in all males. Independently, dominant (i.e., highest-ranking) males within groups had higher cortisol concentrations than subordinate males, and immigrant males had higher cortisol concentrations than dominant males.     

云南拉沙山黑白仰鼻猴交配行为和出生季节

灵长类的交配模式对于了解和掌握雄性的交配策略和社群的稳定机制非常重要,但是目前有关亚洲灵长类交配模式的数据较少;因此,该研究于2011年1—12月,分别采用全事件取样法和焦点动物瞬时扫描取样法收集了拉沙山黑白仰鼻猴群的交配行为和出生数据。猴群全年交配,有2个峰期,一个是繁殖交配高峰期(8一10月);另一个在出生季节,但其非繁殖交配的生物学意义尚不清楚。雌性通过俯卧/注视雄性或跳落邀配。爬跨射精比为8.8,射精交配稀少(11.4%),这说明雄性并非每次交配都射精,因而支持黑白仰鼻猴交配模式的主体为多次爬跨射精或处于从单次爬跨射精到多次爬跨射精连续谱上段的观点。雄性邀配的射精爬跨多于雌性,说明多次爬跨射精不仅是雄性的一个交配策略,而且可以决定交配模式在连续谱的位置。交配时间后延6~7个月,交配频次与婴猴出生率相关。拉沙山猴群出生模式为严格的季节性,这进一步证实了前人的观点。婴猴出生具有一定的同步性,且不同猴群婴猴出生的同步模式不同。     

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.     

Fighting and Mating Between Groups in a Cooperatively Breeding Mammal, the Banded Mongoose

Many cooperatively breeding animals actively defend a territory containing resources such as food and shelter, which are essential for reproduction. Some observations, however, indicate that conflicts between groups are often triggered by the attempts of males or females, or both, to gain extra‐group copulations. We studied interactions between 12 groups of banded mongooses (Mungos mungo) in Uganda to test whether the frequency of inter‐group encounters was linked to the reproductive status of females, and conducted an experiment to examine the responses of individuals to mongooses from other groups. The rate at which focal groups fought with other groups was higher when its females were in estrous, suggesting that many fights take place over access to mates. Both males and estrous females were instrumental in instigating encounters with rival groups, and extra‐group copulation in the midst of a fight was observed on three occasions. We experimentally simulated encounters with foreign individuals by presenting each of six groups with cages containing a male and a female from a rival group. Subordinate males were the first to investigate these ‘intruders’, spent more time around the intruders' cages, and were more aggressive to the intruders than either dominant males or females. Subordinate males directed more attention and aggression towards the male intruder than the female intruder. We suggest that male banded mongooses actively seek extra‐group copulations in pursuit of paternity, while females may actively seek extra‐group copulations as a way of reducing inbreeding depression.     

Patas monkey copulations: One mount,repeat if necessary

Early, anecdotal reports of patas monkey (Erythrocebus patas) sexual behavior suggested that these primates were series-mount copulators. In 1975, limited evidence was presented in favor of single-mount copulations as the species-typical pattern for patas. The situation remained confused, however, as indicated by statements in a recent review article. This paper adds to our knowledge of patas sexuality by presenting quantitative data on the copulatory behavior of two additional adult males. Both males usually gave pelvic thrusts to intravaginal ejaculation once they had mounted a female and gained intromission. Mounts without ejaculation were clearly failed attempts at copulation, rather than segments of a stereotyped series-mount pattern. All of the available quantitative data indicate that the species-typical mating pattern for patas monkeys is copulation in a single mount.     

Signals of female reproductive quality and fertility in colony‐living baboons (Papio h. anubis) in relation to ensuring paternal investment

The fitness of a female's offspring depends cruicially on the traits, genetic and paternal, that the father contributes. As such, females may either have an interest in behaviorally choosing the highest‐quality male, or in reliably signaling their fertility status to males. Combining hormonal data on a female's ovulatory fertile window with a behavioral context, we suggest that captive female olive baboons (Papio h. anubis) provide fathers with reliable signals of their fertile period. One signal, the maximum anogenital swelling (AGA), typically coincided with a 4‐day fertile window of ovulation, which occurred 2–3 days prior to deturgescence. As expected from previous studies, AGA swelling indicated general attractiveness to males, and males attended to the relative attractiveness of females. Males approached and copulated with females significantly more often during the 4‐day window around ovulation, irrespective of the absolute swelling stage. The two adult males present in the group were both able to copulate with consistent partners as at least two cycling females were available in most months; the dominant male was more selective about the timing of his copulations close to ovulation during the maximal swelling phase. Females with ovulatory but nonconceptive cycles were less attractive to males, especially during their maximal AGA swelling phase. Am. J. Primatol. 71:529–538, 2009. © 2009 Wiley‐Liss, Inc.     

Sexual Behaviour of Sumatran Long-tailed Macaques (Macaca fascicularis)

The sexual behaviour of wild long-tailed macaques (Macaca fascicularis) was studied in the Gunung Leuser National Park, Sumatra, Indonesia. All females showed some swelling of the sexual skin, but the frequency and maximum size of the swelling decreased with age. The frequency of copulations and consortships for a given female increased with increasing degree of swelling or coloration. No regular cycles could be found in the occurrence of swellings, copulations and consortships. Periods for which a female had consortships tended to be long (up to 5–6 weeks on end). These two results suggest that in the wild the predictability of the moment of ovulation is very low. The consortships were not exclusive: both the male and the female occasionally copulated with others. All females had many different male partners and, as ovulation signalling was not clear, none of these males could have any certainty about paternity of a female's offspring. Yet, the highest-ranking males probably had the best chances to father children because they were more often involved in sexual interaction (both copulations and consortships), especially around the estimated date of conception. This does not hold for the nulliparous females who were virtually ignored by the higher-ranking males. Consortships were occasionally actively maintained by the female, for whom a direct advantage of consorting might be an increased safety against conspecifics and predators. One advantage of mating with many different males might be a reduced risk of infanticide.     

Male dominance rank and reproductive success in an enclosed group of Japanese macaques: with special reference to post-conception mating

The mating behaviour and reproductive success of male Japanese macaques (Macaca fuscata) were studied in relation to the female sexual cycles, which were monitored from the plasma profiles of gonadotropins and ovarian hormones. Based on observations of the mating behaviour during four successive mating seasons and paternity identification by DNA fingerprinting in 35 out of 37 offspring born in the subsequent birth seasons, the correlations between (1) male dominance rank and timing of mating, and (2) male dominance rank and reproductive success were examined. The results may be summarized as follows. (1) The number of copulations with ejaculation by any male was positively correlated with the male dominance rank, but not with the identified numbers of offspring fathered by each male. (2) Males could not choose ovulatory females as mating partners: the number of copulations with ejaculation with females during ovulatory weeks was not related to the male's rank. Monopolized copulations in consortship were mostly observed between high-ranking males and non-lactating parous females after conception. (3) Paternity testing showed that the male copulating most frequently with a female was not the identified father in 11 out of 15 cases. Prediction of the fathers of offspring was difficult even from the number of copulations occurring at around the estimated time of ovulation. An adaptive explanation of these correlations is discussed.     

Mating behaviors of the proboscis monkey (Nasalis larvatus)

The mating behaviors of the proboscis monkey were observed in a riverine forest along a tributary of the Kinabatangan River, Sabah, Malaysia, for a period of 30 months. Solicitation for copulation was initiated frequently by males and occasionally by females. Most copulations involved only one mount; however, some multiple-mount copulations were observed and a maximum of six mounts per copulation were recorded. The mean duration of mounts was about 27 sec. Nonsexual mounts (female-female, female-juvenile/infant, juvenile-juvenile, and juvenile-infant) were also observed. Female-female mounts occurred shortly after failed solicitations toward males were observed. Harassment by juveniles and/or infants was observed during copulation; however, these harassments apparently did not interfere with copulation. Sexual swelling was evident in 77.4% of copulating females, with copulating subadult females showing the most distinct swelling.     

Application of paternity discrimination by DNA polymorphism to the analysis of the social behavior of primates

Paternity in many primate species cannot be established reliably on behavioral grounds. For instance, Japanese macaques (Macaca fuscata) have a multi-male group structure and promiscuous mating patterns. On the other hand, accurate evaluation of male reproductive success is needed to analyze primate behavior. DNA finger-printing techniques were applied to 2 captive groups of Japanese macaques in the Primate Research Institute of Kyoto University for identification of paternity. Also, mating behavior of a captive group was observed in order to compare the reproductive success of each male with that expected on the basis of his observed mating activity. The number of offspring of full adult males was not related to their social rank although the number of copulations with ejaculation was highly correlated with their social rank. Monitoring of the female sexual cycles from the plasma profiles of gonadotropins and ovarian hormones suggested that males could not choose females at days of ovulation. The results of two-free-ranging wild troops, like those of the captive groups, indicated that high-ranking males could not monopolize the paternity of offspring. The results of paternity discrimination in Japanese macaques were compared with results from patas monkeys (Erythrocebus patas) in a discussion of social structure and male reproductive success. Some aspects of polymorphism detection techniques are also discussed.     

Sexual behavior of wild Barbary macaque males (Macaca sylvanus)

Recent assertions that the Barbary macaque (Macaca sylvanus) is a multiple-or serial-mounting species are incorrect. Data are presented from over 300 copulations observed among wild Moroccan Barbary macaques which establish empirically that males of this macaque species are single mounters. The average length of an ejaculatory copulation was 8.7 sec, with a range of 6 to 14 sec. Ejaculation occurred an average of 6.3 sec after mounting, with an average of nine pelvic thrusts per ejaculation. Males appeared capable of ejaculating twice within 16 min, and three consecutive times within 37 min. Characteristically, only one mount and ejaculation occurred during a sexual association between an estrous female and each of her consorting males. Schemes of macaque evolution which incorrectly classify Barbary macaques as a multiple-mounting species should be viewed cautiously.     

Do Dispersing Monkeys Follow Kin? Evidence from Gray-cheeked Mangabeys (<Emphasis Type="Italic">Lophocebus albigena</Emphasis>)

Among social vertebrates, immigrants may incur a substantial fitness cost when they attempt to join a new group. Dispersers could reduce that cost, or increase their probability of mating via coalition formation, by immigrating into groups containing first- or second-degree relatives. We here examine whether dispersing males tend to move into groups containing fathers or brothers in gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda. We sampled blood from 21 subadult and adult male mangabeys in 7 social groups and genotyped them at 17 microsatellite loci. Twelve genotyped males dispersed to groups containing other genotyped adult males during the study; in only 1 case did the group contain a probable male relative. Contrary to the prediction that dispersing males would follow kin, relatively few adult male dyads were likely first- or second-degree relatives; opportunities for kin-biased dispersal by mangabeys appear to be rare. During 4 yr of observation, adult brothers shared a group only once, and for only 6 wk. Mean relatedness among adult males sharing a group was lower than that among males in different groups. Randomization tests indicate that closely related males share groups no more often than expected by chance, although these tests had limited power. We suggest that the demographic conditions that allow kin-biased dispersal to evolve do not occur in mangabeys, may be unusual among primates, and are worth further attention.     

Alpha-male sooty mangabeys differentiate between females’ fertile and their postconception maximal swellings

Alpha-male sooty mangabeys in four separate social groups discriminated between a female’s fertile and her postconception maximal swelling, confirming a previous finding that one alpha male, but not other males in the group, refrained from mounting females during the postconception maximum swelling. During a 3-hr observation session, the males mounted females an average of 2.2 ± 0.3 times during the females’ fertile maximal swelling, while there were no mounts by alpha males during the females’ postconception maximal swelling. Alpha males also showed higher durations of following and frequencies of genital inspection toward females during the fertile maximal swelling. Additionally, we collected blood samples from four females three times per week to monitor estradiol (E ₂), progesterone (P₄), and luteinizing hormone (LH) changes during both swelling phases. Peak E₂ concentrations preceded the maximal swelling during both the conception and the post-conception swelling, though to a greater extent during the latter period. Although 3×-weekly blood samples showed significantly greater E₂ concentrations during the postconception swelling, daily samples to confirm the results revealed one instance of comparable concentrations of E₂ during a fertile swelling. Thus, peak E₂ concentrations may not differ during the conception and postconception swelling cycles, though the duration of the E₂ elevation is longer during the postconception swelling. LH concentrations, corresponding to the conception and postconception maximal swelling, were significantly different, while P₄ concentrations were not. The behavioral results indicate that alpha males discriminate between a fertile swelling (associated with ovulation) and a nonfertile swelling (occurring approximately 49 days postconception); however, whether this discrimination is tied to the difference in the hormonal pattern has yet to be demonstrated.     

Movement and reproductive behavior of solitary male redtail guenons (Cercopithecus ascanius)

Adult male redtail guenons (Cercopithecus ascanius) live as resident males in heterosexual groups or as nonresident males outside groups. Data are reported here on movement and temporary intrusions by nonresident males in heterosexual groups. These data further elucidate the reproductive strategies of this class of individual. Observations of three radiocollared males provided data on the details of their movement relative to groups. Regular sampling of three heterosexual groups provided data on patterns of nonresident males' intrusions. During peak mating months, nonresident males formed loose affiliations with groups. The males affiliated with one group at a time, with each affiliation lasting several weeks. Nonresident male intrusions in groups were unevenly distributed and were not correlated with the number of potentially fertile females in each group. Estimates of male density indicate that there were about two nonresident males per group, which suggests an adult sex ratio of three females per male within the study area. Nonresident male redtail guenons apparently do not spread their reproductive efforts over several groups at once, but instead each male tends to direct his attention toward the group offering the best opportunity for reproductive payoffs. Factors that determine which groups they attempt to infiltrate may include the characteristics of resident males, female choice, or both, but the number of fertile females probably has no effect. The male low density and female-biased sex ratio among adults should facilitate resident males' attempts to monopolize fertilizations in groups; however, resident males were unable to prevent copulations by nonresident males even when only one nonresident was intruding in a group.     

短尾猴和日本猴雄性性行为的比较研究

本文比较研究了短尾猴和日本猴的雄性性行为。短尾猴属单次爬跨射精型种类,每次交配平均持续23.2秒,日本猴属多次爬跨射精型种类,每次交配平均持续8.2分,交配期间雄性平均爬跨雌性lO.6次才能达到射精。短尾猴第1顺位雄性是群中的主要交配者,它占有交配总数的70.9 %;而日本猴第5顺位以下的雄性占交配总数的64%。交配中,两种猴雄性间相互打搅行为的发生频率大致相当。短尾猴高顺位雄性的打搅行为能使低顺位雄性的交配中断,但日本猴高顺位的打搅行为只能使低顺位雄性交配的54.3%中断。     

Comparison of behavioral sequence of copulation between chimpanzees and bonobos

We compared sex differences in behaviors leading to copulation of chimpanzees (Pan troglodytes) in the Kalinzu Forest, Uganda with those of bonobos (Pan paniscus) at Wamba, D.R. Congo, using the same definition. Female chimpanzees were more likely to initiate copulation than female bonobos. While most of copulations (96%) were initiated by males in bonobos, among chimpanzees only 63% of copulations were initiated by males. Female bonobos initiated an interaction leading to copulation when males approached them within a short distance. On the other hand, both male and female chimpanzees initiated behavior at a longer distance. Higher proceptivity and a higher copulation rate during the maximal swelling period of female chimpanzees might suggest that they gain greater benefits from a high frequency of copulations than do female bonobos.     

Influence of Female Copulation Calls on Male Sexual Behavior in Captive Macaca fascicularis

We investigated the function of copulation calls—vocalizations by females during mating—in captive groups of long-tailed macaques. We tested predictions of the contest-competition, sperm competition, synchronized orgasms, mate again, alpha-male notification and graded-signal hypotheses. We observed 371 copulations of 36 females wherein the presence or absence of a copulation call was clear. Females call equally often with different males and shortly after ejaculation. Copulation calls occurred equally with copulations with and without ejaculation. Calls did not incite disruptions of the mating. Following calls females mated again, more often than expected, with their mating partner. Both pregnant and fertile females uttered copulation calls. Two females conceived and mated mainly with the alpha male then. We conclude that copulation calls do not incite male contest competition for sexual access to females and that it is unlikely that calls synchronize male and female orgasms. Several hypotheses remain plausible, but not all predictions are borne out unequivocably. This alerts us to the possibility that the calls could have multiple beneficial effects; natural selection might strike a compromise among functions. Investigation of the mate again, sperm competition and alpha-male notification hypotheses, and of hypotheses not tested in our study concerning female breeding overlap and female-female agonism, is required.     

Male mating strategies and reproductive constraints in a group of wild tufted capuchin monkeys (Cebus apella nigritus)

Tufted capuchin monkeys (Cebus apella) provide an extreme example of active female sexual solicitation of males. In spite of being targeted by females for sex, males may delay copulation for hours or days. Data were collected on the sexual interactions in one wild capuchin group at the Estação Biológica de Caratinga in Brazil from September 1996 to August 1997. All successful conceptions during this year occurred in the dry season, yet sexual behavior was observed during 9 months of the year. This study tested whether male sexual response to female proceptivity was seasonally‐mediated. Male consortship participation, solicitation of females, latency to copulation, and copulation frequency were compared between fertile and nonconceptive females. Seasonal patterns in copulation interference, mating style, and alternative mating strategies were also examined. Thirty‐two copulations were observed. The alpha male was solicited for significantly more consortship days per female, but his mating success, in terms of copulation frequency, did not differ from that of two other adult males in the group. In the dry season, when the females were fertile, the males showed increased contest competition for mates, a higher frequency of alternative mating strategies against copulation interference, and increased monitoring of the females' condition. However, contrary to expectations, the alpha male's latency to copulation was significantly longer in the fertile season than in the nonconceptive months, and no males were observed to mate more than one time per day, even at the conceptive peak. Male mating strategies were affected by both season and rank, and there was evidence for reproductive constraints on males throughout the year. Limited male ejaculatory capacity and male choice in the timing of copulations within female proceptive phases may both be important factors in driving the sexual dynamics of this species. Am. J. Primatol. 67:313–328, 2005. © 2005 Wiley‐Liss, Inc.     

Effect of Mating Activity and Dominance Rank on Male Masturbation Among Free‐Ranging Male Rhesus Macaques

The adaptive function of male masturbation is still poorly understood, despite its high prevalence in humans and other animals. In non‐human primates, male masturbation is most frequent among anthropoid monkeys and apes living in multimale–multifemale groups with a promiscuous mating system. In these species, male masturbation may be a non‐functional by‐product of high sexual arousal or be adaptive by providing advantages in terms of sperm competition or by decreasing the risk of sexually transmitted infections. We investigated the possible functional significance of male masturbation using behavioral data collected on 21 free‐ranging male rhesus macaques (Macaca mulatta) at the peak of the mating season. We found some evidence that masturbation is linked to low mating opportunities: regardless of rank, males were most likely to be observed masturbating on days in which they were not observed mating, and lower‐ranking males mated less and tended to masturbate more frequently than higher‐ranking males. These results echo the findings obtained for two other species of macaques, but contrast those obtained in red colobus monkeys (Procolobus badius) and Cape ground squirrels (Xerus inauris). Interestingly, however, male masturbation events ended with ejaculation in only 15% of the observed masturbation time, suggesting that new hypotheses are needed to explain masturbation in this species. More studies are needed to establish whether male masturbation is adaptive and whether it serves similar or different functions in different sexually promiscuous species.     

Testing multiple hypotheses for the maintenance of male homosexual copulatory behaviour in flour beetles

Diverse animal groups exhibit homosexual interactions, yet the evolutionary maintenance of such behaviours remains enigmatic as they do not directly increase reproductive success by generating progeny. Here, we use Tribolium castaneum flour beetles, which exhibit frequent male homosexual copulations, to empirically test several hypotheses for the maintenance of such behaviours: (1) establishing social dominance; (2) practice for future heterosexual encounters; and (3) indirect sperm translocation. We found no evidence that Tribolium males use homosexual copulations either to establish dominance or to practice behaviours that increase their subsequent heterosexual reproductive performance. Our results provide limited support for the hypothesis of indirect sperm translocation: when males from two genetic strains mated with females immediately following a homosexual copulation, females produced progeny sired not only by the directly mating male, but also by that male’s homosexual partner. However, this phenomenon was detected in only 7% of homosexual pairs, and in each case such indirectly sired progeny accounted for < 0.5% of females’ total progeny. Direct observations indicated that mounting males often released spermatophores during homosexual copulations. These observations suggest that homosexual copulations may be a behavioural mechanism that allows males to expel older, potentially low‐quality sperm. Additional work is needed to test this new hypothesis, and to determine whether sperm release during homosexual copulations occurs in other groups.