Behavioral and cardiophysiological responses of common marmosets (Callithrix jacchus) to social and environmental changes

Under captive conditions common marmosets (Callithrix jacchus) show socially monogamous propensities. Male and female form a social bond as characterized by signs of behavioral arousal during separation of the pairmates, high levels of affiliative interactions between pairmates and agonistic responses towards strange conspecifics. In the present study behavioral and cardiophysiological responses of mated individuals of common marmosets were recorded while the animals were in an unfamiliar environment (1) alone, (2) with the pairmate, or (3) with an opposite-sexed stranger. Pairmates of 6 established pairs were tested in 3 replicates yielding a total of 36 trials per experiment. A trial was divided into three 10-min segments (baseline; unfamiliar environment; reunion). Behavioral responses were videotaped with a remote controlled camera system installed within the cage. Systolic (SBP) and diastolic blood pressure (DBP), and heart rate (HR) as well as locomotor activity (ACT) were recorded telemtrically through peritoneally implanted transmitters. The individuals’ responses measured while in an unfamiliar environment was only reduced by the pairmate, but not by an opposite-sexed stranger. No affiliative behaviors occurred between strange conspecifics, whereas aggressive and sexual behaviors were observed. During reunion with the pairmate individuals recovered physiologically. The present study shows that an individualized pair bond exists between pairmates of common marmosets. Further, it becomes evident that establishing a social bond with the pairmate is important for maintaining physiological homeostasis.     

The pairbond in the titi monkey (Callicebus moloch): intrinsic versus extrinsic contributions of the pairmates

Aspects of a monogamous relationship can be inferred by observing reactions of mated individuals to unfamiliar conspecifics. The present study examined the behaviours shown by male and female titi monkeys (Callicebus moloch) toward an opposite-sex stranger, and the effect of their pairmate's absence or presence on these encounters. Behaviours within unfamiliar heterosexual pairs showed superficial similarities to behaviours of mated pairs. Although there were few affiliative behaviours between unfamiliar individuals, animals were often in spatial proximity and even performed sexual behaviour. The visual presence of a pairmate clearly affected encounters between unfamiliar heterosexual pairs in several respects. The presence of a male pairmate had a much stronger influence on all behavioural measures compared to the presence of a female pairmate. Possible functional aspects of these results are discussed.     

Sociality in Callithrix penicillata: II. Individual Strategies During Intergroup Encounters

In social animals, intergroup interactions, whether through agonistic and competitive behaviors or affiliative ones, can influence important parameters such as home range, territory sizes, and access to resources, which may directly affect both female and male fitness. We studied the intergroup interaction patterns of a wild group of black-tufted-ear marmosets (Callithrix penicillata) in central Brazil. Agonistic interactions occurred at low frequencies during intergroup encounters. The marmosets directed agonistic interactions without physical aggression primarily against same-sex individuals, suggesting that male and female aggression patterns are shaped by their sexual interests. However, females of the focal group also directed agonistic behavior toward extragroup males that attempted copulation. The marmosets appeared to use intergroup encounters to gather information about possible partners and extragroup reproductive opportunities. Intergroup sexual interactions occurred mainly in the form of copulations or attempted copulations by all adults, with the exception of the dominant female. Our results suggest that a possible reproductive strategy used by males is to attempt fertilization of extragroup females. Adult males copulated with the same extragroup female during several opportunities, which suggests sperm competition or the establishment of social bonds with neighboring females.     

Close Proximity of the Heterosexual Partner Reduces the Physiological and Behavioral Consequences of Novel-Cage Housing in Black Tufted-Ear Marmosets (Callithrix kuhli)

The present studies assessed the extent to which heterosexual pairmates could buffer marmosets (Wied's black tufted-ear marmoset,Callithrix kuhli)against stress. Six male and six female marmosets from established groups were exposed to two experimental manipulations together with a control condition. Each condition lasted a total of 4 days. For the two experimental conditions, animals were removed from the family group and housed in a novel cage for 48 h in either the presence or the absence of the heterosexual pairmate. During the 48-h novel-cage housing period and for 48 h upon reunion of the subjects with the family group, concentrations of urinary cortisol were measured in the first void sample of the day and behavioral observations were conducted. When animals were housed alone in a novel cage they exhibited significant elevations in levels of urinary cortisol after 24 and 48 h of novel-cage exposure. In contrast, when marmosets were housed in the novel cage in the presence of the pairmate, levels of urinary cortisol did not change across the 4-day period. The presence of the social partner also reduced the behavioral manifestations of exposure to novelty. Upon reunion with the family group, animals that had been housed in the novel cage alone spent significantly more time in close proximity to the pairmate than animals that had been housed with the partner. A second experiment was conducted to determine the effect that separation from the pairmate, only (independent of any effects of novelty), had on levels of cortisol. Concentrations of urinary cortisol were measured in subjects housed in the familiar home cage, but in the absence of the pairmate, over a 48-h period and compared to concentrations of excreted cortisol immediately prior to separation. Separation from the pairmate did not elevate cortisol levels when the subject was housed in the home cage, suggesting that elevated cortisol levels in animals housed alone in the novel cage were in response to novelty exposure rather than to separation from the pairmate. Since the physical presence of the heterosexual partner reduced the physiological and behavioral effects of novel-cage housing, social attachments might function as homeostatic regulators of HPA function in marmosets.     

Neuroendocrine response to female ovulatory odors depends upon social condition in male common marmosets, Callithrix jacchus

Male mammals show rapid behavioral and hormonal responses to signals from sexually receptive females. However, rapid endocrine responses to female signals have not been observed in a nonhuman primate. Here, we tested the behavioral and hormonal response of male common marmosets (Callithrix jacchus) to isolated scent secretions from ovulatory females or to vehicle control scent. Fifteen males were tested in their home cage for behavioral and hormonal responses. These males showed increased investigative and arousal behaviors to the ovulatory scent compared to the vehicle scent. Time sniffing the scent substrate and the duration of erections were significantly elevated in relation to the vehicle scent. Thirty minutes after presentation of ovulatory scent, males showed a significant increase in testosterone compared to the vehicle, but there was no difference in cortisol values. To better control for scent presentation, 15 additional males were tested under a controlled scent exposure. Current social housing condition influenced the male's testosterone response to the ovulatory scent. Single and paired males showed significant increases in testosterone levels with the ovulatory scent but did not increase cortisol levels. Single males also showed the highest change in testosterone with the ovulatory scent, but fathers showed no changes. These results indicate that a rapid hormonal response to sexually arousing cues occurs in marmosets, and the data suggest that a male's social condition influences how he responds to sexually relevant cues.     

Olfactory preferences, scent marking, and "proceptivity" in female hamsters

Two appetitive sexual behaviors of female hamsters, attraction to odors of males and vaginal scent marking, were investigated and the correlations of each to reproductive states were determined. Both estrous and diestrous females were more attracted to the odors of intact males than to the odors of females or castrated males; this differential attraction was more pronounced for estrous females. Lactating females, but not pregnant females, were also preferentially attracted to odors of intact males. Thus, odors alone provided sufficient information to allow sexual discrimination by females, and estrous, diestrous, and lactating females were preferentially attracted to odors of intact males whereas pregnant females were not. Reproductive condition had no influence on responses to odors of castrated males or diestrous females. Vaginal scent marking was strongly influenced by reproductive state: Marking frequency was low in estrous, pregnant, and early lactation females, but high in late lactation and diestrous females, suggesting a function of advertisement of approaching receptivity. Thus sexual preferences based on olfactory cues and vaginal scent-marking frequency differed in their relationships to reproductive conditions. It is suggested that in other species such relationships between appetitive sexual behaviors and reproductive condition will depend on the species social organization, ecological niche, and taxonomic group, and consequently that the concept of preceptive behaviors should be broadened to include all appetitive sexual behaviors of females, not just those that are correlated with the hormonal state characterizing estrus.     

Relationship between social interactions and sexual maturation in female Saguinus oedipus oedipus

4 female Saguinus oedipus oedipus were paired with strange, unrelated males while 5 remained in their natal family groups. A comparison of the frequency of selected social interactions involving these females when sexually immature versus mature was made. The frequency of sexual and affiliative interactions in male-female pairs was basically unchanged by the female's maturation. Mother-daughter interactions were also not changed in a consistent fashion by the daughters' maturation. Females with strange, unrelated males, either alone or as part of their natal group, displayed increases in marking behavior in association with sexual maturation.     

Body Weight of Wild and Captive Common Marmosets (Callithrix jacchus)

Captive studies and occasional trappings of wild individuals indicate that callitrichids have small size and body weight and lack sexual dimorphism. We compared body weights of captive and wild Callithrix jacchus obtained by repeatedly weighing subjects from two populations in Brazil. We obtained captive data by routinely weighing 138 individuals from the Universidade Federal do Rio Grande do Norte colony and wild data via regular trapping of 243 individuals in 15 free-ranging groups from IBAMA's field site in Nísia Floresta. We assigned all subjects to one of four age classes—infant, juvenile, subadult, and adult—according to their birth dates or size, reproductive status, and dental development. There is no significant difference between males and females in any of the four age classes, but captive subjects were heavier than wild ones in all age classes but infant. Reproductive and nonreproductive adult females showed no statistical difference in weight. These results accord with previous reports of lack of body size sexual dimorphism in common marmosets and suggest that differences between wild and captive common marmosets are not constitutional, but are instead a consequence of diet and physical activity. The absence of weight difference between reproductive and nonreproductive females suggests that any possible advantage from high rank is outweighed by the costs of reproduction in common marmosets.     

Is Self‐Grooming by Male Prairie Voles a Predictor of Mate Choice?

Self-grooming by mammals is a form of scent dissemination in which individuals anoint themselves with salivary, anogenital, and other body odours. Self-grooming has been proposed to be a sexually selected trait favoured in reproductive competition and sexual attraction. We tested the hypothesis that females would show a mating preference for males that self-groomed more than a reproductive competitor that groomed less. In mate-choice experiments in which females had a choice of two tethered males, non pair-bonded females did not choose males based on their frequency of self-grooming. In a second experiment in which pair-bonded females in postpartum oestrus had access to their current mate and two strange males, strange males groomed significantly more than pair-bonded mates, yet attained the fewest copulations. Non pair-bonded females and pair-bonded males and females groomed significantly less often than did non pair-bonded males. Self-grooming behaviour was consistent with the sexual attraction hypothesis, but the frequency of self-grooming did not increase a male's mating success. We conclude that the frequency and time spent self grooming are not good predictors of mating success.     

Sex-specific effects of dietary fatty acids on saliva cortisol and social behavior in guinea pigs under different social environmental conditions

Background

Unbalanced dietary intakes of saturated (SFAs) and polyunsaturated (PUFAs) fatty acids can profoundly influence the hypothalamic-pituitary-adrenal (HPA)-axis and glucocorticoid secretions in relation to behavioral performances. The beneficial effects of higher dietary PUFA intakes and PUFA:SFA ratios may also affect social interactions and social-living per se, where adequate physiological and behavioral responses are essential to cope with unstable social environmental conditions.

Methods

Effects of diets high in PUFAs or SFAs and a control diet were investigated in male and female guinea pigs after 60 days of supplementation. Plasma fatty acid patterns served as an indicator of the general fatty acid status. HPA-axis activities, determined by measuring saliva cortisol concentrations, social behaviors, and hierarchy ranks were analyzed during group housing of established single-sexed groups and during challenging social confrontations with unfamiliar individuals of the other groups.

Results

The plasma PUFA:SFA ratio was highest in PUFA supplemented animals, with female levels significantly exceeding males, and lowest in SFA animals. SFA males and females showed increased saliva cortisol levels and decreased aggressiveness during group housing, while sociopositive behaviors were lowest in PUFA males. Males generally showed higher cortisol increases in response to the challenging social confrontations with unfamiliar individuals than females. While increasing cortisol concentrations were detected in control and PUFA animals, no such effect was found in SFA animals. During social confrontations, PUFA males showed higher levels of agonistic and sociopositive behaviors and also gained higher dominance ranks among males, which was not detected for females.

Conclusions

While SFAs seemingly impaired cortisol responses and social behaviors, PUFAs enabled adequate behavioral responses in male individuals under stressful new social environmental conditions. This sex-specific effect was possibly related to a general sex difference in the n-3 PUFA bioavailability and cortisol responses, which may indicate that males are more susceptible to changing environmental conditions, and shows how dietary fatty acids can shape social systems.

     

Electroantennogram responses of the potato tuber moth, <Emphasis Type="Italic">Phthorimaea operculella</Emphasis> (Lepidoptera; Gelichiidae) to plant volatiles

Electroantennograms (EAGs)were recorded from males and females of the potato tuber moth,Phthorimaea operculella in response to a broad range of plant volatile compounds belonging to diverse chemical classes.The responses to 27 compounds were evaluated,which indicated significant differences in EAGs between chemicals as well as between sexes.The fatty acid derivatives comprising essentially green leaf volatile components elicited significantly greater responses in females.The response profile of males was,in general,lower than that of females.EAG responses to the oxygenated and hydrocarbon monoterpenes were lower in both males and females.Dose -response studies indicate differences in response between the sexes and concentrations,suggesting the existence of sexual dimorphism. Compounds belonging to the fatty acid derivatives class appear to be important for an oligophagous pest such as the potato tuber moth and the findings are discussed in relation to host plant selection in this species.     

Mate choice and sexual conflict in <Emphasis Type="Italic">Brachionus plicatilis</Emphasis> (Rotifera)

Male mate choice in Brachionus plicatilis is based on information from coronal receptors and contact chemoreception of a glycoprotein signal on the body surface of females. Male mating behavior is modulated by mating signal quality and strength, which determines male mating persistence and circling intensity. We probe the sensory abilities of males by better resolving their discrimination of female age. Males preferentially initiate mating with young females, but not too young. Males circle 0.2 h old females just hatched from resting eggs only about 1/2 as frequently as 12 h old females. Males are even more discriminating of females with whom they copulate, preferring 3 h old females significantly more than 0.2 h or 6 h old females. In contrast, males cannot distinguish between virgin females and those who have already copulated. Similarly, males circled and copulated with females hatching from resting eggs with equal frequency as those hatching from amictic eggs. The counterpoint to male mate choice is female resistance to mating. When males contact females, the females respond with one of four behaviors: no response, acceleration, foot flipping, or coronal retraction. In 65% of male–female encounters, there was no initial response by females. However, when males began circling females, females accelerated 11.1 times more often than when males were absent. The second type of evasive female behavior was foot-flipping, which tends to knock off males attempting to circle the female. In the presence of circling males, females performed foot-flipping behavior three times more often than in the absence of males. Coronal retraction, where they stop swimming and withdraw their corona, was observed less frequently than acceleration or foot-flipping, and there was no difference in the presence or absence of males. These data are interpreted in the context of sexual conflict, where the behaviors that optimize male and female fitness differ. Guest editors: S. S. S. Sarma, R. D. Gulati, R. L. Wallace, S. Nandini, H. J. Dumont & R. Rico-Martínez Advances in Rotifer Research     

Response to novelty inSaimiri andCallicebus: Influence of social context

Responses to novel objects by pair-livingSaimiri andCallicebus and grouplivingSaimiri were investigated in two experiments. In the first, titis and squirrel monkeys were tested in the presence and absence of an opposite-sexed pairmate. The species were differentially affected by the absence of the pairmate: titis of both sexes were distressed and object interest was attenuated; squirrel monkeys were not distressed and object scores (particularly females') increased. Nonsocial differences in object exploration principally involved the tempo and mode of investigation; squirrel monkeys were quicker and more vigorous than titis. In the second experiment, presence of a novel object was found to attract and arouse grouplivingSaimiri, as indicated by the change in the frequency and nature of social interactions and spatial distribution. Within- and between-sex social interactions reflected the typical female nucleus-peripheral male pattern seen inSaimiri groups in other environments. Species differences in investigatory patterns were considered to be contributing elements in the maintenance of distinctive life-styles.     

Sequential Analysis Reveals Behavioral Differences Underlying Female‐Biased Predation Risk in Stalk‐Eyed Flies

Stalk‐eyed flies are classic models of how sexual selection can drive morphological and behavioral elaboration. Exaggerated ornaments born by stalk‐eyed flies could impose locomotor costs and increase susceptibility to predation; however, a previous study determined that behavior, not eye span, was the major influence on predation risk. Despite the importance of behavior, relatively little is known about how these flies avoid and deter predators. We created an ethogram of behaviors and used it to score individual interactions of male and female Teleopsis dalmanni paired with an actively foraging, generalist arachnid predator (Phidippus audax). Sequential analysis was employed to identify temporal patterns in behavior and determine how males and females differ in their approaches to avoiding predation. Our results indicate that males and females significantly differ when specific behaviors were employed. Patterns in the behavioral transitions suggest that males are more aggressive than females and are more likely to approach a predator to jab, abdomen bob, or display. Males elicited more retreat responses from the predator, whereas females elicited more attacks. Although the behavioral repertoires of male and female stalk‐eyed flies are indistinguishable, their uses of the behaviors differ, particularly the sequential order of presentation, suggesting a strong sex difference in anti‐predatory behavior.     

幼小鼠对种内几种化学信息的识别和反应

50年代以来,国际上相继开展了一些关于化学信息在小家鼠繁殖中作用的研究,并在实验室中揭示了一些反应:如集群雌鼠气味使雌鼠性周期延长的Lee-Boot效应,雌鼠气味能解除集群雌鼠对性周期的抑制、并促使它们同期发情的Whitten效应,以及陌生雄鼠气味中断妊娠的Bruce效应等等。但是,在成鼠间起作用的几种化学信息,是否能被幼鼠感受,对幼鼠的发育和性成熟是否产生影响,还是一个未知的问题。 影响小鼠发育的因素很多,除环境因子外,近来还出现了有关社群因素中外激素对小鼠性成熟影响的报道,发现雄鼠或给予雄激素的雌鼠有促进幼雌鼠性成熟的作用,范志勤发现父本气味和陌生雄鼠气味对幼雌鼠性成熟均有促进作用。但是,目前关于种内雌鼠气味、集群雌鼠气味、幼鼠气味影响性成熟的研究尚不多见。有关各种气味对性成熟效应的比较的报道亦少。本文的目的在于通过实验方法,阐明种内的几种化学信息,诸如父本、陌生雄性、雌性、集群雌性、幼雌等几种气味,对幼雌小鼠性成熟的影响,并据此了解幼鼠识别这几种信息的能力。     

Behavioral strategies and hormonal profiles of dominant and subordinate common marmoset (Callithrix jacchus) females in wild monogamous groups

New insights into the mating systems of common marmosets suggest that they are mainly monogamous, although polygyny and polyandry occasionally occur. Long-term monitoring of wild common marmosets has shown that some reports of polygynous groups (i.e., groups that contain more than one reproducing female) in fact indicate an unbalanced reproductive output associated with extragroup copulation. In this study we describe the behavioral and hormonal profiles of common marmoset (Callithrix jacchus) females living in three wild monogamous groups (Q, PBf, and T), varying from five to 11 individuals, at Nísia Floresta field station, RN, Brazil. The mating system of the groups was previously characterized in terms of affiliative, sexual, and mate-guarding behaviors. Behavioral data were collected once a week, and fecal samples were collected at least twice a week for 10-16 months, depending on the group. A preferential allogrooming relationship was recorded between dominant males and females. Under field conditions the reproductive inhibition of subordinate females appears to be more behavioral than hormonal, since subordinate females of the three groups ovulated and two conceived during the study. In these cases, the subordinate and dominant females reproduced 1 month apart, and infanticide (one case confirmed and one suspected) appeared to be part of the reproductive strategy of dominant females. Following the infanticide, ovarian inhibition (group T) or emigration and return to the natal group (group PBf) were observed. In the third group (Q) the subordinate female showed hormonal profiles compatible with pregnancy, but no infants were seen. These findings reflect the different alternatives that wild subordinate common marmoset females use to reproduce.     

Female-typical sexual behavior of rhesus and defeminization by androgens given prenatally

Adult rhesus monkeys were observed in standardized tests for female-typical sexual and related social responses. In the first experiment reported, 7 castrated males and 5 spayed females were paired with each of 4 intact males on two occasions following intramuscular injection with estradiol benzoate (EB) (6 micrograms/kg X 14 days) and on two other occasions without such treatment. In tests without EB, males and females did not behave differently toward the intact male partners, and all responses were displayed at low frequencies. In tests with EB, females showed reliably higher frequencies than males of approaching, sitting close to, grooming, and soliciting, and they presented to a higher proportion of the male partner's sexual contacts. EB reliably increased the frequency of display of all of these same five responses in females but not in castrated males. The intact male partners displayed reliably fewer approaches, sexual contacts, mounts, intromissions, and ejaculations to castrated males than to spayed females regardless of estrogenization. In a second experiment 10 intact adult pseudohermaphroditic females and 6 intact control females were tested following EB injections with each of the same 4 intact males. Pseudohermaphrodites were experimentally produced by injecting pregnant females with either testosterone propionate (TP) or dihydrotestosterone propionate (DHTP). Pseudohermaphrodites, regardless of type of androgen used in their production, showed reliably fewer solicits than controls to male partners. Moreover, they displayed most of the other responses at lower average frequencies than controls. Frequencies of intromission and ejaculation by intact male partners were reliably lower with pseudohermaphrodites than with control females, but frequencies of approach, sexual contact, and mount were not reliably different. We conclude that in this testing and measurement situation male and female rhesus monkeys differ markedly in the degree of expression of female-typical sexual behaviors, and genotypic males are behaviorally less responsive to estrogens than females. Exposing genotypic females to androgens during fetal life decreases the expression of female-typical, estrogen-influenced responses, and the effect is most pronounced on those soliciting responses that subserve proceptivity.     

人工饲养长江江豚的同性性行为和自慰行为

雌雄性之间的性行为对鲸类的生存和繁衍有着极其重要的意义。然而不具有繁殖功能的同性性行为和自慰行为在多种鲸类中存在。因此对鲸类非繁殖性性行为研究,将有助于深入认识该物种性行为特点和规律,并解决室内饲养可能存在的问题以及促进可控性人工繁殖的成功。本研究以人工饲养的7头长江江豚为研究对象,定义并描述了14种性行为。其中,同性之间的性行为定义为同性性行为,雌雄个体单独的性行为定义为自慰行为。雄性同性性行为发现于所有定义的性行为中,但雌性同性性行为仅在7种性行为中观察到。同性性行为（3633次）占总性行为（5563次）的65.31%,自慰行为（254次）占4.57%。同性性行为中,雄性之间的同性性行为（3438次,94.63%）远多于雌性同性性行为（195次,5.37%）。两头有父子关系的江豚（阿福和淘淘）之间的雄性同性性行为最多（1921次,55.88%）,雄性江豚之间的同性性行为可能存在结盟竞争关系或教育练习作用。两头青少年雌豚（F7和F9）之间的同性性行为最活跃（117次,60.00%）,雌性江豚之间的同性性行为很可能具有结伴交流的功能。     

Influence of gonadal hormones on the behaviour of pair-living Mongolian gerbils (Meriones Unguiculatus) towards the cagemate versus a non-cagemate in a social choice test

Laboratory, semi-natural and field observations indicate that the Mongolian gerbil may naturally live in pairs or family groups. Endocrine influence on behaviour towards cagemates and non-cagemates was investigated. The males tested were intact or castrated. The hormonal condition of the females was controlled by gonadectomy and oestrogen and progesterone replacement treatment. The duration and number of visits to the incentive animals were recorded in a choice test, which allowed restricted contact between the experimental and incentive animals. Anoestrous females approached the intact cagemates more than the non-cagemates, while the intact males approached the non-cagemates more often. A comparison of the female behaviour under the different female endocrine conditions tested showed that females significantly increased their response in oestrus towards the strange intact males but not towards their cagemates. Experimental intact males analogously increased their response towards the strange oestrus female but not towards the cagemate. In tests which involved castrated males either as experimentals or incentives, no behavioural change was seen relative to the endocrine condition of the female. The hormonal effects seen were thus connected with the social relationship, as the hormone-induced changes were seen only in behaviour towards a strange animal.     

Non-reproductive copulation behavior among Tibetan macaques (<Emphasis Type="Italic">Macaca thibetana</Emphasis>) at Huangshan,China

Non-reproductive copulation, which takes place outside of the mating season and does not result in conception and birth, was studied in a free-ranging group of Tibetan monkeys (Macaca thibetana) at Mt. Huangshan, China, in the birth seasons of 1992 and 1997. We employed all occurrence and focal animal samplings to record sexual and related behaviors and affiliation interactions, respectively. Compared with sexual behavior in mating season, non-reproductive copulation occurred at a lower frequency, with less frequent ejaculation, less harassment, shorter mount duration, and an absence of pause with vocalization. It often took place in a situation in which non-lactating females were involved in social conflict or approached males for mating. Neither pregnant nor lactating females were observed to mate in the birth seasons. Copulation during the birth season did not increase a sexually receptive female’s delivery the next year, nor was it associated with increased proximity, grooming, or agonistic aid for the mating pair. However, copulated pairs spent more time co-feeding, presumably reflecting an increased tolerance on the part of the male. Adolescent males, who rarely copulated in the mating season, engaged in mating activity in birth seasons as well. Therefore, though birth-season copulation had no reproductive functions, it may have fulfilled social functions for females, such as post-aggression appeasing by males or gaining access to resources. This also offered good opportunities for adolescent males and females to develop their sexual skills for later competition.