Social Tolerance in Wild Female Crested Macaques (Macaca nigra) in Tangkoko‐Batuangus Nature Reserve,Sulawesi, Indonesia

In primates, females typically drive the evolution of the social system and present a wide diversity of social structures. To understand this diversity, it is necessary to document the consistency and/or flexibility of female social structures across and within species, contexts, and environments. Macaques (Macaca sp.) are an ideal taxon for such comparative study, showing both consistency and variation in their social relations. Their social styles, constituting robust sets of social traits, can be classified in four grades, from despotic to tolerant. However, tolerant species are still understudied, especially in the wild. To foster our understanding of tolerant societies and to assess the validity of the concept of social style, we studied female crested macaques, Macaca nigra, under entirely natural conditions. We assessed their degree of social tolerance by analyzing the frequency, intensity, and distribution of agonistic and affiliative behaviors, their dominance gradient, their bared‐teeth display, and their level of conciliatory tendency. We also analyzed previously undocumented behavioral patterns in grade 4 macaques: reaction upon approach and distribution of affiliative behavior across partners. We compared the observed patterns to data from other populations of grade 4 macaques and from species of other grades. Overall, female crested macaques expressed a tolerant social style, with low intensity, frequently bidirectional, and reconciled conflicts. Dominance asymmetry was moderate, associated with an affiliative bared‐teeth display. Females greatly tolerated one another in close proximity. The observed patterns matched the profile of other tolerant macaques and were outside the range of patterns of more despotic species. This study is the first comprehensive analysis of females’ social behavior in a tolerant macaque species under natural conditions and as such, contributes to a better understanding of macaque societies. It also highlights the relevance of the social style concept in the assessment of the degree of tolerance/despotism in social systems. Am. J. Primatol. 75:361‐375, 2013. © 2013 Wiley Periodicals, Inc.     

Hormonal Correlates of Paternal Care Differences in the Hylobatidae

Only one of the 15 species of monogamous hylobatids, the siamang (Symphalangus syndactylus), demonstrates direct paternal care in the form of infant‐carrying, providing a unique model for examining hormonal correlates of paternal care differences between siamangs and gibbons. We used behavioral data and fecal hormone analysis to investigate (1) differences in monthly percent father–infant proximity in relation to monthly fecal androgen metabolite concentrations from infant birth to the late postpartum period between siamangs and gibbons, (2) the pattern of change in fecal androgen and fecal estrogen metabolite concentrations during the 8‐week peripartum period between siamangs and gibbons, and (3) the change in mean fecal glucocorticoid metabolite concentrations at 1‐month postpartum from individual baseline between siamangs and gibbons. Father–infant proximity increased as androgen concentrations decreased over the postpartum period in siamangs but not in gibbons. Androgen concentrations increased around birth in siamangs during the 8‐week peripartum period, but exhibited a decreasing trend around birth in gibbons. Estrogen concentrations increased from pre‐ to postpartum in siamangs during the 8‐week peripartum period, but exhibited a decreasing trend from pre‐ to postpartum in gibbons. The difference in mean glucocorticoid metabolite concentrations from baseline was greater in siamangs than gibbons. Our data suggest a relationship between specific steroid hormone patterns and differences in paternal care among the hylobatids, warranting further investigation of such proximate mechanisms.     

Social stimulation and the resumption of copulation in Rhesus (Macaca mulatto) and stumptail (Macaca arctoides) Macaques

Copulatory data derived from observations of social groups of rhesus and stumptail macaques were analyzed to test the hypothesis that pairs of animals would resume copulation significantly sooner if a second male copulated with the female shortly after the first male’s ejaculation. Data from both groups supported the hypothesis. These results, extending previous studies in Macaca nemestrina,suggest that the shortening of copulatory intervals by social stimuli occurs in several species, both in social groups and in experimentally created triads. These findings also are consistent with the hypothesis that socially mediated resumption of mating is related to intrasexual competition among males.     

Hormonal Correlates of Maternal Style in Captive Macaques (Macaca fuscata and M. mulatta)

Previous studies on nonhuman primate maternal styles showed that variation in infant-directed behavior falls along two dimensions, traditionally labeled as protectiveness and rejection. We investigated maternal styles in rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques living in analogous captive social groups, and correlated them with the levels of estrogen metabolites excreted in female feces during the perinatal period. We focally observed mother-infant pairs 3 hours per week during the first 12 weeks of infant life. We collected fecal samples twice a week from each mother, starting 4 weeks before delivery and ending 4 weeks after delivery. Three significant components were extracted by principal component analysis from 15 different infant directed behaviors, each reflecting a different aspect of mothering style: rejection is correlated with behavioral measures of maternal opposition to contact; protectiveness is correlated with maternal solicitude; and independence is correlated with time in contact, grooming and cradling. Levels of estrogen metabolites are significantly correlated to rejection but not to protectiveness or independence, indicating that, in nonhuman primates, individual endocrine changes related to maternal behavior might specifically affect the timing of contact interruption.     

Maintenance of high-density lipoprotein blood levels prior to spontaneous abortion in pig-tailed macaques (Macaca nemestrina)

Blood was drawn throughout the first half of the pregnancies of 24 pig-tailed macaques (Macaca nemestrina) to evaluate longitudinal high-density lipoprotein (HDL) changes. In all 15 normal pregnancies, HDL decreased at least 50%; the mean value for the group fell from 0.45 gm/liter to 0.17 gm/liter. HDL began to fall after about four weeks of pregnancy. However, no comparable HDL change occurred in nine pregnancies that terminated in spontaneous abortions. This lack of an HDL decrease was unexpected. Subsequent studies showed that the predominant decrease was in the HDL₂ subfraction. The data indicate that the normal physiologic metabolism or utilization of HDL is aberrant early in pregnancies ending in spontaneous abortions and may be due to a dysfunctional fetal-placental unit.     

Patterns of dominance and affiliation in wild pig-tailed macaques (Macaca nemestrina nemestrina) in West Sumatra

Patterns of agonistic and nonagonistic behaviors were studied in a troop of wild pig-tailed macaques in West Sumatra, Indonesia. The animals were provisioned and the identities of all adult and adolescent individuals were known. The females could be divided into high-, mid-, and low-ranking subsets of individuals. Most grooming occurred within, instead of between members of these subsets. The members of each subset also tended to feed together at the baiting sites, and they probably represented groups of close kin. Among females, grooming appeared to be a conciliatory behavior and was generally performed by the subordinate partner, while mounting was performed by the dominant partner and appeared to be a reassertion of dominance. High-ranking males tended to form agonistic alliances with females and to exchange grooming with estrous females. Low-ranking males did not have such associations with females and were frequently the targets of agonistic alliances of females and juveniles. Mounting between males appeared to be a conciliatory behavior. It seemed effective since severe aggression between males was not observed. The subordinate partner mounted more frequently than the dominant one, but the direction of mounting was apparently controlled by the latter. This suggests that, among pig-tailed macaques, the dominant male plays an important role in the coexistence of males in the troop.     

Affiliation Between Aggressors and Third Parties Following Conflicts in Long-Tailed Macaques (Macaca fascicularis)

Studies on cercopithecine monkeys have shown that soon after an agonistic conflict, victims have increased rates of affiliation with the agressor—reconciliation—but not with other group members. Postconflict affiliation is thought to function to restore disturbed relationships and to reduce social tension. This study on a captive group of long-tailed macaques (Macaca fascicularis) is focused on postconflict affiliative behavior of the aggressor. Increased rates of contact between female aggressors and kin of the victim occurred, as well as between female aggressors and their own kin. Furthermore, there were increased rates of contact between aggressors—males and females—and other group members. The increase in contacts with the victim's kin was selective, i.e., it could not be ascribed to the increased contact tendency with group members in general, and was not a side effect of the aggressor's proximity to the victim due to reconciliation. The increase in contacts with own kin was not selective. The fact that male aggressors do not have increased postconflict contacts with their kin or with kin of the victim is in agreement with the notion that males are less integrated in the nepotistic matrilineal network than females are. The fact that studies by others that focused on the victim evidence no increase in postconflict contacts with kin of the opponent or with other group members may be explained by the aggressor's larger influence over the postconflict situation: to reduce social tension, it might be more effective to affiliate with the aggressor than with the victim. Our findings emphasize that conflicts influence the behavior of other monkeys besides the direct contestants and, thus, indicate that the disturbance of social homeostasis is a matter of concern for all group members.     

Socioecological Context of Parturition in Wild Japanese Macaques (Macaca fuscata) on Yakushima Island

Female primates may adopt special feeding, foraging, and social strategies around the time of giving birth. We observed 8 females during the prepartum period, the day of birth, and the postpartum period in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. We collected data on their activity budgets, quantitative feeding and foraging behavior, and on female-male interactions. On the day of birth, females spent less time moving and feeding, and more time resting relative to other periods. Overall dietary diversity as well as arthropod foraging also decreased on the day of birth. Females fed mostly on mature leaves, new leaves and shoots during prepartum periods but mostly on fruit during postpartum periods. Decreased feeding on leaves and increased feeding on fruit probably changed as a result of seasonal availability, independently of parturition. Feeding on flowers, fungi and other items remained constant over all periparturitional periods. On the day of birth, new mothers had fewer social interactions with males and spent more time out of proximity with other adults than in other periods. Females rejected grooming presentations from males, groomed less with males, spent less time 3 m of males, and received less aggression from males on the day of birth. In the postpartum period, interactions with males returned to prepartum values. Grooming with females did not differ across the three periods. These results suggest that interactions with males may be costly for females on the day of birth.     

亲缘关系与啮齿类动物的社会行为

在漫长的进化过程中 ,动物除了在形态结构、生理生化以及遗传等方面适应周围环境之外 ,也产生了与环境相适应的行为 ,其中种内个体社会联系的行为称为社会行为。由于自然选择提高了个体的生存价值和广义适合度 (ｉｎｃｌｕｓｉｖｅｆｉｔｎｅｓｓ) ,所以如果个体间亲缘程度不同 ,在自然选择的作用下必然会产生不同的结果。亲缘关系与社会行为的研究源于行为生态学 ,其中以Ｈａｍｉｌｔｏｎ[32 ] 提出的亲缘选择和广义适合度理论为代表 ,将亲缘关系和自然选择联系起来 ,扩展了达尔文自然选择理论的范围 ,较好地解释了利他行为 (ａｌｔｒｕｓ…     

Social Contact Following Severe Aggression in Rhesus Macaques (Macaca mulatta): A New Test of the Consolation Hypothesis

Previous studies on macaque species revealed no evidence of consolation: affiliative contact between the loser of an aggressive interaction and a third party. However, typically, the researchers used short observation periods and latency to make first affiliative contact as a dependent measure. Based on social stress buffering literature, I predicted that by employing longer observation periods and percentage of time in affiliative contact as a dependent measure, I would be more likely to detect increases in affiliative contact following aggression. I observed adult female rhesus macaques for 1 hr after they received severe aggression and for 1 hr after some affiliative contact, and measured time spent in affiliative contact using instantaneous recording at 30-sec intervals. Contrary to prediction, victims of attack did not spend a greater percentage of time in affiliative contact postaggression as compared to postaffiliation. Subjects were also less likely to initiate contact with other individuals and were more likely to have contact with individuals that were dominant to their aggressor, following aggression. These results provide converging evidence that affiliative contact is not increased following aggression in macaques. I discuss the failure to bear out the predictions based on the social stress buffering literature in terms of rhesus social dynamics, the nature of aggression as a stressor, and possible mechanisms for the social stress buffering effect.     

Social Behavior of Captive Indochinese and Insular Long-Tailed Macaques (Macaca fascicularis) Following Transfer to a New Facility

There are measurable differences in behavior, physiology, social organization, and geographic distribution within and between various species of macaques. We collected information on the social behavior of captive Macaca fascicularis from Indochina and island populations after they had been transferred to a new environment and new social groups. While some changes in behavior occurred over time, we found no decrease in high levels of agonistic behaviors. We interpret this finding in light of previous research reporting that long-tailed macaques show low levels of habitatuation to novelty and are highly aroused in comparison to other macaque species. We found predictable differences in behavior for males, females, and infants, in which infants played more, females had higher levels of contact proximity to other individuals, and males exhibited more sexual and threat behavior. A comparison of social behavior in long-tailed macaques from different origins indicate that Indochinese macaques are generally less affiliative and Indochinese males are more aggressive than their insular counterparts. Differences among macaque species, and within the fascicularis-group, should be considered in management of captive colonies and when interpreting research data.     

Decrease in sexual initiative and responsiveness in female rhesus macaques (Macaca mulatta) during pregnancy

Although the sexual behavior of female rhesus macaques (Macaca mulatta) has been reported to decrease during pregnancy, systematic studies have been largely confined to reports of male behavior. Therefore, we designed a study to examine changes in female sexual behavior during pregnancy. Six cycling multiparous female rhesus macaques were paired during the periovulatory period of the menstrual cycle and during the first and second halves of pregnancy with six sexually experienced males of the same species. Each female was paired with the same male in all tests. The means of the behavioral measures scored on days 11–13 of the menstrual cycle, 35–56 of pregnancy, and 147–168 of pregnancy were compared. Females showed a significant decrease in the present contact ratio and the rate of threat-aways during pregnancy. Males showed lower rates of threatening-away, contacting, mounting, intromitting, and ejaculating when females were pregnant. The extent to which the decrease in male sexual behavior can be accounted for by an increase in female rejection is uncertain, but it is probably as significant as any loss of attractiveness that might accompany pregnancy.     

The Importance of Social Condition in the Hormonal and Behavioral Responses to an Acute Social Stressor in the Male Siberian Dwarf Hamster (Phodopus sungorus)

Social condition is an important factor in determining the behavioral and hormonal responses to a social stressor in the Siberian dwarf hamster (Phodopus sungorus). We predict that males housed with a female or a family (female and pups) will show an increase in the magnitude of the behavioral and hormonal responses to a male intruder compared to those of individually housed males. Three treatment groups were studied: individually housed males that had been previously group-housed in same-sex colonies (males,n= 10), males housed with a female (male + female,n= 9), and males housed with their female and pups (male + family,n= 12). Males were monitored for aggressive behavior toward an intruder male for 10 min. Blood samples were taken at baseline and after the encounter. Male + female and male + family groups spent more time in aggressive behavior (P< 0.05), such as attacking (P< 0.05) and fighting (P<0.05), than did individually housed males. These same groups showed significant increases in plasma cortisol after the encounter (P< 0.01) whereas there were no significant increases in plasma cortisol in solitary males. All groups showed significantly lower levels of plasma testosterone (male,P< 0.001, male + female,P< 0.05; male + family,P< 0.01) whereas a significant increase in prolactin occurred only in the male + family group (P< 0.05). There was a significant positive correlation between postencounter cortisol levels and total number of minutes spent in aggressive behavior (P< 0.05). These results demonstrate that the introduction of a novel intruder male results in an activation of the hypothalamic–pituitary–adrenocortical axis and a suppression of the reproductive axis. Furthermore, pairing of a male with a female alters the behavioral and hormonal responses to an intruder male.     

Mechanisms Underlying Microbial-Mediated Changes in Social Behavior in Mouse Models of Autism Spectrum Disorder

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Dominance index: A simple measure of relative dominance status in primates

A simple measure of relative dominance status (cardinal rank) is described which we have termed the dominance index. Like more familiar techniques for assessing rank order, it is based on the direction of aggressive and submissive behaviors between all possible paired combinations of animals in a social group. Using data from five groups of female rhesus monkeys, it reliably produced the same ordinal ranks as fight interaction matrices. There was also good agreement with the cardinal ranks produced by two additional measures of dominance and with those produced by observer ratings. The dominance index can be calculated when fights have not actually occurred and is largely independent of the frequency of agonistic interactions. It has, therefore, wide application and can estimate dominance during brief sampling periods (one hour) and also in stable groups when agonistic interactions are low. Its application is described in experiments in which the male in a group of females was changed and the hormonal status of the females was altered. Estrogen increased female dominance status relative to other females.     

Social Relationships in Free-Ranging Male Macaca arctoides

Macaque social relationships differ greatly between species. Based on captive studies that focus mainly on females, researchers have classified stumptail macaque (Macaca arctoides) social relationships as tolerant, as indicated by a high rate of affiliation, frequent aggression, and symmetrical conflicts. To accumulate more data on male social relationships, which are relatively understudied, and to generate comparative data, we investigated male social relationships in a provisioned group of 68 free-ranging, naturally dispersing stumptail macaques in southern Thailand. We collected continuous focal animal and ad libitum data on 7 adult and 2 subadult males, recording social behavior during 283 contact hours between December 2006 and March 2007. Stumptail macaques of this population were less tolerant than predicted based on previous studies on captive groups: Rates of spatial proximity, affiliation, and aggression were low, most males directed affiliative behavior toward higher-ranking males, and conflicts were generally of low intensity and relatively asymmetrical. Thus, male stumptail macaques of the focal group appear to differ in their social style from a previous study of a captive group that mainly comprised of females. In some traits, they are even more intolerant than rhesus macaques, an intensively studied intolerant macaque species. We also compare our data on stumptail macaque males to those on other male macaques, but available data are too sparse to draw final conclusions.     

Coevolution of Facial Expression and Social Tolerance in Macaques

The purpose of this study is to test the hypothesis that social tolerance drives the evolution of facial expression in macaques. Macaque species exhibit a range of social styles that reflect a continuum of social tolerance. Social interactions in more tolerant taxa tend to be less constrained by rank and kinship than in less‐tolerant macaques. I predicted that macaques that are more tolerant would exhibit a wider range of facial displays than less‐tolerant species because interactions that are open to negotiation are characterized by greater uncertainty than interactions that are constrained by rank or kinship. To test this hypothesis, I conducted a phylogenetically informed regression analysis (N = 11) using previously published data on repertoire size and two quantitative measures of social tolerance (conciliatory tendency and counter‐aggression). As predicted, macaques with more tolerant social styles tended to have larger repertoires than less‐tolerant species. These results support the hypothesis that increased social tolerance favors the elaboration of communication to mitigate uncertainty.     

前额叶皮层在社交行为中的作用

社交行为对于个体身心健康和社会发展都极其重要。社交行为障碍已成为多种精神类疾病的典型临床表征,对个体的发展有严重不良影响。前额叶皮层作为调节社交行为的关键脑区之一,参与了社交、情绪、决策等高级功能,其内部神经元、神经胶质细胞的活动变化及相互作用对调节社交行为有着重要影响,而且前额叶皮层与其他脑区之间的协作也会影响不同的社会行为。本文回顾了前额叶皮层中神经元、神经胶质细胞以及脑区投射与社交行为关系的最新研究,系统综述了前额叶皮层在社交行为调节中的作用,以期为社交障碍的神经机制和有效诊疗提供参考。     

Postconflict Affiliation and Stress-Related Behavior of Long-Tailed Macaque Aggressors

Previous studies on macaques and baboons showed that after agonistic conflicts aggressees as well as aggressors show an increase in stress-related behavior such as scratching. Reconciliation reduces stress-related behavior of the aggressee. We investigated the influence of various affiliative postconflict behaviors of the aggressor on the aggressor's scratching rates in captive long-tailed macaques: reconciliation, contacts with the aggressee's kin (or substitute reconciliation), and contact with other group members (or triadic affiliation). After a conflict, the aggressor showed an increase in rates of scratching. Scratching rates were reduced after reconciled conflicts compared to nonreconciled conflicts. Substitute reconciliation did not reduce scratching when we controlled for the influence of reconciliation, i.e., the aggressor might not interpret it as a substitute for reconciliation. Triadic affiliation did not reduce scratching rates, hence, triadic affiliation probably does not console the aggressor. Scratching rates after reconciliation are significantly lower than scratching rates after triadic affiliation. This proves that the stress-reducing effect of reconciliation is not due to the calming effect of general body contact but that the stress reduction is specifically associated with contacts with the former opponent. The contestants are anxious about their relationship, and only reconciliation takes away this anxiety. Reconciliation is thus an important social repair strategy.     

Menstrual cycles in rhesus monkeys (Macaca mulatta) are unaffected by a single dose of the anesthetics ketamine and xylazine administered during the midfollicular phase at laparoscopy

To identify an anesthetic regimen that produces more complete relaxation and analgesia than ketamine hydrochloride (Ketaset®) alone, a combination of ketamine (15 mg/kg body weight) and the hypnotic xylazine (Rompun®, 0.33 mg/kg) was evaluated. Since the desired experimental application required that the anesthetic not interfere with normal hormonal events during the menstrual cycle, this combination administered on day 6 of the cycle was tested to determine whether hormonal surges, incidence of ovulation, or cycle length would be altered relative to the use of ketamine alone. In five of six animals, ketamine plus xylazine had no effect on the occurrence of timely surges of estrogen, luteinizing hormone (LH), or follicle-stimulating hormone (FSH), or on ovulation as determined by the presence of a corpus luteum at laparoscopy and normal serum concentrations of progesterone. There were no significant differences between the cycle during treatment and previous cycles in the same animal for length of the menstrual cycle (26.0 ± 2.3 [5] days; X? ± S.D. [n] or luteal phase (13.4 ± 2.4 [5] days). Likewise, these values did not differ from those of ten control monkeys treated with ketumine only on day 5 or 6 of the cycle (incidence of ovulation, 10/10; cycle length, 27.9 ± 1.8 [10]; luteal phase length, 15.1 ± 1.4 [10], P > 0.05). Patterns of circulating progesterone were not altered by the addition of xylazine anesthesia. These findings indicate that xylazine, given in the midfollicular phase, did not alter ovulatory events or menstrual cycle characteristics in rhesus monkeys. Ketamine plus xylazine apparently provides anesthesia appropriate for laparoscopy.