Approach to a social stranger is associated with low central nervous system serotonergic responsivity in female cynomolgus monkeys (Macaca fascicularis)

It is widely hypothesized that individual differences in central nervous system (CNS) serotonergic activity underlie dimensional variation in "impulsive" vs. "inhibited" social behavior in both humans and nonhuman primates. To assess relative impulsivity in a social context, a behavioral challenge involving animals' exposure to a social stranger (termed the "Intruder Challenge") was recently validated in adolescent and adult male vervet monkeys (Cercopithecus aethiops sabaeus). Among these animals, monkeys that quickly approached the intruder were found to have lower cerebrospinal fluid (CSF) concentrations of the serotonin (5-HT) metabolite, 5-hydroxyindoleacetic acid, than less impulsive animals. In the present study we extended these observations to determine whether approach to a social stranger, as operationalized by the Intruder Challenge, is similarly associated with diminished CNS serotonergic function in female cynomolgus monkeys (Macaca fascicularis). Study animals were 25 adult monkeys that had been housed for 2 years in stable social groups. In each animal, the rise in plasma prolactin concentration induced by acute administration of the 5-HT agonist, fenfluramine, was used to assess "net" central serotonergic responsivity. When exposed later to an unfamiliar female of the same species in a catch-cage placed for 20 min within the subjects' home enclosure, monkeys that approached to within 1 m of the intruder (median latency to approach=3 min) were found to have significantly smaller prolactin responses to fenfluramine (diminished serotonergic responsivity) compared to "inhibited" animals that failed to approach the intruder (t=2.9, df=23, P<0.009; rpb=-0.51). Neither approach behavior nor the animals' fenfluramine-induced prolactin responses covaried significantly with nondirected expressions of arousal (or anxiety) or with aggressive behaviors exhibited during testing. We conclude that in female cynomolgus monkeys, social impulsivity (vs. inhibition) correlates inversely with individual differences in CNS serotonergic activity, as assessed by neuroendocrine challenge.     

Dominance, cortisol, and behavior in small groups of female cynomolgus monkeys (Macaca fascicularis)

The relationships among social rank, basal cortisol concentrations, and social behavior were assessed in adult female cynomolgus monkeys (Macaca fascicularis). Subjects were 157 unrelated, reproductively intact animals housed in 30 small groups. Rank determinations were made monthly. Blood samples were collected on two occasions, 4.5 and 7.5 months following initial group formation. Regular behavioral observations were conducted on a subset of animals over a period of 4 weeks, 9 months following group formation. Analyses revealed that serum cortisol values were significantly correlated across the two sampling periods, with no significant change in absolute values. While social rank was positively correlated across both samples, there was no relationship between rank and cortisol. However, dominant and subordinate animals did differ in the rates of performance of aggressive and submissive behaviors. These data suggest that social rank does not influence baseline serum cortisol in adult female cynomolgus monkeys, despite stability in measures of rank and cortisol and the presence of the usual behavioral differences between dominants and subordinates.     

Social status determines sexual phenotype in the bi-directional sex changing bluebanded goby Lythrypnus dalli

The behavioural mechanisms and patterns of protandrous sex change in bluebanded gobies Lythrypnus dalli were investigated and compared to the well-described behaviour patterns of protogynous sex change. To do this, unisex groups of males and females were established; behavioural and anatomical changes were recorded over a 42 day period as social status and sexual phenotype were determined. In all cases, social status, rather than the expression of a particular behaviour, accurately predicted final sexual phenotype. Rates of submissive behaviour, but not aggressive behaviour, were predictive of each discrete status class. Multiple individuals changed sex simultaneously if their sexual phenotype and social status were discordant, a novel finding suggesting that once a social hierarchy is established, individuals determined their sexual phenotype, regardless of initial sex, based on a simple operational principle: if subordinate express female, if dominant or not subordinate express male. This work demonstrates that similar mechanisms underlie sex change in both directions in L. dalli and potentially other sex changing species.     

The influence of rank on affect perception by pigtailed macaques (Macaca nemestrina)

Previous studies of affect perception in nonhuman primates have involved young animals and/or manipulations of early experience. Based upon data suggesting that middle-ranked monkeys in small social groups show patterns of behavior different from their low- or high-ranked counterparts, the current study examined the role of social rank in affect perception by normally reared, adult female pigtailed macaques. Employing color videotapes as the presentation medium, we observed animals as they watched unfamiliar animals display social (aggressive or submissive) or nonsocial behavior. Virtually all threats were recorded as the subjects watched the submissive presentations, and most submissive signals occurred while watching aggressive behavior tapes. Middle-ranked monkeys were most attentive during all presentations, and levels of disturbance behavior were related to rank of the watcher and type of presentation observed. The results suggest that dominance status is an influence in the process of affect perception.     

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.     

Estradiol effects on behavior and serum oxytocin are modified by social status and polymorphisms in the serotonin transporter gene in female rhesus monkeys

Despite the well-documented relation between estradiol (E2) and behavior, exposure to stressors may modify sensitivity to E2. The effects of E2 on behavior are, in part, likely related to their modulation of the serotonin (5HT) and oxytocin systems. The short allele (s-variant) polymorphism found in the promoter region of the SLC6A4 gene that encodes the 5HT transporter (5HTT) modulates responsivity to stressors. The current study used ovariectomized adult female rhesus monkeys to evaluate how exposure to the psychosocial stressor of social subordination and polymorphisms in the gene encoding 5HTT influence the behavioral effects of E2 and immunoreactive serum oxytocin. Dominant females had higher levels of oxytocin than subordinate animals even though E2 increased immunoreactive serum oxytocin in all females. E2 increased affiliative behaviors in all animals, with even more of these prosocial behaviors directed at dominant females. S-variant females, regardless of social status, were more aggressive toward more subordinate cage mates and these behaviors too were increased by E2. Subordinate s-variant females are most often involved in agonistic behavior, less affiliative behavior, and were less responsive to the anxiolytic action of E2. The results show that the short allele of the 5HTT gene synergizes with psychosocial stress exposure to affect the behavioral efficacy of E2 while confirming the actions of E2 for producing generalized behavioral arousal in females. Whether differences in the central action of 5HT and/or oxytocin are responsible for this effect requires further study.     

Social dominance does not increase oxidative stress in a female dominance hierarchy of an African cichlid fish

In many group living animal species, individuals use aggression to gain and maintain social dominance to secure access to ecological resources and potential mates. While social dominance has many fitness benefits, there are also potential costs associated with frequent agonistic interactions and status display. One potential cost of social dominance is oxidative stress, the imbalance of reactive oxygen species and antioxidant capacity. In the cichlid species Astatotilapia burtoni, dominant males are aggressive, hold a breeding territory, and have an activated reproductive system resulting in larger gonads. Subordinate males are submissive, school with females, and are nonreproductive. Females are submissive under natural conditions, but in a female-only group, a dominance hierarchy will form with dominant females taking on male-typical behaviours including aggression, territory defence, and increased androgen levels. However, in contrast to males, social dominance is not linked to increased activation of the reproductive system in females, allowing us to test whether social dominance alone exposes individuals to increased oxidative stress. We compared dominant and subordinate females in female-only groups in five markers of oxidative stress. Dominant females did not have higher levels of oxidative damage compared to same-sex subordinates. This result contrasted to the trend in males in which dominant males had higher oxidative damage than their subordinate counterparts. Our findings suggest that the oxidative cost of social dominance is limited and support the notion that previously reported associations between high rank and increased oxidative stress is most likely driven by increased investment in reproduction.     

Relation between the dominance rank of female rhesus monkeys and their access to males

Systematic observations were made on 12 measures of the sexual, aggressive, and social interactions of 24 male–female pairs of rhesus monkeys in six social groups, each consisting of one male and four ovariectomized females tested in a large room. Each female in a group was treated in turn first with estradiol alone and then with estradiol and progesterone in combination. When hormone-treated, the female was also observed during pair tests with the male in the same large observation room (four males, eight females, 240 group tests, 240 pair tests). The dominance ranks of females during group tests were determined post hoc by means of the dominance index [Zumpe & Michael, American Journal of Primatology 10:291–300, 1986]. In all six groups, the most dominant female virtually monopolized the male, and the subordinate females' interactions with the male, assessed during pair tests, were almost completely suppressed during group tests. This “dominant female effect” was a robust phenomenon that depended solely on female dominance rank. It was independent of the identity and hormonal status of females and of the social preferences of males as expressed in pair tests. These findings demonstrate the existence of female mate competition in an Old World primate.     

Plasma prolactin changes following fenfluramine in depressed patients compared to controls: An evaluation of central serotonergic responsibility in depression

In an attempt to evaluate the responsiveness of the serotonergic neurotransmitter system in depression, fenfluramine, a serotonin releasing agent, was administered to 18 depressed patients and 10 controls, and placebo was administered to 16 of the depressed patients in a double-blind paradigm. Plasma prolactin levels were measured prior to and for five hours following fenfluramine. Fenfluramine produced a significant increase in prolactin in both patients and controls. However, the prolactin response to fenfluramine whether measured as an absolute increase or percent increase from baseline was significantly less in depressed patients than controls. This difference remained equally statistically significant when age-and-sex-matched pairs of depressed patients and controls were compared. These results suggest that the central serotonergic system is less responsive in depressed patients than controls.     

Gonadal hormones modulate the display of submissive behavior in socially defeated female Syrian hamsters

There are striking differences in the behavioral response to social defeat between male and female Syrian hamsters. Whereas males exhibit a prolonged behavioral response to defeat (i.e., conditioned defeat), many females remain aggressive or show only a transient submissive response following defeat. The current study tested the hypothesis that sex steroids underlie this differential behavioral responsivity to social defeat. Female hamsters were ovariectomized and implanted with Silastic capsules containing estradiol (E(2)), testosterone (T), progesterone (P), dihydrotestosterone (DHT), or a blank capsule (no hormone replacement). After a 3-week recovery period, each subject was placed inside the home cage of a larger, more aggressive female for four 5-min defeat trials. The following day, each animal was tested for conditioned defeat by testing it in its own home cage in the presence of a smaller, non-aggressive intruder. Submissive, aggressive, social, and nonsocial behaviors were subsequently scored. Hamsters receiving E(2) or T displayed significantly lower levels of submissive behavior than did animals receiving P, DHT, or no hormone replacement. There were no significant differences in aggressive behavior among groups. These data suggest that gonadal hormones can influence submissive behavior in female hamsters. Collectively, these results suggest that the sex differences observed in conditioned defeat may, in part, be explained by sex differences in circulating gonadal hormones.     

Social monitoring via close calls in meerkats

Social monitoring of the actions of group members is thought to be a key development associated with group living. Humans constantly monitor the behaviour of others and respond to them in a flexible way depending on past interactions and the current social context. While other primates have also been reported to change their behaviour towards other group members flexibly based on the current state of their relationship, empirical evidence is typically linked to contextually specific events such as aggressive or reproductive interactions. In the cooperatively breeding meerkat (Suricata suricatta), we investigated whether subordinate females use frequently emitted, non-agonistic close calls to monitor the location of the dominant female and whether they subsequently adjust their response based on recent social interactions during conflict and non-conflict periods. Subjects discriminated between the close calls of the dominant female and control playbacks, responding by approaching the loudspeaker and displaying submissive behaviour only if they were currently threatened by eviction. Our results suggest that meerkats assess the risk for aggressive interactions with close associates depending on social circumstances, and respond accordingly. We argue that social monitoring based on non-agonistic cues is probably a common mechanism in group-living species that allows the adjustment of behaviour depending on variation in relationships.     

Retrospective case–control study of hyperglycemia in group‐housed,mature female cynomolgus macaques (Macaca fascicularis)

Background Captive cynomolgus macaques are prone to obesity, increasing their risk for developing hyperglycemia and type 2 diabetes mellitus (T2DM). Social rank may be a contributing risk factor predisposing macaques to adverse health events. Methods Using retrospective health records from 259 animals, a matched case–control study was conducted to assess risk factors for developing hyperglycemia in group‐housed, adult females aged 10 or older. Univariable exact and conditional logistic regression models were used to analyze the data. Result The odds of developing hyperglycemia were significantly greater in animals with more frequent counts of injury. Similarly, subordinate animals had higher odds of developing hyperglycemia than affiliates. Conclusions Subordinate social status may increase the risk of hyperglycemia in mature female cynomolgus macaques. Opportunities for subordinates to alter feeding strategies are reduced in captivity. This may be associated with increased social stress around feeding, and for animals housed long‐term could predispose them to obesity and hyperglycemia.     

社群压力对圈养雌性亚洲象动情的影响

亚洲象是中国一级濒危保护动物,改善圈养亚洲象的繁殖状况是亚洲象保护工作的重要内容之一。本研究旨在通过分析社群压力对圈养雌性亚洲象应激和动情状况的影响,从而探究圈养雌性亚洲象长期不动情的原因。通过放射性免疫法检测雌性亚洲象尿液中皮质醇、孕酮和雌二醇水平以及粪便中皮质醇和雌二醇水平,以雌激素水平反映亚洲象的动情状况,以皮质醇水平反映亚洲象的应激状态,以争斗行为和友好行为的发生情况反映圈养群体的社群压力。研究发现：(1)处于优势地位的个体表现出更多的斗争行为,处于从属地位的个体受到更多的攻击行为;(2)优势个体的皮质醇水平显著高于处于从属地位个体的皮质醇水平;(3)优势个体的雌二醇和孕酮具有小幅周期性波动,而从属个体的雌二醇和孕酮水平没有表现出明显的波动。从本研究结果可以看出圈养亚洲象群体中优势个体对从属个体的行为抑制可能是导致从属个体雌激素水平低,长期不能参与繁殖的原因。     

The relationship between aggressive behavior and menstrual cycle stage in female rhesus monkeys (Macaca mulatta)

The aggressive behavior of eight adult female rhesus monkeys, living in a captive social group, was studied prior to and during a breeding season extended by vasectomizing all the adult males in the group. Female reproductive status was ascertained by: recording all adult female-adult male copulations, detecting menstruation by vaginal swabbing, and analyzing serum progesterone levels by radioimmunoassay. Females were more aggressive during the follicular stage of their menstrual cycle than the luteal stage or during the period prior to the onset of seasonal ovarian activity. Increases in aggression were limited to increases in the milder forms of agonistic behavior, primarily threatening gestures. Although the females showed their highest rates of noncontact aggressive response categories during the follicular stage, several showed highest rates of contact aggressive response categories in the precycling period.     

Patterns of female dominance in Propithecus diadema edwardsi of Ranomafana National Park, Madagascar

Many lemur species are characterized by some form of female dominance, ranging from female feeding priority to complete female dominance, although this is a rare trait in primates and other mammals. The status of the Milne-Edwards' sifaka (Propithecus diadema edwardsi), a diurnal lemur, is ambiguous. Some short-term studies have found little or no aggression. The aim of the current, long-term study was to quantify the intersexual-dominance patterns of this sifaka. The distribution, outcome, and context of aggressive interactions were studied in four groups of wild sifakas. The majority of intersexual aggressive interactions were decided, with the loser expressing submissive behavior. Intersexual aggressive interactions occurred in all social contexts, and within all social contexts the females won the vast majority (92.7-96.0%) of aggressive interactions. While aggression rates were low (0.22/hr), this evidence suggests female dominance. We propose that female dominance exists because it provides a fitness advantage to both males and females.     

Sequences of primate signs. Review of teaching sign language to chimpanzees,edited by R. Allen Gardner,Beatrix T. Gardner,and Thomas E. Van Cantfort. Albany,State University of New York Press, 1989, 324 pp, 20 fig, 45 tab, $59.59 (cloth), $19.95 (paper)

Female social dominance over males is thought to characterize most of the prosimian primates of Madagascar. It has been reported in Propithecus verreauxi coquereli in the wild but intersexual relations were not fully characterized. In this paper we examine female-male spatial and agonistic relations in semi-free-ranging P. v. coquereli in order to evaluate intersexual social dominance and related behavioral asymmetries. Two hundred hours of focal sampling were conducted on two pairs of P. v. coquereli at the Duke University Primate Center, Durham, NC. Behavioral categories including approach, departure, follow, pass, replace, and aggression were scored and recorded. Our results show strong asymmetry of aggressive encounters, suggesting female dominance over males. No submissive signals were observed. The analysis of spatial relations showed that males were more active than females in maintaining proximity and, on average, male spatial movements could be predicted by female location and activities more often than vice versa. These results indicate a spatially central role for the female of each pair. © 1992 Wiley-Liss, Inc.     

Novel hyperprolactinemia and hyperprolactinemic anovulation model using the cynomolgus monkey (Macaca fascicularis)

We investigated the relationship between the menstrual cycle and hormone levels in cynomolgus monkeys, and developed a sulpiride-induced hyperprolactinemic anovulation model. On this study, we demonstrated the usefulness of the commercial human prolactin immunoradiometric assay kit for the measurement of cynomolgus monkey serum samples. In the normal menstrual cycle of the cynomolgus monkey, serum prolactin concentrations were not significantly different between luteal and follicular phases. However, the serum prolactin concentration tended to elevate at the ovulation stage. And serum progesterone began to increase after an estradiol surge, and then declined before the ensuing preovulatory rise in estradiol. During the luteal phase, the serum concentration of progesterone was elevated. Moreover, we aimed to develop an anovulation model, using sulpiride-induced hyperprolactinemia in the cynomolgus monkey. The serum prolactin level gradually increased during the twice-daily administration of sulpiride, and the drug produced as big a response at 5 mg/kg. In this study, the length of the menstrual cycle was approximately 29 days in normal cynomolgus monkeys. When treatment with sulpiride had been continued for more than one month, serum progesterone and estradiol levels fell to within the range seen in the follicular phase of the normal cycle, and the absence of ovulation was recognized by laparoscopy. Moreover, in this period we found that amenorrhea or anovulatory menstruation in the experimental animals. We could produce an anovulatory model induced by sulpiride repeatedly administered over a long time period. Our findings suggest that the cynomolgus monkey is useful as a endocrinological model that uses prolactin as a parameter and as an anovulatory model; thus, it could be a useful model for the hyperprolactinemic amenorrhea and/or anovulation seen in humans.     

Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta)

We recently reported (Michael & Zumpe: American Journal of Primatology 15:157–170, 1988) evidence for the hypothesis that copulations by pairs of rhesus monkeys are linked more closely to the ovulatory phase of the female's menstrual cycle when a male has access to several females in different cycle phases rather than access to females in the same cycle phase. We have now used data from this earlier study to assess the role of female dominance. Artificial menstrual cycles were induced with hormone injections in two of four ovariectomized females in eight social groups (each consisting of one male and four females). The artificial cycles were either synchronized or offset by 7-day increments. There were differences in the behavioral interactions of the higher-ranking (dominant) and lower-ranking (subordinate) hormone-treated females in each group. The amount of male sexual activity received by dominant and subordinate females differed little, but dominant females initiated significantly more sexual activity (P<.0001) than did subordinate females. Dominant females were significantly more aggressive (P<.0001) toward other females and received more direct and redirected aggression from males. Males generally initiated and maintained more social contacts with dominant than with subordinate females, and dominant females were less active than subordinates in initiating and maintaining social interactions with males. The findings provide new evidence for both female mate competition and mate choice by males for higher-ranking females.     

Squirrel monkey dominance and social behavior as related to group size and group structure

Adult male and female squirrel monkeys were tested in nonsocial adaptation and pairwise and triad social situations differing in sex composition. Social behaviors, nonsocial behaviors, and dominance hierarchies were observed during social testing. Dominance hierarchies were similar in groups differing in size and social structure. Nonsocial behaviors decreased in females and submissive animals paired with males or dominant monkeys. Aggressiveness between females decreased and the beginnings of coalitions between females were observed in the presence of a male. The social behavior patterns, but not dominance hierarchies, are consistent with behaviors observed in larger groups of squirrel monkeys.     

Effects of gonadal steroids on agonistic behavior of female Peromyscus leucopus

The role of gonadal hormones in modifying agonistic behavior of female P. leucopus was examined by means of ovariectomy and treatment with estradiol benzoate (EB), progesterone (P), or testosterone propionate (TP). Aggression was lower in diestrous females than in proestrous females, and was eliminated by ovariectomy. Submissive behavior increased following ovariectomy; surgery had no effect on investigative behavior. Administration of EB had no effect on aggressive or submissive behavior, but higher dosages caused an increase in investigative and sexual behavior. Higher dosages of P increased aggression; P had no effect on submissive or investigative behavior. An increase in aggression also resulted from administration of high levels of TP. TP also caused an increase in investigative behavior, and had no effect on submissive behavior. These results may be due to direct effects of the administered hormones on behavior or to indirect effects such as a stimulation of prolactin secretion or alteration of adrenal function.