Seasonal breeding in rhesus monkeys: Influence of the behavioral environment

The accepted model of breeding seasonality in rhesus monkeys states that females become reproductively active in response to an environmental cue and that males become sexually active in response to ovulating females. This model must be modified to include direct responses of the male to the physical environment, endocrine responses of males to sexual activity, and responses of the female to the sexual activation of fellow group members. The complex set of social stimuli that influences the breeding readiness of both sexes may serve to delimit more precisely the annual periods of conception and birth than would be the case if each individual responded only to the changing physical environment.     

Hormonal response to restraint in rhesus monkeys

Abstract: The purpose of this study was to characterize the hormonal responses to a restraining system in four adult male rhesus monkeys (Macaca mulatta) in preparation for a spaceflight project. After the monkeys were accustomed to food and water (Phase I), blood-volume-regulating hormones were measured during three phases: 10 days in a metabolic cage (Phase II), 16 days sitting in a restrained position in a specially designed metabolism chair (Phase III) and 10 days in metabolic cage (Phase IV). An increase of active renin (30%) and vasopressin (25%) was observed at the end of Phase III. A decrease of atrial natriuretic peptide (ANP), urodilatin, and sodium excretion occurred during the first days of Phase III. Catecholamines were unchanged. A dramatic increase (tenfold) in urinary excretion of growth hormone occurred during all of Phase III and at the beginning of Phase IV. These findings are similar to those found in man during isolation inactivity and during confinement stress.     

Social context affects how rhesus monkeys explore their environment

This study reports on social modulation of exploratory behavior and response to novelty by members of a captive rhesus monkey colony. The group was trained to split in half, with one subgroup composed of dominant members only, the other of subordinates. The animals were then presented the same initially novel stimuli (i.e., sand-filled metal boxes containing hidden food items) in two social contexts differing in hierarchical composition. In a combined context, all group members (i.e., both subgroups together) were simultaneously presented the stimuli. In a split context, only members of the top or bottom half of the group (i.e., each subgroup in turn) was independently presented the stimuli. Subordinates responded similarly to dominant animals in the combined context but differently in the split context, where they were far more hesitant. Rank-related differences were evident in the way animals used their home compound and in their approach and responsiveness toward the stimuli. These findings show that social context influences how animals explore novel situations, possibly reflecting different social roles or status effects on the perception of social structure. Also, despite the complexity of primate social relationships, the separation technique produced no permanent or adverse effects on the social integrity of the group. This study shows that manipulating the social environment through separation training can be a powerful tool for assessing contextual influences on behavior. Am. J. Primatol. 44:205–214, 1998. © 1998 Wiley-Liss, Inc.     

肾脏和肾神经在应激、钠盐所致高血压中的作用

本工作采用电生理、生化、放免、电镜等方法,探讨了慢性应激和盐致高血压大鼠交感神经系统和肾脏功能的改变。实验在雄性ＳＤ大鼠上进行。结果表明：（１）高盐大鼠肾血浆流量（ＲＰＦ）和尿钠排泄明显增加,而应激大鼠ＲＰＦ显著下降。（２）电镜显示高盐大鼠近曲和远曲小管上皮细胞及线粒体变大,应激则使细胞萎缩、线粒体变小。（３）高盐大鼠肾皮质ＮａＫＡＴＰ酶活性下降,应激可使其恢复。（４）频谱分析显示应激大鼠低频波动（０２～０９Ｈｚ）明显增加。（５）应激导致大鼠肾素活性（ＰＲＡ）及血管紧张素Ⅱ（ＡＮＧⅡ）水平升高,并能使高盐大鼠低ＰＲＡ和ＡＮＧⅡ水平升高。（６）大鼠去除双侧肾神经后,应激无法造成血压升高、ＲＰＦ下降和ＰＲＡ、ＡＮＧⅡ上升。上述结果提示：肾交感神经系统兴奋性增加介导的肾脏机制,可能在应激和／或盐致高血压发病过程中具有重要作用。     

Further characterization of the G blood group system of rhesus monkeys

We describe a new antiserum that has the unique ability to distinguish homozygous from heterozygous genotypes in the G blood group system of rhesus monkeys. With this new typing serum (reagent), all 10 possible genotypes in this system can be distinguished and the utility of blood typing for genetic studies has been greatly increased.     

Social enrichment of the environment with infants for singly caged adult rhesus monkeys

The practicability of social enrichment for singly caged adult rhesus monkeys was examined. Twenty-nine weaned rhesus monkey infants were removed from breeding troops to avoid overcrowding and were placed with unfamiliar singly caged adults. An adult-infant pair was considered compatible when (1) the two animals started huddling with each other within the first 5 days after pair formation and (2) the infant showed no signs of depression and took its share from a limited amount of favored food. Adult-infant pairs were compatible in 90% (26/29) of cases. Compatibility depended neither on the sex, age, and origin of the adult nor on the sex of the infant. There was no evidence that partners lost interest in each other during 7–11 months of follow-up observations. Three adults exhibiting stereotypical behavior abandoned their peculiar habits after they had lived with their young companions for 4 months. It was concluded that the often-heard notion that rhesus monkeys are highly aggressive should not prevent simple attempts to provide singly caged animals with a companion.     

Some observations on psychosocial stressors,immunity, and individual differences in nonhuman primates

Many studies would appear to support an important relationship between behavior and the regulation of the immune response, at the core of the developing field of psychoneuroimmunology (PNI). However, wide variations are noted in the strength of this relationship, even for the same species under very similar circumstances. The present paper reviews work from our laboratory in both young and adult pigtail and bonnet macaques describing the ranges of variability in both behavioral and immunological responses to social separation and social conflict. It is shown that the magnitude of immune changes that follow a social stressor often covary with the magnitude of the behavioral changes that are observed. Second, there is support for the observation that there are specific behaviors such as social affiliation that may mitigate untoward behavioral and immunological consequences of social stressors. Finally, studies are reviewed which suggest that assessment of autonomic reactivity as reflected in cardiovascular regulation might provide an important clue to the relative risk for immune modulation under challenge. © 1996 Wiley-Liss, Inc.     

Atretogenic action of estrogen in rhesus monkeys: Effects of repeated treatment

The effects of 17β-estradiol (E₂), administered in Silastic capsules for 24 hours at intervals of 10 or 14 days, on follicular development and menstrual cycle characteristics were studied in 13 rhesus monkeys. In seven monkeys receiving E₂ at l0-day intervals for 50 treatment periods, new follicles frequently developed between treatments but usually regressed. In seven instances, the follicles persisted longer than expected but were steroidogenically suppressed and regressed spontaneously. Ovulation occurred in only two instances. In six monkeys receiving E₂ at 14-day intervals, new follicles developed regularly, with seven ovulations occurring in 37 treatment periods. A persistent anovulatory follicle was noted in only one instance. Menstruation occurred with equal frequency, and the interval from treatment to onset of menstruation was not significantly different regardless of treatment or the occurrence of ovulation; the intervals between menstruation approximated those of normal menstrual cycles. In general, following termination of treatment, menstrual cycles returned to normal quickly. These data indicate that E₂ administered intermittently at 10-day intervals effectively suppresses ovulation, and they provide new insight into the actions of E₂ on folliculogenesis in primates.     

Extinction of rhesus monkeys (Macaca mulatto) in Xinglung,North China

An isolated population of rhesus monkeys living in Xinglung County, north of Beijing (latitude 40⪤gree N), was a natural population at the northernmost range of the species in Asia. Rhesus had been reported there at the end of the last century, based on a few specimens, but were not well known by zoologists until the beginning of the 1960s. The population remained approximately 50–60 individuals in the 1960s but then declined to only 4 or 5 monkeys about 5 years ago. It has been confirmed by local hunters and two recent field trips that the population is now probably extinct. As a result, the northern extent of the remaining natural range of the rhesus macaque in Asia has dropped 650 km southward to the Jiyuan Nature Reserve on the border of Hunan and Shanxi provinces, just north of the Yellow River.     

Early agonistic experience and rank acquisition among free-ranging infant rhesus monkeys

Several aspects of agonistic experience are described for freeranging infant rhesus monkeys (Macaca mulatta)on Cayo Santiago. Even before infants are fully integrated with peers in rank dominance based on maternal ranks,infants of highranking mothers tend to be threatened less frequently by other members of the group and are less likely to be threatened by unfamiliar individuals than are infants of lowranking mothers. There is no evidence that fearful interactions between pairs of infants are related to their mother’s ranks before 22 weeks of age. However, an imperfect hierarchy can be constructed for infants between 27 and 30 weeks of age. At this age,infants of higherranking mothers are also more likely to receive protection when threatened than are infants of lowerranking mothers. When protected, their protectors are less likely to emit fearful gestures to the infants’ threatener. Close female relatives appear to play a large role in the protection of infants and may be more directly responsible for the differences described above than the mother, other relatives, or other highranking members of the group. It is suggested that more than one mechanism, including intervention by the mother and by close female relatives,may be important in rank acquisition among peers.     

The influence of behavioral context and social characteristics on the physical aspects of social grooming in rhesus monkeys

The extent to which dominance status and sex can influence the physical act of grooming was examined in two groups of rhesus monkeys. Both the sex and the dominance status of the groomee, but not of the groomer, were found to affect the body sites groomed and the positions assumed by the animals during the grooming bout. Females were groomed more on the back and head and less on the tail, rump, upper leg, and lower arm than males. Females with infants tended to face away from the groomer. Higher-ranking groomees were groomed more on the tail and rump and less on the upper leg and back than lower-ranking groomees. Higher-ranking groomees spent more time lying down during grooming than lower-ranking groomees, while lower-ranking groomees faced away from the groomer more then higher-ranking groomees. The behavioral interactions just prior to and immediately after grooming were also recorded. Although the onset of grooming was preceded by social interactions between the partners, the end of grooming was followed by a complete break in interactions. Particular types of social signals displayed by the groomee just prior to grooming were highly correlated with the grooming of specific body sites. These results suggest that the groomee controls the behavior of the groomer by the social signals it displays and the positions it maintains during the grooming bout. Thus, the grooming act itself may play an important role in the social relationships between group members.     

Effects of social reorganization on cellular immunity in male cynomolgus monkeys

Exposure to acute stressors has been shown to impair cellular immunity in human beings and other animal species. Comparatively little is known, however, about the effects of long-term stressors on immune function and how individual behavioral characteristics may mediate differences in immune function and clinical disease susceptibility. To determine the effects of social stress on cellular immunity and reactivation of a latent herpesvirus, 20 Herpes B virus-positive male cynomolgus monkeys were exposed to four periodic reorganizations of social group memberships over 5 months. Observations were made to categorize individuals as high or low in expression of aggressive, fearful, and affiliative behaviors. Complete blood counts, lymphocyte proliferation tests, and natural killer cell cytotoxicity assays were performed immediately before and 4 days after reorganizations. Herpesvirus-specific immunoglobulin G antibody levels were measured, and oral and conjunctival swabs were cultured for virus. Reorganization was associated with increased lymphocyte counts (P = 0.0009) and decreased lymphocyte proliferation in response to phytohemagglutinin (P < 0.005), particularly among monkeys showing high levels of fear (P = 0.0137). High-aggressive monkeys showed lower baseline natural killer cell activity (P = 0.0013) and higher lymphocyte counts (P = 0.013) than low-aggressive monkeys. Herpesvirus antibody titers decreased over time (P < 0.004) and no positive virus cultures were obtained. Measures of cellular immunity and behavior were unrelated to virus-specific antibody titers. These results suggest that repeated exposure to a social stressor alters several measures of cellular immunity, and that some of these changes may be predicted by individual differences in agonistic behavior. In contrast to human studies, the results suggest that some psychological stressors may not cause reactivation of a common herpesvirus in this species. © 1996 Wiley-Liss, Inc.     

Breeding-season relationships of immature male rhesus monkeys with females. I. Individual differences and constraints on partner choice

Several aspects of breeding-season relationships with mature females are described for free-ranging immature male rhesus monkeys (Macaca mulatta)on Cayo Santiago. At puberty, immature males are still groomed by mature females, as they were as infants, but no longer receive active protection from females other than their mothers. A further, potentially beneficial, aspect of their associations with females lies in the opportunities to observe closely the tactical social and sexual interactions of receptive females with adult males. However, immature males themselves rarely copulate with females. Developmental constraints may explain the finding that most females observed by immature males were relatives but that high-ranking males showed a particular preference for adolescent relatives, whereas the preference of low-ranking males was for adult relatives. A further finding was that while there was a tendency for immature males to devote a greater proportion of their total observation time to females that ranked above their mothers than to those of inferior rank, these were also the females from which males received the most aggression, while most of the females with which the males groomed or copulated were lower ranking than the males’ mothers. Of three hypotheses concerning three possible types of social constraint which might account for such a finding, the data supported only one—that particular levels of aggression within these relationships are compatible only with certain other elements (observations), and not with others (grooming, copulation).     

Infant-directed behavior in young rhesus monkeys: Sex differences and effects of prenatal androgens

Young (3–4 years old) laboratory-reared rhesus monkeys were observed in five 15-minute tests with 1–15-day-old infants. Males and females were equally likely to investigate infants. Females communicated more with infants by grin-lipsmacking and gurgling–-gestures that were not shown by any males. More females presented the ventrum to infants than did males. Females contacted infants more than did males by grooming, crouching over, and having full body contact with them. To see whether prenatal androgens produced the male pattern of response, we conducted similar tests with pseudohermaphrodites (prenatally androgenized genetic females) and neonatally castrated males. On most sexually dimorphic behaviors, pseudohermaphrodites behaved more like females than like males. Castrated males, like females and pseudohermaphrodites, crouched over infants more than did intact males. Castrated males differed from females only on one infant-directed response, the grin-lipsmack. These comparisons showed that defeminization of the repertoire of infant-directed responses was measurable only in intact males. We conclude accordingly that prenatal androgens alone are not responsible for defeminization of this repertoire and that a contribution from postnatal androgens is likely to be necessary.     

安徽恒河猴的微生物学和寄生虫学检测

对安徽省实验猕猴中心的安徽恒河猴进行了微生物（包括病毒和病原菌）和寄生虫检测。对恒河猴的病毒检测结果发现,猕猴疱疹病毒1型（BV）和猴痘病毒（SPV）抗体的阳性率分别为20．7％（6／29）和10．0％（2／20）,20只恒河猴中没有发现猴反转录D型病毒（SRV）、猴免疫缺陷病毒（SIV）和猴T细胞趋向性病毒Ⅰ型（STLV—1）的抗体。5只受检的人工繁育的安徽恒河猴没有感染沙门菌、皮肤病原真菌、志贺菌和结核分枝杆菌的这四种病原菌。肉眼检测恒河猴体表,未发现体外寄生虫。39份人工繁殖的恒河猴粪便样品的总寄生虫感染率为38．5％,检测到溶组织内阿米巴和5种蠕虫（粪类圆线虫、猴结节线虫、绦虫、钩虫、蛔虫）,感染率最高的是粪类圆线虫和猴结节线虫。本次调查表明,安徽恒河猴无特殊疾病,健康状况基本良好,可以建立普通级的实验恒河猴,实现安徽恒河猴的实验动物化。     

Water metabolic parameter changes in rhesus monkeys during exposure to prolonged restriction of motor activity

The objective of this investigation was to determine the effect of prolonged restriction of motor activity (hypokinesia [HK]) on several parameters of water metabolism in primates. The studies were performed on 12 rhesus monkeys aged 4–5 yr (5.10–6.85 kg) during the hypokinetic period of 90 d and during the prehypokinetic period of 30 d. They were divided into two equal groups: the first group was placed under ordinary vivarium conditions (vivarium control animals) and the second group was subjected to 90 d of HK (hypokinetic animals). For the simulation of the hypokinetic effect, the primates were immobilized on their abdomens in special tables. The legs of the monkeys were immobilized with hip and knee joints extended. The primates retained freedom of movement at elbow, wrist, and ankle. During the preexperimental period of 30 d and during the experimental period of 90 d, the following variables were determined: body weight, total body fluid content, specific total body fluid, mean fluid consumed and eliminated in urine, specific plasma resistance, hematocrit level, and plasma concentrations of sodium (Na) and potassium (K). In the hypokinetic primates, body weight decreased significantly when compared to the controls. Mean fluid intake, total body fluid, and specific total body fluid decreased, whereas mean daily fluid loss and specific mean daily fluid elimination increased significantly. Specific plasma resistance, hematocrit level, and plasma electrolyte concentrations increased significantly when compared to the control primates. It was concluded that prolonged restriction of motor activity induces significant changes in water metabolic parameters of primates leading in decreased total water content of the body.     

Baroreflex sensitivity in obesity: relationship with cardiac autonomic nervous system activity

Objective: The aim of this study was to test the hypothesis that baroreflex sensitivity (BRS), assessed by indirect measurement of aortic pressure, is blunted in obesity. Additionally, the potential effect of cardiac autonomic nervous system (ANS) activity, aortic compliance, and metabolic parameters on BRS of obese subjects was investigated. Research Methods and Procedures: A group of 30 women with BMI >30 kg/m² and a group of 30 controls with BMI <25 kg/m² were examined. BRS was estimated by the sequence technique, cardiac ANS activity by short‐term spectral analysis of heart rate variability (HRV), and aortic compliance by the method of applanation tonometry. Results: BRS was lower in obese women (9.18 ± 3.77 vs. 19.63 ± 9.16 ms/mm Hg, p < 0.001). The median values (interquartile range) of the power of both the high‐frequency and low‐frequency components of the HRV were higher in the lean than in the obese participants [1079.2 (202.7 to 1716.9) vs. 224.1 (72.7 to 539.6) msec², p = 0.001 and 411.8 (199.3 to 798.0) vs. 235.8 (99.4 to 424.5) msec², p = 0.01 respectively]. Low‐to‐high‐frequency ratio values were higher in the obese subjects [0.82 (0.47 to 2.1) vs. 0.57 (0.28 to 0.89), p = 0.02]. Aortic augmentation values were not significantly different between lean and obese subjects. Multivariate analysis demonstrated a significant and independent association between BRS and age (p = 0.003), BMI (p < 0.001), and high‐frequency power of HRV (p < 0.001). These variables explained 72% of the variation of BRS values. Discussion: BRS is severely reduced in obese subjects. BMI, age, and the parasympathetic nervous system activity are the main determinants of BRS. Baroreflex behavior is of clinical relevance because an attenuated BRS represents a negative prognostic factor in cardiovascular diseases, which are common in obesity.     

Ontogeny and stability of separation and threat-induced defensive behaviors in rhesus monkeys during the first year of life

Twenty-six rhesus monkeys were tested repeatedly at 4, 8, and 12 months of age to characterize the expression and development of their defensive responses induced by separation from their mothers and exposure to a potential threat. Results demonstrated that by 4 months of age infant monkeys engaged in adult-like context-dependent responses and adaptively regulated these responses in relation to the changing context. When separated from their mothers and alone, infants at 4 months of age were active and emitted frequent coo vocalizations. However, when exposed to the profile of a human face, infants responded by becoming behaviorally inhibited and freezing. At 8 months of age, a dramatic reduction in infants' separation-induced coos was observed, whereas their duration of threat-induced freezing remained unchanged. At 12 months of age, a further decrease in cooing occurred, while freezing duration was maintained. No sex differences were found in the expression of these behaviors or their developmental patterns. Individual differences in separation-induced cooing and threat-induced freezing were apparent and remained stable over the three ages studied. However, within animals no relation was found between individual differences in cooing and freezing. These data demonstrate important differences in the developmental patterns for the expression of cooing and freezing over the first year of life. Marked individual differences in separation-induced cooing and threat-induced freezing were apparent and remained stable from 4–12 months of age. The data support the hypothesis that these different defensive responses reflect different adaptive responses that likely have different underlying mechanisms. The similarities between these defensive responses in rhesus monkeys and humans suggests that understanding the factors that promote the development of individual differences in monkeys will illuminate important factors that promote individual differences in humans. Am. J. Primatol. 44:125–135, 1998. ©1998 Wiley-Liss, Inc.     

Seasonal rank changes for adolescent and subadult natal males in a free-ranging group of rhesus monkeys

Changes in dominance rank for adolescent and subadult natal males in a semi-free-ranging rhesus macaque group were seasonal. Three 4-year-old natal males of the highest-ranking matriline occupied high ranks in the adult male dominance hierarchy during the premating period. In the mating season they dropped in rank, and this decrement was related to a concomitant drop in their alliances. After the mating season, these males rose in rank along with their two 3-year-old kin to occupy ranks 2–5 and 7–8 in the adult male dominance hierarchy. Three-year-old natal males of matrilines lower ranking than first did not become integrated into the hierarchy at this time.