Serum cortisol concentrations of single-housed and isosexually pair-housed adult rhesus macaques

Possible social distress was evaluated in 20 adult rhesus macaques housed in compatible isosexual pairs (5 female pairs, 5 male pairs) for the purpose of social environmental enrichment. Serum cortisol concentrations of paired animals were compared with serum cortisol concentrations of individually housed adult rhesus macaques of both sexes (5 females, 5 males). In both sexes, cortisol concentrations of paired animals (means 10 females = 19.5 +/- 2.9 micrograms/dl; means 10 males = 17.5 +/- 4.6 micrograms/dl) showed no significant difference (p always greater than 0.1) with those of single animals (means 5 females = 20.5 +/- 2.1 micrograms/dl; means 5 males = 15.9 +/- 2.6 micrograms/dl). Both in male and in female pairs, dominant partners had cortisol concentrations that were equivalent to those of their subordinate counterparts. It was concluded that neither female nor male adult rhesus macaques experience more distress when sharing a cage with a compatible partner of the same sex than when living alone.     

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.     

Mother and peer attachment under conditions of fear in rhesus monkeys (Macaca mulatta)

Attachment behavior of six infant rhesus monkeys was examined in a fear situation under two experimental conditions. When both a familiar agemate and the infant's mother were present in separate cages, the infants spent significantly more time in proximity to their mother than to their agemate. When a caged agemate and an empty cage were present, the infants distributed their time approximately equally between the empty cage and the agemate. Five additional behavioral measures also indicated that the infants did not use their peers as mother substitutes in a fear-arousing situation. These findings supportHarlow's postulate of independence of the infant-mother and agemate affectional systems.     

Evidence for direct inhibitory effects of dopamine on zona glomerulosa secretion of 18-hydroxycorticosterone in rhesus monkeys

This study was designed to more selectively investigate the dopaminergic regulation of 18-hydroxycorticosterone (18-OHB) and aldosterone production by the adrenal zona glomerulosa. Mature rhesus monkeys received either an infusion of dopamine (2 micrograms/kg/min) or 5% dextrose (0.2 ml/min) over a 60 min period (N=6). Dopamine had no effect on plasma levels of renin activity, cortisol, corticosterone, aldosterone or blood pressure. However, dopamine suppressed (p less than 0.05) plasma 18-OHB levels from a baseline of 31.6 +/- 3.5 ng/dl to 23.6 +/- 2.1 ng/dl at 60 min after onset of infusion. This observation is in agreement with some studies in humans but differs from others in which no depression in 18-OHB was observed following dopamine infusion. Dopamine infusion markedly (p less than 0.001) suppressed plasma PRL levels by 30 min after onset of infusion. Corticosteroid responses to metoclopramide (200 micrograms/kg) after dexamethasone 1 mg im every 6 h X 5 days or placebo treatment (vehicle im every 6 h X 5 days) was then evaluated. Dexamethasone significantly suppressed basal cortisol, corticosterone, 18-OHB and aldosterone. Although dexamethasone blunted the prolactin response, it did not inhibit the aldosterone response to metoclopramide. The 18-OHB response to metoclopramide was increased (p less than 0.01) following dexamethasone treatment. Following dexamethasone suppression, 18-OHB levels were still lowered (p less than 0.05) by dopamine infusion. These results suggest that dopamine selectively inhibits zona glomerulosa production of 18-OHB and aldosterone in rhesus monkeys.     

Behavioral responses of unrelated adult male rhesus monkeys familiarized and paired for the purpose of environmental enrichment

An attempt was made to pair ten unrelated, adult male rhesus monkeys that had been kept in single cages for several years. Potential companions were first given the opportunity to establish clear-cut rank relationships (unidirectional fear-grinning and/or withdrawing) during a 5-day period of noncontact familiarization. Only then were they paired in a different double cage. Rank relationships were confirmed within the first 6 minutes after pairing without the occurrence of any biting and fighting. A total of four physical aggressions (slapping) were observed in all five dyads during 5 hours of observations on the first 5 days after pairing. It was concluded that the establishment of clear-cut rank relationships prior to pairing was instrumental in this extremely low incidence of aggression.     

The relationship between maternal rank and companion choice in immature macaques (Macaca mulatta andM. radiata)

Eight bonnet and eight rhesus macaques, ranging from 5–8 months of age, were observed with respect to their choices of companions. These data were then correlated with the dominance ranks of the mothers of the companions involved. Preliminary results showed that the maternal ranks of the rhesus infants were significantly correlated with the maternal ranks of their companions; no such correlation could be demonstrated for the bonnet monkeys. Thus the partner choices of rhesus infants appeared to be more constrained than were those of the bonnets. The results were discussed in relation to the social systems of bonnet and rhesus macaques. Supported in part by faculty research grant D-552, Chancellor's Patent Fund DG #44, and by RR00169 to the California Primate Research Center.     

Time budget of caged rhesus monkeys exposed to a companion,a PVC perch,and a piece of wood for an extended time

The present investigation assesses the percentage of time that rhesus monkeys (Macaca mulatta) are kept occupied by a more complex cage environment. Sixty animals were continuously exposed for at least 1.5 years to a compatible companion for social interaction, a suspended plastic pipe for perching, and a branch segment for gnawing. The behavior of the partners of each pair was recorded for 60 minutes when the animals were not distracted by human activities. Individuals spent an average of 23.5% of the time interacting with the companion, but only 10.4% with the plastic pipe and 4.8% with the branch segment. Differences were statistically significant. Females were socially more active than males. Subadult animals (3.5–4 years) used both inanimate objects significantly more than did adult animals (9–30 years). It was concluded that (1) a compatible companion, a suspended plastic pipe, and a loose branch segment remain effective stimuli for caged rhesus monkeys after more than 1 year of exposure and (2) a compatible companion is of greater stimulatory value–particularly for adults–than are inanimate objects.     

Behavioral responses of unrelated rhesus monkey females paired for the purpose of environmental enrichment

An attempt was made to socialize unrelated and unfamiliar adult rhesus monkey females that had lived in single cages for more than one year. Partners first were given the opportunity for noncontact familiarization in partitioned double cages. They were then transferred into an ordinary double cage. Clear-cut rank relationships were evident within the first 90 minutes of pair formation in 94% (17/18) of dyads tested. Only 28% (5/18) of pairs resorted to fighting (in no case with infliction of serious injury), while 50% (9/18) engaged in social grooming or hugging during this initial phase of pair formation. Eighty-three percent (15/18) of pairs were compatible, with none of the partners showing signs of depression and none inflicting serious injury on the other. Seventeen percent (3/18) of pairs were incompatible (two cases of depression, one serious tail injury) and were separated. It was concluded that the barren environment of singly caged rhesus monkey females can be enriched with little risk by carefully making them compatible companions.     

Food-neophobia in semi-free ranging rhesus macaques: effects of food limitation and food source

This study characterizes food neophobia in semi-free ranging rhesus macaques. In experiment one, monkeys received novel and familiar foods during periods of normal provisioning and when provisioning was suspended. The monkeys did discriminate between novel and familiar foods and continued to exhibit neophobia when provisioning was suspended. In experiment two, food was either tossed to subjects or placed in the habitat so that monkeys discovered food without the observer in close proximity. Rhesus macaques were more likely to eat a novel food that was hand-tossed to them compared to food they discovered in their habitat. This study suggests that food neophobia is a robust trait in rhesus macaques and that a history of provisioning may affect the expression of the trait.     

The influence of day-night cycles and the additive effects of methamphetamine and illumination on the spontaneous activity in rhesus monkeys (Macaca mulatta)

The spontaneous activity of rhesus monkeys in a cage situation was measured under 12 hr. day-night cycles in Exp. I. Without exception, all the subjects (n=10) proved to be more active in the daytime than at night. In Exp. II the effect of methamphetamine upon spontaneous activity was investigated in light and dark conditions. It is supposed in the present study that methamphetamine and illumination raise the arousal level of the subjects and increase their spontaneous activity. The results show that the spontaneous activity of rhesus monkeys, which are thought to be visually dominant, greatly depends on illumination. That is, rhesus monkeys move around well in light conditions but little in dark conditions. Methamphetamine increases spontaneous activity, however, in dark as well as in light conditions. Interaction between methamphetamine and illumination effects was not significant. It would appear from these results that both internal and external factors—methamphetamine and illumination—feed into a common pool of the arousal level which controls spontaneous activity.     

Oxytocin is luteolytic in the rhesus monkey (Macaca mulatta)

Oxytocin (10 mi.u./microliter/h) or vehicle (0.5% chlorobutanol in saline, 1 microliter/h) was chronically infused directly into the corpus luteum of normally cyclic rhesus monkeys, by means of an Alzet pump-ovarian cannula system. Infusion of oxytocin (N = 6) or vehicle (N = 5) began 6 days after the preovulatory oestradiol surge, and daily peripheral blood samples were taken. Oxytocin caused a significant (P less than 0.05) decrease in progesterone, beginning 1 day after treatment, and oestradiol after 4 days; progesterone and oestradiol remained significantly depressed until menstruation. However, peripheral LH concentrations remained unchanged. The duration of the luteal phase, menstrual cycle and the onset of menses from the initiation of oxytocin infusion were significantly (P less than 0.01) shorter when compared to those of vehicle-treated controls. These results show that oxytocin can induce functional luteolysis in the primate and supports the hypothesis that oxytocin of luteal origin may play a role in spontaneous luteolysis.     

Intraluteal infusions of prostaglandins of the E, D, I, and A series prevent PGF2 alpha-induced, but not spontaneous, luteal regression in rhesus monkeys

A luteotropic role for prostaglandins (PGs) during the luteal phase of the menstrual cycle of rhesus monkeys was suggested by the observation that intraluteal infusion of a PG synthesis inhibitor caused premature luteolysis. This study was designed to identify PGs that promote luteal function in primates. First, the effects of various PGs on progesterone (P) production by macaque luteal cells were examined in vitro. Collagenase-dispersed luteal cells from midluteal phase of the menstrual cycle (Day 6-7 after the estimated surge of LH, n = 3) were incubated with 0-5,000 ng/ml PGE2, PGD, 6 beta PGI1 (a stable analogue of PGI2), PGA2, or PGF2 alpha alone or with hCG (100 ng/ml). PGE2, PGD2, and 6 beta PGI1 alone stimulated (p less than 0.05) P production to a similar extent (2- to 3-fold over basal) as hCG alone, whereas PGA2 and PGF2 alpha alone had no effect on P production. Stimulation (p less than 0.05) of P synthesis by PGE2, PGD2, and 6 beta PGI1 in combination with hCG was similar to that of hCG alone. Whereas PGA2 inhibited gonadotropin-induced P production (p less than 0.05), that in the presence of PGF2 alpha plus hCG tended (p = 0.05) to remain elevated. Second, the effects of various PGs on P production during chronic infusion into the CL were studied in vivo. Saline with or without 0.1% BSA (n = 12), PGE2 (300 ng/h; n = 4), PGD2 (300 ng/h; n = 4), 6 beta PGI1 (500 ng/h; n = 3), PGA2 (300 ng/h; n = 4), or PGF2 alpha (10 ng/h; n = 8) was infused via osmotic minipump beginning at midluteal phase (Days 5-8 after the estimated LH surge) until menses. In addition, the same dose of PGE, PGD, PGI, or PGA was infused in combination with PGF2 alpha (n = 3-4/group) for 7 days. P levels over 5 days preceding treatment were not different among groups. In 5 of 8 monkeys receiving PGF2 alpha alone, P declined to less than 0.5 ng/ml within 72 h after initiation of infusion and was lower (p less than 0.05) than controls. The length of the luteal phase in PGF2 alpha-infused monkeys was shortened (12.3 +/- 0.9 days; mean +/- SEM, n = 8; p less than 0.05) compared to controls (15.8 +/- 0.5). Intraluteal infusion of PGE, PGD, PGI, or PGA alone did not affect patterns of circulating P or luteal phase length.(ABSTRACT TRUNCATED AT 400 WORDS)     

A review of sexual initiating behavior by male and female cynomolgus monkeys and some species comparisons

The sexual initiating behavior of male and female cynomolgus monkeys (Macaca fascicularis) observed during standard laboratory tests is reviewed and compared with that of rhesus monkeys (M. mulatta) observed under identical conditions. Species differences in sexual behavior are related here to differences in habitat, sexual dimorphism, and the dominance gradient between the sexes. Compared with rhesus monkeys, cynomolgus monkeys appear to be more arboreal, less sexually dimorphic, and have a smaller dominance gradient between the sexes. They exhibit a facultative single-mount copulatory pattern rather than the serial mount pattern of the rhesus monkey. Female cynomolgus monkeys are less dominated than rhesus females by their male partners. Direct aggression between mates is more frequent and redirected aggression occurs less often than in rhesus monkeys. These behavioral differences affect the interpretation of changes in initiation rates that occur (1) during the menstrual cycle, (2) when females are ovariectomized and given hormone replacement treatments, and (3) when males are castrated and treated with androgens. We conclude that estradiol in the female and testosterone in the male increase the sexual motivation of both the treated and the untreated partner. Valid interpretations of changes in initiation rates depend on accurate and exclusive definitions of behavior and on a consideration of the behavioral context in which they are made.     

Thymic regulation of primate fetal ovarian-adrenal differentiation

We report that fetal thymectomy inhibits oogenesis and induces abnormal ovarian differentiation in rhesus monkeys. In utero thymectomy (n = 5) elevated plasma follicle-stimulating hormone (7.8 +/- 1.1 microgram/ml vs. 4.2 +/- 0.5 microgram/ml; P less than 0.05) and decreased plasma prolactin (24.5 +/- 3.3 ng/ml vs. 76.3 +/- 11.2 ng/ml; P less than 0.05) concentrations compared with intact controls (n = 12), but did not change plasma luteinizing hormone, estradiol, cortisol, dehydroepiandrosterone sulfate, or thymosin-alpha 1 concentrations. In utero thymectomy reduced the weight of neonatal ovaries and adrenal glands, but not hepatic, renal, splenic, or total body weights. After fetal thymectomy, newborn ovaries (n = 8) contained a reduced total number of germ cells (123,926 +/- 11,651 vs. 432,034 +/- 40,311; P less than 0.001). The percentages of individual germ cell types were similar between thymectomized and intact groups (n = 11) except for an increased percentage of preantral-antral follicles in the thymectomy group (P less than 0.01). Our results indicate that the primate fetal thymus regulates antenatal ovarian follicular development, perhaps by interactions between the nascent immunologic and pituitary-ovarian systems.     

Interplay between various aspects in social relationships of young rhesus monkeys: Dominance,agonistic help,and affiliation

Relationships between group-living primates depend strongly on their position in the group dominance hierarchy and on their relationships with other group members. The influence of various behaviours on social relationships of immature rhesus monkeys (Macaca mulatta) was investigated here. Dominance ranks were established and related to the degree of affiliation in a dyad. Older monkeys were mostly dominant to the younger ones, regardless of kinship. Subordinate monkeys left proximity of their dominant members more often than they were left by them both among siblings and non-siblings, but the effect of dominance rank on the amount of play initiation and grooming in a dyad differed between these two types of dyads. The amount of agonistic help two individuals provided for each other was low among immatures. Nevertheless, pairs of siblings gave help to each other in agonistic conflicts more often than non-siblings, and such help was more often reciprocated between siblings than between non-siblings. Help in agonistic conflicts was positively correlated with the amount of time monkeys spent playing, grooming, or in proximity. Adults tended to interfere less in conflicts of frequent sibling play partners or non-sibling grooming partners. No evidence was found for young monkeys to exchange reciprocally grooming for agonistic help. It is argued that the time monkeys spend interacting with each other in affiliative interactions increases their familiarity and thus promotes close relationships between them. On the whole, young monkeys' relationships, like those between adults, are influenced strongly by their kinship, and position in the dominance hierarchy.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Sexual preferences during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta)

Eight groups of rhesus monkeys each consisting of one male and four ovariectomized females were observed while two of the females were treated with hormones to produce artificial menstrual cycles. These were either synchronized or offset by 7-day increments. Sexually preferred females, defined by the numbers of ejaculations per test, received almost twice as many ejaculations as did non-preferred females during all synchronized and offset cycles and during all cycle phases. However, short-term changes in partner preference occurred when the midcycle phase of non-preferred females coincided with the middle or late progesterone phase of preferred females, suggesting a negative effect of progesterone on behavior during the menstrual cycle. There were highly significant differences between preferred and non-preferred partners for almost all of their sexual and social interactions, and preferred partners showed longer proximity and grooming times as well as higher levels of sexual activity. Partner preferences accounted for more of the behavioral variance between pairs than did female dominance, although males sought the proximity of dominant females independently of their partner preferences. Thus, in a setting uncomplicated by male mate competition, sexual preference by male rhesus monkeys is a robust phenomenon depending on complex interactions between dominance, hormonal status, and the individual behavior of female partners.     

Effect of age and breeding season on the developmental capacity of oocytes from unstimulated and follicle-stimulating hormone-stimulated rhesus monkeys

Effects of age and season on the developmental capacity of oocytes from unstimulated and FSH-stimulated rhesus monkeys were examined. Immature cumulus-oocyte complexes were matured in vitro in modified CMRL-1066 medium containing 20% bovine calf serum and subjected to in vitro fertilization followed by embryo culture. After fertilization, ova from unstimulated prepubertal monkeys displayed lower development to morula (4%) than those from unstimulated adult females (18% in breeding season and 22% in nonbreeding season). No developmental difference was found between ova from unstimulated adult monkeys in breeding and nonbreeding seasons. However, ova from FSH-primed prepubertal monkeys displayed greater development to blastocyst stage (54%) than those from adult monkeys in the breeding season (16%) and nonbreeding season (0%); and ova from FSH-primed adult females in the breeding season had significantly (P < 0.05) greater developmental competence than those obtained in the nonbreeding season (> or = morula stage, 54% vs. 3%; blastocyst stage, 16% vs. 0%). These data indicate that 1) rhesus monkey oocytes acquire developmental competence in a donor age-dependent manner, and 2) animal age and breeding season modulate the effect of FSH on oocyte developmental competence in the rhesus monkey.     

In vitro maturation of ovarian oocytes from unstimulated rhesus monkeys: assessment of cytoplasmic maturity by embryonic development after in vitro fertilization

One-hundred and sixty-six cumulus-enclosed oocytes, obtained from ovaries of unstimulated rhesus monkeys, were subjected to six different treatments in vitro--two types of media (simple = TALP; complex = CMRL) x three levels of gonadotropins (none, FSH, FSH + hCG)--to assess their ability to undergo maturation, fertilization, and embryo development. A summary of development in culture for all experimental treatments is as follows: 58% of oocytes underwent germinal vesicle breakdown; 37% extruded a first polar body; 17% had more than one pronucleus and/or two polar bodies after insemination (i.e., were activated/fertilized); and 12% cleaved (i.e., developed) to at least the 2-cell stage in vitro. Of 45 oocytes incubated only in medium (either simple or complex) without gonadotropins, only 3 were activated/fertilized (6.7%), and only one embryo developed to at least the 2-4-cell stage (2.2%). There were no differences between oocytes incubated with only FSH and oocytes incubated with FSH + hCG. Activation/fertilization (20.7% vs. 6.7%) and embryo development (greater than or equal to 2 cells; 15.7% vs. 2.2%) were significantly higher in treatments with than without gonadotropin supplementation. There were no statistically significant differences attributable to incubation in different media during oocyte maturation. Cumulus-enclosed oocytes recovered from unstimulated ovaries of rhesus monkeys can resume maturation during culture in vitro, as shown by their ability to be fertilized and by the cleavage in vitro of the resultant zygotes.     

Corpus luteum function during the early postpartum interval in lactating rhesus monkeys: in vivo and in vitro response to exogenous gonadotropin.

The response of the postpartum corpus luteum to exogenous gonadotropin was studied in 12 lactating rhesus monkeys given daily injections of either human chorionic gonadotropin (HCG, n = 6) or saline (control, n = 6) for 4 days immediately following parturition. Peripheral blood samples were collected daily. On the 5th day postpartum, luteectomy was performed progesterone production by dispersed luteal cells was examined. Whereas progesterone in the peripheral circulation of control monkeys progressively declined between days 1 and 5 postpartum, progesterone levels increased significantly (p less than 0.025) with the onset of HCG treatment and remained significantly (p less than 0.025) elevated above the controls throughout the period of HCG treatment. However, despite the daily administration of HCG, circulating progesterone levels declined (p less than 0.05) between days 3 and 5 postpartum. The weight of the corpus luteum excised from HCG-treated macaques was significantly (p less than 0.005) greater than that of the controls. Dispersed cells from corpora lutea of saline-treated monkeys produced progesterone in vitro under control conditions (nutrient medium alone) and responded to the addition of high (100 ng/ml), but not low (1 ng/ml), levels of HCG with increased steroidogenesis. Although luteal cells from HCG-treated macaques tended to produce more progesterone in vitro than cells from control monkeys, they also exhibited a 50-fold reduction in sensitivity to HCG in vitro. These data suggest that the corpus luteum of lactating postpartum rhesus monkeys exhibited steroidogenic function which was stimulated by exogenous gonadotropin. However, prolonged exposure of the corpus luteum to high levels of exogenous gonadotropin appeared to produce a state of refractoriness to additional gonadotropic stimuli.