Reproductive performance in capture-acclimated female rhesus monkeys (Macaca mulatta)

Behavioral and physiological data were collected over a three-year period on a colony of compound-housed rhesus monkeys (Macaca mulatta) to examine endocrine influences on sexual behavior. The reproductive performance of the experimental animals was compared to controls which were not routinely handled. The groups did not differ significantly with regard to the percentage of conceptions or other parameters of reproductive biology. The demonstration that manipulations attendant to data collection did not jeopardize reproductive success has important implications for research on primate colonies which are maintained primarily for breeding purposes. Additionally, female copulatory behavior was found to be a reliable indicator of ovulation which allows for an accurate prediction of the parturition date.     

Physical activity of adult female rhesus monkeys (Macaca mulatta) across the menstrual cycle

Physical activity is an important physiological variable impacting on a number of systems in the body. In rodents and several species of domestic animals, levels of physical activity have been reported to vary across the estrous cycle; however, it is unclear whether such changes in activity occur in women and other primates across the menstrual cycle. To determine whether significant changes in activity occur over the menstrual cycle, we continuously measured physical activity in seven adult female rhesus monkeys by accelerometry over the course of one menstrual cycle. Monkeys were checked daily for menses, and daily blood samples were collected for measurement of reproductive hormones. All monkeys displayed ovulatory menstrual cycles, ranging from 23 to 31 days in length. There was a significant increase in estradiol from the early follicular phase to the day of ovulation (F(1.005,5.023) = 40.060, P = 0.001). However, there was no significant change in physical activity across the menstrual cycle (F(2,12) = 0.225, P = 0.802), with activity levels being similar in the early follicular phase, on the day of the preovulatory rise in estradiol and during the midluteal phase. Moreover, the physical activity of these monkeys was not outside the range of physical activity that we measured in 15 ovariectomized monkeys. We conclude that, in primates, physical activity does not change across the menstrual cycle and is not influenced by physiological changes in circulating estradiol. This finding will allow investigators to record physical activity in female primates without the concern of controlling for the phase of the menstrual cycle.     

Psychological well-being in paired adult female rhesus (Macaca mulatta)

We assessed the effects of social living (pairing) on improving the psychological well-being of adult female rhesus macaques (Mucuca mulutta) housed under laboratory conditions. We measured well-being in 12 pairs and 12 singly housed females through multiple indices of health (hematology, clinical morbidity, and body weight), stress (immune responses), behavior (preferences for social proximity, exhibition of species typical affliative behavior, and rates of abnormal behavior), and reproduction (frequency of ovulation, rates of conception, and infant survival). We selected adult females that had been living in single-unit cages and paired them in larger cages. Care was taken to allow females to become familiar with one another before pairing took place, and pairs that fought were separated before serious injuries occurred. Singly-housed control females were also paired for 1 week and then separated to balance the stressful effects expected to occur during the initial pairing and to assure that they were equivalent to the experimental animals in their ability to live socially. We concluded that pairing adult female rhesus monkeys was a positive experience for both the dominant and subordinate members of the pairs. They chose to spend the majority of their time involved in amicable social interactions, were more active, and they indulged in less nail biting than singly-housed controls. There were no differences in reproduction, rates of clinical morbidity, or immune stress responses among the groups. However, pairing alone may not be sufficient to assure the well-being of laboratory-housed rhesus macaques, because rates of abnormal behaviors such as stereotyped movements remained high. © 1994 Wiley-Liss, Inc.     

Parturition in rhesus monkeys (Macaca mulatta)

During five years of birth season fieldwork, we observed two births and three peri-birth instances of behavior of free-ranging rhesus living in Kathmandu, Nepal. These constitute the first two recorded free-ranging rhesus births, and we compare them to the behavior which has been observed in captivity and expected in the wild. The free-ranging parturition behavior was characterized by a general lack of contact with other troop members and by overall inconspicuousness. In the first birth we observed, the troop moved about 70 m up the hill, leaving the laboring female behind on an open hillside. Two males, a female and a juvenile returned and rested about 20 m from the delivering female. During the second delivery, the female stayed with the troop and seemed to participate normally in most troop interactions, although she avoided physical contact with other troop members. We propose that this near-normal behavior may help to assure successful parturition by allowing the female the needed social isolation and inconspicuousness without any loss of troop protection. It may also partly explain why births have not been observed during previous studies. Observations of rhesus parturition behavior reported from studies of captive monkeys and reports from other free-ranging primate studies are compared with our data.     

Effects of androgen administration on sexual invitations by female rhesus monkeys (Macaca mulatta).

Pairs of adult rhesus monkeys of opposite sexes (12 pairs) were studied during 1-h mating tests (986 tests). Ovariectomized females received 5 microgram oestradiol intravaginally throughout to keep them attractive to males and maintain a relatively constant level of male sexual activity. Females were given subcutaneous silastic implants of testosterone to change their sexual receptivity. A threefold change in sexual invitations resulted from the implantation and removal of testosterone in the absence of any major changes in the behaviour of their male partners. These changes in invitational behaviour therefore reflected an action of the hormone upon an internal mechanism within the female subserving sexual motivation which was independent of changes in the behaviour of the male. Radioimmunoassay of plasma testosterone (109 samples) and plasma oestradiol (86 samples), and gas-liquid chromatography of vaginal secretions (306 samples), facilitated the monitoring of variables needed to interpret the results.     

Testosterone administration to ovariectomized female rhesus monkeys (Macaca mulatta) reduces the frequency of pulsatile luteinizing hormone secretion

In the male rhesus monkey testosterone (T) retards the frequency of intermittent LH secretion. The purpose of the present study was to determine whether this action of T is demonstrable in the female. Five ovariectomized rhesus monkeys, bearing indwelling cardiac catheters, were implanted s.c. on one or more occasions with T-containing Silastic capsules. Sequential blood samples were collected for 8 h every 10 min before T treatment and usually at 1, 2, 4, and 8 days thereafter. Plasma LH concentrations were measured in duplicate by radioimmunoassay and subsequently analyzed with a computerized algorithm. Sustained increments in circulating T (5-13 ng/ml) in ovariectomized monkeys resulted in a progressive reduction in LH pulse frequencies from approximately 1 pulse every 60 min before initiation of T treatment to 1 pulse every 100-150 min at 48 h thereafter. In most cases the deceleration in pulsatile gonadotropin secretion continued, and by 4-8 days of T treatment LH pulse frequencies as low as 1 pulse every 5 h were observed. The onset of the T-induced deceleration in LH pulse frequency was generally associated with an increase in LH pulse amplitude and with a decline in mean LH levels. This LH response in the female to T treatment was similar to that previously reported for male castrates.     

Sterilization and its behavioral effects on free-ranging female rhesus monkeys (Macaca mulatta).

In order to control population growth rates, a decision was made to sterilize most of the free-ranging, wild rhesus macaque females of Silver Springs, Florida. Between October 1987 and March 1988, the five females who had been sterilized and released in the fall of 1986 were matched with five intact females in a behavioral study. While there were differences between the behaviors of the sterilized and intact females, the differences can be attributed more to differences in age, rank, and other factors than to the sterilization. Clinical data collected and reported on the monkeys is unremarkable.     

Hydranencephaly in two rhesus monkeys (Macaca mulatta)

Spontaneously occurring hydranencephaly was diagnosed at necropsy and confirmed histologically in two stillborn fetuses that were delivered from young female rhesus macaques (Macaca mulatta).     

Skeptical responding in rhesus monkeys (Macaca mulatta)

Signalers that misinform sufficiently open may become devalued as sources of information; however, “skepticism” and any comparison involved in testing reliability entail a cost that involves delays and energy expenditure. Skepticism may be less costly though, if, as a rule, animals are not equally skeptical of the signals of all conspecifics. Animals with the ability to recognize individual conspecifics and to recall past encounters with them may have the capacity to restrict skepticism to subsets of animals that are most likely to benefit from deception. We played tape-recorded alarm calls of high- and low-ranking rhesus monkeys(Macaca mulatta) to their groups in a feeding context once daily over 8 consecutive days at the Yerkes Primate Center Field Station. Over the sequence of playbacks, response was greater to the calls of high-ranking monkeys, adult response patterns were different from those of juveniles, and for adults especially, decline in responsiveness was punctuated by partial resurgences of response. These differences may be the consequence of the adults’ more extensive histories of interaction with group members that, though generally reliable, vary with respect to the potential benefits of deceptive signaling.     

Sociability and responses to video playbacks in adult male rhesus monkeys (Macaca mulatta)

Studies of several primate species have suggested the existence of a personality dimension typically labeled ‘Sociability,’ which reflects an animal’s tendency to interact with others. The hypothesis that Sociability is related to social skill was tested in the present study by exposing six high- and six low-Sociable adult male rhesus macaques to videotaped presentations of unfamiliar males displaying aggressive or affiliative behaviors. Low-Sociable animals displayed higher frequencies of yawn, lower activity and tended to have higher durations of watching during the presentations that displayed social signals, and significantly fewer lipsmacks to presentations that depicted no social behavior. In response to viewing threats, tooth-grinds, yawns, and lipsmacks, both low- and high-Sociable animals’ most frequent response was to gaze avert; low-Sociable animals, however, had nearly twice the latency to gaze avert than did high-Sociable animals. The low-Sociable animals’ greater tendency to ‘sit and stare’ during the videotaped playbacks suggests that low-Sociable animals have poorer social skills. The possible developmental origins of variation in Sociability, and the functional consequences of such variation for survival and reproduction are discussed.     

Timing of sexual maturity in female rhesus monkeys (Macaca mulatta) housed outdoors

A comparison of the age and season at first parturition was made for spring-born female rhesus monkeys and for females born in the fall to mothers who had been laboratory-housed before being transferred outdoors. Females (N = 9) born during the fall had first parturition during the spring and summer, as did all spring-born females (N = 68), and not during the fall as would be predicted if age were the determining factor. A separate analysis of post-menarchial, spring-born females (N = 5) beginning in September at 29 months of age revealed that the ensuing 12 months were characterized by low serum levels of oestradiol (less than 50 pg/ml), progesterone (less than 1.0 ng/ml), LH (less than 7.0 ng/ml), and FSH (less than 5.50 micrograms/ml). First ovulation subsequently occurred in the fall in all subjects at a mean age of 41.9 +/- 0.1 months, and was preceded by significant elevations in basal LH and FSH, coincident in time with the transition of summer to fall (September). Female copulatory behaviour was restricted to the period surrounding first ovulation, beginning some 2 weeks before and ceasing within 3 days after the oestradiol peak. The most rapid gain in weight occurred during the summer months before first ovulation, and was associated with significant elevations in serum GH and prolactin. These data suggest that season may influence the timing of sexual maturation in rhesus monkeys kept outside in such a way that the occurrence of first ovulation is restricted to the fall and winter months.     

Dietary content may prevent secondary hyperparathyroidism in female rhesus monkeys (Macaca mulatta)

Macaque laboratory chows provide relatively more calcium (Ca) and vitamin D (D) than human diets; this may influence skeletal aging. To evaluate this possibility, parameters of skeletal relevance in premenopausal and naturally postmenopausal rhesus monkeys were measured in a cross-sectional study. Serum osteocalcin (Oc) was elevated in the postmenopausal group (P < 0.01), but levels of parathyroid hormone (PTH) and 25-hydroxyvitamin D (25OHD) were not different. Subsequently, in premenopausal animals, dietary Ca and/or D intake was reduced to optimal human levels for 8 weeks prior to the evaluation of the skeletal parameters. Serum 25OHD concentration was reduced (P < 0.01) and a trend (P=0.10) towards increased PTH was observed in both low D groups. In addition, serum alkaline phosphatase (ALP) levels were increased in the low Ca group (P < 0.01). In conclusion, skeletal turnover, as measured by serum Oc, was increased in naturally postmenopausal rhesus monkeys in the absence of hyperparathyroidism. Dietary D reduction causes a decline in serum 25OHD and an upward trend in PTH.     

Estrous behavior of free-ranging rhesus monkeys (Macaca mulatta)

The sexual behavior of a group of free-ranging rhesus monkeys (Macaca mulatta) was studied for 13 consecutive months in an attempt to determine whether or not sexual activity occurred year-round, and the importance of sexual attraction to rhesus monkey social organization.Estrous behavior was seen both inter-menstrually and peri-menstrually, producing a shorter mean estrous cycle length than reported by other workers. New data was gathered on the interrelationships among age, dominance rank, and sexual activity; son-mother and brothersister matings; and sexual favoritism among free-ranging rhesus monkeys.A few females who failed to conceive during the fall breeding season showed cyclic estrous behavior throughout the entire annual cycle. Hypotheses are given as to possible physiological bases for birth season sexual cycles.Several forms of inter-animal bonding, including sexual bonding, are enumerated, and their importance to rhesus monkey social organization discussed.     

Activated coagulation time for rhesus monkeys (Macaca mulatta)

The activated coagulation time test provided a rapid yet accurate measurement of the intrinsic clotting system in rhesus monkey (Macaca mulatta) whole blood. Other advantages of this test included reproducibility, no requirement for control samples, low cost and commercial availability. The mean activated coagulation time value for 60 normal rhesus monkeys was 96 seconds with a range of 77 to 125 seconds. There were no significant differences due to sex, venipuncture site and time of blood collection.     

Feeding tactics in juvenile rhesus monkeys (Macaca mulatta)

In a group of rhesus monkeys, feeding tactics of juveniles were studied in a competitive situation in which food presentation had been modified, and where food was supplied in a feeding trough six times a day. Juvenile offspring of high-ranking mothers remained longer in the feeding area gathering food. In contrast, juvenile offspring of low-ranking mothers went less often to the feeding area, primarily to collect food. Low-ranking juveniles also gathered the food faster than did dominants and used longer feeding bouts. High-ranking juveniles interrupted their feeding more spontaneously than did subordinate ones. Low-ranking juveniles did so more often as a result of avoiding and being startled. Juvenile males entered the feeding area to satisfy their food requirements more often than females, but were also aggressively expelled more than females. No relation was found between age in months of juveniles and any feeding parameters or causes of interruption. Nor were significant differences found between young and old juveniles. Juvenile rhesus appear to use different tactics in accessing food according to their sex and to their mothers' dominance rank.     

Estradiol administration and the sexual activity of castrated male rhesus monkeys (Macaca mulatta)

To examine whether estradiol might be effective in maintaining sexual behavior after castration or after testosterone withdrawal, we have observed male rhesus monkeys during daily 1-hr tests alternately with each of two ovariectomized, estradiol-treated females (four males, four females, eight male-female pairs, 798 tests). Estradiol (2-5 micrograms/kg sc/day) or vehicle was administered in counterbalanced order immediately after castration and again immediately after withdrawal of testosterone propionate treatments (800 micrograms and 1.6 mg sc/day). There were no significant differences in behavior during vehicle and estradiol treatments to indicate that estradiol helped to maintain male sexual activity. Instead, estradiol treatment tended to interfere with the capacity to intromit. This supported the results of other studies, namely, that the systemic administration of estradiol does not enhance the sexual behavior of castrated male macaques, and raises questions about the role of both aromatization and estrogen receptors in the male primate brain.