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.     

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.     

Self-agency in rhesus monkeys

Rhesus monkeys (Macaca mulatta) have shown the ability to monitor their own mental states, but fail the mirror self-recognition test. In humans, the sense of self-agency is closely related to self-awareness, and results from monitoring the relationship between intentional, sensorimotor and perceptual information. Humans and rhesus monkeys were trained to move a computer icon with a joystick while a distractor icon partially matched their movements. Both humans and monkeys were able to monitor and identify the icon they were controlling, suggesting they have some understanding of self-agency.     

Confirmatory factor analysis of personality structure in adult male rhesus monkeys (Macaca mulatta)

Reports from different laboratories have suggested that nonhuman primates have somewhat similar dimensions of personality. To date, however, no attempts have been made to statistically replicate a specific factor structure. In the present report, two independent observers recorded the behavior of 58 adult male rhesus monkeys, and then rated the animals with the use of a 50-item personality instrument. A confirmatory factor analysis (CFA) of the ratings resulted in the replication of a previously described four-factor personality structure [Maninger et al., American Journal of Primatology 61:73-83, 2003]. The first two dimensions-Sociability and Confidence-showed strong loadings and are similar to Affiliation and Agency dimensions in humans. The remaining dimensions-Equability and Irritability-were less clear, and it is possible that additional traits will have to be identified before a more robust structure can be established for these dimensions.     

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.     

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.     

Effects of puzzle feeders on pathological behavior in individually housed rhesus monkeys

Self-injurious behavior (SIB) occurs in about 10% of individually housed monkeys. Monkeys with SIB bite their own bodies frequently, occasionally inflicting wounds as a result. At present, there is no standard treatment for this phenomenon. We examined the effectiveness of puzzle feeders in alleviating SIB in monkeys with a veterinary record of self-inflicted wounding. Two groups of monkeys (SIB and controls) were exposed to puzzle feeders for a 6 week period. Three levels of maze difficulty were examined. All monkeys used the feeders, but manipulation was confined to a brief period immediately after the feeders were loaded each day (1000 h) and was infrequent during the later sampling periods (1100 and 1400 h). The most difficult maze yielded a slight increase in usage at 1100 h. During the puzzle feeder phase, whole body stereotypies, including pacing and rocking, were reduced substantially in all monkeys at 1000 h when feeder manipulation was at its highest. However, self-biting in the SIB group was unchanged. Some monkeys actually bit themselves while manipulating the feeder. Long-term effects on abnormal behavior were assessed by comparing behavior during the feeder phase to baseline periods and to a phase in which the monkeys were provisioned with treats placed directly into their food box. Whole body stereotypies, including pacing, were reduced during both treatment phases; however, the reduction was associated only with the 1000 h observation. Puzzle feeders were more effective than treats alone in alleviating whole body stereotypies. Self-biting was unchanged through all phases. Puzzle feeders are beneficial from the perspective of eliciting manipulation. They also yield transient reductions in whole body stereotypy, an effect that does not extend beyond the direct manipulation of the feeder. Puzzle feeders are ineffective in alleviating self-injurious behavior. Am. J. Primatol. 46:213–227, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Effect of testosterone on epididymal proteins in castrated rhesus monkeys

The effect of testosterone on regulation of epididymal protein synthesis has been investigated in castrated rhesus monkeys (Macaca mulatta). The proteins in the treated monkeys were characterized using polyacrylamide gel electrophoresis (under nondenaturing and denaturing conditions) and electrofocusing. At least four distinct proteins have been shown to be synthesized by the monkey epididymis under testosterone influence. Two of these proteins were detected following two days of testosterone treatment while the other two proteins were detected after a six-day treatment period. None of these proteins was detectable in monkeys treated with estradiol for six days. Electrofocusing of epididymal cytosol proteins from untreated and testosterone-treated and castrated monkeys also confirmed the presence of four androgen-dependent proteins in this species. The isoelectric points of these proteins were shown to range between 5.8 and 6.4. The molecular weights of these proteins were found to vary between 47,500 and 66,000. The in vitro incorporation of ³H-labeled amino acids was markedly greater in the androgen-primed epididymis as compared with the control tissue.     

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.     

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.     

Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys

Among captive primates, inanimate environmental enrichment can lead to measurable changes in behavior indicative of an improvement in psychological well-being. Although this has been demonstrated repeatedly for singly caged primates, the relationship is not as well studied for pairhoused animals. Study of the pair-housed setting has become increasingly relevant because of the social housing mandate of the Animal Welfare Act regulations. We therefore observed 68 juvenile rhesus monkeys born in 1988 and 1989 and living in mixed-sex pairs from the ages of 2 to 3 years. All pairs were compatible. Half of the pairs received two types of enrichment, while the remaining pairs served as controls. Enriched and control juvenile subjects differed in the amount of time that they spent being inactive, playing, and drinking, but did not differ in the amount of time they spent interacting with their partner. Grooming and play were the two most common socially directed activities in both groups, a species-appropriate pattern. Males played more and vocalized less than did females. Overall, enriched and control subjects spent equivalent amounts of time located within a social distance of one another, but there was some difference between groups in allocation of behaviors while near the pairmate. Environmental enhancers were frequently utilized, and led to relatively small changes in behavior between control and enriched subjects, suggesting that the presence of a partner for juvenile rhesus monkeys acts as a form of enrichment that may dilute the effects of inanimate environmental enhancements. © 1994 Wiley-Liss, Inc.     

Low potency of intact male rhesus monkeys after long-term visual contact with their female partners

We have examined the possibility that prolonged visual contact between future sexual partners, in the absence of any direct sexual contact and mating activity, is sufficient to produce the familiar-female phenomenon and is associated loss of male potency. For 1 year, 32 intact, feral-reared male rhesus monkeys were housed so that 14 males were in constant visual contact with their four future testing females, and 18 of the males were without any visual contact with females. After 1 year, each male was then tested once with each ovariectomized, estrogen-treated female (128 tests). Males in the group having prolonged prior visual contact (group II) were significantly less potent than males without prior visual contact (group I), and this difference was not related to plasma testosterone levels, prior history, time since capture, or presumed age. Group II males had fewer ejaculations during tests and ejaculated with fewer partners, and this appeared to be because they required significantly more stimulation (mounting and thrusting) to reach ejaculation. The data suggested that the familiar-partner phenomenon was not restricted to the male and was associated with increased social affinity and decreased agonistic tension between partners. Under natural conditions, the phenomenon may encourage troop transfers and outbreeding, and in laboratory studies, prior visual contact between testing partners should be regarded as a potentially uncontrolled source of variation.     

Four-year study of controlled timed breeding of rhesus monkeys (Macaca mulatta)

As part of the timed breeding colony at Tulane National Primate Research Center, exogenous progesterone administration (5 mg/day for 10 days) has been used to select conception dates by inducing artificial luteal phases in female rhesus monkeys. A retrospective analysis of data obtained during four breeding seasons (1998-2001) revealed that conceptions occurred an average of 18 days after the last administration of progesterone. The age of the female to be bred, previous pregnancy history, and timing of breeding during the breeding season were determined to be critical factors in the success of the procedure. The benefit of this method of timed breeding is that it does not require tracking of menstrual cycles, which can be labor-intensive and requires that animals be monitored several months in advance of breeding to determine each female's individual cycle length. It also provided an efficient use of breeding-age males.     

Relative numerical middle in rhesus monkeys

Animals show vast numerical competence in tasks that require both ordinal and cardinal numerical representations, but few studies have addressed whether animals can identify the numerical middle in a sequence. Two rhesus monkeys (Macaca mulatta) learned to select the middle dot in a horizontal sequence of three dots on a touchscreen. When subsequently presented with longer sequences composed of 5, 7 or 9 items, monkeys transferred the middle rule. Accuracy decreased as the length of the sequence increased. In a second test, we presented monkeys with asymmetrical sequences composed of nine items, where the numerical and spatial middle were distinct and both monkeys selected the numerical middle over the spatial middle. Our results demonstrate that rhesus macaques can extract an abstract numerical rule to bisect a discrete set of items.     

Deciduous tooth dimensions in fetal rhesus monkeys from mothers with induced diabetes

Thirty-four measurements of the deciduous dentition in 21 fetal rhesus monkeys from diabetic mothers (FDM) and 36 nondiabetic fetuses were compared in order to assess the effects of induced maternal diabetes on the teeth of third-trimester fetuses. After exclusion of 14 variates due to significant age-related variation, univariate statistical analysis suggested a trend toward smaller teeth in the FDMs. Multivariate discriminant function analysis indicated not only a clear separation between the two groups, with molar breadths and some incisor lengths and breadths serving as the best discriminators, but also that the deciduous dental dimensions in FDMs are smaller than in nondiabetic fetuses.     

Profiling serum antibodies to Mycobacterium tuberculosis proteins in rhesus monkeys with nontuberculous Mycobacteria

Recent evidence indicates that the prevalence of diseases caused by nontuberculous mycobacteria (NTM) has been increasing in both human and animals. In this study, antibody profiles of NTM in rhesus monkeys (Macaca mulatta) were determined and compared with those of monkeys infected with Mycobacterium tuberculosis complex (MTBC). Antibodies against 10 M. tuberculosis proteins, purified protein derivative (PPD), and mammalian old tuberculin (MOT) were detected in 14 monkeys naturally infected with NTM by indirect ELISA. Sera from 10 monkeys infected with MTBC and 10 healthy monkeys were set as controls. All antigens showed high serological reactivities to MTBC infections and low reactivities in healthy monkeys. NTM infections showed strong antibody responses to MOT and PPD; moderate antibody responses to 16kDa, U1, MPT64L, 14kDa, and TB16.3; and low antibody responses to 38kDa, Ag85b, CFP10, ESAT-6, and CFP10-ESAT-6. According to the criteria of MTBC, only CFP10, ESAT-6, and CFP10-ESAT-6 showed negative antibody responses in all NTM infections. Taken together, these results suggest that positive results of a PPD/MOT-based ELISA in combination with results of antibodies to M. tuberculosis-specific antigens, such as CFP10 and ESAT-6, could discriminate NTM and MTBC infections. Two positive results indicate an MTBC infection, and a negative result for an M. tuberculosis-specific antigen may preliminarily predict an NTM infection.     

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.