Determinants of behavioral rhythmicity during artificial menstrual cycles in rhesus monkeys (Macaca mulatta)

Reproductive success in many mammals depends on synchrony between copulation and ovulation, which is insured by the phenomenon of heat in the female. Certain anthropoid primates including rhesus monkeys do not show heat but may copulate throughout the menstrual cycle, especially when pairs are isolated from conspecifics. In social groups, however, mating mostly occurs around midcycle. We wished to test the hypothesis that copulations are more closely linked to ovulation when males have simultaneous access to several females in different cycle phases. Artificial menstrual cycles were therefore induced by giving hormones to ovariectomized female rhesus monkeys observed in small social groups that each consisted of four females and one male. The cycles of two hormone-treated femlab in each group were either made to synchronize or be offset by 7-day increments so that the estradiol peak of one female occurred 7 days before, and 7 and 14 days after, the estradiol peak of the other. Radioimmunoassay of plasma samples (N = 224) confirmed the timing of the estradiol peaks. Results from eight unique male-female groups (4 males, 8 females, 16 male-female pairs, 718 tests) fully supported the hypothesis. Compared with synchronized cycles, the amplitudes of rhythmic changes in offset cycles were reduced for ejaculations made by males but greatly enhanced for ejaculations received by females. We propose that this socio-hormonal integration of behavior in the group is highly adaptive and enhances the reproductive success of both males and females.     

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.     

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.     

A comparison of the behavior of Macaca fascicularis and Macaca mulatta in relation to the menstrual cycle

Observations on oppositely sexed pairs of M. fascicularis and M. mulatta revealed certain differences. M. fascicularis showed single-mount copulations, higher potency, less grooming activity, and milder but more frequent aggressive exchanges than the rhesus monkey. These differences might be due to the lower dominance gradient between the sexes and less sexual dimorphism in M. fascicularis than in M. mulatta. There were changes in the sexual, grooming, and aggressive interaction in relation to the menstrual cycle, indicating the suitability of M. fascicularis for hormone-behavior studies. Comparison of data from 30 and 60 min tests showed that important behavioral changes did not become apparent unless animals were given enough time to interact.     

Paternity exclusion in six captive groups of rhesus monkeys (Macaca mulatta)

Five genetic markers were employed to attempt to identify the fathers of 135 Macaca mulatta offspring living in large outdoor field cages. Family studies of two of these markers to confirm mode of inheritance of phenotypes had not heretofore been reported. Of the 284 exclusions required to identify the fathers of all 135 monkeys, 198 (or 70 percent) were possible using only these five genetic polymorphisms. For 58 (or 43 percent) of these 135 offspring the father was identified. These data were applied to estimate the association between dominance rank of fathers and reproductive success. Fertility of first- and second-ranking fathers was judged to be about twice as high as that of third- and fourth-ranking fathers.     

Female menstrual cyclicity and sexual behavior in stumptail Macaques (Macaca arctoides)

The sexual behavior and female reproductive cycles of a captive group of stumptail macaques (Macaca arctoides)were monitored during a 12-month period. The data, consisting of 303 ad libitummounts and copulations and 125 hr of focal-female testing, were analyzed by their frequency of occurrence during the three hormonal phases of the female menstrual cycle. Regularly cycling females exhibited statistically higher frequencies of all sexual behaviors compared to the amenorrheal controls. Contrary to previous reports which indicate no variation in sexual behavior throughout the reproductive cycle in this species, our data show marked increases in copulations during the periovulatory phase. Male dominance rank is associated with sexual behavior only at midcycle.     

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.     

Colon cancer in aged captive rhesus monkeys (Macaca mulatta)

The age-related incidence of malignant neoplasia was surveyed from a total of 301 necropsy cases of rhesus monkeys ranging in age from 13–37 years performed in the Pathology Service Unit of the Wisconsin Regional Primate Research Center during the past 15 years. All our aged monkeys lived in indoor cages and were fed with monkey chow and supplemental fruits during the past decades. In this survey, we found a total of 51 malignant neoplasms, and among them 25 cases were colon cancer. The incidence of colon cancer increased with advancing age: 3.2% at 13–19 years, 9.2% at 20–25 years, 13.5% at 26–29 years, and 20.7% at 30–37 years. Most cancers were located in the cecum and transverse regions with a unicentric origin. Two multicentric cases were associated with chronic hypertrophic colitis. Precancerous polypous lesions were not found in all cases. Histologically, all cases were mucinous adenocarcinoma and had local invasion to the muscular wall. Metastasis to the mesenteric lymph nodes was found in only two cases. As in humans, colon cancer is a common outcome of aging in nonhuman primates. Am. J. Primatol. 44:19–27, 1998. © 1998 Wiley-Liss, Inc.     

Growth of the masseter muscle in rhesus monkeys (Macaca mulatta)

The growth of the masseter muscle in eight infant, juvenile, and adolescent female rhesus monkeys (M. mulatta) was examined over a 2.5 year period using serial radiographic cephalometric techniques with the aid of radiopaque muscle markers. The radiopaque markers, which are composed of small pieces of root canal broach inserted into the muscle belly, make it possible to determine longitudinal masseter muscle growth as well as migration of the masseter muscle relative to the mandible. It was found that the masseter muscle increased in length by 64% during the total growth period, most of which occurred between 6 and 18 months of age. Relative to the cranium, the masseter muscle grew markedly inferiorly and only slightly posteriorly. Relative to the mandible, the masseter migrated in a posterior and slightly superior direction, keeping pace with the ramus and condyle as they grew posteriorly and posterosuperiorly throughout the study period. It was concluded that: 1) radiopaque muscle markers are a valuable tool for analysis of muscle growth and alteration of muscle location; 2) the masseter muscle in the rhesus monkey undergoes elongation, probably due to addition of sarcomeres at the fiber-tendon junctions; and 3) posterior migration of the masseter muscle relative to the corpus of the mandible, probably due to the nature of its periosteal attachment, results in a stability of the anteroposterior position of the masseter muscle despite the anterior displacement of the mandible.     

The albumin polymorphism and bilirubin binding in rhesus monkeys (Macaca mulatta)

Family studies confirmed a codominant mode of inheritance of albumin phenotypes identified in Macaca mulatta. Preliminary epidemiological and bilirubin binding studies suggest that selection favors the variant allele by reducing risks of hyperbilirubinemia and might be responsible for this otherwise rare polymorphism.     

Segregation distortion and differential fitness at the albumin locus in rhesus monkeys (Macaca mulatta)

The observed patterns of segregation of two co-dominant alleles at the macaque albumin locus in 400 rhesus monkey offspring were compared with those expected for five segregating mating phenotypes. Rates of reproductive loss and conception were also compared among females of each albumin phenotype. The common albumin allele in macaques, Al^A_mac, segregated more frequently than expected when the mother was heterozygous but less frequently than expected when she was homozygous for Al^B_mac. In both cases, the phenotype identical to that of the mother appeared to be favored. Mothers who were either homozygous for Al^A_mac or heterozygous were also found to experience higher conception rates than mothers homozygous for Al^B_mac. It is hypothesized that phenotypic differences in bilirubin binding, and in competitive binding by dietary constituents, by albumin influences both these results and the nonrandom distribution of Al^B_mac in Asian macaques.     

Behavioral,immunological, and hormonal responses associated with social change in rhesus monkeys (Macaca mulatta)

Twelve animals to be socially reorganized in a group of 49 animals were compared with ten animals in a socially stable group (n = 51) for reproductive hormones, cortisol concentrations, immune function, and behavioral patterns for a 6 week baseline and 16 week postreorganization period. Cortisol values, mitogen-induced lymphocyte blastogenesis, and rates of behavior reflected social events. Increased cortisols, increased noncontact aggression, and decreased mitogen response were associated with animal introductions. Increased cortisol concentration and decreased mitogen response correlated significantly only in animals removed from the group for trauma, and females successful at group membership exhibited lower cortisol concentrations. High-ranking animals in small stable groups exhibited significantly higher lymphocyte proliferation than middle- or low-ranking animals. While relative ranks established in small groups were maintained following reorganization, baseline cortisol values, immune measures, or male testosterone values did not predict success at group membership. © 1996 Wiley-Liss, Inc.     

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.     

High-resolution chromosomes of rhesus macaques (Macaca mulatta)

Late-prophase high-resolution chromosomes were successfully cultured for 22 of 27 Macaca mulatta samples. Twelve of the successful cultures were adequate for karyotyping high-resolution spreads. High-resolution chromosome technique provides an important contribution to primate genetics because it can be used to identify chromosomal anomalies undetected in metaphase spreads and may be useful for paternity exclusion analysis.     

Demography and pedigree structure of an SPF colony of rhesus monkeys (Macaca mulatta)

The SPF rhesus colony at the M.D. Anderson Cancer Center in Bastrop, Texas, was analyzed with the aim of determining the demographic and genetic effects of stringent selection for virus-free breeders, permanent quarantine, continued surveillance, and culling of animals that show evidence of viral infection. The analysis shows minimal effects on population viability and loss of genetic variability in comparison with the traditionally managed (non-SPF) portion of the population.     

Comparative studies with six extenders for sperm cryopreservation in the cynomolgus monkey (Macaca fascicularis) and rhesus monkey (Macaca mulatta)

Ejaculated spermatozoa from cynomolgus monkeys and rhesus monkeys were frozen in straws with six different extenders (TTE, DM, mDM, LG-DM, G-DM, and TCG) containing glycerol. Sperm motility and head membrane and acrosomal integrity were evaluated after freezing and thawing, and the cryoprotective effects were compared among the extenders and the two species studied. The results showed that sperm motility and motility recovery with the six extenders were comparable for the cynomolgus and rhesus monkeys. There was no significant difference in sperm motility and head membrane integrity among the six extenders in either the cynomolgus or rhesus monkeys (P>0.05). However, a slightly but statistically lower percentage of acrosomal integrity was found with TCG in both species compared to the other extenders (P<0.05). These findings demonstrate that TTE, DM, mDM, LG-DM, G-DM, and TCG are equally suitable extenders for the cryopreservation of spermatozoa from cynomolgus and rhesus monkeys.     

Surgical and microscopic anatomy of parotid and submandibular salivary glands of rhesus monkeys (Macaca mulatta)

Wedge biopsy of the caudal borders of the parotid or submandibular salivary glands of rhesus monkeys avoids major nerves, ducts, and blood vessels. This is a minor surgical procedure that provides adequate material for in vitro studies and causes no significant postoperative complications. Gross and light microscopic anatomy of the rhesus and human salivary glands are similar. We have concluded that rhesus monkeys are good models for human salivary diseases, including radiation sialoadenitis.     

Metric characteristics of the canine dental complex in prenatally androgenized female rhesus monkeys (Macaca mulatta).

Permanent maxillary canine teeth (C1) are appreciably larger in males than in females in most nonhominid Anthropoidea. Mandibular canines (C1) and mandibular first premolars (P3), against which C1 are sharpened in honing behavior, reflect commensurate sexual dimorphism. These three teeth constitute the canine dental complex. The canine complex crown metrics of seven mature genetically female rhesus Macaques, androgenized by prenatal exposure to testosterone propionate, were compared with a control sample (N = 12) for evidence of masculinization. The C1 and C1 were measured for clinical crown lengths (L) and mesiodistal and buccolingual widths. The functionally significant and highly dimorphic honing dimensions (HD), which approximate the honing surfaces of P3, were noted. In t-test comparisons, the C1 L and P3 HD in androgenized monkeys were significantly larger than those of the control group (P less than 0.05). Identical results were obtained with White's nonparametric ranking technique. Standardized lateral skull radiographs showing earlier dental formative stages were available for five of the seven animals, and these were compared with radiographs of control skulls. The developing C1 were longer and wider than in the controls. This was not reflected in the crown metrics of mature animals because of marked dental attrition. We concluded that androgens can masculinize the female rhesus canine complex, if given during critical periods of prenatal development. We hypothesize that genes encoding the male canine complex are normally activated by endogenous fetal androgens during such critical periods.     

Mandibular growth in the rhesus monkey (Macaca mulatta)

Mandibular growth of 42 rhesus monkeys (Macaca mulatta) was analyzed quantitatively and qualitatively. Four groups of animals were defined according to dentitional age (i.e., infant, juvenile, adolescent, young adult). At each age growth was observed for a 24 week period. Since some animals were observed at more than one stage of development, 57 periods of growth were studied. The growth incremental data were collected by superimposing serial cephalograms on mandibular implants. Growth and remodeling of both the skeletal and dento-alveolar components of the rhesus mandible were greatest in the infant monkeys and were less in successive age groups. Posterior relocation of the ramus was noted in all age groups while bone deposition on the anterior and inferior borders of the mandibular body was greatest in the younger animals. The most pronounced dental changes also occurred in the younger animals while the dentitions of the adolescent and adult animals were generally more stable. This study demonstrates that the rate and direction of normal mandibular growth varies with the age of the animal. Furthermore, mandibular growth is quantified at four defined maturational levels to provide a set of values illustrating normal mandibular growth. These values can also be used as control data for experimental studies.     

Early predictors of self-biting in socially-housed rhesus macaques (Macaca mulatta)

The development of self-biting behavior in captive monkeys is little understood and poses a serious risk to their well-being. Although early rearing conditions may influence the expression of this behavior, not all animals reared under similar conditions self-bite. The purpose of this study was to examine the effects of three rearing conditions on biting behavior and to determine whether early infant behavior can predict later self-biting. The subjects were 370 rhesus macaques born at the National Institutes of Health (NIH) Animal Center between 1994 and 2004. They were reared under three conditions: mother-reared in social groups (n=183), peer-reared in groups of four (n=84), and surrogate-peer-reared (n=103). Significantly more surrogate-peer-reared animals self-bit compared to peer-only or mother-reared animals. There was no sex difference in self-biting, but this result may have been affected by a sex bias in the number of observations. The durations of behaviors exhibited by the surrogate-peer-reared subjects were recorded in 5-min sessions twice a week from 2 to 6 months of age while the animals were in their home cages and play groups. In the play-group situation, surrogate-peer-reared subjects who later self-bit were found to be less social and exhibited less social clinging than those that did not self-bite. Home-cage behavior did not predict later self-biting, but it did change with increasing age: surrogate clinging and self-mouthing decreased, while environmental exploration increased. Our findings suggest that surrogate rearing in combination with lower levels of social contact during play may be risk factors for the later development of self-biting behavior.