Gestation length in rhesus macaques (Macaca mulatta)

We describe some of the sources of variation in gestation length among rhesus macaques. the data were obtained from the timed-mating breeding program at the California Regional Primate Research Center (CRPRC). Information about approximately 700 pregnancies that resulted in spontaneous vaginal deliveries of liveborn young is presented. The average length of these pregnancies was 166.5 days. In this population, older females with higher parities had significantly longer pregnancies and significantly heavier infants than other females did. Other factors, including infant sex, month of conception, maternal reproductive history, and paternal identity, had no consistent effect upon gestation length.     

Feeding habits of the rhesus monkeys (Macaca mulatta) of Jaipur and Galta,India

Between September 1987 and May 1988, the time budgets of two groups of rhesus monkeys were investigated. One group inhabited an old Observatory which is now a tourist attraction in the center of Jaipur, India. The other group lived in a hilly forest/temple complex on the outskirts of Jaipur known as Galta. Because it was believed that the monkeys of these two different areas ate different proportions of natural and provisioned food, it was expected that they would have different time budgets. To determine differences in time budgets, a combination of census taking and 10-minute interval scan samples were used to collect comparative data. The analysis of the data revealed that there were differences in the time budgets of the two groups — the Observatory monkeys foraged more, moved less, engaged in fewer aggressive acts, and slept less during the day than the Galta group. These differences are mainly attributed to the 1984–1987 drought, site differences in the variety of natural food resources, and the manner in which the monkeys are provisioned.     

4040 SNPs for genomic analysis in the rhesus macaque (Macaca mulatta)

Although the rhesus macaque (Macaca mulatta) is commonly used for biomedical research and becoming a preferred model for translational medicine, quantification of genome-wide variation has been slow to follow the publication of the genome in 2007. Here we report the properties of 4040 single nucleotide polymorphisms discovered and validated in Chinese and Indian rhesus macaques from captive breeding colonies in the United States. Frequency-matched measures of linkage disequilibrium were much greater in the Indian sample. Although the majority of polymorphisms were shared between the two populations, rare alleles were over twice as common in the Chinese sample. Indian rhesus had higher rates of heterozygosity, as well as previously undetected substructure, potentially due to admixture from Burma in wild populations and demographic events post-captivity.     

Ecology of rhesus macaques (Macaca mulatta) in northwest Pakistan

The feeding ecology of rhesus monkeys,Macaca mulatta, was studied between 1978 and 1981. The study site, located in the Murree Hills of northwestern Pakistan, supported a mixed coniferous-deciduous forest community and was characterized by a high degree of human disturbance. We used a linear transect method to sample the species composition and structure of the vegetation. Comparison of these data with historical records showed that the forest has undergone major changes in the last hundred years. Data on feeding behavior were collected through on-the-minute focal animal sampling. The monkeys spent about 45% of the day feeding. Their preferred foods were grass, clover, and other ground herbs that occur in the disturbed sites. Fruit accounted for less than 9% of feeding records. The rhesus monkey may be pre-adapted to living in disturbed-site, forest-edge communities. The evolutionary history of Macaca mulatta may be tied closely to the disappearance of forest and the spread of meadows and savannahs over the last million years.     

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.     

A ten-month study of endogenous testosterone levels and behaviour in outdoor-living female rhesus monkeys (Macaca mulatta)

Endogenous testosterone levels were measured in association with sexual, aggressive, and social/affiliative behaviors in 11 outdoor-housed female rhesus monkeys over a ten-month period. Several behaviors (sex directed toward the male, sex received from the male, aggression directed toward the male, submission directed toward the male, submission directed toward the female, and groom another female) were significantly (p<0.05) positively correlated with testosterone in from one to five females. No trends were strong enough across all females to suggest that any of these correlations have species-wide significance. Factor analysis revealed clearcut clusters of behaviors, but elevations in testosterone were not strongly associated with any of these clusters. It is concluded that endogenous testosterone levels have little measurable effect on overt behavior in female rhesus monkeys.     

Effects of early experience on the behaviour of yearling rhesus monkeys (Macaca mulatta) in the presence of a strange object: classification and correlation approaches

Special techniques are needed to help us understand the long-term effects of infants' experiences of their relationships with their mothers, especially when direct experimental control of the interaction between mother and young is impossible, or could distort their relationship. A classification approach is developed to show how outcomes in individuals can be predicted from their earlier experiences and characteristics. Four-week-old rhesus monkey infants' characteristic levels of enterprise persisted through their first year, but could be reduced in certain individuals who had been kept off their mothers by high rates of early maternal rejection. Correlational approaches are difficult to interpret when they fail to confirm simple effects of experience or of individual characteristics, because they are based on groups not individuals, and because certain individuals can affect the values of correlation coefficients in ways that cannot be specified without using a classification approach. The possible effects on correlation coefficients of inconsistent individuals, and of being unable to specify which infants respond in which ways to relevant variables were discussed.     

A comparison of the mating behavior of adolescent and adult female rhesus macaques (Macaca mulatta)

This study compares adult and adolescent female rhesus macaques with regard to (1) characteristics of their copulatory partners, (2) their proceptive behaviors, and (3) adult male behaviors toward them during estrus. We conducted focal follows of 24 adolescent and 65 adult free-ranging estrous female rhesus macaques on Cayo Santiago during two mating seasons. Compared to adult females, adolescents presented sexually to males at higher rates; copulated more frequently with rankless young male, and extra-group males; and, in one of two mating seasons, were ignored more frequently by males to whom they presented sexually. Adolescents tended to copulate with ranked, resident males at higher frequencies on days when the operational sex ratio (adult males:estrous adult females) was high. Males directed “muzzle-up” signals to adolescents at lower rates than to adults in one of two mating seasons, although this effect vanished when males who might have fathered adolescent females were excluded from analysis. Adolescents did not differ consistently from adults in strength of the correlation between proximity maintenance (dyadic Hinde's Index) and copulation rate, or in approach rate to males. Adolescent females, relative to adult females, presented sexually more to rankless young males, but did not present more to ranked, resident males. Both proximate (e.g. endocrine) and ultimate (e.g. differential fecundity; female-female mate competition) explanations may account for the reported differences between adult and adolescent female rhesus macaque sexuality.     

Phylogeny of rheusus monkeys (Macaca mulatta) as revealed by mitochondrial DNA restriction enzyme analysis

Mitochondrial DNA, purified from 36 samples of 23 local populations which are widely distributed in Vietnam, Burma, and 10 provinces of China, has been analyzed to model the phylogeny of rhesus monkeys. The 20 local populations of China may represent nearly all major populations in China. Using 20 restriction endonucleases of 6-bp recognition, we observed a total of 50–61 sites in the various samples. By combining the cleavage patterns for each enzyme, the 36 samples were classified into 23 restriction types, each of which was found exclusively in the respective population from which samples were obtained. By combining the earlier study of Indian rheusus monkeys, phylogenetic trees, which have been constructed on the basis of genetic distance, indicate that rhesus monkeys in China, Vietnam, India, and Burma can be divided into seven groups. Integrating morphological and geographical data, we suggest that rhesus monkeys in China, Vietnam, and Burma may be classified into six subspecies—M. m. mulatta, M. m. brevicaudus, M. m. lasiotis, M. m. littoralis, M. m. vestita, and M. m. tcheliensis-and rhesus monkeys in India may be another valid subspecies.M. m. tcheliensis is the most endangered subspecies in China. Divergence among subspecies may have begun 0.9–1.6 Ma. The radiation of rhesus monkeys in China may have spread from the southwest toward the east. The taxonomic status of the Hainan monkey and the Taiwan monkey require further investigation.     

Inhibin-like and gonadotropin-like immunoreactivity in pituitary cells of male monkeys (Macaca fascicularis,Macaca mulatta)

Summary Inhibin-like immunoreactivity was detected by immunocytochemistry in the pituitaries of untreated male crab-eating macaques (cynomolgus monkey) and rhesus monkeys, in rhesus monkeys actively immunized against FSH, and in one orchidectomized crab-cating macaque. Localizations were performed by the immunogold-silver staining with 5-nm colloidal gold-conjugated second or third antibodies and by the alkaline phosphatase-anti-alkaline-phosphatase technique. Two different inhibin-specific antisera, raised against the -subunit or the entire inhibin molecule, provided identical staining patterns. Positive label was confined to the pars distalis of the pituitary and occurred exclusively in the cytoplasm of morphologically different cell types throughout the pars distalis in all pituitaries. Staining was most prominent in clusters of chromophobic cells. The presence of inhibin-like activity in the pituitary of an orchidectomized monkey with undetectable serum inhibin levels suggests that inhibin is produced within the pituitary gland. Co-localization studies for the -subunits of the gonadotropic hormones revealed that on average 82% of the gonadotropes were bihormonal. Using the same protocol, co-localization of inhibin-like activity with gonadotropin-like immunoreactivity revealed only a small degree of common distribution (<15%). Inhibinpositive cells were frequently in close proximity to gonadotropic cells and, thus, paracrine effects of inhibin on gonadotropin-synthesizing cells are conceivable.     

How social relationships influence a monkey's choice of feeding sites in the troop of Japanese macaques (Macaca fuscata fuscata) on Koshima islet

When the individual Japanese macaques of the Koshima troop feed on natural food, they usually feed alone. In situations where animals usually feed without other animals, there is a possibility that subordinate animals may avoid feeding sites at which dominant animals are feeding. This paper examines whether social relationships such as kinship or dominance exert any influence on an animal's choice of feeding sites, by analyzing episodes in which an animal approached and climbed into a tree where other animals were. As a result, it was found that social relationships did not influence whether an animal climbed into a tree where other animals were feeding, and that no particular age-sex pair co-fed. Agonistic interactions frequently occurred when the inter-individual distance was less than 1 m. From these findings, the feeding sites were divided into two spaces: (1) a tolerance feeding space, and (2) an intolerance feeding space. It is presumed that animals can feed without entering others' intolerance feeding spaces when food is abundant, as it was in the present study period. Thus social relationships do not influence an animal's choice of feeding sites in such a situation.     

Determination of genetic status in a closed colony of rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>)

The long-term management of breeding colonies requires some measure of genetic diversity in the animal population. For the maintenance of breeding colonies of monkeys used for biomedical research, known pedigrees supply precise data to determine the genetic status of colonies. We present data of genetic analyses in an old closed colony of rhesus macaques (Macaca mulatta) that was established in 1932 with 100 animals. For more than 40 years, the animals were kept on an isolated island and, in 1980, single-male breeding groups were established. A total of 333 DNA samples of these animals were typed to 20 microsatellite markers using multiplex PCR in order to verify inbreeding coefficient () and level of heterozygosity. We found an average heterozygosity of 64% and obtained =–0.03293 (±0.00573). Our results indicate that the reproductive strategy used was effective because consanguineous breeding was avoided. A continuous genetic program must be carried out in order to obtain better quality primates for biomedical research.     

Responses of foster-mothers and troop members to adopted newborns in a captive group of rhesus monkeys

Two rhesus monkey males and two females, born to females caged singly, were exchanged with same-sex infants born to females in a large troop which was held in an enclosure in a different building. The ages of the infants were between 24 and 120 hr. The selected foster mothers (FMs) immediately accepted the foreign infants, allowed them to suckle and treated them as their own offspring. Compared with interactions with previous offspring, the FMs initially tended to be more possessive and restrictive of their foster infants: generally they took longer before they allowed the infants to sit at a distance from them and more readily retrieved them. The foster infants tended to be more active (‘fidgety’) than natural (control) offspring born to the troop. Non-related members of the troop, differentiated between foster and control groups. These troop animals more frequently approached and sat in proximity, often in fur-contact with, touched, groomed, and lipsmacked to, foster infants than control infants. The attractiveness of the fostered infants seemed to be slightly associated with the FMs' dominance rank. The foster infants were therefore viewed by others as having assumed the role afforded by the FMs' rank. Thus both FMs and other troop members recognized the unfamiliarity and novelty of the foster infant but the infants were still accepted into the group. We suggest that the different treatment of the foster infants by the troop may have consequences on the infants' future social development.     

Hierarchy,kinship and social interaction among Japanese monkeys (Macaca fuscata)

The study reports the relationship between hierarchy, genetic relatedness and social interaction in captive Japanese macaques. Grooming and proximity were found to be positively related to both dominance rank and degrees of relatedness. Ranks also positively correlated with threats while no relationship was observed between genetic relationships and agonistic interactions. The removal of a-male tightened the male hierarchy while the female hierarchy became relatively loose. Affiliative behaviour became more correlated with ranks than degrees of genetic relatedness. In the absence of α-male, the next dominant male avoided involvement in either agonistic or afliliative interactions with reintroduced animals and group females.     

The fine structure of the thymus of the fetal and neonatal monkey (Macaca mulatta)

Summary The morphologic features of the fetal and neonatal thymus were investigated by light and electron microscopy to determine developmental changes. Primitive epithelial cells differentiate into reticular epithelial cells, medullary epithelial cells, elongated epithelial cells, Hassall's corpuscles and cysts. Thymocytes first appear at 50 days fetal age and the number of thymocytes is amplified from 75–150 days fetal age. Minor differences between the fetal thymus of the monkey and that of other species were observed. Possible functions for the various cellular components of the fetal monkey thymus are discussed.This research was supported in part by grants 5-F3-CA-28, 793-02 and FR-0167 from the National Institutes of Health.     

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.     

Development of co-feeding relationships in immature free-ranging Japanese monkeys (Macaca fuscata fuscata)

The co-feeding relationships of immature Japanese monkeys in the provisioned situation were studied. The most frequent co-feeders for immature females were diversified as compared to those for immature males. The number of immature females who showed strong co-feeding relationships with their mothers gradually decreased with age in both high- and middle/low-ranking matrilines, but the percent decrease was greater for middle/low-ranking immatures. Almost all immature females who displayed strong co-feeding relationships with adult males were from middle/low-ranking matrilines. Strong co-feeding relationships with mothers among immature males from high-ranking matrilines remained until 4 years of age. In contrast, strong co-feeding relationships with mothers among middle/low-ranking immature males decreased rapidly in the first year of life, and most 1- to 4-year-olds showed no strong co-feeding relationships with other group members. It is considered that middle/low-ranking mothers may not provide their immatures with a secure base for obtaining food in the provisioned situation.     

Body Size and Proportions and Pelage Color of Free-Ranging Macaca mulatta from a Zone of Hybridization in Northeastern Thailand

Rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques belong to the same species, and are parapatric within a zone that lies between 15° and 20° N on the Indochinese peninsula. Researchers have reported probable hybrids between the 2 species from that zone, but have not studied the extent of introgression. To test for phenotypic evidence of hybridization, we collected body mass, morphometrics (body size and proportions), and pelage color readings from free-ranging rhesus living close to the zonal boundary at Wat Tham Pa Mak Ho (WTPMH), Wang Saphun district, Loei province, northeastern Thailand (17°14′N, 101°47′E). Female WTPMH rhesus macaques (n =12) were 10–20% smaller, but with a greater relative tail length than the captive Chinese or Indian female rhesus. Female WTPMH were larger than the free-ranging long-tailed macaques, but with similar limb proportions and a shorter relative tail length. The WTPMH rhesus macaques also displayed the bipartite pelage color pattern typical of Macaca mulatta . The evidence suggests slight contribution of long-tailed macaques to the gene pool of the WTPMH population. Further sampling of other macaque populations within the zone and genetic analysis are essential to address better the question of hybridization. Determination of the distribution and range of biobehavioral variation of macaques within the zone is urgently needed, because their habitat is being rapidly destroyed by deforestation, and their demography and social structure are threatened by artificial disturbance.     

The fine structure of the conducting system of the monkey heart (Macaca mulatta)

Summary In the sino-atrial (S-A) node of the monkey heart two types of muscle cells occur: 1. typical nodal cells which are the predominant cells and form the nodal fibers. 2. Intercalated clear cells with various diameters (4 to 12 m) and containing poorly developed myofibrils, rich in glycogen and demonstrating poor staining properties. These latter cells are dispersed, few in number, and never form discrete fibers of themselves, but are intercalated between the cell rows of the typical nodal fibers. Such intercalated clear cells become more numerous at the periphery of the node. Interconnection between the S-A node and the conventional atrial muscle is established by a progressive transformation of nodal fibers into atrial fibers producing an intermediate (or junctional) type of fiber at the nodal periphery. However, in addition, few nodal fibers make direct contact with the atrial cardiocytes. Our light and EM studies have failed to prove the existence of truly specialized internodal pathways. Nevertheless intercalated clear cells, nodal-like cells, junctional or intermediate type of cells are relatively frequent in valvular regions (Thebesian, Eustachian, A-V, fossa ovalis) and less frequent in other regions of the atrial wall.This study was conducted in part in the Department of Histology and Embryology of the Medical University in Budapest.     

Biochemical genetics of macaques. I. 6-phosphogluconate dehydrogenase polymorphisms in Macaca mulatta and Macaca speciosa

Starch gel electrophoresis of erythrocytes from 1812 Macaca mulatta has unequivocally demonstrated that the 6-phosphogluconate dehydrogenase (6PGD) isozymes are controlled by two autosomal codominant alleles. Limited data on erythrocytes from 89 Macaca speciosa were also consistent with autosomal codominance.This work was supported in part by NIH Grants HD 07835 (WHS) and RR-00167 (Wisconsin Regional Primate Research Center) and by the Research Committee of the UW Graduate School (Project No. 170207).Paper No. 2146 of the Laboratory of Genetics, and Publication No. 16-045 of The Wisconsin Regional Primate Research Center.