Ontogeny of locomotion in rhesus macaques (Macaca mulatta): II. Postural and locomotor behavior and habitat use in a free-ranging colony.

This study quantifies changes in postural and locomotor behavior as well as habitat use across the life span of free-ranging rhesus macaques (Macaca mulatta) in the Cayo Santiago colony in Puerto Rico. It focuses on developmentally related changes from birth to adulthood, and complements an earlier study by Turnquist and Wells ([1994] J Hum Evol 26:487-499) on the early postnatal ontogeny of the musculoskeletal system of the same colony. A total of 6,551 locomotor and postural events was analyzed. Selection and use of substrate correlated well with age. The more sedentary adult and dependent infant select safe, wide, horizontal arboreal settings in contrast to the older Infant IIs and Juveniles, who are learning locomotor and postural skills through independent chase and play. Infant macaques, when independent, often employ a low center of gravity and widely abducted limbs in order to broaden their contact with the base of support. This study shows that the previously reported ontogenetic changes in morphology are closely paralleled by changes in postural and locomotor behavior, and these in turn are correlated to changes in habitat use, particularly during the formative years.

Bone mineral density, osteopenia, and osteoporosis in the rhesus macaques of Cayo Santiago.

This cross-sectional study investigates metabolic bone disease and the relationship between age and bone mineral density (BMD) in males and females of a large, well-documented skeletal population of free-ranging rhesus monkeys (Macaca mulatta), from the Caribbean Primate Research Center Museum collection from Cayo Santiago, Puerto Rico. The sample consists of 254 individuals aged 1.0-20+ years. The data consist of measurements of bone mineral content and bone mineral density, obtained from dual-energy X-ray absorptiometry (DEXA), of the last lumbar vertebra from each monkey. The pattern of BMD differs between male and female rhesus macaques. Females exhibit an initial increase in BMD with age, with peak bone density occurring around age 9.5 years, and remaining constant until 17.2 years, after which there is a steady decline in BMD. Males acquire bone mass at a faster rate, and attain a higher peak BMD at an earlier age than do females, at around 7 years of age, and BMD remains relatively constant between ages 7-18.5 years. After age 7 there is no apparent effect of age on BMD in the males of this sample; males older than 18.5 years were excluded due to the presence of vertebral osteophytosis, which interferes with DEXA. The combined frequency of osteopenia and osteoporosis in this population is 12.4%. BMD values of monkeys with vertebral wedge fractures are generally higher than those of virtually all of the nonfractured osteopenic/osteoporotic individuals, thus supporting the view that BMD as measured by DEXA is a useful but imperfect predictor of fracture risk, and that low BMD may not always precede fractures in vertebral bones. Other factors such as bone quality (i.e., trabecular connectivity) should also be considered. The skeletal integrity of a vertebra may be compromised by the loss of key trabeculae, resulting in structural failure, but the spine may still show a BMD value within normal limits, or within the range of osteopenia.

Skeletal survey of Cayo Santiago rhesus macaques: osteoarthritis and articular plate excrescences.

OBJECTIVES: This study was performed to complement studies on spondyloarthropathy in rhesus macaques by quantifying and characterizing another major form of arthritis and contrasting it with osteoarthritis. METHODS: Skeletons of 269 macaques of known age and troop affiliation from the free-ranging Cayo Santiago colony (Caribbean Primate Research Center) were macroscopically surveyed for the presence of articular changes of osteoarthritis, articular plate excrescences, and calcifications that project back over the joint surface in all diarthrodial joints. Statistical tests were used to establish the independence of pathological conditions, age, gender, troop membership, and specific joint involvement. RESULTS: Subchondral articular surface excrescences or calcific plate-like articular surface overgrowth were noted in 17% and osteoarthritis in 18% of Cayo Santiago macaques. Distribution of joint involvement and sex ratio (1:1) of the former condition were independent of either troop membership or the distribution of osteoarthritis. CONCLUSION: Three major forms of arthritis are common in rhesus macaques: osteoarthritis, spondyloarthropathy, and a category that might be referred to as apical plate excrescences (APE). The latter is very different from spondyloarthropathy, rheumatoid arthritis, osteoarthritis, gout, and infectious arthritis. It is quite similar to what in the past has been referred to as the radiographic form of calcium pyrophosphate deposition disease (CPPD) in humans. A new name has not been offered for the identification/categorization of this phenomenon in dry bone. Its occurrence in rhesus macaques appears to present a natural model for characterization of genetic, immunologic, and environmental aspects of this phenomenon. The acronym APE is offered for consideration in naming this category of arthritis in skeletal material.

Pendular motion in the brachiation of captive Lagothrix and Ateles.

Pendular motion during brachiation of captive Lagothrix lagothricha lugens and Ateles fusciceps robustus was analyzed to demonstrate similarities, and differences, between these two closely related large bodied atelines. This is the first captive study of the kinematics of brachiation in Lagothrix. Videorecordings of one adult male of each species were made in a specially designed cage constructed at the DuMond Conservancy/Monkey Jungle, Miami, FL. Java software (Jandel Scientific Inc., San Rafael, CA) was used for frame-by-frame kinematic analysis of individual strides/steps. Results demonstrate that the sequence of hand and tail contacts differ significantly between the two species with Lagothrix using a new tail hold with every hand hold, while Ateles generally utilizes a new tail hold with only every other hand hold. Stride length and stride frequency, even after adjusting for limb length, also differ significantly between the two species. Lagothrix brachiation utilizes short, choppy strides with quick hand holds, while Ateles uses long, fluid strides with longer hand holds. During brachiation not only is Lagothrix's body significantly less horizontal than that of Ateles but also, within Ateles, there are significant differences between steps depending on tail use. Because of the unique nature of tail use in Ateles, many aspects of body positioning in Lagothrix more closely resemble Ateles steps without a simultaneous tail hold rather than those with one. Overall pendulum length in Lagothrix is shorter than in Ateles. Tail use in Ateles has a significant effect on maximum pendulum length during a step. Although neither species achieves the extreme pendulum effect and long period of free-flight of hylobatids in fast ricochetal brachiation, in captivity both consistently demonstrate effective brachiation with brief periods of free-flight and pendular motion. Morphological similarities between ateline brachiators and hylobatids are fewer and less pronounced in Lagothrix than in Ateles. This study demonstrates that Lagothrix brachiation is also less hylobatid-like than that of Ateles.

Naturally occurring inflammatory arthritis of the spondyloarthropathy variety in Cayo Santiago rhesus macaques (Macaca mulatta).

OBJECTIVE: The establishment of an animal model is a major priority in the battle to control inflammatory arthritis. Exploration to date has not yet identified a viable model for rheumatoid arthritis (RA), while artificial (e.g., collagen-induced) models do not seem to accurately represent RA. They, at least superficially, resemble human spondyloarthropathy. This study assesses the evidence for a common naturally-occurring spondyloarthropathy in a colony of free-ranging rhesus macaques. METHODS: Skeletal elements of 275 Macaca mulatta of known age and troop affiliation from the Cayo Santiago colony [Caribbean Primate Research Center (CPRC)] were surveyed for the presence of spondyloarthropathy and osteoarthritis. Fisher exact tests established the independence of each pathological condition, age, sex, troop and specific joint. RESULTS: Spondyloarthropathy was evident in 10% of females and 7% of males. In surviving troops, its frequency in 82 animals over 8 years of age was 20%. The skeletal distribution of spondyloarthropathy was independent of troop membership. Osteoarthritis affected 20% of females and 4% of males and was independent of their troop. Significant differences in the frequencies of specific joint involvement were found when the natural model, particularly in the polyarticular subgroup, was compared to the collagen-induced model. CONCLUSIONS: Naturally-occurring spondyloarthropathy afflicts 20% of susceptible-aged individuals in surviving macaque troops at the CPRC. This phenomenon appears to present a unique natural model for the characterization of the genetic, immunological and environmental contributions to this disease, which afflicts 0.5-5% of the human population. This natural model would appear to supplant the need for the collagen-induced large animal model.

Osteoarthritis of the hand in nonhuman primates: a clinical, radiographic, and skeletal survey of Cayo Santiago rhesus macaques.

We describe the relative prevalence and pattern of distribution of osteoarthritis (OA) in the hands of elderly (> 15 years) rhesus macaques using clinical, radiographic, and skeletal examinations. In the clinical study the prevalence of nodes was 72% and 16% in the distal inter-phalangeal joints (DIPJ) and proximal inter-phalangeal joints (PIPJ), respectively, 31% of all monkeys had polyarticular nodes. Radiographic OA was present in 55%, 9.1%, and 0% of the DIPJs, PIPJs, and thumb base, respectively. Skeletal OA as defined by joint surface eburnation for the DIPJ, PIPJ, and thumb base were 16%, 8%, and 2%, respectively. A similar pattern of hand OA with humans is described except for the thumb base OA. This may be due to the relatively rudimentary manipulative role of the macaque thumb. The finding of polyarticular nodal OA raises the possibility of a common pathogenensis for IPJ OA amongst primates.

Current status of the Caribbean Primate Research Center Museum.

The history of the Caribbean Primate Research Center Museum, including the Cayo Santiago Skeletal Collection, is briefly reviewed. Since 1971 skeletons of free-ranging rhesus monkeys from Cayo Santiago have been systematically collected for osteological research. Since 1981 the skeletons from the six species of New and Old World monkeys maintained at Sabana Seca have also been collected. The CPRC Museum was established the following year to house this comparative skeletal collection, as well as alcohol-stored tissue specimens and a library. The current status of the collection, including numbers and types of specimens, and use policies, are presented to give an overview of the research potential of the Museum for biological, anthropological, pathological, and biomedical research.

Reduction of passive extension and radiographic evidence of degenerative knee joint diseases in cage-raised and free-ranging aged rhesus monkeys (Macaca mulatta).

The knee joints of aged (greater than or equal to 15 years) rhesus macaques raised and maintained in individual cages were compared with those of formerly free-ranging monkeys using radiographs and measures of passive joint flexion and extension. Free-ranging monkeys had a significantly higher prevalence (p less than 0.01) and severity (p less than 0.0003) of degenerative joint diseases (osteoarthritis and/or pseudogout) based on radiographic findings and significantly (p less than 0.02) more restricted passive knee joint extension than caged animals of the same age.

Passive joint mobility in patas monkeys (Erythrocebus patas): rehabilitation of caged animals after release into a free-ranging environment.

A previous study of passive joint mobility in patas monkeys (Erythrocebus patas) showed that laboratory-caged animals had significantly greater mobility in most joints than age/sex matched free-ranging monkeys. Passive joint mobility on 27 of the same animals was measured 6 months after the caged animals were released onto a 40-hectare island. The results show that within 6 months of becoming free-ranging, typical passive joint mobility is restored. Thus, although caging directly affects measurements of morphologically-determined features in patas monkeys, confinement itself does not necessarily prevent rehabilitation if the immature monkeys are released into a free-ranging environment.

Reproductive performance, population dynamics and anthropometrics of the free-ranging Cayo Santiago rhesus macaques.

This report summarizes demographic data collected on the Cayo Santiago colony of rhesus monkeys from 1976-1983 and compares the results with those from 1959-1964 [8,9]. For males and nonpregnant/nonlactating, pregnant, and lactating females mean (+/- 1 SD), body weights, crown-rump lengths, and ponderal indices are tabulated for each age on a large (n = 586) single sampling of this free-ranging population of macaques.

Forelimb musculature and ligaments in Ateles, the spider monkey.

The forelimb anatomy of Ateles, the spider monkey, is a key factor in its locomotor adaptation because of its extensive use of bimanual suspensory locomotion in addition to climbing and quadrupedal walking (Mittermeier, 1978; and Fleagle and Mittermeier, 1980). The detailed description of the muscles and ligaments of the forelimb of Ateles provided in this paper can be of considerable use not only to primate morphologists interested in both extant and fossil primates but also to functional anatomists. All measurements were made on fresh, unembalmed specimens. Standard anatomical descriptions of the musculature, cross-sectional areas of the muscles, dry weights of muscle bellies, and relative proportions of antagonistic muscles are reported as are the joint ligaments and potential range of motions of the joints. These anatomical data are compared briefly to published data on Alouatta, the howler monkey, which is predominantly a quadruped (Fleagle and Mittermeier, 1980; and Schön Ybarra, 1982).

Influence of age, sex, and caging on joint mobility in the patas monkey (Erythrocebus patas).

Normal range of joint mobility in the extremities of the patas monkey, Erythrocebus patas, was established for a free-ranging colony of 64 animals at La Parguera, Puerto Rico (Caribbean Primate Research Center). Eighty-five animals that had been caged (30" X 30" cages) for up to 5 years were used for comparison. Passive joint mobility of anesthetized animals was measured with a goniometer. Nine parameters (five on the forelimb and four on the hindlimb) were measured on each animal. The data were sorted into subsets according to the animal's age, sex, place of birth, and type of confinement, if any. The number of animals in each subset was recorded and the mean (in degrees) and standard deviation for each parameter were calculated. A P less than or equal to 0.05 on two-tailed Student's t-tests was considered significant. Comparisons between free-ranging males and females showed significant differences in one or two parameters for all age groups. A cross-sectional sample of free-ranging animals of both sexes showed that significant changes in joint mobility occurred only in the first 18 months of life. Joint mobility of all caged animals, however, was highly variable, and even between the more mature animals there were significant differences in several parameters. Almost all comparisons of subsets of the same age and sex showed significant differences between caged and free-ranging animals in at least one parameter. When the caged animals were laboratory-born, however, these differences were significant in five out of nine parameters. The results suggest that, although caging itself affects joint mobility, the age of first confinement may have an even greater effect than the length of the confinement.

Blood values of free-ranging patas monkeys (Erythrocebus patas).

Free-ranging patas monkeys (Erythrocebus patas) from El Guayacán island, Puerto Rico, were surveyed to establish values for the hemogram, serum biochemicals, calcium, and phosphorus. Results were tabulated for males and nonpregnant/nonlactating, pregnant, and lactating females. A summary of blood values from previous studies on captive patas monkeys was also tabulated for comparison.