Effect of tetanus toxoid inoculation on mortality in the Cayo Santiago macaque population

Tetanus was a major cause of mortality in the free-ranging population of rhesus monkeys (Macaca mulatta) on Cayo Santiago. From 1977 to 1984 the mean (±1 SD) annual total mortality rate (excluding neonatal deaths within 48 h postpartum, abortions, and stillbirths) was 6.39% ± .94%, and the mean annual tetanus mortality rate was 1.33% ± .45%. Tetanus deaths accounted for 19.5% of the total mortality in the colony. In 1985, all monkeys on the island, except infants and six adult monkeys, were given primary inoculations of tetanus toxoid. The following year, boosters were administered, and yearlings received primary inoculations. One fatal case of tetanus and one recovery from mild disease occurred in uninoculated adult monkeys in 1985, but no additional cases have been observed since. For 1985–1986 the mean annual total mortality rate was 3.69% ± .05%, and the mean annual tetanus mortality rate was .08% ± .08%. Thus, during the 2 years after inoculation against tetanus, the mean annual total mortality rate and the mean annual tetanus mortality rate declined by 42.2% and 94.0%, respectively, when compared to the 8-year period (1977–1984) prior to inoculation. These differences were significant [(χ² = 12.48; P < .005), (χ² = 16.94; P < .005)]. The elimination of tetanus infections through mass inoculation of the Cayo Santiago colony is expected to have a profound impact on the demography of the population by increasing the rate of population growth, by decreasing the differential rates of increase of the component social groups, and by changing the age distribution of the population.     

Epiphyseal union and dental eruption in Macaca mulatta

Age of dental eruption and epiphyseal fusion is estimated for the permanent dentition and long bone epiphyses of rhesus macaques (Macaca mulatta), with 299 skeletons of individuals with known age of death, from the Cayo Santiago skeletal collection. Epiphyses at a given joint tend to fuse at the same time. While males and females tend to have the same pattern of epiphyseal fusion, females' epiphyses fuse earlier than those of males, espeically at the elbow and knee joints. The order of epiphyseal fusion in rhesus macaques follows the general primate pattern. Times of dental eruption for males and females are generally the same, except for the relatively late eruption of the canine in the males. The order of eruption follows a common primate pattern (dm2?M1?I1?I2?M2?(P3,P4)?C?M3). Multiple regressions were calculated in order to allow determination of developmental state, or predictions of chronological age, from epiphyseal fusion and/or dental eruption scores in juvenile rhesus macaques. Standard deviations of residuals from these regressions indicate considerable variation in developmental state among aminals of the same chronological age. The lack of correlation between residuals from the separate skeletal and dental regressions, indicates that skeletal and dental development are largely independent.     

A study of intragroup biological change induced by social group fission in Macaca mulatta using discrete cranial traits

Eight discrete cranial traits are used as biological indicators to investigate the effect of social group fission on intragroup genetic change leading to intergroup differentiation in Macaca mulatta. The timing of discrete cranial trait frequency change and group fission coincide, indicating a possible causal relationship between fission and genetic change. A significant change in the male mating population during and after fission is proposed as the mechanism causing intragroup genetic change, along with the effects of fluctuations in segregation ratios.     

The hemogram,serum biochemistry,and electrolyte profile of the free-ranging Cayo Santiago rhesus macaques (Macaca mulatta)

Sixty-four male and 33 female free-ranging rhesus monkeys (Macaca mulatta) from one of six social groups on the island of Cayo Santiago, Puerto Rico, were surveyed to establish normal values for the hemogram and serum biochemical and electrolytes for the colony. Mean values (± 1 SD) are reported by sex for each of three age groups (2–3, 4–9 and ≥ 10 years). All adult females (≥ 4 years) were pregnant. There were significant differences for a number of variables compared to the range reported in the existing literature, and among the age and sex groups in the sampled population.     

Aging in the musculoskeletal system of rhesus monkeys: I. Passive joint excursion

In order to describe ontogenetic change in the musculoskeletal system of rhesus monkeys, 126 Macaca mulatta from Cayo Santiago, ranging in age from 7 months to 21 years, were examined under anesthesia. Passive joint excursions were measured at the wrist, elbow, shoulder, hip, and knee. Mean ranges of excursion at these joints differed significantly between age groups and by sex. The potential for most movements appeared to decrease approximately 25 degrees over the first two decades of the macaque life span, and males generally showed less potential for movement than females in all age groups. These results are similar to those obtained for humans and are consistent with patterns of positional behavior, trauma, and osteoarthritis observed in this rhesus monkey population. Thus, to fully describe the locomotor strategy of rhesus monkeys, age- and sex-related variation in locomotor anatomy and functional capacity must be considered.     

Age- and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free-ranging rhesus macaques.

Normative age- and gender-related changes in body composition, serum lipids, testosterone, and insulin-like growth factor (IGF-1) were examined in the Cayo Santiago free-ranging rhesus macaques. In both adult males and females, body weights, crown-rump lengths, and circumference of the limbs were lowest in the oldest group (20+ years of age) as compared with other adult age classes. Body fat, as reflected in subcutaneous fatfold thickness and waist/thigh ratios, were higher in adult females than adult males. This gender dimorphism was first detectable among the 6-9 year old age group. Greatest body fat among females was observed in the 10-14 age group, whereas in males the highest values were observed in the 15-19 age group. Differences in body composition were also observed with respect to reproductive status. Although there were no gender differences in overall cholesterol levels, there were age-related differences between males and females, and only in males were cholesterol values positively related to adiposity. There were no age- or gender-related differences in triglyceride values, but levels were significantly higher in pregnant females in comparison with other reproductive states. Levels of testosterone were not significantly related to any morphometric parameter and values did not decrease significantly with age. Levels of IGF-1 exhibited a significant age-related decrease among adult males, and females had higher levels independent of age. The similarities between the present findings and human studies suggest that further studies in the free-ranging rhesus macaques would provide a bridge between studies of laboratory-housed primates and studies of human beings with respect to the etiology of obesity and life-history changes in body composition and endocrine and metabolic parameters.     

The relationship of tooth size to body size in a population of rhesus monkeys (Macaca mulatta)

Tooth areas correlate significantly with long bone measurements in a skeletal population of rhesus monkeys from Cayo Santiago. Correlations are relatively large for the troop as a whole, as well as for males and females separately. Femur and humerus length measurements show the highest correlations with tooth size.     

Sociometrics of Macaca mulatta: II. Decoupling centrality and dominance in rhesus monkey social networks

The concept of the linear dominance hierarchy and a much less precise notion of a central/peripheral ordering of individuals have been prominent among the ideas about social organization of monkey groups. Although the latter has seldom been quantified, the ranks of individuals in the two orders are usually assumed to be correlated. This paper reports on a longitudinal study of a free-ranging group of rhesus monkeys. The individual histories of progression of dominance rank and an independently determined measure of centrality in the social grooming network are compared among a set of males. Centrality is not a static correlate of dominance rank as implied by the findings of short-term studies. Rather, centrality is a more sensitive indicator of status than is dominance rank, to which it is related in a dynamic fashion. Small changes in dominance rank may be followed by large changes in centrality. An increase in centrality may facilitate rise in dominance rank. These findings suggest a complex psychology of status, rather than a simple causative relation between the two variables.     

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

Abstract: 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 bases, 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.     

The formal hierarchy of rhesus macaques: An investigation of the bared-teeth display

Teeth-baring in a large captive rhesus monkey group (Macaca mulatta) was observed over a 30-month period. Its directional consistency among adults was significantly higher than that of aggression. The unidirectionality was so extreme that the facial display must be seen as a formal status indicator; ie, a signal of which the direction is independent of short-term contextual variation. As such, it seems adapted for communication about the state of the relationship. Formal dominance relationships among adults could be arranged in a hierarchy which approached perfect linearity. Focal observations demonstrated that teeth-baring was associated with withdrawal. It was uncommon among foraging monkeys, perhaps because dominant animals paid less attention to their subordinates in this context. The speed of rank acquisition by young females, in terms of received teeth-baring, was highest among peers and lowest against the group's old matriarchs. The age at which dominance over unrelated adult females was achieved correlated negatively with the amount of affiliative contact with these females. This translates into a positive correlation between bonding and rank establishment, indicating that dominance processes may be indistinguishable from social integration.     

恒河猴细菌感染性子宫出血模型内膜组织基质金属蛋白酶1、9及其抑制剂的表达

目的　探讨基质金属蛋白酶 1、9在炎性子宫出血中的作用。方法　运用免疫组化链霉素抗生物素蛋白 过氧化物酶染色法 (SP)检测细菌感染性子宫出血恒河猴模型组子宫内膜组织中基质金属蛋白酶 1、9(MMP 1、MMP 9)及其抑制剂 (TIMP 1)的表达 ,用正常恒河猴子宫内膜作对照。结果　模型组子宫内膜组织间质、腺上皮中MMP 1、9的表达明显高于正常对照组 ,而TIMP 1的表达与正常组水平相似。结论　基质金属蛋白酶 1、9的高度表达可能与炎症导致的异常子宫出血有关。     

Yersinia pseudotuberculosis infection in breeding monkeys: detection and analysis of strain diversity by PCR

In the last three decades, several monkeys reared in outdoor/indoor-outdoor breeding colonies and cages of the Primate Research Institute, Kyoto University, died of yersiniosis caused by Yersinia pseudotuberculosis, necessitating introduction of a method to detect the bacteria rapidly and thus allow preventive measures to be undertaken. A rapid nested polymerase chain reaction (PCR) method for identification of Y. pseudotuberculosis in fecal samples and a random amplified polymorphic DNA (RAPD)-PCR approach for distinguishing between bacterial strains were therefore developed. Yersinia pseudotuberculosis isolates from monkey specimens were found to be classifiable into several types. To determine the source of infection, hundreds of fecal samples of wild rats, pigeons, and sparrows were collected from around the breeding colonies and cages, and subjected to PCR analyses. Yersinia pseudotuberculosis was detected in 1.7% of the fecal samples of wild rats. The DNA fingerprints of the bacteria revealed by RAPD-PCR were the same as that of one strain isolated from macaques, suggesting the wild rat to be a possible source of infection.     

Behavioral effects of enrichment on singly-housed,yearling rhesus monkeys: An analysis including three enrichment conditions and a control group

Three cohorts of yearling rhesus monkeys (Macaca mulatta) were maintained in single cages for one year as part of a derivation program to produce a breeding colony of specific pathogen-free (SPF) monkeys. During this year of social restriction, subjects were provided with three different types of environmental enrichment (physical, feeding, and sensory) to counteract the known effects of social restriction and to quantify the effects of these different conditions of enhancement on their behavior. Focal animal observations were conducted on enriched and control subjects for all cohorts. Enrichment conditions were presented in a different order to each cohort. Monkeys provided with enrichment spent significantly more time playing and less time self-grooming than did control monkeys in unenriched cages, suggesting that the overall enrichment program was of some benefit to the monkeys, because these changes in behavior were in species-typical directions. Among enriched subjects only, there were significant differences in the amount of time spent drinking, grooming, feeding, playing, exploring, and using enrichment across the three enrichment conditions. Both the physical and feeding enrichment conditions led to species-appropriate changes in behavior, therefore enhancing psychological well-being as some define it. Sensory enrichment was of little benefit. The first cohort was housed indoors, received less stimulation from the environment outside of the single cage, and used enrichment more than did the other two cohorts housed outdoors. This suggests that the external environment influences behavior in the single cage and that enrichment may be most effective for animals housed indoors. © 1995 Wiley-Liss, Inc.     

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.     

Conservation note: Socioecology and conservation of macaques and langurs in Varanasi,India

A survey of rhesus monkeys (Macaca mulatta) and hanuman langurs (Presbytis entellus) was conducted in urban and forest areas of Varanasi, India. Data were collected on group size and composition. Nine groups of rhesus monkeys inhabited various urban niches, but langurs were completely absent from urban areas. Approximately 159 rhesus monkeys and 720 langurs lived in the forested area. Both the urban and the forested habitats of this area are being reduced in size, and it is suggested that these populations be moved to nearby forest preserves.     

News from the molecular frontier. Review of Paternity in Primates: Genetic Tests and Theories R. D. Martin,A. F. Dixson,E. J. Wickings eds. Karger, 1992, xi + 287 pp, $198.50

We have previously demonstrated that the exogenous administration of estradiol-17β (E₂) to rhesus monkeys induces atresia of the dominant preovulatory follicle (DF); and that this effect is mediated centrally, via the inhibition of follicle-stimulating hormone, and is also exerted directly at the level of the ovarian granulosa cell. We wished to investigate whether the local effect of E₂ is transduced through interaction with the nuclear receptor for estrogen, particularly in light of certain evidence that suggests a general lack of estrogen receptor (E-R) in the rhesus monkey ovary, except in the germinal epithelium. In the present study, we evaluated the presence of E-R by both autoradiographic and immunocytochemical techniques. Frozen sections of ovaries from rhesus females were incubated in experiment 1 with either ³H-E₂ or ¹²⁵I-E₂, in the presence or absence of excess, non-radioactive ligand or analogues diethylstilbestrol (DES) or the receptor antagonist 4-OH-tamoxifen (TAM). ³H-E₂ binding was most intense over functional corpora lutea, and was reduced to background with excess DES; label was also evident over antral follicles, Image analysis showed specific binding of ¹²⁵I-E₂ by ovaries. In experiment 2, cryostat sections were processed for immunocytochemical staining using the per-oxidase-anti-peroxidase (PAP) method and the H222 monoclonal antibody to the E-R. Intense, specific label was observed over nuclei of germinal epithelium, but, additionally, for the first time, to granulosa cells of antral follicles and other compartments of the ovary. In this paper, we report the first evidence for estrogen binding to rhesus monkey ovary; tins binding is specific, apparently receptor mediated, and corroborated independently by autoradiographic and immunocytochemical means. We herein provide substantial support for estrogen's dramatic effects being exerted directly at the level of the monkey ovary. © 1993 Wiley-Liss, Inc.     

The origins of allometry: size and shape polymorphism in the common waterstrider, Gerris remigis Say (Heteroptera, Gerridae)

Changes in size, whether ontogenetic or phylogenetic, tend to be associated with changes in shape. This allometry can arise through two different evolutionary mechanisms: (1) selection acting primarily on overall size may be associated with changes in shape because of physiological and mechanical constraints or differential responses of different body components; or (2) selection acting primarily on shape (on the size of specific body components) may be associated with changes in overall size because of genetic correlations, and thus correlated responses, of other body components. To assess the relative importance of these two mechanisms, shape polymorphism is examined along two axes of size dimorphism (sex and wing morphology) in the common waterstrider, Gerris remigis Say. Eight measurements were made of body and appendage components of 234 adults, from three independent populations. Univariate and multivariate analyses reveal that both sexes and wing morphs differ significantly in size and shape. Shape differentiation along the two axes of size dimorphism is found to be dissimilar, partially independent of size, and strongly correlated with the ecological specialization of the various morphs. These observations suggest that selection is acting directly on shape, and thus that allometry in this species primarily reflects shape-mediated changes in size (mechanism 2), rather than size-mediated changes in shape. The role of developmental processes in facilitating this shape differentiation is discussed.     

Effects of inter- and extramuscular myofascial force transmission on adjacent synergistic muscles: assessment by experiments and finite-element modeling

The effects of inter- and extramuscular myofascial force transmission on muscle length force characteristics were studied in rat. Connective tissues at the bellies of the experimental synergistic muscles of the anterior crural compartment were left intact. Extensor digitorium longus (EDL) muscle was lengthened distally whereas tibialis anterior (TA) and extensor hallucis longus (EHL) were kept at constant muscle–tendon complex length. Substantial differences were found in EDL force measured at the proximal and distal tendons (maximally 46% of the proximal force). EDL with intact inter- as well as extramuscular connections had an increased length range between active slack and optimum length compared to EDL with extramuscular connections exclusively: optimum muscle length was shifted by more than 2 mm. Distal EDL lengthening caused the distal force exerted by TA+EHL complex to decrease (approximately 17% of the initial force). This indicates increased intermuscular myofascial force transmission from TA+EHL muscle complex to EDL muscle.

Finite-element modeling showed that: (1) Inter- and extramuscular myofascial force transmission leads to a substantial distribution of the lengths of the sarcomeres arranged in series within muscle fibers. Distribution of stress within the muscle fibers showed that the muscle fiber cannot be considered as a unit exerting equal forces at both ends. (2) Increased heterogeneity of mean fiber sarcomere lengths (i.e., a “parallel” distribution of length of sarcomeres among different muscle fibers) is found, particularly at high muscle lengths. This also explains the shift in muscle optimum length to higher lengths.

It is concluded that inter- and extramuscular myofascial force transmission has substantial effects on muscle length–force characteristics.     

Somatosensory evoked potentials of median and tibial nerves in rhesus monkeys (Macaca mulatta) under captivity: influence of ontogenic status in neonatal, infant, young, adult, and senile stages

Background Somatosensory evoked potentials (SEPs) constitute a useful neurophysiologic tool commonly used to assess the functionality and developmental degree of the nervous system. Objective To analyze somatosensory pathways of the Macaca mulatta species throughout different ontogenetic statuses. Methods Twenty non‐human primates were divided into five age‐dependant groups. Recording of SEPs was executed by stimulation of lower limb at the tibial nerve and upper limb and recorded at the median nerve. Results Two wave series were observed for all groups for both limbs studied. Significant differences were found at the upper right limb at C4, C7 and also for the antecubital fossa site. The lower limbs showed a single significant right‐wing deflection. Conclusions Differences found in signals generated by the nervous system in response to somatosensory stimuli among the studied groups are thought to be developmental in origin, as the most remarkable deviations were seen in younger monkeys.