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Rhesus macaque (Macaca mulatta) group formation and housing: wounding and reproduction in a specific pathogen free (SPF) colony.

In the present report, we examined the effects of group formation strategy and corral design on wounding and reproduction rates in rhesus macaques. Specifically, we examined group formation using a staged strategy, in which small groups of animals were introduced incrementally over a period of weeks, and a rapid formation strategy, in which all animals were introduced in 1 day. We also examined group formation using a divided corral design that facilitated visual and social separation of individuals, and an undivided corral design that did not facilitate visual or social separation. Dependent measures were wounding and reproductive rates over each of the 2 years that followed group formation. Results indicate that incrementally releasing subgroups of animals, and using a corral design that provides for visual and social separation of individuals, are effective strategies for reducing rates of traumatic wounding when forming multimale-multifemale rhesus macaque breeding groups. However, it must be noted that differences in formation strategy and corral design did not lead to higher reproductive rates. We conclude that incrementally releasing animals in hierarchical subgroups, and using a divided vs. undivided housing design, reduced intra-group wounding and associated demands on veterinary and animal management resources following formation of rhesus macaque breeding groups.

Animals↗

Linear enamel hypoplasia in gibbons (Hylobates lar carpenteri).

This study describes the expression of linear enamel hypoplasia (LEH), a sensitive dental indicator of physiological stress, in Thailand gibbons (Hylobates lar carpenteri). Previous studies of enamel hypoplasia in hominoids have focused on great apes, with little attention given to the expression of this stress indicator in gibbons. In that gibbons differ from both monkeys and great apes in numerous life history features, LEH expression in gibbons might be expected to show significant differences from both. In this study, 92 gibbon specimens from two sites in Thailand were compared with several samples of monkeys and great apes in their expression of LEH. The intertooth distribution of LEH in gibbons was compared to that of chimpanzees and rhesus monkeys. Gibbon populations from both sites exhibit LEH frequencies intermediate between those of the monkey samples, in which LEH prevalence is usually low, and those of the great ape samples, in which LEH prevalence is high. Gibbons differ significantly from monkeys, but not great apes, in the number of individuals whose teeth record multiple stress events. Multiple episodes of stress are rarely recorded in the teeth of monkeys, while multiple stress events occur with higher frequency in gibbons and great apes. Taxonomic variation in the duration of crown formation, the prominence and spacing of perikymata on dental crowns, life history features, and/or experience of physiological stress may explain these patterns. The intertooth distribution of LEH in gibbons is, for different reasons, unlike that of either chimpanzees or rhesus monkeys. The mandibular canines of gibbons have significantly more LEH than any of their other teeth. Aspects of crown morphology, perikymata prominence/spacing, enamel thickness, and crown formation spans are potential causes of taxonomic variation in the intertooth distribution of LEH.

Animals↗

Myxoma of bone in a nonhuman primate.

A myxoma of the mandibles in an adult female Macaca mulatta is described. The left mandible was markedly enlarged by the tumor, which extended from the symphysis to the temporomandibular joint. The tumor had extended a short distance across the symphysis into the right mandible. It was composed of a glistening mucinous material. Radiographs of the tumor showed a large expansile radiolucent lesion of the left mandible without soft tissue involvement. Light microscopy demonstrated capillaries, stellate shaped cells with processes up to 15 mu long, very few other cell types, and an amorphous ground substance. Electron microscopic examination revealed similarity to the myxoma of bone of man. The oxytalan fibers discovered in this myxoma have not been found in myxomas before and suggest the tumor is odontogenic in origin. The incidence of spontaneous neoplasia in general and that of spontaneous oral tumors in particular in nonhuman primates are reviewed.

Animals↗

Prevalence of antibodies to selected viruses in a long-term closed breeding colony of rhesus macaques (Macaca mulatta) in Brazil.

The rhesus macaque breeding colony of the Oswaldo Cruz Foundation (FIOCRUZ) was established in 1932 from a founding stock of 100 animals. This population has remained closed to new animal introductions for almost 70 years. A serologic survey was performed to determine the prevalence of antibodies to selected viruses as a first approach to identifying viral pathogens endemic in this population. Banked serum samples were tested for antibodies to simian immunodeficiency virus (SIV), simian T-lymphotropic virus (STLV), simian type D retrovirus (SRV), cercopithecine herpesvirus type-1 (B virus), rhesus cytomegalovirus (RhCMV), measles virus (MV), and hepatitis A virus (HAV). All samples were negative for antibodies against the simian retroviruses. The overall prevalence of antibodies was 95% for RhCMV, 45% for B virus, 35% for HAV, and 1% for MV. Prevalence was found to vary by age group.

Animals↗

Scalp EEG for the diagnosis of epilepsy and photosensitivity in the baboon.

Spontaneous seizures have been observed in several baboon species housed at the Southwest National Primate Research Center (SNPRC), including Papio hamadryas anubis and cynocephalus/anubis, hamadryas/anubis, and papio/anubis hybrids. The goal of this study was to establish a noninvasive, reliable electroencephalographic technique to characterize epilepsy phenotypes and assess photosensitivity in these subspecies. Thirty baboons with witnessed seizures, and 15 asymptomatic baboons underwent scalp electroencephalograms (EEGs) with photic stimulation (PS). The sensitivity and specificity of surface EEG for identifying interictal epileptic discharges (IEDs) in baboons with witnessed seizures were examined. The morphology of IEDs, electroclinical features of seizures and responses to PS, reproducibility of EEG findings, and intrarater reliability were also evaluated. Twenty-three seizure baboons (77%) demonstrated IEDs, predominantly with frequencies of 4-6 Hz in 18 baboons and 2-3 Hz in six baboons. Two seizure animals had a mixture of 2-3-Hz and 4-6-Hz IEDs. All animals with 2-3-Hz IEDs were 3 years old or younger. Myoclonic seizures (MS) and generalized tonic-clonic seizures (GTCS) were recorded in 13 baboons (43%). PS activated IEDs in 15 baboons (50%) and seizures in nine baboons. The presence of IEDs or seizures was not associated with a particular gender or species (Fisher exact test, alpha=0.05). Seizures were more common in animals >3 years old, while PS-induced IEDs and seizures were more prevalent in P.h. anubis/cynocephalus crosses compared to P.h. anubis. In the asymptomatic controls, IEDs were recorded in five baboons (33%), and photoparoxysmal responses were observed in two (13%). Surface EEG is a sensitive and reliable instrument for characterizing the epilepsy encountered in Papio species. Electroclinically, the seizure animals had generalized epilepsy with photosensitivity. The variation in IED morphology may be age-related or it may reflect different epileptic phenotypes. Ketamine provoked IEDs and seizures in most seizure animals and only in a few asymptomatic baboons; therefore, it may enhance the sensitivity of surface EEG for detecting a predisposition to epilepsy.

Animals↗

Transmission of STLV in a closed colony of macaques.

A 3.3% seroprevalence of simian T-lymphotropic virus (STLV) was found in a closed breeding and research colony of rhesus and cynomolgus macaques in Thailand. Epidemiology of STLV within the colony was assessed by means of a retrospective analysis of banked and freshly collected serum samples, and a review of the animals' medical records. Evidence was found that the virus had been imported into the colony by some of the original animals, and was subsequently transmitted both vertically and horizontally. The cell-associated nature of STLV was demonstrated by iatrogenic transmission of the virus following a whole blood transfusion, but there was no transmission to animals that received only serum from the same infected donor. Transmission by all routes was infrequent, as indicated by the overall seroprevalence of 3.3% (14 of 420 samples) after the colony had been closed for 11 years. Maternal-infant transmission appeared to be < 12%.

Animals↗

Tetanus antibody titers and duration of immunity to clinical tetanus infections in free-ranging rhesus monkeys (Macaca mulatta).

Prior to 1985 tetanus was a major cause of mortality in the free-ranging colony of rhesus monkeys on Cayo Santiago, accounting for almost a quarter of annual deaths. In 1985 and 1986 all animals (except infants) received primary and booster doses, respectively, of tetanus toxoid. In subsequent years primary immunizations were given to all yearlings, and boosters were administered to all 2-year-old animals during the annual capture of the colony. The main objectives of the tetanus immunization program were to reduce the pain and suffering caused by tetanus infections and to decrease mortality in the colony. Other objectives were to evaluate the efficacy of the two-dose tetanus toxoid immunization protocol and to determine whether additional boosters might be required to provide adequate long-term protection against tetanus infections. The immediate effect of the mass immunization program was the elimination of clinical tetanus infections in the population and a 42.2% reduction in the overall mortality rate. Since the immunization program began, no cases of tetanus have been observed in the colony, except in two unimmunized infants, and it has not been necessary to give tertiary injections of tetanus toxoid to maintain protection against infection. A sample collected in 2004 of the original cohort of monkeys immunized in 1985 and 1986 showed that 93.3% (14/15) had protective tetanus antibody titers (>0.01 IU/ml) at the ages of 20-23 years, which is close to the life expectancy of the Cayo Santiago rhesus macaques. Two intramuscular doses of tetanus toxoid provided long-term, if not lifelong, protection against tetanus for rhesus monkeys living in a tropical clime where tetanus is enzootic and the risk of infection is great.

Animals↗

Human culture and monkey behavior: Assessing the contexts of potential pathogen transmission between macaques and humans.

An in-depth understanding of the contexts and patterns of human-macaque interactions can play an important role in assessing and managing the potential for pathogen transmission. The Padangtegal Monkey Forest in Bali, Indonesia, and the Upper Rock Nature Reserve in Gibraltar are two sites that have been relatively well studied in regard to human-macaque interactions. This article presents an overview of interaction patterns between humans and macaques at these sites along with a description of the cultural, demographic, and contextual differences between local and nonlocal humans at the sites. Differences in these two sites' interaction patterns included bite rates, the role of food in aggressive interactions, and the context in which the interactions took place. Similarities included overrepresentation by adult male macaques in interactions and a substantial impact by local cultural and demographic factors. These similarities and differences are interpreted as resulting from differences in macaque species and behaviors, and human demography, culture, and behavioral patterns.

Adolescent↗

Seasonal or ecological differences in diet and molar microwear in Cebus nigrivittatus.

Dental microwear analyses have raised new hopes and questions for functional morphologists. One hope is that analyses will allow insights into subtle dietary differences of extinct species. One major question is whether seasonal and/or habitat differences in dental microwear are reliably detectable. The extensive collections of Cebus nigrivittatus obtained by the Smithsonian Venezuelan Project allowed us to examine seasonal and habitat differences in dental microwear. Specimens were collected from three distinct ecological life zones that are distinguished by both the amount of rainfall and its seasonability. Environmental variation is generally correlated with variation in resource availability which, in C. nigrivittatus, affects diet. Published field studies indicate that these animals depend more on dry hard fruit and chitinous invertebrates during drier times and succulent fruits and caterpillars during wetter times of the year. As in previous microwear analyses, epoxy replicas were prepared from dental impressions, and the replicas were examined under a scanning electron microscope. Two micrographs were taken of facet 9 on M2 of each specimen. Mean values for the proportion of pits (vs. scratches), pit width, and scratch width were computed for each of 62 individuals and compared between ecological zones and collecting dates by using a multiple comparison test. Results indicate that, while seasonal differences in molar microwear in C. nigrivittatus are perhaps reliably detectable, 1) they are small in magnitude, 2) they are only detectable in certain ecological life zones, and 3) they are not of the order of magnitude that will obscure major interspecific differences in molar microwear such as those between C. apella and C. nigrivittatus.

Analysis of Variance↗

Changes in skull components of the squirrel monkey evoked by growth and nutrition: an experimental study.

Twenty weanling 6-month-old male squirrel monkeys were allotted to the following treatments: 1) first control animals were killed at weaning; 2) second control animals were killed when 24 months old; and 3) malnourished animals were fed on a low-protein diet and killed at age 24 months. Lateral and vertical teleradiographies were taken. Growth of the neurocranial and splanchnocranial components were measured by volumetric (size estimators) and morphometric (shape estimators) indices. All facial components grew. The neurocranial components showed a heterogeneous behavior: The anteroneural component remained stable, and the increase of the midneural component was compensated by a decrease in the posteroneural component. Malnutrition affected the growths of 1) the craniofacial complex, 2) the splanchnocranium, and 3) the respiratory and midneural components. Growth influenced skull shape through 1) increases of the splanchnocranium and the midneural component relative to the neurocranium; 2) decreases of the masticatory and optic components relative to the splanchnocranium, and 3) decreases of the anteroneural and posteroneural components relative to the neurocranium. Malnutrition influenced skull shape through the relationship between the anteroneural component and the neurocranium. These results confirmed the existence of functional interrelationships among the cranial components. A new approach to craniological studies is suggested.

Animal Nutritional Physiological Phenomena↗

Morphology of the pubis and preauricular area in relation to parity and age at death in Macaca mulatta.

Some adult human females show bone resorption (pitting) at the dorsal aspect of the pubis and preauricular area of the ilium. The etiology of pelvic bone resorption is attributed alternatively to reproduction and to pelvic anatomy. While most researchers infer that pelvic pitting is related to reproduction, only a few studies are based on women of known parity. Degree of pubic resorption is directly associated with both parity (Suchey et al.: Am. J. Phys. Anthropol. 51:517-539, 1979; Bergfelder and Hermann: J. Hum. Evol. 9:611-613, 1980) and age (Suchey et al.: Am. J. Phys. Anthropol. 51:517-539, 1979). The relationship between parity and degree of resorption of the preauricular area is equivocal, found to be significant by Dunlap (A Study of the Preauricular Sulcus in a Cadaver Population, Ph.D. dissertation, East Lansing, Michigan State University, 1981) but not by Spring et al. (Am. J. Phys. Anthropol. 79:247-252, 1989); both studies report that age is not associated with resorption of the preauricular area. Other mammals evidence public resorption, but the morphology of the preauricular area is less well known. This study addresses the issue on the etiology of pelvic bone resorption using a sample of Macaca mulatta (the free-ranging population from Cayo Santiago) for which parity and age at death are known for all specimens. The following results are reported. Resorption of the pubis is common among females but infrequent among males. Contrary to Rawlins (Am. J. Phys. Anthropol. 42:477-488, 1975), the degree of pubic resorption in female macaques is significantly related to both parity and age at death.(ABSTRACT TRUNCATED AT 250 WORDS)

Age Factors↗

Dental microwear in live, wild-trapped Alouatta palliata from Costa Rica.

One problem with dental microwear analyses of museum material is that investigators can never be sure of the diets of the animals in question. An obvious solution to this problem is to work with live animals. Recent work with laboratory primates has shown that high resolution dental impressions can be obtained from live animals. The purpose of this study was to use similar methods to begin to document rates and patterns of dental microwear for primates in the wild. Thirty-three Alouatta palliata were captured during the wet season at Hacienda La Pacifica near Canas, Costa Rica. Dental impressions were taken and epoxy casts of the teeth were prepared using the methods of Teaford and Oyen (1989a). Scanning electron micrographs were taken of the left mandibular second molars at magnifications of 200x and 500x. Lower magnification images were used to calculate rates of wear, and higher magnification images were used to measure the size and shape of microwear features. Results indicate that, while basic patterns of dental microwear are similar in museum samples and samples of live, wild-trapped animals of the same species, ecological differences between collection locales may lead to significant intraspecific differences in dental microwear. More importantly, rates of microwear provide the first direct evidence of differences in molar use between monkeys and humans.

Alouatta↗

Dental microwear and diet in Venezuelan primates.

Recent microwear analyses have demonstrated that wear patterns can be correlated with dietary differences. However, much of this work has been based on analyses of museum material where dates and locations of collection are not well known. In view of these difficulties, it would be desirable to compare microwear patterns for different genera collected from the same area at the same time. The opportunity to do this was provided by the collections of the Smithsonian Venezuelan Project (Handley, 1976), in which multiple primate genera were collected from the same humid tropical forest sites within the same month. The monkeys represent a wide range of dietary preferences, and include Saimiri, Cebus, Chiropotes, Ateles, Aotus, Pithecia, and Alouatta. As in previous microwear analyses, epoxy replicas were prepared from dental impressions, as described by Rose (1983) and Teaford and Oyen (1989). Two micrographs were taken of facet 9 on an upper second molar of each specimen. Computations and analyses were the same as described by Teaford and Robinson (1989). Results reaffirm previously documented differences in dental microwear between primates that feed on hard objects versus those that do not--with Pithecia and Alouatta at the extremes of a range of microwear patterns including more subtle differences between species with intermediate diets. The subtle microwear differences are by no means easy to document in museum samples. However, additional results suggest that 1) the width of microscopic scratches may be a poor indicator of dietary differences, 2) large and small pits may be formed differently, and 3) there are very few seasonal differences in dental microwear in the primates at these humid tropical forest sites.

Analysis of Variance↗

Matrilineal distribution of louse egg-handling techniques during grooming in free-ranging Japanese macaques.

Grooming behavior of which the primary function appears to be the removal of lice on other (Tanaka and Takefushi [1993] Anthropological Science 101:187-193) was studied in Japanese maceques at Jigokudani Monkey Park, Japan, June 1990-July 1993. Several louse egg-handling techniques used during grooming were identified (with differences in efficiency) in a free-ranging group. In the low-ranking maternal lineages, the distribution of these techniques is quite homogeneous, suggesting social transmission with goal emulation (one form of social learning) based on maternal kin. However, there is considerable variation in the high-ranking matriline. The social system of dominance--the tendency of subordinates to groom more often than to be groomed--may result in oblique transmission of more effective techniques from low-ranking monkeys to some offspring of high-ranking females.

Animals↗

Brief communication: linear enamel hypoplasia and the shift from irregular to regular provisioning in Cayo Santiago rhesus monkeys (Macaca mulatta).

This study investigates changes in the prevalence of linear enamel hypoplasia (LEH) before and after the shift from irregular to regular provisioning in the Cayo Santiago rhesus monkey population. Prior to 1956, monkeys on this island colony did not receive consistent provisions, and were reported to be in poor health (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). A regular provisioning program, instituted in August 1956, resulted in the improved health of individuals and the growth of the population (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). LEH, a developmental defect of enamel, is a sensitive indicator of systemic physiological stress (Goodman and Rose [1990] Yrbk. Phys. Anthropol. 33:59-110). It was therefore hypothesized that the prevalence of LEH would be higher in monkeys who were irregularly provisioned than in monkeys who experienced regular provisioning. To test this hypothesis, teeth were examined for LEH in a sample of 181 female rhesus monkeys. The results support the hypothesis: the mean number of defects was statistically significantly higher in the preprovisioned group than it was in the postprovisioned one. When LEH prevalence was assessed using only defects occurring on antimeric pairs, the preprovisioned group again had a higher prevalence than the postprovisioned one, although the difference was not statistically significant, most likely because of the reduced sample size. The results of this study indicate that changes in LEH prevalence, at least in this population of rhesus monkeys, are associated with changes in nutritional status.

Animals↗

Comparison of simian immunodeficiency virus and human immunodeficiency virus encephalitides in the immature host.

The simian immunodeficiency virus (SIV) is closely related to the human immunodeficiency virus (HIV) in genomic organization and morphology. More important, SIV and HIV are both primate lentiviruses that cause transmissible immunodeficiency and encephalitis, with an apparently increased virulence in the immature host. The neuropathological features in common between SIV encephalitis in juvenile macaque monkeys and HIV encephalitis in children include the invasion of brain with virus-laden macrophages, the formation of multinucleated (syncytial) giant cells, and white matter lesions and subtle white matter astrocytosis. Important differences include giant cell leptomeningitis and evidence of necrosis and karyorrhexis in brain macrophage infiltrates in SIV-infected monkeys. These changes probably represent a more acute inflammatory process. The importance of future studies to define pathogenetic features of SIV encephalitis, using molecularly characterized isolates with varying neurovirulence and host range, are emphasized.

Acquired Immunodeficiency Syndrome↗