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.     

Geophagy as a therapeutic mediator of endoparasitism in a free-ranging group of rhesus macaques (Macaca mulatta)

Parasite levels were determined for 141 members of a naturally formed social group of rhesus macaques living under free-ranging conditions. Results indicate that group members harbor Trichuris trichiura, Balantidium coli, and large numbers of Strongyloides fuelleborni. Parasite counts decrease significantly with age in this population. Females have significantly fewer parasites than males and a significantly lower prevalence of multiple infections. There were no rank effects regarding parasitosis. While 89% of the animals examined are infected with one or more species of enteric parasite, the prevalence of diarrhea is negligible (2%). The low prevalence of diarrhea in the presence of high parasite loads may be due to the practice of geophagy, which is engaged in by 76% of group members. Soil eaten by these monkeys contains large amounts of kaolinitic clays. Kaolin-based pharmaceuticals (i.e. Kaopectate^®) are commonly used in human populations to treat diarrhea and intestinal upsets. The mechanical and pharmaceutical properties of the natural kaolinite-based clays may counteract the effects of parasitosis in this free-ranging population. Am. J. Primatol. 44:71-82, 1998. © 1998 Wiley-Liss, Inc.     

Aspects of fight interference in free-ranging and compound-dwelling rhesus macaques (Macaca mulatta)

Patterns of fight interference (agonistic aiding) were compared among three groups of rhesus monkeys (Macaca mulatta) living in two settings: (1) two groups at Cayo Santiago (Caribbean Primate Center); and (2) one group at the Yerkes Regional Primate Research Center (YRPRC). A total of 1,227 interference episodes were recorded in 1,650 hours of observation. The only significant intergroup difference was the increased tendency of males at YRPRC to aid aggressors rather than victims. Among other findings, females aided relatives, interfered against target animals dominant to themselves, aided juveniles, and aided victims more consistently and frequently than did males. Importantly, female interference became more male-like in pattern when aid was given to nonrelatives. Neither the dominant males nor males in general displayed a unique or consistent tendency to interfere in fights in a manner which could be interpreted as controlling aggression. The males' interference patterns also did not suggest they were forming coalitions to either attain or defend status rankings. It is concluded that, overall, observations of compound-dwelling and free-ranging rhesus monkeys reveal similar relationships. Further, while female rhesus monkeys interfered in fights in a manner consistent with the control of aggression and protection of kin, the motives of male interferers remain unknown; however, their behavior is consistent with the hypothesis that they were reducing intermale tensions while, at the same time, minimizing physical risk.     

Multiple sirehood in free-ranging twin rhesus macaques (Macaca mulatta)

Rhesus macaque females regularly copulate with a number of partners, and produce a single offspring per reproductive cycle in over 99% of cases. We used genotyping of 10 STR markers to determine paternity in the Cayo Santiago population of rhesus macaques. About 1,500 monkeys have been analyzed to date, with their marker genotypes entered into a computerized database. These data enable us to report the first documented case in any cercopithecine nonhuman primate species of the production of twin offspring sired by different males.     

The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand

BACKGROUND: Long-tailed and rhesus macaques are widely used in biomedical research; therefore, the known blood group is important. METHODS: The human-type ABO blood group was determined in wild or semi-wild long-tailed and rhesus macaques in Thailand. A total of 729 long-tailed and 160 rhesus macaques from 20 localities were temporarily caught. RESULTS: The frequency profiles of blood groups, calculated by averaging the frequency of each troop in long-tailed and rhesus macaques, were AB > O > B > A at 29.6%, 27.4%, 27.2%, and 15.8%, and B > AB > A > O at 39.6%, 33.4%, 18.2%, and 8.8%, respectively. Irrespective of locality, the frequencies were AB > O > B > A of 29.6%, 28.0%, 24.4%, and 18.0%, and AB > B > A > O of 37.5%, 28.7%, 26.9%, and 6.9%, respectively, for all long-tailed and rhesus macaques. The frequency profile of blood groups in Thai rhesus macaques was somewhat similar to that in the parapatric long-tailed macaques; however, it was different from other rhesus populations where only group B was detected. CONCLUSIONS: Our data support the hypothesis that Indochinese rhesus macaques are hybrids between rhesus and long-tailed macaques in the past.     

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.     

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.     

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.     

Juvenile rheumatoid arthritis in a rhesus monkey (Macaca mulatta)

A juvenile rhesus macaque (Macaca mulatta) developed a symmetrical erosive polyarthritis involving both large and small diarthrodial joints. Neither an infectious nor a metabolic etiology could be determined. This case shares many clinical and pathological features with the polyarticular form of human juvenile rheumatoid arthritis.     

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.     

Sebaceous gland adenoma in a rhesus monkey (Macaca mulatta)

A tumor mass was identified below the shoulder region of a 5-year-old male rhesus monkey (Macaca mulatta). The mass was excised and diagnosed as sebaceous gland adenoma based on the microscopic findings. Morphologically it appeared as an elevated, dome-shaped, circumscribed mass of 3.6 x 2.8 x 3.2 cm in dimension with tan speckled color. Histologically, the tumor was composed of mature, sebaceous cells (sebocytes), basal cells arranged in a mass of irregular shapes and sizes, with a characteristic appearance of poly or multilobular structure. Sebocytes were well differentiated with foamy cytoplasm in the center of the lobules and poorly or undifferentiated densely staining basal cells in the periphery of the lobules. Cellular changes in the adjacent lymph node included hyperplasia of plasma cells, macrophages and lymphoid elements with typical mitosis.     

A non-invasive technique for the control of intestinal parasites in rhesus macaques (Macaca mulatta).

Control of intestinal parasites is a major concern in maintaining the health and well-being of captive primates. This study established that percutaneous application of ivermectin was as effective as subcutaneous administration for the control of nematodes in captive rhesus macaques. The method is less intrusive than the standard subcutaneous or oral delivery routes and did not adversely affect the health of any of the study subjects.     

Paternity assessment in rhesus macaques (Macaca mulatta): Multilocus DNA fingerprinting and PCR marker typing

Establishing kinship relations in primates using modern molecular genetic techniques has enhanced the ability to scrutinize a number of fundamental biological issues. We screened 51 human short tandem repeats (STRs) for cross-species PCR amplification in rhesus macaques (Macaca mulatta) and identified 11 polymorphic loci with heterozygosity rates of at least 0.6. These markers were used for paternity testing in three social groups (M, R, and S) of rhesus macaques from Cayo Santiago, Puerto Rico. Several consecutive birth cohorts were analyzed in which approximately 200 males were tested for paternity against more than 100 mother/infant pairs. Despite a combined exclusion rate of more than 99.9% in all three groups, some cases could not be solved unequivocally with the STR markers and additional testing of the MHC-associated DQB1 polymorphism. A final decision became possible through multilocus DNA fingerprinting with one or more of the oligonucleotide probes (GATA)₄, (CA)₈, and (CAC)₅. Paternity assessment by multilocus DNA analysis with probe (CAC)₅ alone was found to have limitations in rhesus macaques as regards the number of potential sires which might be involved in a given case. Multilocus DNA fingerprinting requires large amounts of DNA, and the ensuing autoradiographic patterns present difficulties in comparisons across gels and even within the same gel across remote lanes. Computer-assisted image analysis was incapable of eliminating this problem. Therefore, a dual approach to DNA typing has been adopted, using STR markers to reduce the number of potential sires to a level where all remaining candidates can be tested by multilocus DNA fingerprinting on a single gel, preferably in lanes adjacent to the mother/infant pair. Am. J. Primatol. 44:1–18, 1998. © 1998 Wiley-Liss, Inc.     

Social relationships between adult male and female rhesus macaques: II. non-sexual affiliative behaviour

The social relationships of adult male rhesus macaques (Macaca mulatta) in Group I of the Cayo Santiago colony were studied over a period of 14 months. Relationships were found in which adult males and sexually mature females were persistently close to one another in nonsexual contexts, both within and across seasons. Males of long tenure and high dominance rank tended to have more female partners, and more persistent relationships, than more recent immigrants of lower rank. Correlations with length of tenure were stronger than those with dominance rank. Closely-related females tended to have persistent relationships with the same male. In most cases the female was primarily responsible for maintaining proximity in non-sexual contexts. Dyads which were persistently within 5 m of each other in the birth season were more likely to form a consortship in the subsequent mating season than those which had a brief relationship. A similar tendency was apparent in the 1 m data but it was not statistically significant. There was no association between persistent proximity during the birth season and the occurrence of long, or multiple consortships, nor with the maintenance of proximity or direction of grooming between consort partners. The pattern of consortships was not closely related to the formation of persistent relationships in the subsequent birth season. Females occasionally received protection from their male partners and, in some cases, spent more time in the feeding corral with them than did other females. Affiliative relationships can be very enduring and may have long-term benefits that were not apparent during the study period.     

Decrease in sexual initiative and responsiveness in female rhesus macaques (Macaca mulatta) during pregnancy

Although the sexual behavior of female rhesus macaques (Macaca mulatta) has been reported to decrease during pregnancy, systematic studies have been largely confined to reports of male behavior. Therefore, we designed a study to examine changes in female sexual behavior during pregnancy. Six cycling multiparous female rhesus macaques were paired during the periovulatory period of the menstrual cycle and during the first and second halves of pregnancy with six sexually experienced males of the same species. Each female was paired with the same male in all tests. The means of the behavioral measures scored on days 11–13 of the menstrual cycle, 35–56 of pregnancy, and 147–168 of pregnancy were compared. Females showed a significant decrease in the present contact ratio and the rate of threat-aways during pregnancy. Males showed lower rates of threatening-away, contacting, mounting, intromitting, and ejaculating when females were pregnant. The extent to which the decrease in male sexual behavior can be accounted for by an increase in female rejection is uncertain, but it is probably as significant as any loss of attractiveness that might accompany pregnancy.     

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.     

Oxytocin and pair compatibility in adult male rhesus macaques (Macaca mulatta)

Pair housing is considered one of the best ways of promoting psychological wellbeing for caged macaques. However, incompatible partnerships can result in stress or aggression. Though previous studies have analyzed the role of variables such as age, weight, gender, and temperament on pair compatibility, few have examined the relationship between physiological parameters and pair compatibility. Oxytocin is known to promote prosocial nonsexual behavior in various primate species and may serve as an indicator of pair compatibility. In this study, we examined the association between peripheral oxytocin levels and prosocial behaviors in isosexual pairs of male rhesus macaques. We hypothesized that animals that demonstrated high levels of prosocial behaviors would have higher oxytocin levels than those showing low levels of the behavior. In addition, to elucidate the relationship between oxytocin and compatibility, we compared peripheral oxytocin between the highly affiliative animals and single‐housed males identified as having multiple unsuccessful pair attempts with multiple partners. We collected plasma oxytocin on 40 pairs of monkeys that had lived together for at least 1 month and 20 single‐housed animals. Further, we simultaneously collected behavioral data on the pairs, recording prosocial interactions (e.g., groom, play). Oxytocin varied among individuals, but was highly correlated between members of a pair (r = 0.58, p < .001). Additionally, prosocial behavior was positively correlated with plasma oxytocin (r = 0.38, p < .02). However, contrary to our expectations, oxytocin did not differ between single and highly affiliative pair‐housed animals (F_(1,38) = 0.71, p = .40). Our results suggest that oxytocin may be associated with the quality of isosexual pairs of male macaques. More work is needed to determine the nature of this relationship.