Absence of Naturally Acquired Tetanus Antitoxin in the Free-Ranging Cayo Santiago Rhesus Monkeys (Macaca mulatta)

Tetanus is enzootic in the free-ranging rhesus monkey colony on Cayo Santiago. The disease accounts for 25% of all mortalities in the population. The high prevalence of tetanus provided a unique opportunity to study the potential roles of geophagia, wounding, and clinical tetanus infections on the development of naturally acquired tetanus antitoxin in rhesus macaques. Eighty-six unvaccinated monkeys, including six that recovered from tetanus, were serosurveyed using a mouse toxin neutralization test. None of the animals had detectable antitoxin titers (<0.001 AU/ml), suggesting that natural immunity to tetanus is either rare or nonexistent in the Cayo Santiago colony.     

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.     

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.     

Leptospiral agglutinins in the Cayo Santiago macaques

The colony of free-ranging rhesus monkeys (Macaca mulatta) on Cayo Santiago, Puerto Rico, was surveyed for leptospiral agglutinins. Only 5 (3%) of 169 monkeys (25% of the population) were seropositive (titers of ? 1:100). An additional 29 animals (17%) had titers ?1:50. The proportions of seropositive males and females were 22% and 18%, respectively, and twice as many adult as immature animals (32% vs. 15%) were positive. In most seropositive monkeys a single serogroup predominated, Icterohaemorrhagiae being recorded in nearly 60% of these animals. In a follow-up survey conducted a year later, 4% of 158 of the original monkeys were seropositive, with titers of from 1:100 to 1:200. None of 22 Rattus rattus captured on Cayo Santiago had agglutinins to pathogenic serovars. Despite contact with rats and ingestion of stagnant water, the serological evidence, the excellent clinical condition, low mortality, and high reproductive rates of the Cayo Santiago macaques indicate that leptospirosis is not a health problem in this free ranging monkey colony.     

Behavioral responses of free-ranging rhesus monkeys to food shortage

During early July 1968, a severe food shortage occurred on Cayo Santiago, an island colony of free-ranging rhesus monkeys (Macaca mulatta). The food shortage produced striking changes in the behavior of the monkeys. Within the one social group intensively studied, the total frequencies of grooming, play and fights decreased significantly; the frequency of matings also dropped; body contact, displacements by other groups, and non-displacement movements decreased, but not in statistically significant amounts. Changes in the percentage of total grooming attributable to related and unrelated monkeys reflected the stability of the rhesus matriline. Comparisons made between Cayo Santiago and other primate groups under analogous situations reveal similar responses to food shortage.     

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.     

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.     

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.     

Differential distribution of antibodies to different viruses in young animals in the free-ranging rhesus macaques of Cayo Santiago

BACKGROUND: The breeding colony of free-ranging rhesus macaques was established in 1938 in Cayo Santiago (CS) with animals collected in northern India. The seroprevalence to cercopithecine herpesvirus type 1 (B virus) and simian retroviruses has been studied previously. RESULTS: This is the first report on the seropositivity to different viruses using samples collected shortly after removing animals (n = 245) from CS. All samples were negative for measles, simian immunodeficiency virus and simian type D retroviruses. The overall prevalence of antibodies was around 50% for simian T-lymphotropic virus I (STLV-I). For B virus, the prevalence was 38%. CONCLUSIONS: Data obtained showed marked differences in the antibody distribution to B virus and STLV-I within the free-ranging colony of rhesus macaques. Implication of these data for the Specific Pathogen Free program at the Caribbean Primate Research Center are also discussed.     

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 timing of fission among free-ranging Rhesus monkeys

Behavioral observations were carried out on a large group of free-ranging rhesus monkeys (Macaca mulatta) on Cayo Santiago from January 1968 to December 1969 and from October through December 1970. During this period, social group A divided. The 24-month study period can be classified into five stages which represent the different phases in the process of group fission. Two criteria for fission were established: the cessation of grooming between adult females of different sub-groups of the main group and the stabilization of the adult female population. The criteria were based on established information on group dynamics and inter-group behavior on Cayo Santiago. Several points became clear from the chronological analysis. Group fission is a long process. The duration of the process of fission and the specification of the season in which fission begins and is completed depends upon the definition applied. For purposes of this analysis, fission was defined as beginning with the onset of spatial fragmentation and corresponded to the initial part of the breeding season. The fission was completed during the breeding season. The duration of the process of fission was 18 months.     

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.     

Effect of parity on bone mineral density in female rhesus macaques from Cayo Santiago

This cross-sectional study investigates the relationship between parity, bone mineral density, and spontaneous osteopenia/osteoporosis in a large skeletal population of female rhesus macaques (Macaca mulatta) from the free-ranging colony of Cayo Santiago, Puerto Rico. The sample consists of 119 mature female monkeys aged 4.0-22.2 years at time of death. The data consist of measurements of bone mineral content (BMC) and bone mineral density (BMD), obtained from dual-energy X-ray absorptiometry (DEXA) of the last lumbar vertebra. After controlling for age, there is a significant increase in BMD of the spine with increasing parity (P = 0.0006), up to a parity of 7 offspring. Thus, high parity initially has a positive effect on BMD in female rhesus monkeys, but this positive effect disappears with parities that are greater than 7 offspring. After controlling for parity, however, age has a negative (P = 0.015) effect on BMD, beginning several years after the attainment of peak BMD (age 9.5 years). Thus, it appears that parity initially mitigates the effects of aging, but the positive effect of parity on BMD is eventually overwhelmed by the aging process. Mean BMC and BMD values are higher in parous females compared to nulliparous females in the same age range. Similarly, females with low parity have significantly lower mean BMD values than do age-matched high-parity controls, and the frequency of osteopenia and osteoporosis is greater in low-parity females. Forty-three percent (43%) of the osteopenic/osteoporotic females in the sample are members of the low-parity group, even though it composes only 13% (16/119) of the entire sample. This study demonstrates that the free-ranging female rhesus monkeys from Cayo Santiago are a good nonhuman primate model for the study of bone mineral density, parity, osteopenia, and osteoporosis.     

Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago. I. Single trait heritabilities

The use of skeletal nonmetric traits in studies of biological relationships often involves the assumption that variation in these traits is genetic. Studies of nonmetric traits in human groups and in inbred strains of mice and rabbits have indicated a genetic component to nonmetric trait variation. Skeletons of animals with known matrilineage membership were obtained from the Cayo Santiago skeletal collection in order to obtain a direct estimate of the heritabilities of several nonmetric traits in the free-ranging population of rhesus macaques on Cayo Santiago. Falconer's (1965) method was used to calculate heritability. Heritability estimates range from zero to one, and half of them are greater than 0.5. This indicates that there is a considerable amount of genetic variation for these traits among the Cayo macaques. There is a significant tendency for traits scoring the number of foramina to have lower heritabilities than those scoring hyperstotic or hypostotic traits.     

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.     

Effects of geographic transfer on the timing of seasonal breeding of rhesus monkeys.

This is a study of the effects of geographic transfer on the timing of seasonal breeding of free-living rhesus monkeys on Cayo Santiago and La Parguera islands in Puerto Rico. The results demonstrated a progressive shift in the breeding season of the transferred group. The full shift required a period of 2 years. Change from one environment to another produced shifts in onset of estrous. The explanation for this phenomenon proposes an interaction between the specific reproductive state of the female, which may or may not be sensitive to a particular environmental change, and the environmental variation which is correlated with onset of breeding.     

Intestinal Parasites of the Free-Ranging Cayo Santiago Rhesus Monkeys (Macaca mulatto)

Free-ranging rhesus macaques on the island of Cayo Santiago, Puerto Rico, were surveyed for intestinal parasites for the first time in over 40 years. Results were compared with the only previous study [10], and the relationships between the prevalence of Strongyloides and dominance rank, body weight, age, and matriline examined in the sampled population.     

Congenital cataracts in a free-ranging rhesus monkey

This report documents the occurrence of congenital cataracts in a visually-impaired yearling rhesus monkey from the same matriline on Cayo Santiago in which a congenitally blind infant was born 2 years previously.     

Preliminary report on yellow long-tailed macaques (Macaca fascicularis) at Kosumpee Forest Park, Thailand

We conducted a census on long-tailed macaques (Macaca fascicularis) at Kosumpee Forest Park, Thailand, and found 15 individuals of yellow pelage color out of a total of 287 individuals. There were three troops, designated A, B and C, but the yellow macaques were found only in B and C troops. The frequency of yellow macaques was 5.2% in the total population and 4.2 and 9.9% in B and C troops, respectively. These frequencies are much higher than those in rhesus macaques (M. mulatta) reared at Cayo Santiago (0.52%). They are, however, lower than those of 10 years ago.     

Male age, dominance, and mating success among rhesus macaques

Some previous primate studies have found a positive correlation between male dominance and mating success when data from subadult males were included in the analyses. The information in this paper suggests that an unconscious bias may have been introduced when data on subadult males were included because of the lower dominance rank of these animals. Data from a study of rhesus monkeys on Cayo Santiago showed that subadult males mated significantly less than adults. Because these monkeys are not fully mature, data on them should not be used in any test for correlation between adult male dominance and mating success. The only significant correlation found for adult male mating success was an inverse one with relation to age. Based on behavioral data young, fully adult males have the best chance of fathering offspring regardless of their dominance rank.