Congenital and hereditary anomalies in the rhesus monkeys (Macaca mulatta) of Cayo Santiago

During seven annual birth seasons, from January 1976 to July 1982, 963 infants were born in the Cayo Santiago, Puerto Rico, colony of free-ranging rhesus monkeys (Macaca mulatta). The reproductive rate for mature females, 4 years of age and older, ranged between 74.1% and 84.7%, with a cumulative mean of 80.8% over 7 years. Live births comprised 95.3% of the total and the secondary sex ratio was 109 male to 100 female births. No twinning was observed. Aborted and stillborn monkeys represented 4.7% of all births. The percentage of stillborn females was greater than that of males (4.0% vs. 3.1%). Neonatal death, defined as mortality within 48 hours postpartum, occurred in 0.8% of the live births. Two cases of congenital abnormalities were observed. The first was an anencephalic, acranial female and the second a congenitally blind male. Both infants were born to matrilineally unrelated 7-and 8-year-old multiparous females with no prior history of delivering malformed offspring. The incidence of each defect, based on 963 births, was 0.10%, with a cumulative incidence of 0.20% for all teratisms seen during the study. Multiple occurrences of a rare, nonpathological and nonlethal hereditary anomaly were also seen. Five "golden" macaques were born into two genetically distinct social groups within the last 2 years of observation. The incidence of this phenotype, based on five cases, was 0.52%, 52 times the expected rate (.01%).     

Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago

Long-lived iteroparous species often show aging-related changes in reproduction that may be explained by 2 non-mutually exclusive hypotheses. The terminal investment hypothesis predicts increased female reproductive effort toward the end of the life span, as individuals have little to gain by reserving effort for the future. The senescence hypothesis predicts decreased female reproductive output toward the end of the life span due to an age-related decline in body condition. Nonhuman primates are ideal organisms for testing these hypotheses, as they are long lived and produce altricial offspring heavily dependent on maternal investment. In this study, we integrated 50 years of continuous demographic records for the Cayo Santiago rhesus macaque (Macaca mulatta) population with new morphometric and behavioral data to test the senescence and terminal investment hypotheses. We examined relationships between maternal age and activity, mother and infant body condition, interbirth intervals, measures of behavioral investment in offspring, and offspring survival and fitness to test for age-associated declines in reproduction that would indicate senescence, and for age-associated increases in maternal effort that would indicate terminal investment. Compared with younger mothers, older mothers had lower body mass indices and were less active, had longer interbirth intervals, and spent more time in contact with infants, but had infants of lower masses and survival rates. Taken together, our results provide strong evidence for the occurrence of reproductive senescence in free-ranging female rhesus macaques but are also consistent with some of the predictions of the terminal investment hypothesis.     

Genealogical and cross-genealogical dominance relations in a group of free-ranging rhesus monkeys (Macaca mulatta) on Cayo Santiago

Observations of dominance relations in a large group of rhesus monkeys on Cayo Santiago were carried out over a period of 25 months. Dyadic interactions in which an aggressive gesture in one individual was followed by a submissive gesture in the other were recorded as fights and considered reliable indices of dominance. The analysis revealed the following characteristics: (1) Maternal dominance over female offspring; (2) maternal dominance over male offspring up the age six years at which time the son leaves his natal group or remains in the group and rises in rank over his mother; (3) dominance of older brothers over younger male siblings until the age of five years at which time the younger brother rises in rank; (4) rank reversal between sisters when the younger sister reaches the age of three to four years; (5) brother-sister relative rank dependency on age until the male sibling reaches three to four years at which time he rises in rank; (6) linear dominance relations in the crossgenealogical dominance hierarchy; and (7) linear, but unstable, dominance relations in the adult male hierarchy. With few exceptions, the pattern of genealogical, cross-genealogical, and adult male dominance relations in the group under study was consistent with data reported for a small social group (group F) on Cayo Santiago and for Japanese macaques.     

Osteon remodeling dynamics in the Cayo Santiago Macaca mulatta: The effect of matriline

At the microstructural level, bones remodel throughout life. This process is recorded in bone cortex as osteons. A more comprehensive understanding of the interaction between genetic regulation and environmental factors in osteon remodeling will increase the value of this skeletal record and enable more accurate reconstruction of individual life histories. The purpose of this study was to examine the contribution of maternal lineage to normal age and sex variation in osteon remodeling dynamics in Macaca mulatta. Femoral cross sections from 57 Cayo Santiago-derived rhesus macaques representing five matrilines were examined to evaluate the effect of genetic relatedness on osteon remodeling dynamics. Analysis of variance revealed an effect of maternal lineage on osteon area and Haversian canal area. The other variables did not differ significantly among matrilines. Analysis of covariance revealed no significant interactions among age, sex, and matriline for any of the microstructural variables.     

Genetic studies of serum transferrins of free-ranging rhesus macaques of Cayo Santiago, Macaca mulatta (Zimmerman 1780)

Transferrin phenotypes of plasma from 687 semi-free-ranging Macaca mulatta living on Cayo Santiago, Puerto Rico, were determined by starch-gel electrophoresis and autoradiography. Fifteen phenotypes, homozygous or heterozygous products of six codominant autosomal alleles, were present in the population. The 687 animals, prior to March 1973, were divided into eight troops plus peripheral males. By March 1, 1973 the size of the population was reduced to 333 animals, consisting of four troops plus peripheral males. The distributions of transferrin phenotypes and allele frequencies were determined for the population of 687 animals and for 287 of the March 1973 population of 333 animals. Gametic ratios of 382 offspring of 126 females were enumerated. Statistical tests of homogeneity and equilibrium were applied to the data. The results of these tests suggest that, with only a few exceptions, the Cayo Santiago macaques, although divided into social groups, form a single population, and the results are in accord with behavioral observations. The authors suggest that the data on transferrins provide a good baseline for future genetic and ethological studies of evolutionary processes in a population of nonhuman primates.     

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.     

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 Costs of Reproductive Success in Male Rhesus Macaques (Macaca mulatta) on Cayo Santiago

Sexual selection acts to increase the success of males possessing advantageous traits in competition over females. In primates, interspecific variability in social and mating systems creates highly variable selective pressures on males, changing the relative strength of both intra- and intersexual selection, and the relative degree of direct vs. indirect male–male competition. Rhesus macaques are an interesting species for studying intrasexual selection and male–male competition, because they exhibit relatively low (for Papionini) body and canine size dimorphism, and exhibit large testes, suggesting reduced direct competition and strong indirect competition. We have undertaken several studies of male rhesus macaques on Cayo Santiago, from analyses of long-term life-history data to shorter term projects that combined noninvasive measures of physiological markers such as concentrations of urinary C-peptide of insulin and androgen and glucocorticoid (GC) concentrations, with measures of behavior and of sexually selected signals (male red facial coloration). We here review these studies, combining data from short-term studies with long-term mortality data to present an integrated picture of both the short- and long-term gross costs of male mating competition. We find that males exhibit many signs of the costs of indirect competition, such as energetic consequences of reduced feeding and high copulation rates. During periods of more direct contest, such as during dominance instability, males are also characterized by high androgen and GC concentrations among high-ranking individuals. Consistent with relatively weak direct male–male competition, male red skin coloration appears to be more related to female choice (intersexual selection) than the signaling of dominance status (intrasexual selection). Forty-five years of life-history data show that male mortality is higher during the mating than the birth season, a pattern we hypothesize to be linked to the costs associated with mating activity. We finish by discussing unresolved issues, such as the costs of sperm competition and the data that are needed to address them.     

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.     

Blood group antigens and the population genetics of Macaca mulatta on Cayo Santiago. I. Genetic differentiation of social groups

The red blood cell phenotypes for eight polymorphic loci were determined for 293 free-ranging Macaca mulatta living on Cayo Santiago; this number represents the total population of the island, disposed in four social groups plus peripheral males. The rhesus population shows significant genetic heterogeneity over blood group systems (loci) and social groups. No particular genetic locus or social group is solely responsible for the genetic heterogeneity observed. The distributions of genotypes for two loci (G and H) do not deviate significantly from Hardy-Weinberg expectations within social groups or in the population as a whole. Correction of the equilibrium expectations for the effect of population subdivision yields no statistically significant results. Overall, the results suggest that the interaction of a variety of processes (random genetic drift, founder effect, migration and selection) may be responsible for the diversity observed. These data, combined with those from further studies, may allow an application of behavioral and genetic knowledge to the study of microevolutionary processes among nonhuman primates.     

Computer-task testing of rhesus monkeys (Macaca mulatta) in the social milieu

Previous research has demonstrated that a behavior and performance testing paradigm, in which rhesus monkeys (Macaca mulatta) manipulate a joystick to respond to computer-generated stimuli, provides environmental enrichment and supports the psychological well-being of captive research animals. The present study was designed to determine whether computer-task activity would be affected by pair-housing animals that had previously been tested only in their single-animal home cages. No differences were observed in productivity or performance levels as a function of housing condition, even when the animals were required to “self-identify” prior to performing each trial. The data indicate that cognitive challenge and control are as preferred by the animals as social opportunities, and that, together with comfort/health considerations, each must be addressed for the assurance of psychological well-being.     

Seasonal weight changes in male rhesus monkeys (Macaca mulatta)

Adult male rhesus monkeys lose weight during the breeding season and regain it during the nonbreeding season. The annual pattern of maximum weight gain just prior to the onset of breeding resembles the seasonal “fattening” seen in squirrel monkeys, but the period of weight gain is less discrete. The magnitude of weight change is less in younger males, in that sexually immature males gain weight in both seasons, but significantly less during the breeding season. Females do not lose weight during the breeding season. Post hoc analyses revealed no significant correlations between male testosterone levels, dominance ranks, weights, or weight changes. The heaviest animals as juveniles were predictably the heaviest as adolescents. The timing of seasonal changes in testosterone did not correlate with the timing of changes in weight; weight losses followed the rise in testosterone, and weight gains continued until early in the breeding season after testosterone levels had already begun to rise. It is suggested that seasonal hormonal changes may influence activities in individuals and that changes in the activities of particular group members may alter the activity patterns of other group members. This alteration of activity patterns due to group influences on individuals as well as individual influences on the group may explain why hormonal regulation of seasonal weight appears to be indirect and why individuals (juveniles) experiencing no seasonal hormonal changes nonetheless show differences in activity patterns and seasonal weight changes.     

Radiation-induced morphologic changes in the rhesus monkey (Macaca mulatta) brain

The right cerebral hemisphere of 24 rhesus monkeys scheduled for necropsy at the completion of another project were studied histopathologically 1-30 days after a single dose of 60Co-irradiation. Histopathologically, inflammation and gliosis consistently occurred at specific time points but varied in severity between individuals. Multifocal hemorrhage, edema, and an acute neutrophilic inflammatory response were observed initially whereas perivascular accumulations of lymphocytes were observed in specimens at the end of the study. Microglia/macrophages were most prominent during the first week after irradiation, whereas astrocytes were reactive throughout the observation period. The early clinical manifestations of the central nervous system (CNS), because of brain irradiation in humans, correspond temporally with acute vascular responses, acute and subacute inflammatory cell responses, and subacute demyelination and reactive astrocytic and microglial responses observed in the rhesus monkey. Initial responses of the CNS to gamma-irradiation may have potential implications for the development of radiation-induced late injury of the CNS.     

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.     

Ampullary carcinoma in a group of aged rhesus macaques (Macaca mulatta)

Ampullary carcinoma was diagnosed in 6 rhesus macaques that ranged in age from 20 to 35 years. Signalment, premonitory signs of disease, and results of clinical biochemical and hematologic analyses varied among animals. Histologically, the neoplastic cells obliterated the ampulla, with regional spread to the duodenum in all 6 animals and to the pancreas in one animal. Two animals had metastases to the lung, and another two had metastases to the pancreoduodenal lymph nodes and liver. One animal had mesocolonic metastasis. Malignant tumors of the ampullary region are rare in domestic animals, and account for less than 5% of all cancers of the digestive tract in humans.