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.     

Estrous behavior of free-ranging rhesus monkeys (Macaca mulatta)

The sexual behavior of a group of free-ranging rhesus monkeys (Macaca mulatta) was studied for 13 consecutive months in an attempt to determine whether or not sexual activity occurred year-round, and the importance of sexual attraction to rhesus monkey social organization.Estrous behavior was seen both inter-menstrually and peri-menstrually, producing a shorter mean estrous cycle length than reported by other workers. New data was gathered on the interrelationships among age, dominance rank, and sexual activity; son-mother and brothersister matings; and sexual favoritism among free-ranging rhesus monkeys.A few females who failed to conceive during the fall breeding season showed cyclic estrous behavior throughout the entire annual cycle. Hypotheses are given as to possible physiological bases for birth season sexual cycles.Several forms of inter-animal bonding, including sexual bonding, are enumerated, and their importance to rhesus monkey social organization discussed.     

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.     

Male leadership change in a free-ranging troop of Indian rhesus monkeys (Macaca mulatta)

The male leadership of a troop of rhesus living at the foot of the Kumaon foothills of India was studied from January to December of 1965. The troop, inhabiting a region of fields and forests, varied in size from a maximum of 20 after the birth season to a minimum of 14 in December during the breeding season. The troop initially contained two adult males with the occasional presence of a third, more peripheral male. This third male disappeared in March and was perhaps identical with the male who began to appear in August and succeeded in displacing the dominant male from the troop. The second initial male succeeded to the dominant position in September. During the breeding season various extra-troop males followed and occasionally penetrated the troop. The second male had difficulty in maintaining his position against one of these, who had perhaps been the peripheral male at the beginning of 1965.     

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.     

Parturition in rhesus monkeys (Macaca mulatta)

During five years of birth season fieldwork, we observed two births and three peri-birth instances of behavior of free-ranging rhesus living in Kathmandu, Nepal. These constitute the first two recorded free-ranging rhesus births, and we compare them to the behavior which has been observed in captivity and expected in the wild. The free-ranging parturition behavior was characterized by a general lack of contact with other troop members and by overall inconspicuousness. In the first birth we observed, the troop moved about 70 m up the hill, leaving the laboring female behind on an open hillside. Two males, a female and a juvenile returned and rested about 20 m from the delivering female. During the second delivery, the female stayed with the troop and seemed to participate normally in most troop interactions, although she avoided physical contact with other troop members. We propose that this near-normal behavior may help to assure successful parturition by allowing the female the needed social isolation and inconspicuousness without any loss of troop protection. It may also partly explain why births have not been observed during previous studies. Observations of rhesus parturition behavior reported from studies of captive monkeys and reports from other free-ranging primate studies are compared with our data.     

Intergroup social dynamics of the Cayo Santiago rhesus (Macaca mulatta) with special reference to changes in group membership by males

Observations were made on the rhesus monkeys,Macaca mulatta living on the island of Cayo Santiago over a two-year period. Agonistic behaviors between members of different groups were the most common type of inter-group interaction, typically occurring in the vicinity of the feeders. Instances of social grooming and copulation between members of different groups were observed very infrequently.Changes in groups membership were made almost exclusively by males, particularly three-and four-year-old animals, and the changes occurred predominantly during the autumn breeding season. Peripheral all-male subgroups were preferred by males changing groups, perhaps because siblings or peer-group associates were to be found in those subgroups. The process of joining a new group by forming an affectional relationship with another male is described briefly. It is suggested that the phenomenon of group membership change by adult males is not an artifact of the island colony but its high frequency may be a consequence of the tremendously overcrowded conditions on the island.     

Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: A comparison with captive pairs

The general course of mother-infant relationships among free-ranging rhesus monkeys (Macaca mulatta) on Cayo Santiago is remarkably similar both qualitatively and quantitatively to that observed in the socially living captive colony at the MRC Unit at Madingley, England. Nevertheless, small but consistent differences appear to be due to differences between mothers in the two environments rather than differences between infants. Captive mothers may be described as more protective and less encouraging of early independence in their infants than free-ranging mothers. Moreover, captive pairs have become more like free-ranging pairs over the years, perhaps as captive mothers have been allowed to raise their infants in the presence of kin. A unitary concept of environmental complexity is not useful in accounting for the results.     

Sterilization and its behavioral effects on free-ranging female rhesus monkeys (Macaca mulatta).

In order to control population growth rates, a decision was made to sterilize most of the free-ranging, wild rhesus macaque females of Silver Springs, Florida. Between October 1987 and March 1988, the five females who had been sterilized and released in the fall of 1986 were matched with five intact females in a behavioral study. While there were differences between the behaviors of the sterilized and intact females, the differences can be attributed more to differences in age, rank, and other factors than to the sterilization. Clinical data collected and reported on the monkeys is unremarkable.     

Hydranencephaly in two rhesus monkeys (Macaca mulatta)

Spontaneously occurring hydranencephaly was diagnosed at necropsy and confirmed histologically in two stillborn fetuses that were delivered from young female rhesus macaques (Macaca mulatta).     

Skeptical responding in rhesus monkeys (Macaca mulatta)

Signalers that misinform sufficiently open may become devalued as sources of information; however, “skepticism” and any comparison involved in testing reliability entail a cost that involves delays and energy expenditure. Skepticism may be less costly though, if, as a rule, animals are not equally skeptical of the signals of all conspecifics. Animals with the ability to recognize individual conspecifics and to recall past encounters with them may have the capacity to restrict skepticism to subsets of animals that are most likely to benefit from deception. We played tape-recorded alarm calls of high- and low-ranking rhesus monkeys(Macaca mulatta) to their groups in a feeding context once daily over 8 consecutive days at the Yerkes Primate Center Field Station. Over the sequence of playbacks, response was greater to the calls of high-ranking monkeys, adult response patterns were different from those of juveniles, and for adults especially, decline in responsiveness was punctuated by partial resurgences of response. These differences may be the consequence of the adults’ more extensive histories of interaction with group members that, though generally reliable, vary with respect to the potential benefits of deceptive signaling.     

Varying responses to feeding competition in a group of rhesus monkeys (Macaca mulatta)

The behaviour of members of a group of rhesus monkeys was observed in experimentally created, competitive feeding situations. Socially dominant members of the group tended to start eating before lower-ranking subjects, and generally ate more. Dominants sometimes used aggression to control access to food, but overall, intermediate-ranking monkeys were involved in most agonistic episodes. Non-dominant subjects improved their feeding performance when food was presented in three piles rather than one pile, often by snatching food and consuming it away from the pile. These general patterns were less evident when realistic snake models were placed on some of the food piles. Feeding was disrupted by the presence of snakes, but notably, subordinates risked feeding in these conditions. Piles containing preferred foods and snakes were eaten from, but a low-preference food (carrot) under snakes went untouched by all subjects. The results suggest that group-members evaluate potential risks and benefits of competing for a restricted resource, and that dominance status, while an important factor, is only one element in the equation.     

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.