Cayo Santiago Research Articles

Free-ranging Cayo Santiago rhesus monkeys (Macaca mulatta): II. Passive joint mobility.

Recent studies on the effects of caging on joint mobility and the correlations between joint mobility and use of the extremities have pointed out the need for baseline values that are readily available in the literature. This report provides normative data on the passive mobility of the major joints of free-ranging Cayo Santiago rhesus monkeys (Macaca mulatta). The sample in this cross-sectional study is large (661 animals including 315 males, 346 females), and it spans the entire age spectrum (24 hours to 25 years) of the population. Included are data on motion in the sagittal plane at six joints: shoulder, elbow, wrist, hip, knee, and ankle. Results indicated that passive joint mobility changes in a nonlinear fashion throughout the life cycle. The apparent rapid decline in mobility from birth through puberty parallels rapid changes in body size and proportions in young animals. Joint mobility is relatively stable in prime-age adults, whereas it is generally more restricted in older monkeys. Both genders follow a similar pattern, but timing differs somewhat. Although the primary purpose of this paper is to present numerical data on the Cayo Santiago population, the results are compared with previous, more limited studies of both captive and free-ranging rhesus macaques.

Group selection models with population substructure based on social interaction networks

AbstractMost models of evolution by group selection assume that groups have discrete boundaries with homogeneous levels of interaction within groups and no interaction between groups. While this assumption is analytically useful, it is not an accurate description of groups in nature. We use a generalization of D.S. Wilson's (Am. Nat. 111:157–185, 1977; The Natural Selection of Populations and Communities. Reading, Mass.: Benjamin/Cummings, 1980) concept of trait‐groups, in which groups are defined as sets of interacting individuals, to estimate the average degree of relatedness among groomers and groomees, referred to here as grooming‐groups. The average degree of relatedness is an important parameter in models of both kin and group selection.Data on grooming among 52 female rhesus macaques drawn from Group F on Cayo Santiago were used to represent the pattern and intensity of affiliative interactions. Degrees of relatedness among individuals and transferrin phenotypes were obtained from demographic and genetic records on the colony. The average degree of relatedness within grooming‐groups was estimated directly by calculating the average degree of relatedness among interactants (groomers and groomees), weighted by their frequency of interaction. Average degrees of relatedness among interactants were also estimated from the subjective frequency of the transferrin C allele.Our analysis indicates that the average degree of relatedness within grooming‐groups is 0.316 when estimated directly and 0.347 when estimated from the subjective frequency of the transferrin C allele. These values are much higher than are usually considered for group selection in primate societies and indicate the relative ease with which altruism may evolve given primate social structures.

Female Primate Sexual Behavior and Conception: Are There Really Sperm to Spare? [and Comments and Reply

Female Primate Sexual Behavior and Conception: Are There Really Sperm to Spare? [and Comments and Reply

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.

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.

Age assessment using cementum annulus counts and tooth wear in a free-ranging population of Macaca mulatta.

Estimates were made of the tooth wear and the number of cementum annuli on lower first molars of Macaca mulatta of known age that had lived on Cayo Santiago, Puerto Rico. It is demonstrated that both these measurements are significantly correlated with age. Neither measurement by itself, however, strongly enough corrected with age to provide a reliable guide to the true age of individuals older than about 14 years, although cementum annulus counts clearly provide a more reliable guide to age determination than does wear. A combination of tooth wear and annulus number is a somewhat better predictor of age, with a multiple regression explaining 19% of the overall variance in age. As has been reported previously in tropical ungulates, there is more than one cementum annulus per year deposited on the M1S of our sample. Comparison with rainfall data indicates that the number of dry intervals in the animal's life corresponds on a one-to-one basis with the number of annuli. It is hypothesized that such dry intervals cause nutritional stress, which in turn is reflected in periods of arrested or slowed growth in the tooth cementum. Also, more annuli are formed per year on the teeth of males than those of females. Stress engendered by intermale competition may play a role in this phenomenon.

“Macaque‐ology” on a Caribbean Island. A review of the Cayo Santiago macaques: History, behavior and biology, edited by Richard G. Rawlins and Matt J. Kessler. Albany, State University of New York Press, 1986, 306 pp., $49.50 (cloth), $18.95 (paper)

“Macaque‐ology” on a Caribbean Island. A review of <i>the Cayo Santiago macaques: History, behavior and biology</i>, edited by Richard G. Rawlins and Matt J. Kessler. Albany, State University of New York Press, 1986, 306 pp., $49.50 (cloth), $18.95 (paper)

Social relationships between adult male and female rhesus macaques: 1. Sexual consortships

The sexual relationships of 15 adult male rhesus macaques (Macaca mulatta), of one social group in the Cayo Santiago colony, Puerto Rico, were studied during the 1981 mating season. Two criteria were used to determine whether or not a focal male was in consort in a given 20-min observational sample. One hundred and thirty-two consortships were recorded. The distribution and duration of all consortships, and the distribution of those consortships that coincided with the estimated time of conception, were positively correlated with male dominance rank and length of tenure. Correlations with dominance were stronger than those with tenure. Older females had more consortships with focal males than younger females. There was no relationship between female rank and the distribution of consortships. Consortships did not give exclusive access to receptive females although they may do in feral situations. Males were primarily responsible for maintaining proximity in about two thirds of consortships. The four top-ranking males were primarily responsible in all but one of their consortships. Almost all of those in which the female was primarily responsible involved younger, slightly lower-ranking males. This pattern may have resulted from the females being attracted to the latter males although other interpretations are possible. The partner who was primarily responsible for maintaining proximity also tended to be the predominant groomer, supporting the view that grooming plays a role in the maintenance of sexual consortships. Almost a third of consortships were with females who had conceived, suggesting that males could not accurately assess female reproductive state. Consortships maintained by the male were longer than those maintained by the female. Males may try to increase their chances of fertilising a female by prolonging the consortship. High-ranking males may have been more successful at this, resulting in the positive correlation between male dominance rank and consortship duration.

The Cayo Santiago Macaques: History, behavior and biology. Edited by R. C. Rawlins and M. J. Kessler

The Cayo Santiago Macaques: History, behavior and biology. Edited by R. C. Rawlins and M. J. Kessler

Ontogenetic plasticity in nonhuman primates: I. Secular trends in the Cayo Santiago macaques.

Although secular trends toward increasing body size are apparent in many human populations, little is known about their occurrence in nonhuman primates. The Cayo Santiago skeletal collection of Macaca mulatta includes 101 adult animals (greater than or equal to 10 years of age) born at different times in the past 3 1/2 decades, so that variation in size may be examined relative to birth year. No secular trends in orbital height were observed in this sample, but in both sexes lengths of adult long bones increased significantly over time, while cranial dimensions and length of the second molar in female also showed significant variation with birth year. These changes were consistent with the history of provisioning of the animals and with fluctuations in population size. Low-order correlations were observed between birth year and body proportions, especially the crural index in males, a pattern that has also been observed in human populations. These findings argue that, in addition to biomechanics and heritage, diet may affect allometric relationships and that an inherent plasticity or malleability of the growth process may be characteristic of nonhuman as well as human primates.

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.

Social relationships between adult male and immature rhesus macaques

Social relationships of adult male rhesus macaques (Macaca mulatta) were studied over a period of 14 months. Sixteen focal males were chosen from a single group in the Cayo Santiago colony, Puerto Rico. Immatures were defined as infants, yearlings and 2-year-olds. There was a tendency for males to spend more time in proximity to immatures in the birth seasons than in the mating season. Time spent in proximity to immatures was correlated with male dominance rank. Several male-immature dyads had persistent relationships and nine were apparent throughout the study period. Most of the latter involved the top-ranking males. There were no consistent effects of sex or rank of the immature on the distribution of persistent relationships. In almost all male-immature dyads the immature was primarily responsible for maintaining proximity. Two ways were found in which immatures could benefit from these relationships. Protection and agonistic aiding of immatures by adult males were rare, but occurred exclusively in dyads with persistent relationships. In addition, immatures apparently gained greater access to food resources as a result of their relationships with adult males. There was no clear evidence of adult males benefiting from these relationships.

Primate population structure: evaluation of models.

Genetic markers among macaques on Cayo Santiago island were analyzed in an attempt to infer aspects of mating structure. Several models that included high levels of gene flow among groups could not be distinguished, but the data are clearly incompatible with group endogamy and with high variance in male fitness. Drift effective size is approximately one half census size in this population.

Carbohydrate impairment and insulin secretory abnormalities among Macaca mulatta from Cayo Santiago.

Rhesus macaques (Macaca mulatta) from Cayo Santiago were examined for evidence of carbohydrate intolerance indicative of potential development of non-insulin-dependent diabetes mellitus (NIDDM). Monkeys 6 to >20 years from natal Groups J, M, and P, an AGED Group (all >20 years), and unrelated monkeys removed from the island in association with other groups (CAYO), were examined with intravenous glucose tolerance tests (iv-GTT). Morphometric measurements were made on all tested monkeys. Impairments included fasting hyperglycemia (>115 mg/dl), impaired glucose clearance (K <2.0%/min), fasting hyperinsulinemia (>150 μU/ml) or hypoinsulinemia (<20 μU/ml), and insulin secretory abnormalities (>500 μU/ml or <75 μU/ml). Natal groups J and M had 31% with impairments, group P had 0% the AGED group had 45%, and the CAYO group had 33%. Impaired glucose clearance was usually attributable to a reduced insulin response. Impairments correlated significantly (p ⩽ 0.05) to body weight and a modified Quetelet index, but not to sex, acute stress, or islet cell antibodies; the relationships to age could not be delineated in this survey. Impairements in monkeys are indicative of various stages in the asynchronous development of carbohydrate intolerance leading to NIDDM.

Secondary sex ratio variation in the Cayo Santiago macaque population.

Secondary sex ratios (SSR) were calculated from 1,385 offspring delivered by 372 females in the Cayo Santiago population of free-ranging rhesus monkeys (Macaca mulatta) from 1976 through 1984. The SSR for the entire colony ranged from 0.86 to 1.46 males per female (combined total: 1.08), but no significant difference was observed (P > .05). SSR values were compared among the troops for each year. The SSR differed significantly among the six social groups (P < .05) only in 1978. The annual SSR of each troop was compared over 9 years. Significant variation was found only in group O. The annual SSR was significantly skewed (P < .05, males > females) for three troops in 3 separate years. The SSR did not vary according to troop rank. No significant difference was found among the 17 matrilines of the population, but comparison of matrilines within each social group revealed a significant difference in the SSR (P < .02) for the three matrilines in group I. This was due to the significantly skewed SSR (P = .0080, females > males) of the DM genealogy in that troop. SSR values were not related to matrilineal rank. Individual dominance rank did not bias the SSR. Complete reproductive histories for 266 females showed no evidence of significantly skewed SSR values. Age-related effects on the SSR were examined by using cross-sectional and cohort-based analyses. The SSR did not vary significantly (P > .05) with maternal age, but it was significantly skewed (P < .05) toward males at the ages of 5 and 9 years. Parity had no significant effect (P > .05) on SSR values. Wide variation occurred in the SSR of the Cayo Santiago population. Rank-related adjustment of the SSR at the level of the troop, matriline, or individual, as reported in short-term studies of other primate social groups, may reflect normal annual variation in the SSR evident only from longitudinal observations of large multigroup primate populations.

Aging in the musculoskeletal system of rhesus monkeys: III. Bone loss.

It is well established that aging of the human skeleton includes the loss of bone mass or density, but little comparative information on age-related osteopenia in other primates is available. In order to determine whether bone loss occurs in normally locomoting nonhuman primates, radiographs of 139 rhesus monkey skeletons from the Cayo Santiago collection were examined, and measures of percent cortical bone (PCT) at the midshaft of second metacarpals, humeri, and femora were calculated. An age-related osteopenia was observed in the metacarpal of adult female macaques, although much individual variation was present. This variability could not be explained by reproductive history (number of offspring), matrilineal affiliation, or degree of osteoarthrosis. However, in a subsample of 15 animals, females who had given birth in the three months prior to death showed lower PCTs than those who had not conceived in the previous mating season. In adult males, PCT did not vary significantly with age, but males that weighed less and those with no/little osteoarthrosis showed lower PCTs than heavier or more arthritic animals, respectively. The multifactorial nature of the variation in PCT observed here suggests that similar processes of bone behavior are involved in the skeletal aging of both humans and rhesus monkeys.

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.

Affiliation and reciprocity in sibling and peer relationships among free-ranging immature male rhesus monkeys

The social relationships of immature male rhesus monkeys ( Macaca mulatta) were studied during 1977, 1978 and 1981 at the Cayo Santiago colony, Puerto Rico. Three types of social relationship were selected for comparison: the sibling relationship, the strong peer relationship and the weak peer relationship. Sibling relationships were initially distinguished from peer relationships on the basis of individual characteristics (age and relatedness), whereas the two types of peer relationship were initially differentiated on the basis of criteria that concerned their structure. Although the three types of relationship showed certain similarities these were far outweighed by differences in the content, diversity, qualities and the relative frequency and patterning of their interactions, and the degree to which their interactions were characterized as reciprocal or complementary. These findings are discussed in relation to a number of questions concerning the sturucture of relationships and it is concluded that, in broad terms, the three types of relationship can be contrasted in terms of a multidimensional quality, their degree of affiliation.

An autocorrelation analysis of genetic variation due to lineal fission in social groups of rhesus macaques

AbstractEmpirical analyses and models of the lineal effects of fission indicate that considerable genetic differentiation may occur at the time of group formation, thus confusing the usual positive relationship between historical affiliation and genetic differentiation. We analyze the effects of fission pattern on variation in highly heritable morphological traits among eight social groups on Cayo Santiago. The analysis is performed using general network autocorrelation methods that quantitatively and directly measure the amount of variation in social group mean morphology that can be explained by fission. All of the fission autocorrelation coefficients are strongly negative, indicating that groups most recently formed by fission are most dissimilar. Also, most of the variation between groups can be explained by the fission pattern, indicating that lineal fission is the most important process generating between‐group variation on Cayo Santiago.

Breeding-season relationships of immature male rhesus monkeys with females. I. Individual differences and constraints on partner choice

Several aspects of breeding-season relationships with mature females are described for free-ranging immature male rhesus monkeys (Macaca mulatta)on Cayo Santiago. At puberty, immature males are still groomed by mature females, as they were as infants, but no longer receive active protection from females other than their mothers. A further, potentially beneficial, aspect of their associations with females lies in the opportunities to observe closely the tactical social and sexual interactions of receptive females with adult males. However, immature males themselves rarely copulate with females. Developmental constraints may explain the finding that most females observed by immature males were relatives but that high-ranking males showed a particular preference for adolescent relatives, whereas the preference of low-ranking males was for adult relatives. A further finding was that while there was a tendency for immature males to devote a greater proportion of their total observation time to females that ranked above their mothers than to those of inferior rank, these were also the females from which males received the most aggression, while most of the females with which the males groomed or copulated were lower ranking than the males’ mothers. Of three hypotheses concerning three possible types of social constraint which might account for such a finding, the data supported only one—that particular levels of aggression within these relationships are compatible only with certain other elements (observations), and not with others (grooming, copulation).