Sons of low-ranking female rhesus macaques can attain high dominance rank in their natal groups

Five adult and subadult sons of middle- and low-ranking female rhesus macaques (Macaca mulatta) were observed to hold high dominance rank in their natal groups during a 12-month study at Cayo Santiago, Puerto Rico. Three of these males also experienced high mating success during at least one mating season. These findings contrast with all previously published accounts of rank acquisition by natal male rhesus macaques in provisioned colonies, and they present a challenge to the hypothesis that natal transfer functions to increase male access to fertile females.     

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.     

Geophagy by the bonnet macaques (Macaca radiata) of southern India: A preliminary analysis

Bonnet macaques (Macaca radiata) in the Marakkanam Reserved Forest of southern India consume termitaria soils. Samples from the ingested termite mounds are compared with samples taken from the surrounding uneaten soils in an attempt to determine why the termitaria soils are eaten. Particle size, clay and primary mineral composition, geochemistry, and scanning electron microscopic analyses are used to search for a possible explanation for geophagy among the bonnet macaques. Kaolin minerals abound throughout the Marakkanam soil sample suite. But the termitaria soils are distinguished by the presence of small amounts of smectite. An abundance of kaolin minerals in combination with small amounts of smectite strongly resembles the mineralogy ofeko, a traditional African remedy for stomach ailments, and Kaopectate™, a western anti-diarrhoeal preparation. The percentage of mature leaves and fruits ofAzadirachta indica consumed by the bonnet macaques is relatively high. Plant feeding deterrents, such as, acid detergent fibre (ADF) and the inherent nature of the fruits ofAzadirachta indica, when consumed in large quantities to act as a purgative, could cause gastrointestinal upsets and diarrhoea. At Marakkanam, bonnet macaques ingest termitaria earth that would act as a pharmaceutical agent to alleviate gastrointestinal upsets and control diarrhoea.     

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.     

Power and limits of DNA-profiling in primate populations: Paternity assessment in rhesus macaques from Cayo Santiago

Paternity testing was performed in one social group (S) of rhesus macaques from Cayo Santiago, Puerto Rico. In 11/15 cases, sires could be identified comparing the multilocus DNA profiles of 19 males to those of the corresponding mother/child dyads. All 19 males could be excluded from paternity in the remaining four cases. Decision making was partly based on likelihoods of DNA profiles, and the theoretical model underlying these calculation is described. In a second social group (M), held in captivity, paternity testing was impeded by a deficit of maternal bands and by an increased extent of band sharing of mothers and their infants. Some possible explanations for these findings, including increased homozygosity in group M, are discussed.     

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.     

Ontogeny of locomotion in rhesus macaques (Macaca mulatta): II. Postural and locomotor behavior and habitat use in a free-ranging colony

This study quantifies changes in postural and locomotor behavior as well as habitat use across the life span of free-ranging rhesus macaques (Macaca mulatta) in the Cayo Santiago colony in Puerto Rico. It focuses on developmentally related changes from birth to adulthood, and complements an earlier study by Turnquist and Wells ([1994] J Hum Evol 26:487-499) on the early postnatal ontogeny of the musculoskeletal system of the same colony. A total of 6,551 locomotor and postural events was analyzed. Selection and use of substrate correlated well with age. The more sedentary adult and dependent infant select safe, wide, horizontal arboreal settings in contrast to the older Infant IIs and Juveniles, who are learning locomotor and postural skills through independent chase and play. Infant macaques, when independent, often employ a low center of gravity and widely abducted limbs in order to broaden their contact with the base of support. This study shows that the previously reported ontogenetic changes in morphology are closely paralleled by changes in postural and locomotor behavior, and these in turn are correlated to changes in habitat use, particularly during the formative years.     

Soils Consumed by Chimpanzees of the Kanyawara Community in the Kibale Forest,Uganda

We previously reported on a study of 4 soils that chimpanzees of the Kanyawara community in the Kibale National Park, Uganda consumed on a near-daily basis. We suggested that iron was a possible chemical stimulus in association with high quantities of Si:Al = 1:1-dominated clay minerals in the consumed material. To test our initial findings, we analyzed 18 samples from the same general area including 7 samples that the chimpanzees did not eat. Among the chemical elements, As, Au, Br, Ca, Cl, Dy, Mg, Ni, Sb, Sr, and I are below detection limits. Only Fe stands out as a potentially important nutritional element present in sufficient quantity to provide a physiological stimulus for chimpanzees living at high elevations near the flanks of the Ruwenzori Mountains. Along with Fe, metahalloysite is present in high amounts in these soils. In its pure crystalline form as a pharmaceutical grade clay mineral metahalloysite may well counteract the debilitating effects of diarrhea, with an effect similar to what is achieved with kaolinite (cf. Kaopectate^TM). An unexpected result, the relatively high nitrogen and carbon in the eaten samples relative to the uneaten group, indicates the chimpanzees may have a higher threshold for organic-rich material than previously believed. Contrarily, the color of the ingested material, depicts a material with less humus than in the uneaten group, a finding that is compatible with previous work reported at other geophagy sites in Africa. Of all the choices of soil available to them, the chimpanzees appear to be selecting highly homogeneous chemical natural earths with well-leached and uniform mineralogical material similar to the uneaten group, but with higher relative amounts of clay size material.     

Control of postpartum mating behavior in free-ranging rhesus monkeys

This paper explores the effect that a dependent rhesus macaque infant (Macaca mulatta) has on the timing of its mother's resumption of mating. Toward this end, behavioral data from the rhesus populations at Tughlaqabad, India, and Cayo Santiago, Puerto Rico, are compared. Specifically, the intervals between parturition and subsequent resumption of mating for individual parous females are examined in order to shed light on the relative importance of environmental and internal factors (such as lactational infertility) in the control of rhesus mating behvior. At both study sites it was found that the later a given female gave birth during a birth season the shorter was her parturition-mating interval and the younger was her infant when she resumed mating activity. It is suggested that this finding is the result of an interaction of environmental and internal factors; both act in concert to determine how soon after parturition a particular rhesus female will resume mating activity.     

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.     

Male reproductive timing in Rhesus macaques is influenced by the 5HTTLPR promoter polymorphism of the serotonin transporter gene

The 5HTTLPR polymorphism in the promoter region of the human serotonin transporter (SLC6A4) gene is known to be associated with various stress-related psychological and psychiatric phenomena. We observed that a similar diallelic polymorphism in the orthologous gene of rhesus macaques (Macaca mulatta) was related to the reproductive life history of 580 males residing in the free-ranging colony of Cayo Santiago, Puerto Rico, between 1985 and 1998. At first glance, the polymorphism appeared to be selectively neutral because no difference in total reproductive output was noted between males of different 5HTTLPR genotypes. However, whereas heterozygotes were significantly more reproductive than homozygotes at intermediate age (10-13 yr), the opposite held true before and after this period (n = 682 offspring; randomization P = 0.014). This association, which explains approximately 7% of the observed variation in sire age, most likely reflects different natal dispersal patterns and represents the first reported instance of a genetic influence on reproductive timing in mammals.     

黄山短尾猴食土行为

从行为生态学角度,依据黄山短尾猴食土行为在年龄、性别、社会等级序位、食土量、食土频率、食土持续时间中的分布和变化规律,结合土壤基本理化性质测定和分析,探讨了黄山短尾猴食土行为。黄山短尾猴对土壤的摄取是寻找和有目的的选择,有些场所是其"喜好"或"常去之处",食土场所通常是以多个体多次取食挖掘而形成的洞穴形式存在。取食土壤颜色黄色或黄棕色,酸性土壤,富含铁、钙、镁等矿物元素,粘土比例较高。社群各年龄段及性别个体均参与食土行为。平均食土行为持续时间在年龄和性别之间无显著差异;平均食土频率和食土量在成年雌性或雄性个体的社会等级序位之间无显著性差异;而成年雌性的平均食土频率和食土量,显著高于其它年龄或性别组,与雌性正值怀孕末期及产仔哺乳期,需要补充大量铁等矿物元素,以维持生理所需和体力消耗有关。典型的植食性动物黄山短尾猴有规律地取食粘土的行为,支持了食土行为具有"食物解毒作用"假说。人工投喂和食土行为的相关性表现为提高了食土频率,可能与粘土能够缓解高热量、低纤维人工食物造成的胃肠不适有关。     

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.     

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.     

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.     

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.     

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.     

Consequences of group fission for the patterns of relatedness among rhesus macaques

When mammalian social groups exceed their optimal size, they often tend to split. In view of the potential evolutionary benefits, it should be more advantageous for animals to stay with kin, rather than nonkin, during such fission events. In the present study, the spontaneous fission of two social groups, R and S, of rhesus macaques living on Cayo Santiago, Puerto Rico, provided the opportunity to compare the kinship structure of the corresponding parent and daughter groups, using information on both maternal and paternal relatedness. In both instances, maternal half-siblings and pairs of animals from the same family were significantly more prevalent in the fission products than in the parent group. During the split of group R, significantly more paternal half-siblings stayed in the remnants of the parent group than joined the seceding group. Our findings are compatible with previous behavioural studies demonstrating that female primates bias their social behaviour more to maternal than to paternal kin, but that both types of half-siblings prefer each other more than unrelated animals. It remains to be clarified by future research, however, whether the observed co-segregation of paternal half-sibs in our study reflects active choice or is a by-product of the group-specific kin structures, prior to fission.     

Rhesus macaque copulation calls: Re-evaluating the “honest signal” hypothesis

Male rhesus macaques sometimes give loud calls while thrusting or dismounting during multi-mount copulations.Hauser (1993) has proposed that these calls (1) impose a cost (increased risk of aggression) on calling males, and (2) increase callers' copulation frequencies, supporting the hypothesis that calls function as honest signals (handicaps) that females use to evaluate male quality during mate choice. This hypothesis was re-examined using data collected at Cayo Santiago, Puerto Rico on 40 focal females and their 56 observed copulatory partners. Although attacks by males against copulating pairs were frequent, they were usually directed only against the female of the pair. Males that called were no more likely than silent males to suffer male escalated attack during or immediately following mount series. Male-female dyads in which the male called during copulation were significantly more likely than non-calling dyads to complete the most copulations observed for any given female. Males that called at least once were significantly more likely than non-calling males to complete at least one copulation with a peri-ovulatory female. A log-linear model revealed that male rank and calling were both associated with likelihood of experiencing at least one peri-ovulatory copulation. However, calling was not associated with reception of demonstrated female mate choice behaviors. Controlling for dominance rank, callers did not experience more female proximity maintenance than non-callers. Nor were callers' hip-grasps refused less frequently than non-callers' hip-grasps. These results cast doubt on the hypothesis that rhesus macaque copulation calls are costly, honest indicators of intrinsic male quality. A contrasting alternative hypothesis, that a male's copulatory calls advertise relative immunity from attacks against his copulatory partners, was not supported either. Thus, the function of rhesus macaque copulatory calls remains unknown. The unusually high rate of copulations amongHauser's (1993) subjects may explain the discrepancy in results, but it is unclear how high copulation rates would increase the cost of copulatory calling to males.