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.     

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.     

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.     

Social rank and cortisol among female rhesus macaques (Macaca mulatta)

In animal societies, some stressful events can lead to higher levels of physiological stress. Such stressors, like social rank, also predict an increased vulnerability to an array of diseases. However, the physiological relationship between social rank and stress varies between different species, as well as within groups of a single species. For example, dominant individuals are more socially stressed at times, while at other times it is the subordinate ones who experience this stress. Together, these variations make it difficult to assess disease vulnerability as connected to social interactions. In order to learn more about how physiological rank relationships vary between groups of a single species, cortisol measurements from hair samples were used to evaluate the effects of dominance rank on long-term stress levels in despotic and less stringent female rhesus macaque hierarchal groups. In despotic groups, cortisol levels were found not to be correlated with social rank, but a negative correlation was found between social rank and cortisol levels in less stringent hierarchies. Low ranking monkeys in less stringent groups secreted elevated levels of cortisol compared to higher ranking animals. These data suggest that variations in the strictness of the dominance hierarchy are determining factors in rank related stress physiology. The further consideration of nonhuman primate social system diversity and the linear degree of their hierarchies may allow for the development of valid rank-related stress models that will help increase our understanding and guide the development of new therapeutics for diseases related to human socioeconomic status.     

Mating patterns,mate choice,and birth season heterosexual relationships in free-ranging rhesus macaques

Birth season adult heterosexual nonkin relationships of 50 free-ranging female rhesus macaques (Macaca mulatta) in two social groups at Cayo Santiago, Puerto Rico were examined using focal follow (289 hr) and ad lib data. Eighty-eight percent of subjects had at least one relationship characterized by particularly high frequencies of spatial proximity, grooming, or both. These were designated “friendships.” Males intervened in aggressive interactions more frequently on behalf of Friends than non-Friends. Female aggressive support of males was extremely rare. Higher-ranking males experienced more friendships than lower-ranking males. High-ranking females had higher-ranking Friends than low-ranking females. Older females had higher-ranking Friends than younger females. Females groomed high-ranking Friends more than they were groomed by them, whereas they groomed low-ranking Friends less than they were groomed by them. In one social group, high-ranking females were more likely than low-ranking females to groom their Friends more than they were groomed by them. Males were more responsible than females for spatial proximity maintenance in 9 of 14 Friend dyads for which sufficient data were available. Neither male nor female dominance rank affected responsibility for proximity maintenance in Friend dyads. Eight of 24 females had friendships with males with whom they had completed copulations during their conception peri-ovulatory period of the preceding mating season. Two of 19 females completed peri-ovulatory copulations with Friends during the following mating season. Friendship was not correlated with either of two demonstrated female mate choice indicators: (1) proximity maintenance during estrus; or (2) cooperation with male “hip-grasp” courtship attempts. Males directed “muzzle-up” courtship signals at lower rates toward Friends than toward non-Friends. These and other investigators' results indicate that (1) protection from aggression is the primary benefit to female rhesus macaques of birth season heterosexual relationships; (2) the most effective protectors are in greatest demand as Friends; and (3) friendship has no effect or an inhibitory effect on mate choice in this species. Benefits to males of friendships were not apparent from this study but may include coalitional support against lower-ranking males.     

A comparison of the mating behavior of adolescent and adult female rhesus macaques (Macaca mulatta)

This study compares adult and adolescent female rhesus macaques with regard to (1) characteristics of their copulatory partners, (2) their proceptive behaviors, and (3) adult male behaviors toward them during estrus. We conducted focal follows of 24 adolescent and 65 adult free-ranging estrous female rhesus macaques on Cayo Santiago during two mating seasons. Compared to adult females, adolescents presented sexually to males at higher rates; copulated more frequently with rankless young male, and extra-group males; and, in one of two mating seasons, were ignored more frequently by males to whom they presented sexually. Adolescents tended to copulate with ranked, resident males at higher frequencies on days when the operational sex ratio (adult males:estrous adult females) was high. Males directed “muzzle-up” signals to adolescents at lower rates than to adults in one of two mating seasons, although this effect vanished when males who might have fathered adolescent females were excluded from analysis. Adolescents did not differ consistently from adults in strength of the correlation between proximity maintenance (dyadic Hinde's Index) and copulation rate, or in approach rate to males. Adolescent females, relative to adult females, presented sexually more to rankless young males, but did not present more to ranked, resident males. Both proximate (e.g. endocrine) and ultimate (e.g. differential fecundity; female-female mate competition) explanations may account for the reported differences between adult and adolescent female rhesus macaque sexuality.     

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.     

Costs and benefits of maternal aggression in lactating female rhesus macaques

Data from over 400 hr of observation of mother-infant rhesus macaques indicate that during the first 12 weeks of lactation infants are at risk from other group members and that mothers use aggression as well as restraining to protect them. Maternal aggression was negatively correlated with infant restraining. High-ranking mothers reacted aggressively to individuals handling their infants more than did middle- and low-ranking mothers. Conversely, middle- and low-ranking mothers restrained their infants more than did high-ranking mothers. Maternal aggression did not vary with infant age. Maternal aggression was directed toward a higher proportion of higher-ranking adult females and their immature offspring and was more likely to be followed by counter-aggression than nonmaternal aggression, i.e. aggression not related to interactions involving the infant. Middle-and low-ranking mothers suffered higher costs in terms of retaliation than high-ranking mothers. It is argued that the occurrence and distribution of maternal aggression among species and individuals should depend on the risk posed to infants by conspecifics as well as on the characteristics of the social structure (e.g. degree of asymmetry of agonistic contests) and of the mother (e.g. her dominance rank) which may affect the probability of retaliation.     

Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago. II. Phenotypic,genetic, and environmental correlations between traits

The general lack of phenotypic correlation among skeletal nonmetric traits has been interpreted as indicating a lack of genetic correlation among these traits. Nonmetric traits scored on animals in the skeletal collection of rhesus macaques from Cayo Santiago are used to calculate phenotypic, genetic, and environmental correlations between traits. The results show that even when phenotypic correlations are low, there may be large, significant genetic correlations among these traits. The genetic correlation pattern suggests that genes which affect nonmetric trait variation act primarily at a local level in the cranium, even though there are genes with pleiotropic effects on skeletal nonmetric traits throughout the cranium. Environmental and phenotypic correlations do not show this neighborhood pattern of correlation.     

Sociometrics of Macaca mulatta: II. Decoupling centrality and dominance in rhesus monkey social networks

The concept of the linear dominance hierarchy and a much less precise notion of a central/peripheral ordering of individuals have been prominent among the ideas about social organization of monkey groups. Although the latter has seldom been quantified, the ranks of individuals in the two orders are usually assumed to be correlated. This paper reports on a longitudinal study of a free-ranging group of rhesus monkeys. The individual histories of progression of dominance rank and an independently determined measure of centrality in the social grooming network are compared among a set of males. Centrality is not a static correlate of dominance rank as implied by the findings of short-term studies. Rather, centrality is a more sensitive indicator of status than is dominance rank, to which it is related in a dynamic fashion. Small changes in dominance rank may be followed by large changes in centrality. An increase in centrality may facilitate rise in dominance rank. These findings suggest a complex psychology of status, rather than a simple causative relation between the two variables.     

A four-year study of the association between male dominance rank, residency status, and reproductive activity in rhesus macaques (Macaca mulatta)

Considerable controversy exists on the nature of the relationship between male dominance rank and reproductive activity. The nature of this relationship has important implications for understanding the manner in which males compete for access to limited resources. Behavioral data on mating patterns were collected over a four-year period from one social group of rhesus macaques on Cayo Santiago. Correlations between dominance rank and reproductive activity were not stable over a four-year period, but changed yearly. Positive, significant correlations were present in the first two years of the study while non-significant correlations were found in the second two years. The variation found in the correlations between rank and mating activity could be accounted for by changes in the mating frequencies of different classes of males. The long-term resident males had declines in ejaculation frequencies over the duration of the study. Males who immigrated into the group had yearly increases in reproductive behavior over three consecutive years. Maturing natal males also increased their levels of reproductive activity from year-to-year. Combining these mating patterns over time resulted in shifting the proportions of matings away from the long-term residents and in favor of the new males. High-ranking males had an advantage in reproductive activity over the first two years of the study, as measured by both the total number of ejaculations and the mean number of ejaculation per male. New males, comprised of recent immigrants and maturing natal males, had a greater level of reproductive activity over the last two years. These results suggest that the effect of rank on reproductive activity is variable and that males utilize alternative tactics to attain access to limited resources. Simple one-factor models explaining the relationship between rank and reproductive activity must be replaced with models explaining how alternate strategies affect male competition and reproductive success in primates.     

Interactions among adult males and females before and after the death of the alpha male in a free-ranging troop of Japanese macaques

This report documents the social interactions among adult Japanese macaques in a free-ranging troop before and after the death of the alpha male, who died at 28 years of age after occupying his rank position for 17 years. The alpha male’s physical condition had deteriorated due to his extreme age for several months before his death. However, he maintained his alpha position. When he was attacked by the second-ranking adult male, he was rescued by the alpha female. Thereafter, whenever the second-ranking male approached him, the alpha male screamed for the alpha female’s support. The number of adult females to whom the alpha male maintained proximity during his last four months was similar to that during the same period of the previous year. Prior to his death, the alpha male was observed in close proximity to the alpha female much more frequently than was the second-ranking male. These results indicate that the alpha male maintained his position by depending on female support and particularly that of the alpha female.     

Quantitative genetics of skeletal nonmetric traits in the rhesus macaques of Cayo Santiago. III. Relative heritability of skeletal nonmetric and metric traits

This study addresses the long-standing controversy in skeletal biology concerning the relative utility of skeletal metric and nonmetric traits for studies of biological relationship. This controversy centers on the relative heritability of these two trait sets. This paper presents heritabilities for a series of skeletal metric and nonmetric traits measured with the same sample of mother-offspring pairs from the Cayo Santiago skeletal collection of rhesus macaques. Skeletal nonmetric traits display significantly greater heritability estimates than metric traits. This difference is due primarily to the high heritability estimates of hyperostotic nonmetric traits. Foraminal traits are not significantly more heritable than skeletal metric traits. The generality of this pattern of heritability values, in which hyperostotic nonmetric traits are more highly heritable than foraminal nonmetric and metric traits, depends on future empirical study of the correlation of heritability values in populations and theoretical work.     

Age- and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free-ranging rhesus macaques.

Normative age- and gender-related changes in body composition, serum lipids, testosterone, and insulin-like growth factor (IGF-1) were examined in the Cayo Santiago free-ranging rhesus macaques. In both adult males and females, body weights, crown-rump lengths, and circumference of the limbs were lowest in the oldest group (20+ years of age) as compared with other adult age classes. Body fat, as reflected in subcutaneous fatfold thickness and waist/thigh ratios, were higher in adult females than adult males. This gender dimorphism was first detectable among the 6-9 year old age group. Greatest body fat among females was observed in the 10-14 age group, whereas in males the highest values were observed in the 15-19 age group. Differences in body composition were also observed with respect to reproductive status. Although there were no gender differences in overall cholesterol levels, there were age-related differences between males and females, and only in males were cholesterol values positively related to adiposity. There were no age- or gender-related differences in triglyceride values, but levels were significantly higher in pregnant females in comparison with other reproductive states. Levels of testosterone were not significantly related to any morphometric parameter and values did not decrease significantly with age. Levels of IGF-1 exhibited a significant age-related decrease among adult males, and females had higher levels independent of age. The similarities between the present findings and human studies suggest that further studies in the free-ranging rhesus macaques would provide a bridge between studies of laboratory-housed primates and studies of human beings with respect to the etiology of obesity and life-history changes in body composition and endocrine and metabolic parameters.     

Osteoarthritis of the hand in nonhuman primates: A clinical,radiographic, and skeletal survey of Cayo Santiago rhesus macaques

Abstract: We describe the relative prevalence and pattern of distribution of osteoarthritis (OA) in the hands of elderly (>15 years) rhesus macaques using clinical, radiographic, and skeletal examinations. In the clinical study the prevalence of nodes was 72% and 16% in the distal inter-phalangeal joints (DIPJ) and proximal inter-phalangeal joints (PIPJ), respectively, 31% of all monkeys had polyarticular nodes. Radiographic OA was present in 55%, 9.1%, and 0% of the DIPJs, PIPJs, and thumb bases, respectively. Skeletal OA as defined by joint surface eburnation for the DIPJ, PIPJ, and thumb base were 16%, 8%, and 2%, respectively. A similar pattern of hand OA with humans is described except for the thumb base OA. This may be due to the relatively rudimentary manipulative role of the macaque thumb. The finding of polyarticular nodal OA raises the possibility of a common pathogenensis for IPJ OA amongst primates.     

Social relationships of immigrant and resident female mountain gorillas,II: Relatedness,residence, and relationships between females

Female transfer is common in mountain gorillas, but most adult females reside with female relatives for at least some of their lives. In four mountain gorilla social groups, co-resident relatives had higher rates of affiliative interaction and lower rates of aggressive interaction, and were more tolerant of each other, than non-relatives. These differences were greater for maternal than for paternal relatives. Non-relatives typically had few affiliative interactions, but some (mostly but not entirely long-term co-residents) had friendly relationships. Females showed reciprocity in affiliative behavior. Long-term residents in two groups maintained less tolerant relationships with more recent immigrants than with each other and than did most pairs of immigrants. The effects of relatedness and residence status on relationships may sometimes be complementary because both factors can lead to similar reproductive interests. A potential exists for some resemblance between female-female social relationships in mountain gorillas and those in female-bonded primate species. However, even female relatives usually spend little time interacting socially with each other, and the benefits of relationships with males outweigh those of relationships with other females. © 1994 Wiley-Liss, Inc.     

Effects of age, dominance, and seasonal changes on proximity relationships in female Japanese macaques (Macaca fuscata) in a free-ranging group at Katsuyama

The present study compares the behavior of old female Japanese macaques (Macaca fuscata) with that of their full adult daughters in a free-ranging group, with respect to dominance and seasonal changes. Old mothers (21 to 25 years old) spent more time resting and alone than did their middle-aged adult daughters (10 to 17 yr old). However, the number of skin-related animals in proximity to the subject females, did not differ between mothers and their adult daughters. Mothers maintained proximity to more non-kin-related immature animals in the mating season than did their adult daughters, perhaps to avoid sexual aggression from males and to reduce the loss of body temperature in the cold. Dominance rank clearly influenced the social interactions of old mothers: high-ranking mothers interacted with more non-related adult females and immature animals than did low-ranking mothers, indicating that old age does not decrease the attractiveness of high-ranking animals.     

Social relationships of immigrant and resident female mountain gorillas. I. Male-female relationships

Adult males are important social partners for all females in mountain gorilla social groups, but male-female relationships can vary in association with variation in female residence status, male age and mating status, and relatedness. Such variation occurred in a large group observed over a 3-year period. All females associated and interacted affiliatively relatively often with a young silverback with whom all mated. Long-term resident females also did so with an old, non-breeding male to whom most were related, but recent immigrants spent little time near him and had few non-aggressive interactions with him. The old male made agonistic interventions to support relatives; interventions in female conflicts by the younger male tended to ameliorate competitive differentials that immigrants faced and may have helped him to retain them as mates. Males aggression toward females was common, most probably served as a mating tactic, and did not involve resource competition. Extensive grooming by an adolescent male suggests that males may also use affiliative behavior to develop mating relationships. Females may have competed for proximity with and social access to the younger silverback; competitive success could influence how well females and their offspring are protected by silver-backs, but the extent of such competition was not clear. Large group size may have heightened differentiation of male-female relationships and competition among females, but comparative data from smaller groups generally corroborate the findings from the large group. © 1992 Wiley-Liss, Inc.     

成年雌性太行山猕猴活动时间分配的季节性变化:食物和温度的影响

活动时间分配是指动物根据环境和自身需求从事各种基本行为和活动的过程,受季节性变化的食物和温度等生态因素的影响。2013年3月至2014年2月,在太行山猕猴国家级自然保护区天坛山管护区,采用目标动物取样法,观察并记录了一个野生太行山猕猴群(WW-1群)内成年雌性个体的活动特征及其季节性变化,旨在了解成年雌性猕猴的日活动时间分配及其影响因素。结果表明:(1)成年雌性猕猴的活动时间分配表现出明显的季节性变化。春季,雌性猕猴花费52.9%时间于休息、19.5%时间于取食、11.8%时间于移动;夏季,用于休息、取食、移动的时间比例分别为53.4%、18.0%和11.3%;秋季,猕猴花费35.9%时间于取食、30.0%时间于休息,15.9%时间于移动;冬季,用于取食、休息和移动的时间比例分别为35.4%、39.7%和8.0%;(2)春季,成年雌性太行山猕猴主要取食种子(35.4%)和树叶(34.3%);夏季,树叶(73.5%)主导其每日食物组成;秋季,主要取食种子(98.1%);冬季,树皮(82.1%)则成为猕猴的主要食物;(3)当每日食物组成以草和树叶为主时,猕猴用于取食的时间增加,移动时间减少;当每日食物组成以种子为主时,则取食时间减少,移动时间增加;(4)随着气温降低,猕猴取食时间增加,而移动时间减少。总之,成年雌性太行山猕猴的日活动时间分配主要受季节性变化的食物资源和气温的影响,它们可通过日活动时间的调整以适应食物和环境温度的季节性变化。