Male rank,reproductive behavior,and reproductive success in free-ranging rhesus macaques

Paternity assessment through DNA fingerprinting by synthetic oligonucleotide probes was applied to one birth cohort in a social group of free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago. The 11 group males and 9 males from other groups were observed mating with the females. Paternity was determined for 11 of the 15 infants. Male dominance rank was not associated with reproductive success. High-ranking resident males (N=5) sired 27% of the infants born during a one-year study. Four of the 11 infants of known paternity were sired by males of other social groups. The four infants of unknown paternity were sired either by males not observed mating with the females or the low-ranking male who was not fingerprinted. Male dominance rank was not associated with reproductive activity during conception cycles. These results suggest that the effect of rank on male reproductive success is not a predictable correlation, but a conditional probability.     

The association between rank,mating effort,and reproductive success in male Barbary macaques (Macaca sylvanus)

The association between social rank, mating effort, and reproductive success of male Barbary macaques (Macaca sylvanus) has been evaluated by longterm behavioral observations and subsequent paternity determination via oligonucleotide DNA fingerprinting in a large semifreeranging group. All offspring born between 1985 and 1988 that survived to at least 1 year of age (n=75) were available for paternity testing. The exclusion of all but one of the potential fathers from paternity was possible in 70 cases (93%). Mating activities were recorded using ad lib. and focal female sampling techniques. The analysis of male mating effort was restricted to the most likely days of conception. Male rank correlated significantly with male mating success in all four breeding seasons and with male reproductive success in three of the four seasons. Mating success and reproductive success also showed a significant correlation, with the exception of one breeding season, in which the proportion of males per fertilizable female was especially high. Poor mating success was almost always associated with poor reproductive success, while good mating success was less predictive for a male's actual reproductive success. This was apparently a consequence of sperm competition, resulting from the promiscuous mating system. Male mating success is not necessarily an unreliable indicator for reproductive success, provided that sufficient sample sizes are available and that conception periods can be determined. Sperm competition and other factors may weaken the association, however.     

A 15-year study of the association between dominance rank and reproductive success of male rhesus macaques

The reproductive success (RS) of 32 males in a captive group of rhesus macaques (Macaca mulatta) between 1978 and 1992 was determined using paternity exclusion analysis. Dominance rank of each male over age 4 was assessed at the end of each breeding season based on agonistic dyadic interactions. The dominance rank and RS of these males were strongly correlated whether or not subadult males were included. The high reproductive success of males that eventually reached alpha rank is primarily responsible for this outcome. These results support the theory that social dominance has evolved in genusMacaca by sexual selection but some changes in male dominance rank and RS during the 15-year period suggest that priority of access is not the sole focus for such selection.     

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.     

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.     

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.     

Association between hybrid status and reproductive success of captive male and female rhesus macaques (Macaca mulatta) at the California National Primate Research Center (CNPRC)

The California National Primate Research Center (CNPRC) houses more than 1,000 rhesus macaques (Macaca mulatta) of mixed Chinese-Indian ancestry. Most of these animals are kept in outdoor field cages, the colony's long term breeding resource. Since 2001, hybrids comprised between 4 and 49% of the field cage populations, but in most cases have represented a maximum of 10% of those populations. The increasing prevalence of hybrids is partly due to management efforts to distribute genetic diversity effectively and minimize genetic subdivisions. However, other factors may also contribute to the spread of hybrids within the colony, most notably variance in socio-sexual behaviors and physical attributes. It is known that hybrids of some species exhibit heterosis, such as early maturation, that can enhance reproductive success, and anecdotal observations of mixed groups of hybrid, Indian and Chinese animals at the CNPRC suggest that hybrids are more sexually active. To determine whether hybrids experienced a reproductive advantage, a study was conducted using birth records of 5,611 offspring born in the CNPRC colony between 2003 and 2009. We found that while the degree of Chinese ancestry (DCA) appeared to influence the maturational schedule of both males and females (maturation was inversely related to proportion of Chinese ancestry), DCA had no independent effect on either male or female RS or rank. Therefore, we have found no evidence that a hybrid phenotype confers an absolute reproductive advantage in our colony.     

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.     

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.     

Geophagy as a therapeutic mediator of endoparasitism in a free-ranging group of rhesus macaques (Macaca mulatta)

Parasite levels were determined for 141 members of a naturally formed social group of rhesus macaques living under free-ranging conditions. Results indicate that group members harbor Trichuris trichiura, Balantidium coli, and large numbers of Strongyloides fuelleborni. Parasite counts decrease significantly with age in this population. Females have significantly fewer parasites than males and a significantly lower prevalence of multiple infections. There were no rank effects regarding parasitosis. While 89% of the animals examined are infected with one or more species of enteric parasite, the prevalence of diarrhea is negligible (2%). The low prevalence of diarrhea in the presence of high parasite loads may be due to the practice of geophagy, which is engaged in by 76% of group members. Soil eaten by these monkeys contains large amounts of kaolinitic clays. Kaolin-based pharmaceuticals (i.e. Kaopectate^®) are commonly used in human populations to treat diarrhea and intestinal upsets. The mechanical and pharmaceutical properties of the natural kaolinite-based clays may counteract the effects of parasitosis in this free-ranging population. Am. J. Primatol. 44:71-82, 1998. © 1998 Wiley-Liss, Inc.     

The association between rank and reproductive success of male rhesus monkeys

The paternity of 202 of 220 offspring of rhesus monkeys housed in six separate half-acre field cages at the California Primate Research Center was determined by genetic marker techniques. Reproductive success of the adult males was statistically significantly correlated (r = 0.76, P <0.0005) with rank. Marked systematic changes in reproductive success were, however, observed for two adult males during the three years covered by this study. Based upon these results and those of another study, it is argued that changes in rank position typically follow, rather than precede, changes in reproductive success.     

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.     

雄性短尾猴的等级顺位、睾酮水平与肠道寄生虫感染强度的关系

在等级森严的非人灵长类群体中,睾酮对雄性顺位维持有着重要作用,且影响着体内寄生虫种类和荷虫量。本研究以栖息于安徽黄山的雄性短尾猴为研究对象,通过计算成年雄性的等级顺位,测定其粪便中睾酮含量以及寄生虫的荷虫量,探讨雄性等级顺位、睾酮水平与健康间的平衡关系。结果表明：共检测出10种肠道寄生虫,包括4种蠕虫、5种原虫和1种螨虫;其中雄性短尾猴个体间睾酮水平（1.00±0.42） ng/g和肠道寄生虫荷虫量（112.44±83.62）EPG均存在显著差异（Kruskal-Wallis H,P<0.05）;等级顺位与睾酮水平呈正相关（Spearman, N=8,ρ= 0.326, P<0.05）,与肠道原虫类的荷虫量呈负相关（Spearman, N=8,ρ= - 0.345, P<0.05）,与肠道蠕虫类的荷虫量无相关性（Spearman, N=8,ρ= 0.065, P>0.05）;睾酮水平与肠道原虫类寄生虫的荷虫量呈负相关（Spearman, N=8,ρ= -0.546, P<0.05）,与肠道蠕虫类的荷虫量无相关性（Spearman, N=8,ρ= -0.013, P>0.05）。本研究表明高顺位雄性拥有更高的睾酮水平,这不仅对其顺位的维持具有重要作用,对原虫类寄生虫也具有明显的抑制作用。     

黄山短尾猴不同顺位等级雄性个体友好行为的比较研究

社会顺位等级制度在灵长类动物中普遍存在,它对动物个体的繁殖和社会行为有广泛的影响.本研究对黄山短尾猴鱼鳞坑YA2群6个不同顺位成年雄性个体,根据顺位高低,将它们分成3组:高顺位组(2只个体)、中等顺位组(2只个体)、低顺位组(2只个体),采用目标动物取样法对它们的社会行为进行研究,结果表明,3组之间(1)接收和发出架桥行为频次差异显著,高顺位组接收架桥次数最多;(2)接收和发出爬跨行为频次差异显著;低顺位组接收爬跨次数最多;(3)发出呈臀行为频次差异显著,但接收呈臀行为频次差异不显著;高顺位组是接收呈臀次数最多,低顺位组发出呈臀次数最多;(4)摇树行为频次差异显著,高顺位组发出摇树行为最多.因此雄性黄山短尾猴友好行为可以体现出社群顺位等级关系,这种社群顺位等级关系和这些友好行为在维持社群稳定上有重要作用.     

The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques,Macaca fascicularis

Demographic changes were recorded throughout a 12-year period for three social groups ofMacaca fascicularis in a natural population at Ketambe (Sumatra, Indonesia). We examined the prediction that females' lifetime reproductive success depended on dominance rank and group size. Average birth rate was 0.53 (184 infants born during 349 female years). For mature females (aged 8–20 yr) birth rate reflected physical condition, being higher in years with high food availability and lower in the year following the production of a surviving infant. High-ranking females were significantly more likely than low-ranking ones to give birth again when they did have a surviving offspring born the year before (0.50 vs 0.26), especially in years with relatively low food availability (0.37 vs 0.10). Controlled comparisons of groups at different sizes indicate a decline in birth rate with rroup size only once a group has exceeded a certain size. The dominance effect on birth rate tended to be strongest in large groups. Survival of infants was rank-dependent, but the survival of juveniles was not. There was a trend for offspring survival to be lower in large groups than in mid-sized or small groups. However, rank and group size interacted, in that rank effects on offspring survival were strongest in large groups. High-ranking females were less likely to die themselves during their top-reproductive years, and thus on average had longer reproductive careers. We estimated female lifetime reproductive success based on calculated age-specific birth rates and survival rates. The effects of rank and group size (contest and scramble) on birth rate, offspring survival, age of first reproduction for daughters, and length of reproductive career, while not each consistently statistically significant, added up to substantial effects on estimated lifetime reproductive success. The group size effects explain why large groups tend to split permanently. Since females are philopatric in this species, and daughters achieve dominance rank positions similar to their mother, a close correlation is suggested between the lifetime reproductive success of mothers and daughters. For sons, too, maternal dominance affected their reproductive success: high-born males were more likely to become top-dominant (in another group). These data support the idea that natural selection has favored the evolution of a nepotistic rank system in this species, even if the annual benefits of dominance are small.     

Consortships and conceptions in captive rhesus macaques (Macaca mulatta)

A captive group of rhesus macaques (Macaca mulatta) was observed during the breeding season to determine if consortship behavior, rather than promiscuous matings, resulted in higher reproductive success for either partner. The 38 adult females in this group were observed “in consort” with the 5 adult or 4 subadult males on 179 occasions. Most of these consortships were short-term, lasting less than one day. Six females engaged in consortships with one male that spanned more than three days, but the majority of these long-term associations did not result in a pregnancy with that male. The term “consortship” has been traditionally accepted as a specific nonhuman primate mating pattern, but the exact nature of this behavioral pattern and its evolutionary importance have been less clearly understood. Consort behavior could be considered a precursor to a monogamous mating system if long-term exclusive sexual associations resulted in higher reproductive success for the participants. But this study demonstrates that for rhesus macaques, who exhibit both consort behavior and more promiscuous matings, there is no clear reproductive advantage to long-term consortships. In light of the inconsistent use of the term consortship, the possible adaptive significance of an exclusive male-female sexual association for the evolution of human mating patterns needs to be reevaluated.     

Male dominance rank and reproductive success in primate groups

The relationship between male dominance rank and reproductive success has been a topic of interest since the beginning of primatology. From a theoretical point of view the existence or absence of this relationship has great implications with respect to the meaning of dominance rank and more general of the social relationships between individuals within social groups. Until fairly recently mating behaviour has been used as an indicator of reproductive success, but these two variables need not be correlated. The relations between mating success, reproductive success, and dominance rank indicate whether selective mating is involved (different mating partners at different phases of fertility, for example through male contest or female choice). With the development of genetic techniques to determine reproductive success directly, it has now become possible to investigate these relations. In our study on wild long-tailed macaques (Macaca fascicularis) we find a relatively strong correlation between rank and reproductive success which is attributable to selective mating by the alpha male during fertile periods of the females. In most previous studies no such clear results have been obtained, and we discuss the differences in outcome in relation to the study conditions, group sizes, and possible differences between species in terms of reproductive strategies.     

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.