Low-ranking Females Research Articles

Social and ecological factors influencing offspring survival in wild macaques.

Premature loss of offspring decreases direct fitness of parents. In gregarious mammals, both ecological and social variables impact offspring survival and may interact with each other in this regard. Although a number of studies have investigated factors influencing offspring loss in mammals, we still know very little on how different factors interact with one another. We therefore investigated fetal and infant mortality in 3 large groups of wild crested macaques (Macaca nigra) over a period of up to 5 years by including potential social causes such as maternal dominance rank, male immigration, between group encounters, and ecological conditions such as rainfall in a multivariate survival analysis using Cox proportional hazards model. Infant but not fetal survival was most impaired after a recent takeover of the alpha-male position by an immigrant male. Furthermore, infant survival probability increased when there was an increase in number of group adult females and rainfall. Fetal survival probability also increased with an increase of these 2 factors, but more in high-ranking than low-ranking females. Fetal survival, unlike that of infants, was also improved by an increase of intergroup encounter rates. Our study thus stresses the importance of survival analyses using a multivariate approach and encompassing more than a single offspring stage to investigate the determinants of female direct fitness. We further provide evidence for fitness costs and benefits of group living, possibly deriving from high pressures of both within- and between-group competition, in a wild primate population.

Pampas deer (Ozotoceros bezoarticus) male–female agonistic behavior toward high and low social ranked females

The pampas deer is an endangered species from the southern cone of South America. Although it is breed in confined groups, there is very scarce information on how their social relationships and aggressiveness are regulated in these groups. As we hypothesized that pampas deer males display different behaviors toward high or low social ranked females, we compared the number and pattern of agonistic behaviors used by pampas deer males to displace high- and low-ranked females. We performed focal observations recording all female–female agonistic interactions resulting in the displacement of an animal in six breeding groups (total = 6 males and 31 females), and calculated the success index for each hind. Then, we recorded all male–female agonistic interactions while animals received food, and compared the total number and the type of interactions used by males to displace high- and low-ranked individuals. Males displaced more frequently high-ranked than low-ranked females (P = 0.006), mainly by their presence (P = 0.0004); males tended to displace low-ranked females more frequently by kicking (P = 0.051). We designed a complementary study to determine if the male–female physical distances may explain that difference. We recorded male–female distances every 5 min for 30 min during 10 days while animals ate ration, and calculated an association index (AI) between each female with the male. Low-ranked females tended to have greater AI accumulated at 5 and 10-min scans (P = 0.071 and 0.077, respectively) than high-ranked females. The changes in the AI may indicate that high-ranked females were displaced during the period with more interactions. We concluded that (1) pampas deer males displayed more agonistic interactions toward high-ranked than low-ranked females; (2) this difference was mainly due to a greater number of displacements of females by mere presence; (3) high-ranked females moved far from males than low-ranked females, reflecting different relationships between them.

Rank effects on social stress in lactating chimpanzees

Given the deleterious consequences associated with chronic stress, individual differences in stress susceptibility can have important fitness implications. These differences may be explained in part by dominance status because high rank is typically associated with decreased aggression and improved nutrition. Here, we examined the relationship between dominance and social stress in lactating chimpanzees, Pan troglodytes schweinfurthii, at Gombe National Park, Tanzania. We did so by pairing daily demographic and behavioural data with faecal glucocorticoid metabolite (FGM) concentrations collected over 37 months. While there was no main effect of rank, interesting differences emerged by adult subgroup size and adult sex ratio (males/females). We found that differences in FGM concentrations between high- and low-ranking females were most pronounced as adult subgroup size and sex ratio increased. Low-ranking females had higher FGM concentrations in larger subgroups and in subgroups biased towards adult males; we observed no comparable change in FGM concentrations amongst high-ranking females. Because low-ranking females were the recipient of significantly more male aggression relative to females of high rank, these patterns may be driven by psychosocial stress in low-ranking females. There was no significant change in diet quality across subgroup sizes; this finding suggests that nutritional stressors were not driving differences in female FGM concentrations. Being susceptible to social stress has important fitness implications as it may constrain low-ranking females from 'choosing' optimal subgroups to take advantage of food resources and/or for the socialization of their offspring.

Vervet Monkeys Solve a Multiplayer “Forbidden Circle Game” by Queuing to Learn Restraint

In social dilemmas, the ability of individuals to coordinate their actions is crucial to reach group optima. Unless exacted by power or force, coordination in humans relies on a common understanding of the problem, which is greatly facilitated by communication. The lack of means of consultation about the nature of the problem and how to solve it may explain why multiagent coordination in nonhuman vertebrates has commonly been observed only when multiple individuals react instantaneously to a single stimulus, either natural or experimentally simulated, for example a predator, a prey, or a neighboring group. Here we report how vervet monkeys solved an experimentally induced coordination problem. In each of three groups, we trained a low-ranking female, the "provider," to open a container holding a large amount of food, which the providers only opened when all individuals dominant to them ("dominants") stayed outside an imaginary "forbidden circle" around it. Without any human guidance, the dominants learned restraint one by one, in hierarchical order from high to low. Once all dominants showed restraint immediately at the start of the trial, the providers opened the container almost instantly, saving all individuals opportunity costs due to lost foraging time. Solving this game required trial-and-error learning based on individual feedback from the provider to each dominant, and all dominants being patient enough to wait outside the circle while others learned restraint. Communication, social learning, and policing by high-ranking animals played no perceptible role.

DO RINGTAILED LEMURS EXHIBIT A SKEWED BIRTH SEX RATIO DEPENDING ON SOCIAL AND ENVIRONMENTAL CONDITIONS? A PRELIMINARY ANALYSIS OF A WILD POPULATION

In a 13-year study, we examined the birth sex ratio (BSR) of wild ringtailed lemurs at Berenty Reserve in Madagascar. Their BSR represented an equal sex ratio at the population level, irrespective of population change. High-ranking females did not always overproduce sons or daughters. In newly formed groups, females did not always overproduce daughters, and the BSR of young females was similar to an equal sex ratio. Thus, our data do not support the Trivers-Willard, local resource competition-population, or local resource enhancement hypotheses. Only one significant skewed BSR was observed: low-ranking females in medium-sized groups overproduced sons. This finding may support the local resource competition-individual hypothesis, but does not do so robustly.

Among-sibling differences in the phenotypes of juvenile fish depend on their location within the egg mass and maternal dominance rank

We investigated whether among-sibling differences in the phenotypes of juvenile fish were systematically related to the position in the egg mass where each individual developed during oogenesis. We sampled eggs from the front, middle and rear thirds of the egg mass in female brown trout of known dominance rank. In the resulting juveniles, we then measured traits that are related to individual fitness: body size, social status and standard metabolic rate (SMR). When controlling for differences among females in mean egg size, siblings from dominant mothers were initially larger (and had a lower mass-corrected SMR) if they developed from eggs at the rear of the egg mass. However, heterogeneity in the size of siblings from different positions in the egg mass diminished in lower-ranking females. Location of the egg within the egg mass also affected the social dominance of the resulting juvenile fish, although the direction of this effect varied with developmental age. This study provides the first evidence of a systematic basis for among-sibling differences in the phenotypes of offspring in a highly fecund organism.

Dominance rank of adult females and mating competition in Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China

Dominance hierarchy reflects resource competition in male primates as well as females. In this study, we collected data on the social rank and mating competition of female Sichuan snub-nosed monkeys from September 2009 to June 2010 in the Qinling Mountains, Shaanxi, China. Displacement was used to determine social hierarchy of the studied wild females. A total of 1223 displacement bouts between adult females and 316 mating behaviors within one-male units (OMUs) were recorded. Competitive displacement among females was very low (0.22 displacements per observation hour). The dominant ranks of females in target OMUs were determined by displacement, from one OMU to another: JB unit: YL > DBC > YCM >XBC > BD; JZT unit: XHW > JG > DT; PK unit: QQ > TM > HF; LP unit: SK > TH > WM. Higher-ranking females performed significantly more sexual behavior than lower-ranking females in this rare monkey. High-ranking females were more likely to win mating contests within those OMUs. Based on these studies, we assessed the social relationships among adult females and clarified possible explanations for the strategies of female mating competition in the OMUs. Furthermore, the notion that reproductive success may also be related to female dominance hierarchies in this polygynous species should be considered in future research.

Variation in personality and fitness in wild female baboons

Studies of personality in nonhuman primates have usually relied on assessments by humans and seldom considered the function of the resulting "trait" classifications. In contrast, we applied exploratory principal component analysis to seven behaviors among 45 wild female baboons over 7 y to determine whether the personality dimensions that emerged were associated with measures of reproductive success. We identified three relatively stable personality dimensions, each characterized by a distinct suite of behaviors that were not redundant with dominance rank or the availability of kin. Females scoring high on the "Nice" dimension were friendly to all females and often grunted to lower-ranking females to signal benign intent. "Aloof" females were aggressive, less friendly, and grunted primarily to higher-ranking females. "Loner" females were often alone, relatively unfriendly, and also grunted most often to higher-ranking females. Aloof and Loner females were rarely approached by others. Personality dimensions were correlated in different ways with three measures previously shown to be associated with fitness: stress levels and two behavioral indices reflecting the closeness of dyadic bonds formed by individuals. Females who scored high on Nice had high composite sociality indices (CSI) and stable partner preferences, whereas females who scored high on Aloof had lower CSI scores but significantly more stable partner preferences. Loner females had significantly lower CSI scores, less stable partner preferences, and significantly higher glucocorticoid levels. It remains to be determined which of the Nice or Aloof personality dimensions is more adaptive, or whether variation is maintained by contrasting effects on fitness.

Digit Ratios and Dominance in Female Baboons (Papio hamadryas and Papio ursinus)

A growing body of literature suggests that the ratio between the second and fourth digits of the hands (2D:4D ratio) is associated with exposure to prenatal sex hormones in a variety of animals including primates. Female baboons form dominance hierarchies composed of matrilines of related individuals, and the social mechanisms contributing to the structure of these hierarchies have been well studied. We here investigated the relationship between inferred prenatal androgen effects (PAE) and female rank in a captive troop of Hamadryas baboons (Papio hamadryas) with a typical social structure and three captive groups of chacma baboons (Papio ursinus) made up entirely of unrelated orphans. Low 2D:4D ratios (high inferred PAE) were associated with higher-ranking females and high 2D:4D ratios (low inferred PAE) with lower-ranking females in both focal species. This negative correlation between 2D:4D ratio and rank suggests prenatal androgens are linked with the maintenance of female ranks within matrilines in troops with a natural social structure and to the ranks acquired by orphan females.

Market powers predict reciprocal grooming in golden snub-nosed monkeys (Rhinopithecus roxellana).

Social grooming is a common form of affiliative behavior in primates. Biological market theory suggests that grooming can be traded either for grooming or other social commodities and services. When no other services are exchanged, grooming is predicted to be approximately reciprocated within a dyad. In contrast, the amount of reciprocal grooming should decrease as other offered services increase. We studied grooming patterns between polygamous male and female in golden snub-nosed monkeys (Rhinopithecus roxellana) from the Qinling Mountains of central China and found that about 29.7% of grooming bouts were reciprocated. However, the durations of grooming bouts offered and returned was asymmetrical within dyads. In bisexual dyads, more grooming was initiated by females than males, which became more pronounced as the number of females per one-male unit increased. The rate of copulation per day for each female was positively correlated with the total duration of grooming time females invested in males.. Females without an infant (non-mothers) directed more grooming towards females with an infant (mothers) and were significantly more likely to be non-reciprocated. There was a significant negative relationship between non-mother and mother grooming duration and the rate of infants per female in each one-male unit. High-ranking females also received more grooming from low-ranking females than vice versa. The rate of food-related aggressive interactions was per day for low-ranking females was negatively correlated with the duration of grooming that low-ranking females gave to high-ranking females. Our results showed that grooming reciprocation in R. roxellana was discrepancy. This investment-reciprocity rate could be explained by the exchange of other social services in lieu of grooming.

Interannual Variation in Nut Abundance Is Related to Agonistic Interactions of Foraging Female Japanese Macaques (Macaca fuscata)

The importance of dominance status to foraging and ultimately survival or reproductive success in wild primates is known; however, few studies have addressed these variables simultaneously. We investigated foraging and social behavior among 17 adult female Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan, from September to November in 2 consecutive years (2004 and 2005) to determine whether interannual variation in food availability was related to variation in agonistic interactions over food resources and the feeding behavior of individuals of different dominance rank. We compared energy obtained with daily energy requirements and also examined the effect of variation in feeding behavior on female survival and reproductive success. Fruiting conditions differed considerably between the 2 yr: of four nut-producing species, the nuts of only Torreya nucifera fruited in 2004, whereas all four species, particularly Fagus crenata, produced nuts in abundance in 2005. The abundance and average crown size of trees of Torreya nucifera were smaller than those of Fagus crenata, and there was a higher frequency of agonistic interactions during 2004, when dominant, but not subordinate, individuals were able to satisfy daily energy requirements from nut feeding alone through longer nut feeding bouts. In contrast, all macaques, regardless of their dominance rank, were able to satisfy their energy requirements by feeding on nuts in 2005. Subordinate macaques appeared to counter their disadvantage in 2004 by moving and searching for food more and maintaining larger interindividual distances. Several lower-ranking females died during the food-scarce season of 2004, and only one dominant female gave birth the following birth season. In contrast, none of the adult females died during the food-scarce season of 2005, and 12 females gave birth the following birth season. These findings suggest that an interaction between dominance rank and interannual variation in food availability are related to macaque behavior, survival, and reproduction.

Communication during sex among female bonobos: effects of dominance, solicitation and audience

Bonobo females frequently form close bonds, which give them social power over other group members. One potential mechanism to facilitate female bonding is the performance of sexual interactions. Using naturalistic observations and experiments, we found various patterns that determined female-female sexual interactions. First, while low-ranked females interacted with all females, sexual interactions between high-ranked females were rare. Second, during genital contacts, females sometimes produced ‘copulation calls’, which were significantly affected by the rank of the caller and partner, as well as the solicitation direction. Third, there was a significant effect of the alpha female as a bystander, while variables relating to physical experience had no effects. Overall, results highlight the importance of sexual interactions for bonobo female social relations. Copulation calls are an important tool during this process, suggesting that they have become ritualised, beyond their reproductive function, to serve as broader social signals in flexible and potentially strategic ways.

Maternal investment in sons and daughters in provisioned, free-ranging Japanese macaques (<i>Macaca fuscata</i>)

It has been suggested that the physical condition of a mother may affect her pattern of investment in her sons or daughters. In addition, when competition over local resources becomes intense, severe aggression among the philopatric sex leads to a higher mortality of the sex and a biased birth sex ratio toward the opposite sex in the low rank. Parental sex-biased investment has been studied in many animal species to test these hypotheses, but the results have been highly inconsistent. We examined maternal sex-biased investment in relation to dominance rank using data on infant growth, infant mortality, birth sex ratio, and delay of subsequent reproduction by rearing current offspring from a provisioned, free-ranging Japanese macaque (Macaca fuscata) troop at Takasakiyama, Japan. The results showed that there was no sex difference in infant body mass among offspring of high- and low-ranking females. Use of the logistic regression model to analyze infant mortality with several independent variables failed to show a statistically significant sex bias. Birth sex ratio did not differ significantly between high- and low-ranking females. Among high-ranking females, there was no significant difference in delivery rate in the next year between those that reared a son and those that reared a daughter. For low-ranking females, however, the delivery rate after rearing daughters was markedly lower than that after rearing sons. Thus, there was no evidence of statistically significant maternal male-biased investment. For low-ranking females, we found a delay in subsequent reproduction for mothers after rearing daughters and no sex difference in offspring mortality. These results suggest that the females increased their offspring’s chances of survival, irrespective of sex, by postponing their subsequent delivery.

Chronic stress, allostatic load, and aging in nonhuman primates.

Allostatic load is the "wear and tear" of the body resulting from the repeated activation of compensatory physiological mechanisms in response to chronic stress. Allostatic load can significantly affect the aging process and result in reduced longevity, accelerated aging, and impaired health. Although low socioeconomic status is associated with high allostatic load during aging, the effects of status-related psychosocial stress on allostatic load are often confounded by lifestyle variables. Chronic psychosocial stress associated with low dominance rank in nonhuman primates represents an excellent animal model with which to investigate allostatic load and aging in humans. Research conducted with free-ranging rhesus monkeys suggests that female reproduction can also be a source of stress and allostatic load. Female reproduction is associated with increased risk of mortality and hyperactivation of the hypothalamic-pituitary-adrenal axis. Reproduction is especially stressful and costly for aging females of low rank. Although many indicators of body condition and neuroendocrine and immune function are influenced by aging, there are marked and stable individual differences among aging females in body condition, plasma cortisol responses to stress, and cytokine responses to stress. These differences are consistent with the hypothesis that there are strong differences in chronic stress among individuals, and that allostatic load resulting from chronic stress affects health during aging. Comparisons between captive and free-ranging rhesus monkey populations may allow us to understand how differences in environmental stress and allostatic load affect rates of aging, and how these in turn translate into differences in longevity and health.

Factors affecting aggression among females in captive groups of rhesus macaques (Macaca mulatta)

Captive groups of primates often exhibit higher rates of aggression than wild, free-ranging groups. It is important to determine which factors influence aggression in captivity because aggression, particularly intense aggression, can be harmful to animal health and well-being. In this study, we investigated the effect of ground substrate as well as season, rank, age, and group size on rates of agonistic interactions per female in seven captive groups of rhesus macaques (n = 70 females, 1,723 focal samples) at the California National Primate Research Center. Agonistic interactions were divided into three categories: displacements, mild aggression, and intense aggression. Females living in enclosures with gravel substrate were 1.7 times more likely to be involved in intense aggression (e.g. chases and physical contact) than females living in enclosures with grass (Poisson regression model: P < 0.001). High-ranking females were at least 1.3 times more likely to be involved in mild (e.g. threats and lunges) aggression than lower-ranking females (low rank: P = 0.03; mid rank: P = 0.001). Females of all ranks were 1.5-1.9 times more likely to be involved in both intense and mild aggression during the breeding season than other seasons. Age and group size did not affect rates of mild or intense aggression. These findings indicate that although some aggression appears to be natural and unavoidable, i.e. aggression during the breeding season, the well-being of captive macaques can be improved by developing grass substrate in outdoor enclosures.

Energetics during reproduction: A doubly labeled water study of lactating baboons

Understanding the costs and regulation of reproduction in primates requires understanding the separate but linked effects of energy availability and total energy expenditure (TEE). We compared variation in TEE and energy intake (EI) between two periods, early lactation and after the resumption of sexual cycling, for eight females from two groups of normally reproducing colony-living baboons (Papio h. anubis). Total energy expenditure was assessed using the doubly labeled water method. TEE was correlated with maternal mass both during early lactation and after the resumption of cycling. TEE after the resumption of cycling was positively related to infant growth rates; mothers with rapidly growing infants had higher energy expenditure. TEE was however unrelated to maternal rank and only weakly associated with reproductive parameters such as delay to conception. EI in early lactation was related to infant mass and interbirth intervals, but unrelated to infant growth or reproductive parameters once cycling had resumed. Energy availability (EA; the difference between intake and expenditure) differed significantly between subordinate and dominant females during early lactation, was highly variable among individuals as a function of body composition, and is suggested to follow a nonlinear relationship as a complex function of social status, lactation stage, infant growth, and female fertility. Thus, as a consequence of reduced energy availability, subordinate females in this captive context may experience reproductive delays even though the total energy expenditure after the return of cycling was similar between high and low ranking females.

The Effects of the Social Hierarchy Destabilization on the Foraging Activity of Eusocial WaspMischocyttarus cerberus styxRichards, 1940 (Hymenoptera: Vespidae: Polistinae)

The genusMischocyttaruscomprises 245 species of neotropical basal eusocial wasps. They form small colonies (rarely more than few tens of individuals); castes are morphologically undifferentiated and determined behaviorally by agonistic interactions. The aim of this study was to verify the effects of the experimental disruption of social hierarchy on foraging activity ofMischocyttarus cerberus styx. We observed six colonies in postemergence phase and recorded data on the foraging activity under two experimental conditions: (1) removal of lower-ranked females and (2) removal of higher ranked females, except the queen. Our results showed that the removal of higher-ranked females had higher effect on the number of foraging trips ofM. cerberus styxthan the removal of lower-ranked females (the number of foraging trips/hour decreased by 66.4% and 32.7%, resp.). Such results are likely due to the social organization of this species and the presence of a distinct class of females, which in this study were regarded as intermediates. Our data also showed that, irrespective of the hierarchical status of the females, the removal of two or three individuals affected significantly the number of foraging trips in this species.

Maternal Infant Monitoring in a Free-ranging Group of Japanese Macaques (Macaca fuscata)

In nonhuman primates, females with infants visually monitor their infants from a distance to detect and consequently avoid potential threats to their infants. We recorded maternal visual monitoring of infants (infant monitoring) ages 7–18 wk in a free-ranging, provisioned group of Japanese macaques (Macaca fuscata). The infant monitoring rate declined as a function of infants’ ages in weeks and increased when the infants were beyond their mother’s reach, indicating that infant monitoring reflects the vulnerability of infants. Females with infants increased infant monitoring when their infants were handled by other group members but not when their infants moved alone. This suggests that intragroup threats (harassment/mishandling or kidnapping) have a relatively stronger influence on infant monitoring than external threats (predation or infanticide) under the condition of this study. Infant monitoring of middle-/low-ranking females was more frequent than that of high-ranking females when their infants were handled by other individuals. This may reflect greater intragroup threats to infants of middle-/low-ranking females; however, further study is needed to confirm this. During important activities (feeding or grooming), the infant monitoring rate was lower than that during other activities (resting or self-directed behavior). However, even during important activities, females with infants increased infant monitoring when infants were handled. This indicates that females with infants face a trade-off between infant monitoring and other important activities, and even if females have to reduce the time spent on important activities, they increase infant monitoring when their infants face greater potential intragroup threats.

How feeding competition determines female chimpanzee gregariousness and ranging in the Taï National Park, Côte d'Ivoire

Socioecological theory suggests that feeding competition shapes female social relationships. Chimpanzees (Pan troglodytes) live in fission-fusion societies that allow them to react flexibly to increased feeding competition by forming smaller foraging parties when food is scarce. In chimpanzees at Gombe and Kibale, female dominance rank can crucially influence feeding competition and reproductive success as high-ranking females monopolize core areas of relatively high quality, are more gregarious, and have higher body mass and reproductive success than low-ranking females. Chimpanzee females in Taï National Park do not monopolize core areas; they use the entire territory as do the males of their community and are highly gregarious. Although female chimpanzees in Taï generally exhibit a linear dominance hierarchy benefits of high rank are currently not well understood. We used a multivariate analysis of long-term data from two Taï chimpanzee communities to test whether high-ranking females (1) increase gregariousness and (2) minimize their travel costs. We found that high-ranking females were more gregarious than low-rankers only when food was scarce. During periods of food scarcity, high rank allowed females to enjoy benefits of gregariousness, while low-ranking females strongly decreased their gregariousness. High-ranking females traveled more than low-ranking females, suggesting that low-rankers might follow a strategy to minimize energy expenditure. Our results suggest that, in contrast to other chimpanzee populations and depending on the prevailing ecological conditions, female chimpanzees at Taï respond differently to varying levels of feeding competition. Care needs to be taken before generalizing results found in any one chimpanzee population to the species level.

Strong and Consistent Social Bonds Enhance the Longevity of Female Baboons

Longevity is a major component of variation in fitness in long-lived iteroparous species [1-4]. Among female baboons, variation in breeding lifespan accounts for approximately 50% of the variation in lifetime fitness [5, 6]. However, we know little about the causes of variation in longevity in primates or other long-lived mammals. Savannah baboons form strong, equitable, and enduring relationships with specific female partners, particularly with close relatives and agemates [7-10]. The quality of females' social relationships influences their ability to cope with stressful events [11-13] and is associated with variation in female reproductive success [9, 14]. Here we show that dominance rank and the quality of close social bonds have independent effects on the longevity of female chacma baboons (Papio hamadryas ursinus). High-ranking females live longer than lower-ranking females. In addition, females who form stronger and more stable social bonds with other females live significantly longer than females who form weaker and less stable relationships. These data extend our understanding of the adaptive value of social bonds in baboons and complement a growing body of evidence that indicates that social bonds have adaptive value in a range of taxa, from mice to humans [9, 14-19].