Does female dominance facilitate feeding priority in black-and-white ruffed lemurs (Varecia variegata) in southeastern Madagascar?

Although many Malagasy lemurs are thought to be female dominant and to have female feeding priority, to date the relationship between these behaviors has been rigorously established only in Lemur catta, and other ways that females might achieve feeding priority have not been examined closely. Erhart and Overdorff [International Journal of Primatology 20:927-940, 1999] suggested that one way female primates achieve feeding priority is to initiate and lead groups to food, thereby gaining access to the food first and positively influencing their food intake compared to other group members. Here we describe female dominance patterns and potential measures of feeding priority in two groups of black-and-white ruffed lemurs (Varecia variegata) that were observed over a 15-month period in southeastern Madagascar. We predicted that the females would 1) be consistently dominant to males, 2) lead groups to food sources more often than males, and 3) have higher feeding rates compared to males when they arrived at food sources first. The results were dissimilar between the study groups. During the study, the oldest adult female in group 1 died. There was no evidence for female dominance in this group, and the remaining (likely natal) female did not lead the group more often, nor did she have a higher food intake than males. Group 1 dispersed shortly after the time frame reported here. In contrast, the resident female in group 2 was dominant to group males (based on agonistic interactions), led the group to food sources more often, and experienced a higher food intake when she arrived first at a food source. How these patterns vary over time and are influenced by the number of females in groups, group stability, food quality, and reproductive condition will be examined in future analyses.     

Male aggression during mating: evidence for sexual coercion in a female dominant primate?

In this article we document male sexual coercion of a Lemur catta female on St. Catherines Island (SCI), USA. Data presented in this paper were collected on one free-ranging L. catta group during October-November 2002 using all-occurrences sampling for agonism and reproductive behavior. We observed a male forcefully attempting to mate with a year-old estrous female. Despite the fact that we observed this female to present to the male during her estrus, throughout the episode the male employed the use of force, and achieved penile intromission on at least one occasion while the female struggled and resisted. We interpret his behavior as sexual coercion. As measured by sexual presents, the female appeared to more strongly prefer two other males as mates, yet each of these males gained fewer mounts and less cumulative time spent in mounts than the coercive male. The coercive male was one of two group males with the lowest observed mating success, suggesting that coercion might be a strategy used by males who are not highly sexually preferred. Females undergo early sexual maturation at this site owing to provisioning, and can therefore enter estrus before fully attaining dominance over males. As such, these data suggest that one consequence of provisioning a wild L. catta population (or of maintaining L. catta in captivity) may be that young females can be the targets of sexual coercion if they reach sexual maturity before fully achieving social dominance over males. In conclusion, male sexual coercion can occur in L. catta despite the female dominance characteristic of this species, and can constrain the mating behavior of females.     

Male Mate Choice in Lemur catta

Though females are generally more selective in mate choice, males may also derive reproductive benefits from exercising mate selectivity if one or more factors limit male reproductive success and females differ in reproductive potential. I used male mating effort as a proxy for male mate choice in ring-tailed lemurs (Lemur catta). I calculated mating effort as the rate of male-male agonism during each female's estrous period 30 min before and 30 min after the first and last mountings with intromission. I collected data on 1 free-ranging Lemur catta troop during 2 consecutive breeding seasons on St. Catherines Island, USA. In both yrs, male mating effort differed significantly among troop females once I adjusted male-male agonistic rates to reflect agonistic intensity, and I corrected for the number of observed mates per female (2000: χ² = 27.43, df = 3, p < 0.0001; 2001: χ² = 21.10, df = 3, p < 0.001). Results strongly suggest male mate choice. Contrary to expectation, males did not expend the greatest mating effort for females with the highest dominance status nor the highest reproductive success. Males preferred females that either: (1) belonged to the age class in which fecundity and infant survival is the highest at this site (4–9 yrs), or 2) were older females (≥10 yrs) with high reproductive success. Female reproductive potential appears to be an important variable determining male mating effort in Lemur catta.     

Social organization of the spotted hyaena Crocuta crocuta. II. Dominance and reproduction

A 4-year study of the social organization of spotted hyaenas in a clan of 60–80 individuals showed that there is a separate dominance hierarchy within each sex. One female and her descendants dominated all others; matrilineal rankings were stable over time because maternal rank is inherited. Cubs of higher ranking females were able to feed at kills in competition with adults more successfully than other cubs, and male offspring of the alpha female were the only males able to dominate adult females. The mating system is highly polygynous: only the behaviourally dominant male was seen to mate, though all other resident males regularly courted females. Among females, there was no correlation between reproductive success and age, size, or social rank. It is postulated that the unusually aggressive sons of the alpha female would probably be highly successful competitors in the context of a polygynous mating system. A primary consequence of female dominance over males is that females and their young have priority of access to food in a highly competitive feeding situation. This competition may have been the selective force that produced female dominance and the associated syndrome of female virilization that is characteristic of the species. Cooperation among related females may be the basis for the matrilineal system, as has been suggested for certain primate species.     

Correlates of Male Consortship Rate in Free-Ranging Rhesus Macaques (Macaca mulatta)

Male–male competition for access to receptive females can take the form of nonrecurring fights and/or a sustained contest over mating opportunities. Male physical condition has been linked to dominance rank and reproductive success in species characterized by intrasexual fights for dominance and access to females. In group-living species characterized by endurance rivalry, however, factors contributing to male reproductive success are less well understood. In such species, particularly seasonally breeding ones with low sexual dimorphism and seniority-based rank, age and social factors other than rank may prove important. In the absence of genetic data, male mate guarding or consortship can serve as an indicator of male reproductive success. To evaluate the contribution of age and intragroup sociality to male consortship rate, I collected behavioral data during one nonmating and one mating season in two social groups of free-ranging rhesus macaques that experience no predation or food scarcity. Higher-ranking males, younger males, or males that exhibited lower rate of intrasexual aggression had higher consortship rates. Male–female dyads that groomed outside consortship did not form consortships as often as dyads that did not engage in nonconsort grooming. This is the first study to identify the significance of male–male aggression and male–female affiliation to male consortship rate in a species characterized by endurance rivalry, high male rank stability, and strong female mate choice. Social behaviors and male age may be particularly important in determining male reproductive success in populations experiencing high food availability and a lack of predation, which are typical of an increasing number of vertebrates in areas densely populated by humans.     

Female feeding priority in bonobos, Pan paniscus, and the question of female dominance

The question of whether bonobos show feeding priority and female dominance has been proposed and examined, both in the wild and in captive studies, with differing results. The relationship between female dominance and female feeding priority has been best studied in prosimian primates. These studies use established criteria of females consistently evoking submissive behavior from males in dyadic encounters for determining female dominance. Although the relationship is complex, female dominance in prosimians is associated with preferential access to food. Data from studies of wild habituated bonobos in the Lomako Forest, Democratic Republic of the Congo, are examined for evidence of both female feeding priority and female social dominance using similar criteria as used for prosimians. Bonobos showed evidence of female feeding priority in small, but not in large, food patches. Male-male competition for mating opportunities at the start of the food bout was related to some, but not all, differences in time spent feeding between the sexes. Female dominance similar to that seen in prosimians was not observed in these bonobos. Males were consistently dominant in dyadic interactions. Female feeding priority with male dyadic social dominance implies that male deference during feeding cannot be excluded as one explanation of interpretations of female dominance in bonobos. Additionally, dominance of male bonobos by females appears to require the presence of female coalition partners. As in other primates with female feeding priority, bonobo females express this trait where food is economically defendable. Unlike prosimians, however, bonobo female feeding priority may result from male deference and the importance of female coalitions in nondyadic interactions.     

Dominance rank reversals and rank instability among male Lemur catta: the effects of female behavior and ejaculation

In this study, dominance rank instability among male Lemur catta during mating was investigated. Also, data on agonism and sexual behavior across five consecutive mating seasons in a population of L. catta on St. Catherines Island, USA, were collected. Instances of male rank instability were categorized into three types. Type 1 consisted of a temporary switch in the dominance ranks of two males, which lasted for a period of minutes or hours. Type 2 dyadic male agonistic interactions showed highly variable outcomes for a period of time during which wins and losses were neither predictable nor consistent. Type 3 interactions consisted of a single agonistic win by a lower-ranked male over a more dominant male. More Type 2 interactions (indicating greater dominance instability) occurred when males had not spent the previous mating season in the same group, but this trend was not statistically significant. The majority of periods of male rank instability were preceded by female proceptivity or receptivity directed to a lower-ranked male. As such, exhibition of female mate choice for a lower-ranking male appeared to incite male-male competition. Following receipt of female proceptivity or receptivity, males who were lower-ranking took significantly longer to achieve their first agonistic win over a more dominant male than did males who were higher-ranked. Ejaculation frequently preceded loss of dominance. In conclusion, temporary rank reversals and overall dominance rank instability commonly occur among male L. catta in mating contexts, and these temporary increases in dominance status appear to positively affect male mating success.     

Feeding behavior and nutrient intake in spiny forest-dwelling ring-tailed lemurs (Lemur catta) during early gestation and early to mid-lactation periods: compensating in a harsh environment

Strong resource seasonality in Madagascar has led to the evolution of female feeding priority and weaning synchrony in most lemur species. For these taxa, pregnancy/early lactation periods coincide with low food availability, and weaning of infants is timed with increased resources at the onset of the rainy season. Reproductive females experience high metabolic requirements, which they must accommodate, particularly when food resources are scarce. Female ring-tailed lemurs (Lemur catta) residing in spiny forest habitat must deal with resource scarcity, high temperatures (～36-40°C) and little shade in early to mid-lactation periods. Considered "income breeders," these females must use resources obtained from the environment instead of relying on fat stores; thus, we expected they would differ from same-sized males in time spent on feeding and in the intake of food and nutrients. We investigated these variables in two groups (N = 11 and 12) of Lemur catta residing in spiny forest habitat during early gestation and early to mid-lactation periods. Focal animal data and food plant samples were collected, and plants were analyzed for protein, kcal, and fiber. We found no sex differences for any feeding or nutrient intake variable for the top five food species consumed. Females in early gestation spent more time feeding compared with early/mid-lactation. Physiological compensation for spiny forest-dwelling females may be tied to greater time spent resting compared with gallery forest conspecifics, consuming foods high in protein, calories, and water, reduced home range defense in a sparsely populated habitat, and for Lemur catta females in general, production of relatively dilute milk compared with many strepsirrhines.     

Dominance and feeding competition in captive rhesus monkeys

The feeding behavior of 16 adult female rhesus monkeys living in three captive social groups was observed. Estimates of relative food intake, feeding rate, and location of feeding in relation to food sources were compared between females of different dominance ranks. Higher-ranking females had greater access to feeding sites and were supplanted or threatened less frequently while feeding than subordinates. However, no consistent differences in estimates of total intake were found between females of high and females of low rank. The effects of dominance on feeding behavior were most pronounced in the group receiving the least food relative to estimates of overall group nutritional requirements. Higher-ranking females, both over the long term and during the study period, tended to produce more surviving offspring. The effects of dominance on reproductive performance appeared to be less related to food intake than to competitive and aggressive interactions, potentially resulting in higher levels of stress for subordinates.     

MALE DOMINANCE, FEMALE MATE CHOICE, AND INTERSEXUAL CONFLICT IN THE ROSE BITTERLING (RHODEUS OCELLATUS)

An intersexual conflict arises when males and females differ in their reproductive interests. Although experimental studies have shown that females often mate with dominant males, it may not always be in the interest of a female to do so. Here we investigated the impact of male dominance on female mate choice and offspring growth and survival in the rose bitterling ( Rhodeus ocellatus ), a freshwater fish with a resource-based mating system. Three experimental mating trials were conducted using males of known dominance rank, but with different levels of constraint on male behavior. Thus, females were able to choose among; (1) males that were isolated from each other; (2) males that could see and smell each other, but could not directly interact; (3) males that could interact fully. Using a combination of behavioral observation and parentage analyses it was shown that female preferences did not correspond with male dominance and that male aggression and dominance constrained female mate choice, resulting in a potential intersexual conflict. The survival of offspring to independence was significantly correlated with female mate preferences, but not with male dominance. A lack of strong congruence in female preference for males suggested a role for parental haplotype compatibility in mate choice.     

Why dominants do not consistently attain high mating and reproductive success: A review of longitudinal Japanese macaque studies

There is wide interest in the effects of reproductive biology, mating partner preference, and rank on mating success (MS) and reproductive success (RS) in primates. In particular, theory stresses importance on the mechanisms for attaining RS. Most theory hedges on competitive ability and priority of access to resources, whether they be food or estrous females. However, the majority of data used in favor of such hypotheses come from relatively short-term studies. We review these hypotheses based on long-term data from provisioned and unprovisioned populations of Japanese macaques. Neither MS nor RS were consistently attained by high-ranking males and females. For males, female choice and mating partner preference is seen to over-ride most male-male competitive behaviors likely to affect MS and RS through priority of access to estrous females. Long-term mating patterns driven largely by female partner preferences, results in decreasing MS and RS for older higher-ranking males. The long-term trend for females to prefer less familiar or novel partners results in higher MS and RS for younger, middle-ranking males. The effects of this vary according to troop size and the duration of male tenure. For females, no consistent trend was recognized for rank related RS in either provisioned or unprovisioned troops. Non-reproductive mating may provide differential benefit to high-ranking females for access to limited food resources in some habitats but overall the relationship was inconclusive. Distribution and defendability of food resource, rather than provisioning per se may be more important.     

Sex and seasonal differences in aggression and steroid secretion in Lemur catta: are socially dominant females hormonally 'masculinized'?

Female social dominance characterizes many strepsirrhine primates endemic to Madagascar, but currently there is no comprehensive explanation for how or why female lemurs routinely dominate males. Reconstructing the evolutionary pressures that may have shaped female dominance depends on better understanding the mechanism of inheritance, variation in trait expression, and correlating variables. Indeed, relative to males, many female lemurs also display delayed puberty, size monomorphism, and 'masculinized' external genitalia. As in the spotted hyena (Crocuta crocuta), a species characterized by extreme masculinization of the female, this array of traits focuses attention on the role of androgens in female development. Consequently, I examined endocrine profiles and social interaction in the ringtailed lemur (Lemur catta) to search for a potential source of circulating androgen in adult females and an endocrine correlate of female dominance or its proxy, aggression. I measured serum androstenedione (A(4)), testosterone (T), and estradiol (E(2)) in reproductively intact, adult lemurs (10 females; 12 males) over four annual cycles. Whereas T concentrations in males far exceeded those in females, A(4) concentrations were only slightly greater in males than in females. In both sexes, A(4) and T were positively correlated, implicating the Delta(4)-biosynthetic pathway. Moreover, seasonal changes in reproductive function in both sexes coincided with seasonal changes in behavior, with A(4) and T in males versus A(4) and E(2) in females increasing during periods marked by heightened aggression. Therefore, A(4) and/or E(2) may be potentially important steroidal sources in female lemurs that could modulate aggression and underlie a suite of masculinized features.     

Balancing contest competition,scramble competition,and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus)

Models of primate sociality focus on the costs and benefits of group living and how factors such as rank, feeding competition, alliance formation, and cooperative behavior shape within‐group social relationships. We conducted a series of controlled field experiments designed to investigate how resource distribution (one or three of four reward platforms) and amount of food on a reward platform affected foraging strategies and individual feeding success in four groups of wild common marmosets (Callithrix jacchus) living in the Caatinga of northeastern Brazil. At our field site, common marmoset groups are characterized by a single breeding female who can produce twin litters twice per year, strong social cohesion, and cooperative infant care provided principally by several adult male helpers. We found that except for the dominant breeding female, rank (based on aggression) was not a strong predictor of feeding success. Although the breeding female in each group occupied the highest rank position and obtained the greatest daily feeding success, all other group members, including adults and juveniles experienced relatively equal feeding success across most experimental conditions. This was accomplished using a balance of behavioral strategies related to contest competition, scramble competition (associated with a finder's advantage), and social tolerance (sharing the same feeding platform). Based on these results, the social structure of common marmosets is best described as “single female dominance,” with the breeding female maximizing food intake needed to offset the energetic costs associated with reproductive twinning and the ability to produce two litters per year. Cooperative infant caregiving, in which the number of helpers is positively correlated with offspring survivorship, requires a set of behavioral strategies that serve to reduce contest competition and promote prosocial behaviors at feeding sites.     

Correlates and Consequences of Dominance in a Social Rodent

In harem‐polygynous societies, body condition is often correlated with dominance rank. However, the consequences of dominance are less clear. High‐ranking males do not inevitably have the highest reproductive success, especially in systems where females mate with multiple males. In such societies, we expect male reproductive success to be more highly skewed than female reproductive success, but reproductive skew in females can still arise from rankings established within matrilineal societies. Dominance can also impact life‐history decisions by influencing dispersal patterns in yearlings. To better understand the function of dominance in harem‐polygynous societies, we studied the causes and consequences of dominance in yellow‐bellied marmots (Marmota flaviventris), a social rodent with skewed male reproductive success and female reproductive suppression. Specifically, we examined body condition as a predictor and the probability of breeding, number of offspring, and dispersal as outcomes of dominance. Additionally, we looked at variation in dominance between males and females and adults and yearlings, because marmots can engage in distinct interactions depending on the type of individuals involved. We found that marmots in better body condition have higher dominance rank than those in poorer condition. In addition, adults are dominant over yearlings. Within yearlings, dominance does not influence dispersal, but those in better body condition are less likely to disperse. Within all adults, individuals in better condition produce more offspring per year. Within adult males, more dominant males have greater reproductive success. Despite previous evidence of reproductive suppression in females, we found no effects of dominance rank on female reproductive success in the current study. The function of dominance in female marmots remains enigmatic.     

Dominance and aggression in social groups of male and female rats

Two experiments were performed to examine aggression and dominance in domestic male and female $\text{Rattus norvegicus}$ living in small mixed-sex (3 males and 3 females) groups. Experiment 1 examined the development of aggression in females. A single female (alpha) within each of the six colonies tested showed the preponderance of attacks on male intruders placed into the home-cage when male colony residents were absent. Over 12 weeks of intruder-aggression training female alphas showed only a mild nonsignificant elevation of aggressive behavior. A comparison of aggression of male and female colony alphas tested with opponents of each sex revealed that aggression was mainly directed at like-sex opponents, and that female attack was more defensive in character than male attack regardless of opponent sex. The highest intensity of aggression occurred when male alphas confronted male intruders. Although intruders never showed offense toward male residents, 61% of intruding males showed offense in response to attack by females.Experiment 2 investigated the relationship between aggressive dominance and competitive measures of dominance within each of 10 mixed-sex colonies. Alpha stat s of male and female colony residents did not reliably predict priority of access to food or water in tests of direct resource competition with like-sex colony members. When colony males were simultaneously tested for copulation, the copulatory behavior of alpha males was significantly greater than that of other colony males. Results are discussed in relation to the role of aggression in the reproductive strategy of male and female $\text{Rattus norvegicus}$.     

Dominance and reproductive success in primates

Theoretical models of the relationship between competition and differential reproduction in primates share the premise that agonistic dominance hierarchies determine differential access to those limited resources which are essential to reproduction. In particular, the priority-of-access-to-estrous-female model is based on the postulate that high rank in males enhances reproductive success. Tests for a correlation between rank and reproductive success in males have produced mixed results. Problems in measuring male reproductive success and in conceptualizing dominance systems are implicated in the diversity of conclusions reached. Other attributes which affect reproductive success have been proposed, and alternative models of mating systems, based on the concepts of reproductive strategies, social skills, and life histories have also been developed. Studies of differential reproduction in female primates are fewer, but have the advantage over male studies of directly measuring infant production and offspring survival. Research on the relationship between rank and reproductive success in females has shown that under conditions of low resource availability, subordinate females sometimes suffer reduced fecundity and infant survival as a result of restricted access to food and water. Under conditions of social stress, low-ranking females may suffer from disruption of their reproductive cycles, resulting in lowered fecundity. Dominant females may also incur reproductive costs as well as benefits for their social position. Better insights into the relationship between dominance and reproduction are potentially offered by improved genetic paternity measures, new models of social and demographic processes, and the recent availability of life history data from field studies.     

Food competition in captive female sooty mangabeys (Cercocebus torquatus atys)

We studied the social and foraging behavior of two captive groups of sooty mangabeys under two different spatial food situations. These food conditions were clumped (food was placed in a box) and dispersed (food was dispersed over the entire enclosure). In each group five adult females and two adult males were observed. As a criterion for food competition, individual differences in the relative food intake were used. Adult female mangabeys had a linear, stable, and unidirectional dominance hierarchy. Access to food was rank dependent among females only under clumped food distribution, as current models of the evolution of primate social systems predict. However, feeding success appeared to be mediated not by female but by male agonistic behavior toward females. High-ranking females received relatively less aggression from males and could, therefore, stay and feed longer in the feeding area. Male tolerance of higher-ranking females seems to mediate female feeding success under restricted food resources. The establishment of a special relationship with a high-ranking male might, therefore, be a strategy to get better access to food. This study demonstrates that female competition for access to food should not be analyzed separately from male influences on females and suggests that a more integral role of males in socioecological models of the evolution of primate social systems should be considered.     

Female rank and reproductive success among arashiyama B Japanese macaques (Macaca fuscata)

Five hypotheses that related female rank and reproductive success were tested in an intact troop of free-ranging, provisioned, Japanese macaques. The hypotheses stated that high-ranking females (1) begin parturition earlier in life than low-ranking females; (2) produce more offspring than low-ranking females; (3) give birth during some optimal time during the birth season to a greater extent than low-ranking females; (4) experience less infant mortality than low-ranking females;and (5) more frequently produce male offspring, while low-ranking females more frequently produce female offspring. A statistical analysis of the data which included three birth seasons and 55 adult females and 34 pubescent females, all of known age, rank, and matrifocal membership in the Arashiyama B troop, revealed few significant results. An association was found between the rank of the matrifocal unit and the age of first birth. However, the relationship was the reverse of hypothesis 1, i.e., females of the lower-ranking matrifocal units began parturition earlier than females of higher-ranking matrifocal units. Therefore, in this troop of Japanese monkeys— where alternative feeding strategies existed— there was little association between female rank and reproductive success.     

Paternity in wild ring‐tailed lemurs (Lemur catta): Implications for male mating strategies

In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males.     

Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus)

Cortisol excretion in males of group living species is often associated with social rank and competition for oestrous females. Rank-related patterns of cortisol levels can be used to study mechanisms of rank maintenance and costs associated with mate competition. Bonobos (Pan paniscus) are interesting because males form a linear dominance hierarchy but are not dominant over females and therefore aggressive male-male competition over access to females alone is not considered to be a successful reproductive strategy. In this study on social correlates of urinary cortisol in wild male bonobos, we investigated the relationship between cortisol levels and several aspects of mate competition, including male rank, aggression rates, and association time with oestrous females. We found that cortisol levels correlated positively with dominance rank when oestrous females were present, but not when they were absent. This result is consistent with the idea that aggressive behaviour plays a minor role in maintenance of high rank. While aggression received from males and females explained within-individual variation in cortisol levels, it was the time spent in association with oestrous females that best explained between-individual variation in male cortisol levels. The observed increase in male cortisol may be associated with spatial proximity to oestrous females and could result from anticipated aggression from other group members, reduced feeding time in the males, or a combination of both.