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.     

Matrilineal rank Inheritance varies with absolute rank in Japanese macaques

In many cercopithecine primates, females form linear dominance hierarchies based on kinship. It is known that female rank follows the rules of matrilineal rank inheritance (MIR): (1) maternal rank inheritance, (2) maternal dominance, and (3) youngest ascendancy among sisters. Although, several determining such variation remain largely unknown. In this paper, I investigate the dominance relation-ships of 69 adult (>6 yr old) female Japanese macaques (Macaca fuscata fuscata) in a free-ranging provisioned troop living in Shiga-Heights (Nagano Prefecture, Japan) and report new evidence of intra-group variation. Dominance relationships among high-ranking females followed MRI within kin units, those among low-ranking females did not. Maternal rank inheritance and youngest ascendancy operated between mother/daughter dyads and sister dyads of high-rank, but not in the dyads of low-rank. The dominance ranks of females from low-ranking kin units were dispersed and less predictable. These findings suggest that MRI varies with absolute dominance rank, and are discussed in relation to other asymmetries between high-and low-rank     

Maternal rank is not correlated with cub survival in the spotted hyena, Crocuta crocuta

Reproductive success in female spotted hyenas, Crocuta crocuta,is positively correlated with social rank. High-ranking femalesare known to produce more offspring, but the effects of maternalrank on early cub survivorship have not been investigated. Cubmortality was examined over a 4-year period in one clan of wild-livingspotted hyenas in Kenya. Data were obtained for 100 cubs in63 litters produced by 27 adult females. Survivorship of cubsfrom birth through their first year was examined as a functionof litter size, sex of cubs, and maternal rank. Overall, cubmortality was high (61%). Contrary to expectation, singletoncubs did not survive better than twins, and there was no differencein survivorship between female and male cubs. High-ranking motherswere not more successful at raising twins or daughters thanwere low-ranking mothers. There was no correlation between cubmortality and maternal rank. Peaks in cub mortality coincidedwith life stage events, including mean age of arrival at a communalden, and age at which cubs began visiting kills. Documentedcauses of mortality included intraclan infanticide, disease,orphaning, predation by lions, and a mechanism of filial infanticidethat has not been previously described in this species: selectivelitter reduction by mothers via partial litter abandonment.No instances of facultative or obligate siblicide were detected.During this study, association between rank and number of cubssurviving to 1 year of age appeared to be due to differencesin reproductive output and not differential survival of cubswithin their first year.     

Role-Reversed Nepotism Among Cubs and Sires in the Spotted Hyena (Crocuta crocuta)

Nepotism is widespread among parents and offspring, and is typically associated with fundamental asymmetries; parents can usually do more to help their offspring than vice versa, and the cost of a given nepotistic behavior is usually less for parents than for offspring. This may not be so among spotted hyenas (Crocuta crocuta); sires never achieve social rank equal to that of their cubs, to whom they provide no obvious paternal care. Nepotism by sires towards their cubs is thus socially constrained. However, the higher social status of cubs might offset cubs’ developmental disadvantages and permit nepotistic treatment of sires by offspring. We therefore sought to determine whether the interactions among spotted hyena cubs and adult males were influenced by kinship, using long‐term observations from one clan of spotted hyenas. Sires exhibited no overt nepotism towards their cubs in most behaviors, but they did associate more closely with their daughters than with unrelated control females. Sires also associated more closely with their daughters than with their sons, with whom they associated no more closely than they did with unrelated control males. Cubs favored their sires by directing less intense aggression towards them than towards unrelated control males. Cubs of both sexes also associated more closely with their sires than with control males after the cubs were independent of the clan's communal den. Although sires evidently recognize their offspring, paternal nepotism by sires towards their cubs is weaker than filial nepotism by cubs towards their sires. The small size and immaturity of cubs thus appear to be weaker constraints on nepotism than is the low social status of their sires.     

Dominance Acquisition During Mammalian Social Development: The "Inheritance" of Maternal Rank

We first review the suite of general problems mammals confrontduring their social development, and then focus on the specificproblem of how group-living mammals acquire their social rank.In particular, we examine maternal rank "inheritance" (MRI)in those mammals for which maternal rank is the primary determinantof female rank. This occurs in many primates and in spottedhyenas. Young primates and spotted hyenas usually attain theiradult status in two stages: they first attain ranks correlatedwith those of their mothers in peer interactions, and subsequentlychallenge and outrank older conspecifics subordinate to theirmothers. Observational learning may be necessary, but is notsufficient, for MRI. In some primates, but not hyenas, youngstersappear to learn their ranks from direct aggression against themby higher-ranking adults. Third-party support appears to promoteMRI in all species examined: the probability and style of maternalinterventions on behalf of infants often vary with rank, andboth kin and nonkin frequently form coalitions that may assistjuveniles during rank reversals.     

Social intelligence in the spotted hyena (Crocuta crocuta)

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like those of cercopithecine primates with respect to size, structure and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.     

Persistence of maternal effects in baboons: Mother's dominance rank at son's conception predicts stress hormone levels in subadult males

Dominance status and reproductive experience are maternal characteristics that affect offspring traits in diverse taxa, including some cercopithecine primates. Maternal effects of this sort are widespread and are sources of variability in offspring fitness. We tested the hypothesis that maternal dominance rank and reproductive experience as well as a male's own age and dominance rank predicted chronic fecal glucocorticoid (fGC) concentrations in 17 subadult wild male baboons, Papio cynocephalus (median age 6.5 years), in the Amboseli basin, Kenya. Among these variables, maternal dominance rank at a subadult male's conception was the sole significant predictor of the male's fGC and accounted for 42% of fGC variance; sons of lower ranking mothers had higher fGC than did those of high-ranking mothers. This result is striking because subadult male baboons are approximately 4-6 years past the period of infant dependence on their mothers, and are larger than and dominant to all adult females. In addition, many males of this age have survived their mothers' death. Consequently, the influence of maternal dominance rank persisted well beyond the stage at which direct maternal influence on sons is likely. Persistence of these major maternal influences from the perinatal period may signal organizational effects of mothers on sons' HPA axis. Although short-term, acute, elevations in GC are part of adaptive responses to challenges such as predators and other emergencies, chronically elevated GC are often associated with stress-related pathologies and, thereby, adverse effects on fitness components.     

Spoiled Brats: Is Extreme Juvenile Agonism in Ring‐Tailed Coatis (Nasua nasua) Dominance or Tolerated Aggression?

Ring‐tailed coatis exhibit an extreme form of juvenile agonism not found in other social mammals. Two groups of habituated, individually recognized, coatis were studied over a 2.5‐yr period in Iguazu National Park, Argentina. Dominance matrices were divided by year and group, resulting in four dominance hierarchies which were analyzed using the Matman computer program. Strong general patterns were seen in both groups during both years. Adult males (one per group) were the highest ranking individuals, followed by male juveniles, female juveniles, adult females, and male and female subadults. The pattern in which young, physically inferior individuals were able to outrank larger adults is different from other social mammal species in that the juvenile coatis aggressively defended food resources and directed aggression towards older individuals. These agonistic interactions may not reflect ‘dominance’ in the traditional sense, and appear to be a form of ‘tolerated aggression.’ This tolerated aggression leads to increased access to food, and should help juveniles during a period in which they need to rapidly gain weight and grow. Because this tolerance of juvenile aggression is reinforced through coalitionary support of juveniles by adult females, agonistic patterns are also consistent with the hypothesis that juvenile rank is being influenced by high degrees of relatedness within coati groups. Although some interesting parallels exist, there is little evidence indicating that these dominance patterns are the same as those found in other social mammals such as hyenas, lions, meerkats, or Cercopithicine primates.     

Patterns of coalition formation by adult female baboons in Amboseli, Kenya

Coalitionary support in agonistic interactions is generally thought to be costly to the actor and beneficial to the recipient. Explanations for such cooperative interactions usually invoke kin selection, reciprocal altruism or mutualism. We evaluated the role of these factors and individual benefits in shaping the pattern of coalitionary activity among adult female savannah baboons, Papio cynocephalus, in Amboseli, Kenya. There is a broad consensus that, when ecological conditions favour collective defence of resources, selection favours investment in social relationships with those likely to provide coalitionary support. The primary features of social organization in female-bonded groups, including female philopatry, linear dominance hierarchies, acquisition of maternal rank and well-differentiated female relationships, are thought to be functionally linked to the existence of alliances between females. Female savannah baboons display these characteristics, but the frequency and function of their coalitionary aggression is disputed. In our five study groups, 4-6% of all disputes between females led to intervention by third parties. Adult females selectively supported close maternal kin. There was no evidence that females traded grooming for support or reciprocated support with nonkin. High-ranking females participated in coalitionary aggression most frequently, perhaps because they derived more benefits from group membership than other females did or could provide support at lower cost. Females typically supported the higher ranking of two contestants when they intervened in disputes between subordinates, so most coalitions reinforced the existing dominance hierarchy. Results indicate that female baboons participate in coalitionary aggression in a manner strongly influenced by nepotism and individual benefits.     

High juvenile mortality in cheetahs (Acinonyx jubatus) and its consequences for maternal care

Juvenile mortality in cheetahs was found to be extremely high compared to other large mammals, with approximately 72.2% of litters dying before they emerged from the lair at eight weeks of age. An average of 83.3% of cubs alive at emergence died by adolescence at 14 months of age, thus cheetah cubs were estimated to have only a 4.8% chance of reaching independence at birth. The instantaneous rate of mortality was highest immediately after cubs emerged from the lair. Before emergence, lion predation was the major source of this mortality, although some cubs died from starvation after they were abandoned by their mothers, or as a result of grass fires and inclement weather. After emergence, predation again accounted for virtually all cub mortality, with lions and spotted hyaenas taking approximately the same proportion of cubs. Overall predation accounted for 73.2% of cheetah cub deaths in this study, with 78.2% of these being killed by lions. The extent of maternal care, in the form of vigilance and antipredator behaviour, mirrored cub susceptibility to mortality and, in the case of vigilance, possibly also starvation. The probability of a cheetah mother responding aggressively to a predator was found also to depend on the species of predator. This study highlights the importance of the influence of juvenile mortality on patterns of parental care.     

Foraging Behaviour of the Brown Hyaena (Hyaena brunnea Thunberg, 1820) in the Southern Kalahari

Observations on six free ranging adult brown hyaenas (Hyaena brunnea) fitted with radio collars and beta lights were supplemented by observations on three untagged large cubs and by tracking spoor. Brown hyaenas are predominantly nocturnal and cover large distances alone each night searching for vertebrate remains and other food. Carrion is mainly located by olfactory sense, although auditory cues are also used. Excess food is often stored for short periods. Wild fruits and birds' eggs are eaten and hunting behaviour is directed towards small vertebrates and insects. Some adaptations of the brown hyaena to its environment are discussed.     

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.     

Early life social and ecological determinants of global DNA methylation in wild spotted hyenas

Environmental factors early in life can have lasting influence on the development and phenotypes of animals, but the underlying molecular modifications remain poorly understood. We examined cross‐sectional associations among early life socioecological factors and global DNA methylation in 293 wild spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya, grouped according to three age classes (cub, subadult and adult). Explanatory variables of interest included annual maternal rank based on outcomes of dyadic agonistic interactions, litter size, wild ungulate prey density and anthropogenic disturbance in the year each hyena was born based on counts of illegal livestock in the Reserve. The dependent variable of interest was global DNA methylation, assessed via the LUminometric Methylation Assay, which provides a percentage methylation value calculated at CCGG sites across the genome. Among cubs, we observed approximately 2.75% higher CCGG methylation in offspring born to high‐ than low‐ranking mothers. Among cubs and subadults, higher anthropogenic disturbance corresponded with greater %CCGG methylation. In both cubs and adults, we found an inverse association between prey density measured before a hyena was 3 months old and %CCGG methylation. Our results suggest that maternal rank, anthropogenic disturbance and prey availability early in life are associated with later life global DNA methylation. Future studies are required to understand the extent to which these DNA methylation patterns relate to adult phenotypes and fitness outcomes.     

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.     

Variability in the development of mother-infant relationships among free-ranging Japanese macaques

Mother-infant relationships were studied during the infant's first year in free-ranging Japanese macaques (Macaca fuscata). Three possible factors controlling the mother-infant relationships were examined using multivariate analysis. Parity was determined to exert the strongest influence on mother-infant relationships. Specifically, during month 1, multiparous mothers showed greater maternal suckling rejection than primiparous mothers, and primparae and multiparae differed in their responses to suckling behavior. During month 6, multiparous mothers prompted independence of their offspring more than primiparous mothers. By month 8, however, parity differences in maternal behavior were substantially reduced. Maternal rank was a less important factor, although during month 1, high-ranking mothers showed greater maternal restriction than low-ranking ones. In the present study, infant gender appeared to have no effect on mother-infant relationships. That most differences were due to parity indicates that mother-infant relations were largely determined by the mothers. This observation conflicts with the “learning-to-mother” hypothesis. Allo-mothering of neonates by nulliparae is rare among Japanese macaques. Primiparous mothers learned appropriate suckling care from handling their own infants.     

Social dominance and feeding patterns of spotted hyaenas

In some parts of East Africa, spotted hyaenas (Crocuta crocuta) live in large groups and at high population densities, and scramble competition among clan members during feeding at large carcasses is reported. By contrast, spotted hyaenas in the Namib Desert of southwestern Africa live in small groups and at low densities. When assembled at carcasses, Namib Desert spotted hyaenas show linear dominance hierarchies. Adult females outrank adult males and usually feed one at a time or with their dependent offspring. Feeding rates at small carcasses in the Namib Desert are approximately equal to those reported in East Africa, but at large carcasses Namib Desert spotted hyaenas show linear dominance hierarchies. Adult females outrank adult males and usually feed one at a time or with their dependent offspring. Feeding rates at small carcasses in the Namib Desert are approximately equal to those reported in East Africa, but at large carcasses Namib Desert spotted hyaenas feed significantly more slowly. Thus lower-ranking individuals eventually gain access to large carcasses but are excluded from smaller ones. We relate these patterns of food consumption to possible evolutionary pathways to social hunting by spotted hyaenas.     

Reconciliation in the Spotted Hyena (Crocuta crocuta)

Theory predicts that it should often be in the best interests of gregarious animals to repair social bonds damaged by within-group conflict. Indeed, reconciliation in many primates takes the form of affiliative behavior occurring shortly after a conflict. Here we inquired whether reconciliation also occurs among spotted hyenas ( Crocuta crocuta ), gregarious carnivores whose social lives share much in common with those of cercopithecine primates. In a large group of free-living hyenas in Kenya, we used focal animal observations to monitor rates at which various affiliative behaviors occurred before and after dyadic aggressive interactions. An affiliative behavior was identified as having a conciliatory function only if it occurred more frequently after than before fights, and if it was also associated with reduced rates of aggression between former opponents during the post-conflict interval. Of all affiliative behaviors monitored, only two types satisfied both these criteria: greeting behavior and non-aggressive approach. Over 72% of conciliatory behaviors occurred within the first five minutes after a fight, and hyenas reconciled after 14.6% of 698 fights. Mean conciliatory tendency (CT) for individual hyenas was 11.3%. Hyenas exhibited higher CTs when they were recipients (victims) of aggression than when they were aggressors, and they showed higher CTs in interactions with non-kin than with kin. Conciliatory tendencies did not vary with age–sex classes of opponents or with rank distance between opponents . Conciliatory tendency in spotted hyenas fell at the low end of the CT range observed among primates.     

Social rank and sex-biased maternal investment in captive japanese macaques: behavioural and reproductive data

This study investigated the relationship between social rank and sex-biased maternal investment in captive Japanese macaques (Macaca fuscata) using reproductive and behavioural data. High-ranking mothers showed a significantly male-biased secondary sex ratio, spent more time in contact with and carried male infants for longer than female infants. Low-ranking mothers showed no bias in secondary sex ratio nor in the time spent in contact with male and female infants, but carried female infants for longer. No differences were observed in the interbirth intervals following male and female infants nor in the frequency and intensity of aggression received by mothers with male and female infants, either in high-ranking or in low-ranking mothers. These results show that Japanese macaque mothers can adopt flexible and rank-dependent rearing strategies.     

Correlates of agonistic and competitive interactions in pregnant baboons

Maternal condition during pregnancy is known to influence fetal viability. Recently, primatologists have suggested that certain characteristics of the fetus may influence maternal condition as well. For example, among captive pigtailed macaques (Macaca nemestrina) mothers of female infants may be at greater risk of injury during their pregnancies than mothers of male infants. Analysis of the rates of aggression, submission, competition, and wounding among free-ranging pregnant baboons (Papio cynocephalus) in Amboseli National Park generally fail to support these findings, but several other factors such as maternal dominance rank, environmental conditions during pregnancy, maternal parity, and fetal age correlate with aggression, submission, competition, and injuries sustained by pregnant female baboons.     

Dominance hierarchy and social relationships in a group of Captive black-and-white snub-nosed monkeys (Rhinopithecus bieti)

Different types of dominance hierarchies reflect different social relationships in primates. In this study, we clarified the hierarchy and social relationships in a one-male unit of captive Rhinopithecus bieti observed between August 1998 and March 1999. Mean frequency of agonistic behaviour among adult females was 0.13 interactions per hour. Adult females exhibited a linear hierarchy with a reversal of 10.9%, indicating an unstable relationship; therefore, R. bieti appears to be a relaxed/tolerant species. The lack of a relationship between the agonistic ratio of the adult male towards adult females and their ranks indicated that males did not show increased aggression towards low-ranking females. Differentiated female affiliative relationships were loosely formed in terms of the male, and to some extent influenced by female estrus, implying that relationships between the male and females is influenced by estrus and not rank alone. A positive correlation between the agonistic ratio of adult females and their ranks showed that the degree to which one female negatively impacted others decreased with reduction in rank. Similarly, a positive correlation between the agonistic ratio of females and differences in rank suggests that a female had fewer negative effects on closely ranked individuals than distantly ranked ones. These data indicate that rank may influence relationships between females. A steeper slope of regression between the agonistic ratio and inter-female rank differences indicated that the extent of the power difference in high-ranking females exerting negative effects on low-ranking ones was larger during the mating season than the birth season, suggesting that rank may influence the mating success of females.