High-ranking Mothers Research Articles

Maternal response to neonatal sibling conflict in the spotted hyena, Crocuta crocuta

Among spotted hyenas, Crocuta crocuta, neonatal aggression in twins is a well-known phenomenon and serves to establish intra-litter dominance soon after birth. As the stronger more aggressive cub presumably attains dominance over its twin, intra-litter dominance presents mothers with an ideal opportunity to assess individual cub fitness and, thereafter, to selectively favor one cub over the other. This study quantified maternal response to sibling conflict in 26 sets of twins born to 16 wild-living females to determine whether mothers of different social ranks exhibited favoritism towards sons or daughters, or in the case of same-sex twins, the dominant or subordinate cub. Maternal response to sibling conflict did not vary with litter sex composition, suggesting that mothers do not favor offspring of one sex over the other. All mothers intervened when their cubs fought and sometimes punished their cubs. Higher-ranking mothers more often punished both cubs, while lower-ranking mothers were more selective and punished the dominant cub. Where sibling aggression was most extreme, rather than favor the dominant sibling, mothers of all ranks made concessions to the subordinate cub that included procuring private nursing bouts for the subordinate and temporarily housing twins in separate dens, presumably to decrease sibling conflict. These findings represent a complex example of parent–offspring conflict and support both the insurance cub hypothesis and resource tracking hypothesis that mothers endeavor to keep all offspring alive for as long as possible in the event that the dominant sibling dies or that resources provide for the rearing of twins.

Bonobos

Bonobos

Costs and strategies of communal den use vary by rank for spotted hyaenas, Crocuta crocuta

Spotted hyaenas house cubs in communal dens during much of the early development period. This practice facilitates social integration of young into the clan's dominance hierarchy. For Crocuta, however, use of communal dens entails costs. Within a clan, social rank is correlated with individual privilege. If costs of denning communally likewise vary with rank, then breeding females may be forced to adopt different denning strategies accordingly. I quantified three costs (den access, visitor aggression, disruption to nursing bouts) in relation to maternal rank for 27 females within one clan. I examined denning strategies that may reduce costs (cub age when transferred to a communal den, social correlates of den selection, daily attendance pattern) to determine whether they varied predictably in relation to mother's rank. Although conflicts among mothers were infrequent, low-ranking females were more likely to be denied access to the communal den entrance and, possibly in response, more often attended their cubs when other mothers were absent. High-ranking mothers were visited more often, but treated less aggressively than were mid- or low-ranking mothers. In efforts to socialize with mothers and cubs, visitors often disrupted nursing bouts. Cub responses to nursing disruptions were correlated with cub survival. Mothers showed rank-related differences in den selection; high-ranking females occasionally chose dens with fewer occupants, while all other mothers chose dens containing the highest number of animals. Mid- and low-ranking mothers were attracted to dens containing high-ranking mothers and cubs. The potential benefits of affiliating with high-ranking individuals are discussed.

Long-term changes in dominance ranks among ring-tailed lemurs at Berenty Reserve, Madagascar

A study was conducted between 1989 and 2001 to monitor changes in the dominance ranks among adult ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. Adult females were observed to be dominant over adult males. Their rank fluctuated greatly. However, in some troops, female rank orders were fairly stable over a period of several years. In general, male ranks were more unstable than female ranks. Most young females aged 3 years occupied the lowest ranks among adult females. However, several were also observed to have attained relatively higher ranks, placing them right beneath their high-ranking mothers; this suggested the existence of "dependent ranks". Mothers were dominant over their daughters. Similarly, older sisters were usually dominant over younger sisters. The mean duration of alpha status for females was 1.95 years, although considerable variation was observed in the duration of the alpha status (1-5 or more years). Most young males aged 3 years initially occupied the lowest ranks in their natal troops, and then they migrated to non-natal troops around the age of 4 years. They ascended in rank between the ages of 4 and 6 years, although there was considerable variation in the acquirement of high rank. The mean duration of alpha status for males was 2.2 years. Larger males were observed to occupy higher ranks. Occasionally, both males and females showed intense aggression (i.e., targeting aggression) towards others.

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 females are known to produce more offspring, but the effects of maternal rank on early cub survivorship have not been investigated. Cub mortality was examined over a 4-year period in one clan of wild-living spotted hyenas in Kenya. Data were obtained for 100 cubs in 63 litters produced by 27 adult females. Survivorship of cubs from birth through their first year was examined as a function of litter size, sex of cubs, and maternal rank. Overall, cub mortality was high (61%). Contrary to expectation, singleton cubs did not survive better than twins, and there was no difference in survivorship between female and male cubs. High-ranking mothers were not more successful at raising twins or daughters than were low-ranking mothers. There was no correlation between cub mortality and maternal rank. Peaks in cub mortality coincided with life stage events, including mean age of arrival at a communal den, and age at which cubs began visiting kills. Documented causes of mortality included intraclan infanticide, disease, orphaning, predation by lions, and a mechanism of filial infanticide that has not been previously described in this species: selective litter reduction by mothersviapartiallitterabandonment.Noinstances of facultative orobligatesiblicideweredetected.During thisstudy,association between rank and number of cubs surviving to 1 year of age appeared to be due to differences in reproductive output and not differential survival of cubs within their first year. Key words: Crocuta, infanticide, mortality, neonate, rank, siblicide. [Behav Ecol]

Infants as a commodity in a baboon market

We used data from adult female chacma baboons, Papio cynocephalus ursinus, to provide the first test of hypotheses on interchange trading and the structure of a biological market (Noë & Hammerstein 1994, Behavioral Ecology and Sociobiology,35, 1–11) within a primate group. The interchange commodities selected were grooming and handling of infants less than 3 months of age. Patterns of grooming in relation to infant handling showed strong evidence for interchange. Grooming for infant access was initiated by potential handlers and was significantly likely to be nonreciprocated. More critically, the data show that infant ‘supply’ created a market effect: grooming bout duration (the price ‘paid’ for handling) was inversely related to the number of infants present in the group. In addition, there was an inverse relationship between grooming bout duration and the rank distance between mothers and handlers, suggesting that higher-ranking mothers could demand a higher price for infant handling. Where rank distance was high, females were able to handle infants without grooming. Dominance could thus be used to disrupt the infant market effect. If biological markets models are to be fully applicable to primate groups (and those of other social mammals) then the potentially distorting effect of dominance needs to be incorporated into the framework. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx).

We present body mass (N = 419) and crown-rump length (CRL, N = 210) measurements from 38 male and 49 female mandrills born into a semifree-ranging colony in order to describe growth from birth to adulthood, and to investigate maternal influences upon growth. Adult male mandrills are 3.4 times the body mass, and 1.3 times the CRL, of adult females. Body mass dimorphism arises from a combination of sex differences in length of the growth period (females attain adult body mass at 7 years, males at 10 years) and growth rate. Both sexes undergo a subadult growth spurt in body mass, and this is much more dramatic in males (peak velocity 551 g/months +/- 89 SEM at 84-96 months). CRL dimorphism arises from bimaturism (females attain adult CRL at 6 years, males after 10 years), and neither sex shows a particular subadult growth spurt in CRL. Sexual size dimorphism thus represents important time and metabolic costs to males, who mature physically approximately 3-4 years after females. Considerable interindividual variation occurs in the size-for-age of both sexes, which is related to maternal variables. Older mothers have heavier offspring than do younger mothers, and higher-ranking mothers have heavier offspring than do lower ranking mothers. Mass advantages conferred upon offspring during lactation by older and higher-ranking mothers tend to persist postweaning in both sexes. Thus maternal factors affect reproductive success in both sexes, influencing the age at which offspring mature and begin their reproductive career.

Offspring Grazing and Suckling Rates in a Sexually Dimorphic Ungulate with Biased Maternal Investment (Ammotragus lervia)

An analysis of resource gain is provided for Ammotragus calves during their first year of age. Both grazing and suckling rates are analysed and potential effects caused by age, sex, mother’s rank and weaning period studied. During their first day of life, calves devote their time mainly to suckling, grazing starting at the second week of age and exceeding suckling rate from the fourth week onwards. When suckling rate reaches a significant decrease (at 2 mo), male calves show a significantly higher grazing rate than female calves, suggesting a higher energetic demand for males at this age. When calves are 1 mo old, sons of high‐ranking mothers devote less time grazing than those of low‐ranking ones, which is in accordance with the higher maternal investment they receive. Grazing rate shows distinctive values for the different weaning periods distinguished in this species, but the resumption of mothers’ sexual activity, when a mother–offspring conflict occurs, does not affect grazing behaviour. These results are consistent with the biased maternal investment recently found in the same study population but focusing on another aspect, i.e. grazing behaviour, which is determined by calves’ own decisions.

CAREER MOVES: TRANSFER AND RANK CHALLENGE DECISIONS BY MALE LONG-TAILED MACAQUES

CAREER MOVES: TRANSFER AND RANK CHALLENGE DECISIONS BY MALE LONG-TAILED MACAQUES

Mechanisms of maternal rank ‘inheritance’ in the spotted hyaena, Crocuta crocuta

Maternal rank ‘inheritance’, the process by which juveniles attain positions in the dominance hierarchy adjacent to those of their mothers, occurs in both cercopithecine primates and spotted hyaenas. Maternal rank is acquired in primates through defensive maternal interventions, coalitionary support and unprovoked aggression (‘harassment’) directed by adult females towards offspring of lower-ranking individuals. Genetic heritability of rank-related traits plays a negligible role in primate rank acquisition. Because the social lives of Crocuta and cercopithecine primates share many common features, we examined whether the same mechanisms might operate in both taxa to promote maternal rank ‘inheritance’. We observed a large clan of free-living spotted hyaenas in Kenya to test predictions of four mechanistic hypotheses. Hyaena rank acquisition did not appear to be directly affected by genetic heritability. Unprovoked aggression from adult female hyaenas was not directed preferentially towards low-ranking cubs. However, high-ranking mothers intervened on behalf of their cubs more frequently and more effectively than low-ranking mothers. Maternal interventions and supportive coalitions appeared to reinforce aggression directed at ‘appropriate’ conspecific targets, whereas coalitionary aggression directed at cubs apparently functioned to extinguish their aggressive behaviour towards ‘inappropriate’ targets. Young hyaenas and primates thus appear to ‘inherit’ their mothers' ranks by strikingly similar mechanisms.

Feeding tactics in juvenile rhesus monkeys (Macaca mulatta).

In a group of rhesus monkeys, feeding tactics of juveniles were studied in a competitive situation in which food presentation had been modified, and where food was supplied in a feeding trough six times a day. Juvenile offspring of high-ranking mothers remained longer in the feeding area gathering food. In contrast, juvenile offspring of low-ranking mothers went less often to the feeding area, primarily to collect food. Low-ranking juveniles also gathered the food faster than did dominants and used longer feeding bouts. High-ranking juveniles interrupted their feeding more spontaneously than did subordinate ones. Low-ranking juveniles did so more often as a result of avoiding and being startled. Juvenile males entered the feeding area to satisfy their food requirements more often than females, but were also aggressively expelled more than females. No relation was found between age in months of juveniles and any feeding parameters or causes of interruption. Nor were significant differences found between young and old juveniles. Juvenile rhesus appear to use different tactics in accessing food according to their sex and to their mothers' dominance rank.

Within-litter sibling aggression in spotted hyaenas: effect of maternal nursing, sex and age

Models that address facultative siblicide in avian species predict that the costs and benefits of sibling aggression will change in relation to the level of food provisioning by parents. In spotted hyaenas, Crocuta crocuta, one of the few mammalian species in which facultative siblicide occurs, aggression rates between siblings were highest when cubs competed for access to maternal milk. In the Serengeti National Park, Tanzania, nursing of cubs by spotted hyaena mothers was influenced by the migratory movements of herbivores and the social status of the mother. Consistent with predictions from avian models, rates of sibling aggression among spotted hyaena littermates were inversely related to levels of maternal input in terms of lactation. Long-distance foraging trips by mothers (commuting trips) resulted in low cub growth. Rates of aggression were higher in years when cub growth rates were low than in years when cub growth rates were medium or high. Rates of aggression between littermates belonging to high-ranking mothers, who nursed their cubs more frequently than low-ranking mothers, were lower than those between siblings of low-ranking mothers. Aggression rates in all-female and all-male litters were higher than in mixed-sex litters. Identical payoff expectations of same-sex litters may provide an explanation for this result. In accordance with predictions from life history theory, aggression rates declined with age and increasing reproductive value of siblings.

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.

Influence of Dominance Rank and Offspring's Sex on the Onset of the Next Reproductional Cycle of Female Japanese Macaques (Macaca fuscata)

Influence of a mother's dominance rank and her yearling's sex on the onset of the next reproductional cycle was studied in a free-ranging troop of Japanese macaques at Jigokudani Monkey Park, the Shiga Heights, Nagano Prefecture, Japan. Yearlings of lower ranking mothers were harassed more frequently by unrelated animals. No difference in the frequency of social interactions between a mother and her yearling was noted with regards to dominance rank or the offspring's sex. However, the onset of estrus in higher ranking mothers was earlier in the subsequent mating season. The present study suggests that local resource competition is not intense and aggression toward yearling macaques by unrelated animals does not affect interactions between a mother and her yearling. It is hypothesized that because higher ranking mothers were in good condition nutritionally, they exhibited estrus earlier.

The Socioendocrinology of Adolescent Development in Male Rhesus Monkeys (Macaca mulatta)

Observations were made on four captive breeding groups of rhesus monkeys in order to measure hormonal, behavioral, and genital changes in adolescent males during the annual mating season. Three questions were addressed with regard to possible effects of social environment upon reproductive maturation: (1) Does male agonistic rank influence adolescent development? (2) Does affiliation between adolescent males and adult females during the mating season influence the males’ reproductive development? (3) Does maternal rank exert any effect upon reproductive maturation in adolescent sons? In many (but not all) cases male rank was positively correlated with circulating testosterone and testes weights during the mating season. Affiliative behavior (allogrooming and sexual interactions) between adolescents and adult females in their social groups bore no relationship to the degree of reproductive maturation in males. Mounts involving intromission were infrequent, but sons of high-ranking mothers gained significantly more intromissions than sons of lower-ranking females. Maternal rank was also found to correlate with circulating testosterone levels, testes weights, growth of the baculum (os penis), and maintenance of body weight in adolescent sons during the mating season. By contrast, levels of β-endorphin in the cerebrospinal fluid of adolescent males did not correlate with social rank, testosterone levels, or genital development. These findings point to possible effects of maternal rank, as well as intermale agonistic rank, in determining reproductive maturation during adolescence in the male rhesus monkey.

Preparation and activation: determinants of age at reproductive maturity in male baboons

Age at maturity is a particularly important life history trait, but maturational data are rare for males in natural populations of mammals. Here we provide information on three maturational milestones and their social and demographic correlates among 43 wild male baboons, Papio cynocephalus, in a natural population in Amboseli National Park, Kenya. We examined (1) age at testicular enlargement, which signals puberty and the onset of subadulthood, (2) age at attainment of adult dominance rank, which we consider to be the beginning of adulthood, and (3) age at first sexual consortship, which is the best measure available for age at first reproduction in male baboons. Testicular enlargement (median age = 5.69 years) occurred earlier among sons of high ranking mothers, and was not influenced by rainfall or seasonality. Attainment of adult dominance rank (median age = 7.41 years) was also accelerated among sons of high-ranking mothers, and among males whose mothers had died while the males were juveniles. First sexual consortship (median age = 7.92 years) was not influenced directly by maternal characteristics, but attainment of adult dominance rank always preceded first consortship. The lag time between attainment of adult rank and first consortship (median = 2.5 months; range = 5–526 days), was predicted by the number of sexually cycling females in the group when the male attained rank, and by how high ranking the male became in his first months as an adult. We suggest that the age at which a male baboon is ready to begin reproducing is influenced by a relatively stable maternal characteristic that exerts its influence early in development, but the timing with which this potential is realized depends on activation by more proximate, often stochastic triggers such as female availability. This two-level organization of influences is likely to contribute to the variance both in age at first reproduction and in lifetime fitness. Differences in the relative magnitude of the two levels will lead to both intra- and interspecific variability in the opportunity for maternal selection and sexual selection.

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.

The social grooming of captive female rhesus monkeys: Effects of the births of their infants

We observed the grooming interactions of 13 female rhesus monkeys (Macaca mulatta)before and for 12 weeks after the births of their infants. Mothers groomed for similar amounts of time before and after the birth of their infants, but after the birth, the grooming they directed to their infants may have been at the expense of that directed to other partners. Lactating females did not receive more grooming from other females but were approached more often, suggesting that they were more attractive. Mothers that groomed their infants most groomed others least, as if grooming time was limited for each mother or as if she was trying to compensate for avoiding interactions with other partners. Mothers of male infants groomed others more than mothers with female infants did, which might be due to mothers with daughters receiving more aggression and therefore avoiding interaction. Experienced and high-ranking mothers groomed their newborn infants considerably more than primiparous mothers did in the 24 hr following birth. Grooming was preferentially directed at close kin before the births of the infants. Mothers tended to groom higher-ranked partners more than they were groomed by them, and they tended to receive more grooming from lower-ranked partners than they gave, as suggested in models of rank attractiveness.

Vigilance in young baboons: effects of habitat, age, sex and maternal rank on glance rate

Abstract. Glance rates, a measure of vigilance, were sampled in infant and young juvenile yellow baboons, Papio cynocephalus, in Amboseli, Kenya, to test ecological and social predictions about the ontogeny of vigilance. Glance rates of young baboons did not vary between closed and open habitats, but did vary with sex, maternal rank and age. Daughters of low-ranking mothers glanced significantly more often than daughters of high-ranking mothers, and the converse was true for males. Glance rates of females, but not males, decreased significantly between 6 and 24 months of age.

Ecological constraints on the behaviour of mother long-tailed macaques (Macaca fascicularis)

The ecological consequence of the effects of different social conditions on the behaviour of females with infants were examined in two different-sized groups of long-tailed macaques (Macaca fascicularis) that inhabited adjacent home ranges in Gunung Leuser National Park in Indonesia. This study aims to test predictions of the “within-group competition/predation avoidance” hypothesis of social organization. Females, particularly those carrying an infant, are considered to experience the most direct effects of environmental constraints on fitness prospects. Data on maintenance behaviour, height in canopy and spatial position were collected for five mothers in a small group and eight mothers in a large group. Comparisons were made on the basis of group size and dominance rank. Mothers from the large group spent less time “feeding” on clumped fruits and more time “foraging” on dispersed food items. Lower-ranking mothers, undergoing the highest rate of within-group competition, foraged most. For macaques in the study area, predation risk is considered to decrease with height in the canopy. Mothers in the small group, assumed to be more susceptible to predation, remained substantially higher in the canopy than mothers in the large group. In both groups, mothers adjusted their height to their spatial position in the group. Lower-ranking mothers were more often found without neighbours, presumably to avoid feeding competition. As a result they stay higher in the canopy than higher-ranking mothers. The results clearly demonstrate that individual females in the same reproductive state and living in the same area, but in different social environments, adapted their behaviour according to the hypothesis.