Ranking Mothers Research Articles

Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free‐ranging female rhesus macaques

The hypothalamic-pituitary-adrenal (HPA) axis modulates individuals' physiological responses to social stress, which is an inevitable aspect of the daily lives of group-living animals. Previous nonhuman primate studies have reported that sex, age, rank, and reproductive condition influence cortisol levels under stressful conditions. In this study we investigated cortisol responses to stress among 70 multiparous, free-ranging female rhesus macaques (Macaca mulatta) on the island of Cayo Santiago, PR. Plasma cortisol samples were collected in two consecutive years under similar conditions. Twenty-two females were sampled both years, and most of those females were lactating in only one of the years. Individual differences in cortisol levels were stable across years, even though reproductive condition changed for most individuals. No relationship was found between age or social rank and cortisol levels. Of the females that changed reproductive conditions, cortisol levels were higher when they were lactating than when they were cycling, and the amount of change in cortisol from cycling to lactating was greatest for low-ranking individuals. Heightened reactivity to stress during lactation may be the result of concerns about infant safety, and such concerns may be higher among low-ranking mothers than among higher ranking mothers. Psychosocial stress and hyperactivation of the HPA axis during lactation can suppress immune function and increase vulnerability to infectious diseases, thus explaining why adult females in the free-ranging rhesus macaque population on Cayo Santiago have a higher probability of mortality during the birth season than during the mating season.

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.

Bonobos

Bonobos

Behavioral processes and costs of co-existence in female spotted hyenas: a life history perspective

We assessed the importance of three behavioral processes on the fitness of individual females as mediated via maternal care in matrilineally organized social groups of spotted hyenas Crocuta crocuta. These were maternal choice of foraging tactic, the maintenance of individual dominance rank (social status) within the adult female hierarchy, and the behavioral support provided by mothers to their daughters when daughters acquired their position in the adult female hierarchy. The effects of all behavioral processes were closely linked. Maternal care was dependent on maternal social status because high ranking females had priority of access to food, and individual maternal choice of foraging tactic was frequency – and social status-dependent when medium prey abundance provided an opportunity for such a choice. At medium prey abundance, low ranking females went on costly long distance commuting trips to forage on migratory herds outside the group territory, whereas high ranking females fed on kills within the group territory. As a consequence, offspring of high ranking females grew faster, had a higher chance of survival to adulthood, and thus high ranking females had a higher lifetime reproductive success. Daughters of high ranking females usually acquired a social status immediately below that of their mother provided they enjoyed the effective support from their mothers as coalition partners, and they gave birth to their first litter at an earlier age than daughters of low ranking mothers. Spotted hyenas are therefore an example of the ‘silver-spoon effect’. This study shows that the frequency-dependent outcome of behavioral processes can be a key determinant of maternal reproductive success in social carnivores and have a profound influence on the reproductive career prospects of offspring.

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.

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.

Social rank and birth sex ratios in rhesus monkeys ( Macaca mulatta)

Data from a captive colony of rhesus macaques ( Macaca mulatta) were used to investigate birth sex ratios. The colony consisted of 6 groups with an average of 11 animals per group. Top ranking mothers gave birth to 67 daughters and only 30 sons. Females of lower rank gave birth to 118 sons and only 84 daughters. There was no difference in birth sex ratio in those females ranking second, third, fourth or fifth in their social group. Bias towards daughters in top-ranking mothers was strongest in matrilines of two adult females at the time of conception; bias towards sons in lower-ranking mothers was strongest in matrilines with three adult females. I argue that top-ranking mothers bias their offspring sex ratio in favour of daughters when founding a matriline, and suggest that they somehow limit recruitment of daughters by other females at this time. I show that within species, variabilities found in birth sex ratios can reflect the investigators' different rank categories as well as the different conditions under which the animals live.

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.

Growth and threshold weaning weights among captive rhesus macaques.

Interspecific analyses of infant growth and the time to maternal reconception (or weaning) demonstrate a consistent threshold for weaning weight at close to four times neonate weight, irrespective of the duration of lactation (Lee et al., [1991] J. Zool. Lond. 225:99-114). Intraspecific variation in the attainment of a threshold weaning weight was determined in a sample of 31 captive infant rhesus macaques, where growth between birth and subsequent parturition was measured along with information on maternal size, weight, and social characteristics. A threshold weaning weight was found, with infants attaining approximately 1,335 g at the time of reconception. Birth weights of the infants were influenced by maternal physical and social variables in that larger mothers, and alpha ranking mothers, produced larger neonates. Postnatal growth rate, which determined the attainment of the threshold weight, was independent of maternal size or condition, but was influenced by offspring sex and the probability of reconception. Future reproductive status of mothers was specifically related to differences in patterns of growth among the infants. Mothers who conceived again at 30 weeks had infants who grew more slowly after the first 12 weeks of life, especially if these infants were sons. Mothers in this colony appeared to make decisions about the need to sustain their infants' growth in relation to their ability to invest in current offspring, which may compromise their subsequent reproduction.

Environmental variation and developmental rate among free ranging yellow baboons (Papio cynocephalus).

Behavioral development was observed for the first 3 months of life on 18 infants from three troops of yellow balloons (Papio cynocephalus) in Mikumi National Park, Tanzania. Developmental rates were determined for each subject on six major behaviors using the slope from regression equations performed on developmental functions changes in behavior with age. These slopes were examined statistically for associations with social and physical variables that were hypothesized to influence developmental rates. Results showed that faster rates of development were significantly associated with certain environmental and social conditions. Infants born late in their cohort, infants born in a more physically immature state, infants living in a large troop, and female infants of low ranking mothers all had significantly faster rates of development than infants at the other extreme in these categories. These results are interpreted as evidence for developmental processes that compensate for environmental or physical conditions that negatively influence survivorship. © 1995 Wiley-Liss, Inc.

Costs of maternal care: infant-carrying in baboons

Infant-carrying, the most costly form of primate parental care other than lactation, was investigated in savannah baboons of Amboseli, Kenya. Measurements of physical growth, counts and length of paces, and simultaneous records of carrying and locomotion were used to evaluate the time, distance, and energetic expenditure of infant-carrying. Finally, we modeled the energetics of independent infant locomotion and considered ontogenetic patterns in the alternative energetic costs of carrying versus independent infant locomotion under assumptions of complete nutritional dependency. The youngest infants were carried by their mothers during all travel and foraging, for a total of 8–10 km/day. By 8 months of age, both carrying time and distance were almost zero. However, daily carrying distance, unlike carrying time, did not decline in the first few months, because older infants were carried disproportionately during rapid travel and, consequently, for greater travel distances per unit carrying time. Females of low dominance rank carried their infants the most; the highest ranking mothers not only carried their infants least but biased their carrying against sons. Although carrying a growing infant is an increasingly costly behavior, during the period of nutritional dependence energetic costs to the mother are appreciably greater if an infant travels independently instead of being carried by its mother. Yet infants increased locomotor independence at a younger age than predicted by a simple model of maternal energetic efficiency. Trade-offs in energetic economy may enhance a mother's future reproduction at the expense of her present infant, may enhance survival of the present infant by promoting early acquisition of developmentally essential skills, or may suggest the importance of additional factors that influence the mother's and infant's behavior.

The influence of maternal rank and infant sex on maternal investment trends in rhesus macaques: birth sex ratios, inter-birth intervals and suckling patterns

In the new colony of rhesus macaques at Madingley, no overall difference was found in the length of the inter-birth intervals following the birth of male and female infants. The lack of overall differences in the reproductive costs of raising sons and daughters, was associated with an absence of differences in suckling patterns between male and female infants. It is argued that similar pre-weaning investment in sons and daughters may be related to the presence of similar growth rates for male and female infants during the first year of life. Most high ranking mothers reproduced in consecutive years, while low ranking mothers were more likely to experience two year long inter-birth intervals. Further analyses revealed that this difference was mainly due to the fact that low ranking mothers always failed to reproduce the year after raising a daughter. Thus, no difference was found in the length of inter-birth intervals between high ranking mothers with infants of either sex and low ranking mothers with sons. The daughters of low ranking females suckled more frequently and making more nipple contacts per bout, and such high nipple stimulation was responsible for the reproductive inhibition experienced by their mothers. It is suggested that the high degrees of nipple stimulation may have been a consequence of the high levels of aggression that low ranking females with daughters have been shown to receive, since their mothers could have allowed frequent ventro-ventral contact in order to protect them. Given that low ranking mothers find daughters reproductively costly to raise, it is possible that such high reproductive costs have played a significant role in the evolution of sex ratio biases at birth. As in other primate populations, in this colony low ranking females produced a greater proportion of sons than daughters, and high ranking mothers showed the opposite trend.

Eight-year study of social and ecological correlates of mortality among immature baboons of Mikumi National Park, Tanzania.

The Cox Proportional Hazards Regression Model was used to examine ecological and sociodemographic correlates of mortality among 164 immature yellow baboons born over an 8-year period at Mikumi National Park, Tanzania. Ecological correlates were derived from seasonal rainfall. Mortality was lowest for immatures born during the late rainy season, when it was likely that nourishment for pregnant and lactating females was greatest. High mortality was associated with above-average rainfall early in the immature's first complete rainy season. This association may result from one or more of the following: exposure, increased ranging, or accelerated vegetation growth, each of which is thought to increase hazards for weanlings. When births for the 8 years of the study were pooled, a birth peak occurred during the early dry season. The larger number of births during a birth peak should intensify competition among mothers and among immatures. Mortality was greatest for immature females born during the season immediately following the birth peak, while lowest for immature females born during the season immediately preceding the peak. Immature female mortality was greatest when the troop size at birth was large, and was most severe for females born to low ranking mothers. The sociodemographic results are consistent with Wasser's hypothesis that cooperative attacks of female baboons upon other troop females suppress the others' reproduction and the vitality of their infants, thereby improving the relative competitive position of the attackers' own young.

Short-term consequences of different breeding histories for captive rhesus macaque mothers and young

Life histories of rhesus monkey mothers (Macaca mulatta) were classified in terms of (1) whether the mothers were top ranking or not, (2) gave birth to more daughters than sons or vice versa, and (3) gave birth at intervals of one year or of more than a year. Bearing daughters at intervals of more than a year was the most common history among top ranking mothers, while bearing sons annually was most common among other mothers. The consequences for the infants and mothers of such histories were examined and (1) infants were more likely to die as neonates if they had an older sister, especially if the sister had been born in the previous birth season; (2) dyads with daughters received more aggression from other adults in the daughter's first year, but not necessarily through the year following the birth of the next infant (3) when mothers of daughters gave birth of the next infant after at least one fallow year, their daughters directed considerable amounts of harassing aggression to their next-born sibling; and (4) mothers of sons but not of daughters delayed longer when they received more aggression from other adults. We discuss the views that birth sex ratios may be affected by a mother's rank rather than how often she is involved in aggressive encounters with other adults; and that in top-ranking mothers, birth intervals may be controlled more by the infant's sex than aggression the family received. Fitting the data into a life history strategy model is done as a provisional and speculative exercise

Early infant development and maternal care in free-ranging vervet monkeys

The interactions of infant vervet monkeys (Cercopithecus aethiops) with their mothers were examined during the first 12 weeks of life. During this period there was a gradual rise in behaviour associated with increasing independence from the mother: female infants were slightly advanced over males on measures of decreasing contact with mothers and increasing rejections from the nipple. There were differences between the mothers in the ways they interacted with their infants such that no consistent maternal styles could be defined. Dominance rank of the mother did however influence her behaviour towards her infant, and high ranking mothers tended to be less rejecting towards sons, but more rejecting towards daughters, than were low ranking mothers. It is suggested that since vervet mothers have access to allomothers they may not be limited to dichotomous mothering styles.