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.     

Patterns of infant handling and relatedness in Barbary macaques (<Emphasis Type="Italic">Macaca sylvanus</Emphasis>) on Gibraltar

Among papionin primates, the Barbary macaque (Macaca sylvanus) shows the most extensive interactions between infants and group members other than the mother. Two different types of interactions occur: (1) long-lasting dyadic interactions between a handler and an infant, and (2) brief triadic interactions between two handlers involving an infant. Previous investigations showed that infant handling by males is best explained as use of infants to manage relationships with other males. In contrast, no adaptive explanation for infant handling by females emerged. Here, we compared the infant-handling pattern between subadult/adult males and subadult/adult females in a free-ranging group of 46 Barbary macaques on Gibraltar to test whether the relationship management hypothesis also applies to female handlers. We further investigated the infant-handling pattern of juveniles and used microsatellite markers to estimate relatedness between infant handlers and the infant’s mother. We found that males, females and juveniles all participated extensively in triadic interactions using infants of above-average related females. In contrast, only males and juveniles were highly involved in dyadic interactions with infants of related females, while females rarely handled infants other than their own. The pattern of infant handling was entirely compatible with the predictions of the relationship management hypothesis for males and mostly so for females. Moreover, our genetic analysis revealed that males and females differ in their partner choice: while females preferred to interact with related females, males had no significant preference to interact with related males. We further discuss the observed above-average relatedness values between infant handlers and the infant’s mother in the light of kin-selection theory.     

Maternal Investment and Infant Survival in Gray-Cheeked Mangabeys (Lophocebus albigena)

Differences among females in infant survival can contribute substantially to variance in fitness. Infant survival is a product of external risk factors and investment by kin, especially the mother, and is thus closely tied with the evolution of behavior and life history. Here we present a 9-yr study (2004–2012) of infant survival and sex ratio relative to age and dominance ranks of mothers and the presence of immigrant males in a free-ranging population of gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda. We consider immigrant males because they are known to increase infant mortality in several other species. We found that infants of older mothers had higher survival than those of younger mothers but that high rank did not confer a significant benefit on infant survival. Female infants had higher survival than male infants. Young, low-ranking females had more male infants than young, high-ranking females, which had slightly more daughters, but this difference declined as females aged because low-ranking females had more daughters as they aged. With limited data, we found a significant relationship between the presence of male immigrants and infant mortality (falls and unexplained disappearances) to 18 mo. Our results suggest that infant survival in gray-cheeked mangabeys is most precarious when mothers must allocate energy to their own growth as well as to their infants, that sons of young mothers are at greatest risk, and that immigrant males can negatively affect infant survival.     

Reproduction in wild female olive baboons

The purpose of this paper is to evaluate several factors that influence female reproduction in a large troop of wild olive baboons (Papio cynocephalus anubis) based on 4 consecutive years of demographic data. Interbirth intervals were significantly shorter for females whose infants died before their next conception than for females whose infants survived. High-ranking mothers of surviving infants had significantly shorter birth intervals than comparable low-ranking mothers, independent of maternal age. This occurred mainly because the interval from resumption of cycling to conception was significantly shorter for high-vs. low-ranking females. Dominance rank did not influence sex ratio at birth, infant survival in the first 2 years, or adult female mortality. Age was also significantly related to interbirth intervals, with older females having shorter intervals. Primiparous females had consistently longer reproductive intervals than did multiparous females, but this difference reached statistical significance only for females whose infants died before the next conception. Primiparous females also experienced significantly higher infant mortality. Data on body size and estrous cycle length indicated no differences between high- and low-ranking females. Nutritional and stress-related mechanisms that may underlie the reproductive advantages of high rank are discussed.     

Differential reproductive success and facultative adjustment of sex ratios among captive female bonnet macaques (Macaca radiata)

In a group of captive bonnet macaques (Macaca radiata) housed at the California Primate Research Center, variance in reproductive success among females is primarily due to differences in infant survival. The infants of low-ranking females have a smaller probability of surviving to 6 months of age than do the infants of other females. In addition, the juvenile daughters of low-ranking females are more vulnerable to behaviourally induced mortality than are other immature animals. Observational evidence indicates that this mortality is the direct result of aggression by unrelated, higherranking adult females. Although infants' sex is not consistently related to survival, yearly fluctuations in the survival of male and female infants are reflected in the extent and direction of the skew in the sex ratio of offspring produced the following year. Years in which the highest proportion of male infants survive are followed by years in which the largest proportions of the birth cohorts are composed of males, and years in which the largest proportions of females survive are followed by years in which the largest proportions of birth cohorts are composed of females. For infant females the probability of surviving is reduced when a substantial proportion of the birth cohort is composed of females. The same pattern is evident among the sons of low-ranking females. The adaptive significance of behaviourally induced variation in reproductive success among females is considered in relation to these data.     

Do Adult Male Spider Monkeys (Ateles geoffroyi) Preferentially Handle Male Infants?

Infant tolerance by adult males has been observed in many primate species with multimale–multifemale mating systems, but males do not usually initiate interactions with infants. In male philopatric species, such as spider monkeys, adult males within a community exhibit high levels of cooperation and affiliation, and they might therefore be motivated to create bonds with potential future allies. Based on this hypothesis we predicted that adult male spider monkeys would participate in infant handling more than adult females and they would preferentially direct handling toward male infants. Between January 2008 and July 2010, we collected 884?h of observation on a community of wild spider monkeys at Runaway Creek Nature Reserve in Belize. During this period we observed 120 incidences of affiliative interactions between infants and adults other than their mother. The adult initiated the majority of nonmother adult–infant interactions (78?%). All available infants (5 males, 7 females) were handled during the study. All 9 of the community adult males handled infants but only 7 of 14 adult females did so. Adult males handled infants significantly more often than did adult females and males also handled young infants more often than older infants. Significant infant sex differences in handling appeared in infants >6?mo when adult males handled males significantly more than females. The patterns of infant handling among age–sex class dyads reflect the affiliative social patterns that we see in adult spider monkeys. These results provide support for the hypothesis that adult males preferentially handle male infants as a strategy for fostering social bonds.     

Vervet monkey grandmothers: Interactions with infant grandoffspring

Social relationships of 30 infants with their maternal grandmothers were studied in a captive colony of vervet monkeys (Cercopithecus aethiops sabaeus).Grandmothers and grandinfants formed affiliative relationships with one another that could be distinguished from the infant’s relationships with nonkin adult females and with other adult female kin. The intensity of the grandmother—grandinfant relationship varied according to several factors which were related to the infant’s vulnerability to mortality and to the grandmother’s ability to provide effective social support. High-ranking grandmothers spent more time near their grandinfants, and initiated more grooming and caretaking of their grandinfants, than did lower-ranking grandmothers. Grandmothers spent more time near their daughter’s first surviving infant than near later-born infants, and when grandmothers had more than one adult daughter, they spent more time near the infant of the younger daughter. These results, combined with the fact that the presence of a maternal grandmother has been associated with a reduction in the rate of infant mortality in this colony (Fairbanks and McGuire, 1986), suggest that grandmothers are actively contributing to the reproductive success of their adult daughters and to the survival of their infant grandoffspring.     

Natal Attraction in Adult Female Baboons (Papio cynocephalus ursinus) in the Moremi Reserve, Botswana

Mammalian females are strongly attracted to infants and interact regularly with them. Female baboons make persistent attempts to touch, nuzzle, smell and inspect other females’ infants, but do not hold them for long periods, carry them, or provide other kinds of care for them. Mothers generally tolerate these interactions, but never initiate them. The function of these brief alloparental interactions is not well understood. Infant handling might be a form of reproductive competition if females’ interest in infants causes distress to mothers or harm to their infants. Alternatively, infant handling might be the product of selection for appropriate maternal care if females who are highly responsive to infants are the most successful mothers. We test several predictions derived from these hypotheses with data collected in a free‐ranging group of baboons (Papio cynocephalus ursinus) in the Moremi Reserve of Botswana. Infants were most attractive when they were very young. Mothers of young infants were approached by other adult females on average once every 6 min, and other females attempted to handle their infants approximately once every 9 min. By the time infants were a year old, their mothers were being approached only once every 30 min and infants were being handled only once every 5 h. Females were more strongly attracted to other females’ infants when they had young infants of their own, and their interest in other females’ infants declined as their own infants matured. Females seemed to be equally attracted to all infants, but had greater access to offspring of their relatives and subordinate females. Females nearly always grunted as they handled infants. As in other contexts grunts are a reliable predictive signal that non‐aggressive behavior will follow, the use of grunts before handling suggests that these interactions were not a form of deliberate harassment.     

Brief communication: Self‐suckling in Barbary macaque (Macaca sylvanus) mothers before and after the death of their infant

We report here self‐suckling in four wild female Barbary macaques (Macaca sylvanus), living in two troops (i.e. “Flat face” and “Large” troop) in the middle‐Atlas Mountains, Morocco. The four females lost their infants due to predation or for unknown causes. Self‐suckling was observed before and after the infants died in the four females living in the “Flat face” troop. When the infants were still alive, self‐suckling was of short duration and it was probably a method to improve milk flow when the infant switched from one nipple to the other. After the infants died, self‐suckling lasted significantly longer and the females were apparently drinking their own milk. Self‐suckling was never observed among the four lactating females in the “Large” troop (including one monkey who lost her infant) and it could thus represent a cultural difference. Moreover, self‐suckling after the death of an infant may be explained by the energetic and immunological benefits that a monkey may gain from drinking their own milk. Finally, self‐suckling may have a stress‐releasing effect on the mothers who have lost their infants. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.     

Spatial structure of chacma baboon groups

A method is presented for measuring the location of individuals with respect to the center or perimeter of a primate group. The method estimates an individual’s domain of danger: the area in which a hidden predator is closer to the individual than to other group members (cf. Hamilton, 1971). A domain is determined by the directions and distances of particular neighbors from a given individual. Animals at peripheral locations have relatively large domains, whereas animals at central locations have relatively small domains. Domains of danger were sampled for members of two groups of chacma baboons (Papio ursinus)in northern Botswana, to test for nonrandom spatial patterns throughout the day. Females with infants had significantly smaller domains than did females without infants. Domains also were correlated with social ranks of females;high-ranking females had smaller domains than did low-ranking females, possibly because high-ranking females were more likely to have infant offspring. For adult males, however,domain sizes were not significantly correlated with social ranks. Immigration status of adult males, rather than social rank, better accounted for spatial positioning.     

How rhesus monkey mothers and infants keep in touch when infants are at risk from social companions

Ten-to 17-week-old rhesus monkey infants that received hits from companions other than their mother at high rates (relative to their rates of involvement in playful social encounters with those companions) tended to be members of mother-infant dyads that were vigilant. Criteria of vigilance were frequent contacts between mother and infant during the first 5 sec of the infants’ social encounters and/or a bias of mother-infant contacts toward that time. Infants that received few hits per encounter came from both vigilant and nonvigilant dyads. When analyzed alone, mothers’ rates showed the same trends. High levels of vigilance tended to reduce infants’rates of making social contacts. Maternal social rank and other measures of the infants’ social involvement were not correlated with vigilance. There is no evidence that mothers and infants were in conflict with each other about interrupting the infants’ encounters. Understanding vigilance becomes important whenever vigilant activity conflicts with other activities. Special problems arise because decisions about vigilance levels require judgments of risk based on the kinds of events that occur only rarely if vigilance is effective. A model providing a framework for studies of vigilance against the risks of infants’ social activities was developed. It recognizes that (1) risk-reducing vigilant behavior can conflict with acquiring information about risk; (2) in social situations where reliable estimates of risk are impossible, individuals might follow rules of thumb (e.g., be restrictive) rather than modify behavior moment by moment according to the current situation;and (3) at the dyad’s optimum balance between vigilance for the current infant and investment in subsequent off-spring, the infant will not be totally protected, so that while dyads at higher risks are more vigilant, the risks are also realized to a greater extent (e.g., itin terms of the number of hits received per encounter).     

Conspecific Influences on Vigilance Behavior in Wild Chimpanzees

Diurnal primates rely on visual monitoring behavior to collect various kinds of ecological and social information. Vigilance behavior is monitoring specifically to detect external threats. Previous studies of vigilance behavior were focused mainly on the influence of predation threats, whereas the influences of conspecific factors, such as intragroup threats, have been relatively unstudied. Individual vigilance is predicted to be inversely related to the group size or the number of individuals nearby if the main target of the vigilance is a predation threat and positively related if the main target of the vigilance is a conspecific threat. I studied wild chimpanzees (Pan troglodytes schweinfurthii) in Mahale Mountains National Park, Tanzania, and measured the vigilance duration when they are resting on the ground via 2-min focal observation. In both males and females, vigilance duration increased as the number of individuals nearby increased. This result agrees with the idea that the chimpanzees are vigilant toward other group members. In addition, maternal vigilance monitors and protects the safety of dependent offspring as the duration of maternal vigilance was longer when a dependent infant was separated from its mother than when the offspring was in contact with its mother. The results indicate that the vigilance behavior in wild chimpanzees was affected by conspecific factors.     

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

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

Breeding-season relationships of immature male rhesus monkeys with females. I. Individual differences and constraints on partner choice

Several aspects of breeding-season relationships with mature females are described for free-ranging immature male rhesus monkeys (Macaca mulatta)on Cayo Santiago. At puberty, immature males are still groomed by mature females, as they were as infants, but no longer receive active protection from females other than their mothers. A further, potentially beneficial, aspect of their associations with females lies in the opportunities to observe closely the tactical social and sexual interactions of receptive females with adult males. However, immature males themselves rarely copulate with females. Developmental constraints may explain the finding that most females observed by immature males were relatives but that high-ranking males showed a particular preference for adolescent relatives, whereas the preference of low-ranking males was for adult relatives. A further finding was that while there was a tendency for immature males to devote a greater proportion of their total observation time to females that ranked above their mothers than to those of inferior rank, these were also the females from which males received the most aggression, while most of the females with which the males groomed or copulated were lower ranking than the males’ mothers. Of three hypotheses concerning three possible types of social constraint which might account for such a finding, the data supported only one—that particular levels of aggression within these relationships are compatible only with certain other elements (observations), and not with others (grooming, copulation).     

Responses of foster-mothers and troop members to adopted newborns in a captive group of rhesus monkeys

Two rhesus monkey males and two females, born to females caged singly, were exchanged with same-sex infants born to females in a large troop which was held in an enclosure in a different building. The ages of the infants were between 24 and 120 hr. The selected foster mothers (FMs) immediately accepted the foreign infants, allowed them to suckle and treated them as their own offspring. Compared with interactions with previous offspring, the FMs initially tended to be more possessive and restrictive of their foster infants: generally they took longer before they allowed the infants to sit at a distance from them and more readily retrieved them. The foster infants tended to be more active (‘fidgety’) than natural (control) offspring born to the troop. Non-related members of the troop, differentiated between foster and control groups. These troop animals more frequently approached and sat in proximity, often in fur-contact with, touched, groomed, and lipsmacked to, foster infants than control infants. The attractiveness of the fostered infants seemed to be slightly associated with the FMs' dominance rank. The foster infants were therefore viewed by others as having assumed the role afforded by the FMs' rank. Thus both FMs and other troop members recognized the unfamiliarity and novelty of the foster infant but the infants were still accepted into the group. We suggest that the different treatment of the foster infants by the troop may have consequences on the infants' future social development.     

Contextual Factors Meditating Contests Between Male Chacma Baboons in Botswana: Effects of Food,Friends and Females

We examined aggressive displays among male chacma baboons (Papio ursinus) over a 23-mo period in the Okavango Delta of Botswana. High-ranking males were more likely than middle- or low-ranking males to participate in displays. Regardless of rank, all males were more likely to participate in chases or physical fights if their opponents rank was similar to their own. Most chases and fights, including those that led to injuries, were also between similarly-ranked males. The rate of both aggressive displays and approach-retreat interactions increased in the weeks before rank reversals, suggesting that rank challenges were preceded by a period when males assessed each others competitive ability and/or motivation. Aggressive displays between disparately-ranked opponents occurred most frequently in contests involving resources of high fitness value: the defense of meat, the defense of estrous females, and the protection of infants against infanticidal attacks. Silent displays were more likely to occur in these three contexts than were displays that occurred as part of more slowly escalating interactions, in which opponents first exchanged calls. Results suggest that competitive encounters among male baboons follow patterns predicted by evolutionary game theory.     

Effects of Reproductive Status on Energy Intake,Ingestion Rates,and Dietary Composition of Female <Emphasis Type="BoldItalic">Cebus capucinus</Emphasis> at Santa Rosa,Costa Rica

The limiting factor for fitness in female primates is the acquisition of high-quality food, i.e., food that is high in energy and nutrients, such as protein, fat, and carbohydrates. Reproductive status can influence female feeding patterns, e.g., lactating females in some primate species consume greater quantities of food and specific nutrients than do nonlactating females. We examined the energy intake, ingestion rate, and composition of the diet in female white-faced capuchins in 3 reproductive states: lactating, gestating, and cycling. We observed 12 reproductively active females for 7 mo and compared their energy intake, ingestion rates, and intake rates of nutrients: protein, fat, sugar, and fiber. Lactating females took in significantly more energy per hour while feeding than pregnant and cycling females did. Lactating females also ingested significantly more food items per hour, but they did not spend more time eating than other females did, and they did not differ in the composition of their diet as measured by insect consumption and proportion of protein. Pregnant and cycling females did not differ from each other in any of the measures. We predicted that as the infants aged and began to move independently to forage and play, their mothers’ energy intake rates would decrease in concert with decreased energy demands by the infant. We found a statistically significant relationship between these 2 factors, with infant age explaining 75.4% of variation in mothers’ energy intake, supporting previous studies that found lactation to be the most energetically expensive reproductive state.     

Effects of group composition on agonistic behavior of captive pigtail macaques,Macaca nemestrina

We surveyed agonistic behaviors of 20 captive groups of pigtail macaques (Macaca nemestrina) housed under identical spatial conditions. Fifteen groups contained one male each; the other five groups contained no adult males. Groups included six to twelve adult females, some of which had infants with them. We found no relationship between social density of groups and incidence of agonistic behavior, but significantly more contact aggression (grab, hit, push, bite) and noncontact aggression (chase, open-mouth “threat,” bark vocalization) occurred among females in groups containing no males than in those containing one male each. Apparently, males played an important role in the inhibition of intragroup conflict. We also found that females in groups containing males exhibited less noncontact aggression if infants were present than if no infants resided in their groups. Thus, competition of females over infants must not have been an important constituent of intragroup conflict under the conditions of this survey.     

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.