The development of infant-caregiver relationships in captive common marmosets (Callithrix jacchus)

The growing independence of infant common marmosets from their caregivers is promoted primarily by their caregivers, who increasingly often prevent the infants from climbing onto them and decreasingly often pick the infants up. Infants achieve independence from their mothers, fathers, and older siblings at different rates and develop characteristically different relationships with them. Infants that are most rejected by caregivers spend the least time on them. When rejected by their parents, infants tend to spend their time with their twins, rather than seeking to climb onto other caregivers. Caregivers do not compensate for unduly large or small amounts of care given by other members of the group. It is argued that if we are to understand the development of caregiver-infant relationships in species with multiple caregivers, we must discover the rules by which infants assess the amount of care they perceive themselves to have received and caregivers assess the amount of care they perceive themselves to have offered. The implications of a simple model based on expected levels of caregiving and careseeking are explored, particularly with respect to competition and compensation.     

Maternal Time Allocation in Two Cooperative Childrearing Societies

This paper examines maternal trade-offs between subsistence/economic activities and caregiving, and it explores the effect of allomaternal investment on maternal time allocation and child care. I examine how nonmaternal investment in two multiple caregiving populations may offset possible risk factors associated with reductions in maternal caregiving. Behavioral observations were conducted on 8- to 12-month-old infants and their caregivers among the Aka tropical forest foragers and Ngandu farmers of Central Africa. Analysis demonstrates that mothers face trade-offs between subsistence/economic activities and infant care. Infants receive less investment when their mothers engage in subsistence/economic activities, indicating a potential risk to those infants. However, results indicate that allomothers target their assistance during times when mothers are engaged in work activities, partially offsetting potential risks associated with the maternal trade-off. The effects of intercultural variability on maternal time allocation and allomaternal investment are also explored as a means of examining the potential impact of their behaviors on infant care.     

Individual and group effects on early caregiver-infant relationships in red-bellied tamarin monkeys

The relationship between changes in caregiver-caregiver and caregiver-infant behaviour was studied during the infants' first month in 10 family groups of red-bellied tamarins, Saguinus labiatus, with twin infants. With infants of a given age, fathers generally spent a higher proportion of time carrying per infant than did mothers, but in most cases these differences were not significant. Mothers and fathers carried significantly more than older siblings did at the beginning and end of the infants' first month. With older infants, caregivers started to rub off infants they were carrying, so that infants started to spend some time off all caregivers. Each caregiver initiated carrying by retrieving an infant from another caregiver, and sometimes retained an infant against a retrieve attempt by another caregiver in order to continue carrying it. Before infants started to spend some time off, time spent carrying by mothers, fathers and older siblings was positively correlated with the percentage of retrieve attempts by other caregivers that they retained against, and, more strongly, with the value of their own number of retains minus the number of retains by other caregivers against them. These results indicate that competition to care for infants has a direct effect on the early development of each caregiver-infant relationship within the family group.     

The benefits of helpers: Effects of group and litter size on infant care in tamarins (Saguinus oedipus)

The Callitrichidae (marmosets and tamarins) typically give birth to twins, and infant care is shared by all group members. The potential benefits to callitrichids of having helpers were investigated in a study of 21 captive cotton-top tamarin (Saguinus oedipus) infants, living in groups with two to 12 older members. Time carried and suckled and amount of food received from other family members were recorded for each infant during the first 12 weeks of life. The results showed that infants in larger groups were carried more and received more food than those in smaller groups. Twin infants in larger families were less likely to be on the same carrier. Singleton infants were carried more than twins but did not receive more food. On average, individual caretakers in larger groups carried less and shared less food with infants than those in smaller groups. When parental contributions to care were analyzed, no effects of group size were found on mothers' contributions to carrying or food sharing, but fathers in larger groups both carried infants less and shared less food with them. There appear to be several benefits of a communal rearing system to cotton-top tamarins. 1) Infants may receive more care in larger families, thus increasing their chances of survival. 2) The burden of care is spread over several animals, reducing the costs to a given individual. 3) The parents, particularly fathers, may benefit most from reducing the costs of investing in the present litter and increasing their ability to invest in future litters.     

Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch)

The purpose of this study was to describe patterns of infant care and development in family groups of the monogamous titi (Callicebus moloch). Three infant titis were observed with their natal family groups over the first six months of life. Field observations of extensive male involvement with infants were confirmed. Adult males were clearly the infants' primary social companions, and infants spent more time in contact with adult males at all ages than with mothers or older siblings. However, mothers and siblings also carried infants at times and interacted with them in affiliative ways (e.g., grooming, nuzzling, play). Mothers often invited nursing, but otherwise it was infants who primarily initiated transfers between carriers and approaches to parents, reminding us that the infants' own activities and their effects on caregivers should not be overlooked in considerations of the patterns of infant care. This is particularly important for those species exhibiting extensive parental involvement by males. It is suggested that substantial male care of young titi infants leads to several important consequences for the infant's social development, including the development of a stronger attachment to the father than the mother.     

Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus)

Fourteen infant cotton-top tamarins from five captive family groups were studied during the first 20 weeks of life. We examined the roles of parents and of siblings of different ages as caregivers and as social companions for the infants, as well as the effects of group composition and group size on these roles. Parents and adult siblings played similar active roles in infant caregiving during the first few weeks after birth, with males showing a greater involvement than females. In groups without other offspring the two parents showed equal infant caregiving behaviour, whreas fathers carried more than mothers did in groups with offspring present. Although infants received more caregiving from males, they showed a preference for contact and proximity with their mothers. No sex differences were found in infant behaviour or in the direction of behaviour by caregivers toward infants. Twins showed greater amounts of both social and solitary play in weeks 15–20 than did singletons, and there was no effect of the number of older siblings on the amount of play shown by an infant.     

川金丝猴非母亲照料行为的影响因素及其母亲获益——以神农架川金丝猴投食群为例

灵长类社会中存在着非母亲成员(成年雌猴、青少年猴和成年雄猴)对婴儿的照料行为,即非母亲照料行为,该行为直接影响新生婴儿的存活与发育以及婴儿母亲的日常活动,是灵长类学研究领域的热点问题.本研究于2019年3月至2019年11月,采用焦点动物取样和瞬时扫描取样,探究了川金丝猴非母亲照料行为的影响因素及其对母亲活动分配的影响...     

Mother-infant relationships in bonnet macaques: Sources of variation in proximity

Family composition is an important predictor of variation in proximity among captive bonnet macaque (Macaca radiata) mothers and their infants. Infants that have several immature sisters in the group are initially more independent that infants with fewer sisters, but as they reach 6 months of age infants with several sisters become less independent than their peers. The effects of the presence of juvenile females on the relative independence of their infant siblings seem to be related to the fact that the members of families with several immature females are the targets of more aggression than are the members of other families.     

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.     

Social relations in a free-ranging troop of stumptail macaques (Macaca arctoides): Male-care behaviour I

The occurrence of male-care behaviour directed from juvenile and adult males to infants was studied in a free-ranging troop of Stumptail macaques. The study period lasted two months comprising about 140 hours of recorded observations. Infants were a focal subgroup and their interactions with older males were recorded. The following variables were examined in relationship to the sending and receiving of male-care: the infant (its age, sex, and dominance rank), older males (their age and dominance rank), and genetic ties. Infants I received more male-care than infants II and differences in the type of male-care received by infants I and II were found. Male infants received more male-care than female infants and sex differences in the type of care received were evident. No relationship was found between the infant’s dominance rank and the amount of male-care received. A substantial amount of male-care behaviour was sent to genetic kin. Two-three year olds displayed more male care than yearlings. Juveniles as a class displayed more male-care than adults. A positive association was found between the juveniles’ dominance rank and the sending of male-care. However, among the adults, the subordinate male displayed more care behaviour than the alpha male. The presence or absence of the mother was found to influence the older males’ interest in the infant. The results are discussed and compared with data available on other primate species. Supported by grants from the Behavioral Science Foundation (U.S.) and by the Mexican Institute of Anthropology.     

Physical Environmental Effects on Infant Care and Development in Captive Callithrix jacchus

Environmental enrichment may affect infant care and development in captive primates. We investigated the effects of this factor in laboratory common marmosets (Callithrix jacchus). An enriched physical environment enhanced the social activities of the marmosets and elicited a greater repertoire of behaviors, without negatively affecting the provision of infant care. In addition, infants in enriched cages displayed certain behaviors sooner than infants in non-enriched cages did, which suggests an increased developmental rate. Infants in enriched cages also ate more solid food and engaged in solitary play and exploration more than ones in non-enriched cages did. Play and exploration probably improve spatial cognition and motor skills, which, together with a higher degree of independence, may allow infants to cope better with laboratory routines and general social interactions later in life than their counterparts reared in less complex enclosures. We conclude that laboratories can significantly increase the welfare of marmosets by providing a more complex physical environment.     

Infant-caregiver interactions in common marmosets (Callithrix jacchus): Consequences of rejections and rub-offs of infants by caregivers

Interactions between common marmoset infants (Callithrix jacchus) and their fathers, mothers, older siblings and twins were examined in captive family groups. The aim was to record infants' behaviour after being rejected in their attempts to get on to caregivers and after being rubbed off by caregivers who had been carrying them. The results showed that infants' behaviour differed according to which caregiver was involved and that behaviours following rejections differed from those following rub-offs. These differences in infants' behaviour had been predicted from previous work which showed that caregivers have a limit to the amount of time they are prepared to devote to infants and that different caregivers give different amounts of care to infants of specific ages.     

The male and female perspective in the link between male infant care and mating behaviour in Barbary macaques

Infant care from adult males is unexpected in species with high paternity uncertainty. Still, males of several polygynandrous primates engage in frequent affiliative interactions with infants. Two non‐exclusive hypotheses link male infant care to male mating strategies. The paternal investment hypothesis views infant care as a male strategy to maximize the survival of sired offspring, while the mating effort hypothesis predicts that females reward males who cared for their infant by preferably mating with them. Both hypotheses predict a positive relationship between infant care and matings with a particular female. However, the paternal investment hypothesis predicts that increased matings come before infant care whereas the mating effort hypothesis predicts that infant care precedes an increase in matings. Both hypotheses are usually tested from the perspective of the proportion of matings and care that individual females engage in and receive, rather than from the perspective of the care and mating behaviour of individual males. We tested the relationships between care and mating from both female and male perspectives in Barbary macaques. Mating predicted subsequent care and care predicted subsequent mating when viewed from the male but not the female perspective. Males mainly cared for infants of their main mating partners, but infants were not mainly cared for by their likely father. Males mated more with the mothers of their favourite infants, but females did not mate more with the main caretakers of their infants. We suggest that females do not choose their mating partners based on previous infant care, increasing paternity confusion. Males might try to increase paternal investment by distributing the care according to their own instead of female mating history. Further, males pursue females for mating opportunities based on previous care.     

The costs of infant carrying in captive cotton-top tamarins

Marmosets and tamarins have a communal rearing system in which all group members help to care for the twin infants characteristic of this family of primates. Helpers are likely to incur time and energy costs by contributing to infant care. Predictions that cotton-top tamarin (Saguinus oedipus) helpers would change their behavior when carrying infants because of reduced mobility and/or a need for increased vigilance were tested in a captive colony. Tamarins carrying an infant spent significantly less time feeding, foraging, moving, or engaging in social activities such as grooming than they did when not carrying. Frequencies of scratching, autogrooming, and scent marking were significantly reduced in carriers, suggesting that their mobility was reduced. However, carriers were significantly less likely to be vigilant (measured by direction of gaze) than when not carrying. Further observations showed that carriers spent more time in concealed areas than they did when not carrying and were probably therefore adopting a cryptic strategy to reduce predation risks to themselves and to infants. These results demonstrate that tamarin helpers pay costs by carrying infants. Some possible compensating benefits are indicated.     

Contributions to infant care in captive cotton-top tamarins (Saguinus oedipus): The influence of age,sex, and reproductive status

Marmosets and tamarins are characterized by a reproductive strategy that includes twinning, and a communal rearing system in which infant care is shared among all group members, both breeders and nonbreeding helpers (often older offspring). In order to test some predictions about the extent to which different age-sex classes should invest in infants, contributions to infant carrying and food-sharing by all family members were measured in captive groups of cotton-top tamarins (Saquinus oedipus) ranging in size from 2 to 12 independent individuals. Fourteen litters were observed from birth to 12 weeks. Carrying by mothers decreased steadily over the study period, while carrying by fathers and other offspring increased for 3–5 weeks, then declined. Infants spent more time carried by siblings than by either parent, but parents did more carrying than individual siblings and, also, shared more food with infants. Older siblings contributed more care than younger siblings did. Adult sons carried infants more than adult daughters did, but immature daughters carried more than immature sons did. However, adult daughters actively offered food to infants more than any other class of helper did. These results were interpreted in the light of hypotheses concerning the reproductive and dispersal strategies of callitrichid species.     

Evidence of allomaternal nursing across one-male units in the Yunnan snub-nosed monkey (Rhinopithecus Bieti)

Background

Allomaternal nursing, common in several species of social mammals, also has been reported in nonhuman primates. However, the function of this behavior in enhancing infant survivorship remains poorly understood.

Methodology and Principal Findings

The study was conducted on a free-ranging group of the Yunnan snub-nosed monkey (Rhinopithecus bieti) in the Baimaxueshan Natural Reserve. Direct observation and ad libitum sampling were used to record allocare behavior during a 20 month field study. R. bieti exhibits a multilevel social organization in which a large single troop, consisting of over 100 individuals, is divided into many one-male units (OMUs: 6∼41). These OMUs coordinate their daily activities, and feed, forage, travel, and rest together. Here we report on one case of infant temporary adoption in which an adult female from one OMU engaged in allomaternal nursing and cared for an infant from a different OMU of the same troop. This event began when the mother and her five-month-old infant were found to became separated accidentally. The victim infant was observed staying in another OMU. Over the next several days we observed a lactating female in the new OMU to care for and nurse both her infant and the immigrant infant, who also was tolerated by and cared for by the harem male.

Conclusions and Significance

Our findings suggest that lactating primate females are primed to care for young infants and, that the misdirected parental care hypothesis may offer the strongest explanation for allomaternal nursing in R. bieti.     

Temporal and structural features of infant calls in relation to caregiving behaviour in common marmosets,Callithrix j. jacchus

The role of infants in the communal rearing system of marmosets and tamarins has received little attention although their demands may not be complied by inadequate helpers. As acoustic signalling plays an important role in their social communication, it is expected to be an effective way for infants to signal their demand for care. As a first approach, this study focussed on the use and quality of ‘tsik’ calls given by infants of common marmosets (Callithrix j. jacchus) in the context of caregiving. The acoustic and non-acoustic behaviour of a group of common marmosets were recorded during the first two weeks of the life of two infants (twins). Vocalizations were classified, and the structure of the infants' ‘tsik’ calls was quantified by measuring specific signal parameters. Infants gave ‘tsik’ calls in close temporal relation to caregiving behaviour. Specific parameters covaried with the subsequent behaviour of potential caretakers. Values of call duration, start frequency, peak frequency, and range were lower when infants' calls were followed by no reaction or an approach of group members, whereas these parameters showed higher values when followed by a transfer of infants. Our results suggest that the actual demand of infants is encoded in the variations of ‘tsik’ calls.     

Mothering Style and Infant Behavioral Development in Yunnan Snub-Nosed Monkeys (Rhinopithecus bieti) in China

Considerable variation in mothering styles is found among primate species, which may be directly related to species-typical differences in social structure, dominance style, patterns of infant development, and rates of intragroup aggression. We predicted that, as egalitarian Asian colobines, mothers of Yunnan snub-nosed monkeys (Rhinopithecus bieti) would adopt a mothering style characterized by low restrictiveness and low rejection. We followed six mother–infant dyads in a provisioned group of Rhinopithecus bieti inhabiting the Baimaxueshan National Nature Reserve, Yunnan, China, and collected 717.2 h of observational data on maternal care and infant development. In the first month after birth, infants were completely dependent on their mothers for nutrition and movement. They began to locomote clumsily during their second month of life. Mothers restricted the movements of their infants only during their first 2 mo of life. Maternal rejection occurred infrequently and never exceeded a mean of two events per hour for a given infant over any 1-mo period. Most rejections were mild, and did not result in a cessation of nursing. Infants were not weaned when they were 12 mo old. Our study offers support for the contention that females of Rhinopithecus bieti adopt a relaxed mothering style in caring for offspring during their first year of life.     

Changes in the rhesus mother-infant relationship through the first four months of life

Measurements of the course of interactions between rhesus monkey infants (Macaca mulatta) and their mothers during the infant's first 16 weeks showed changes in the tendencies of both partners to be together and apart. Referring only to the partner who was primarily responsible for an age-related change, by using a single index of responsibility for contact or proximity, was found to be an oversimplification. Maternal rejecting behaviour may have been primarily responsible for changes in the time spent apart only during the first 6 weeks. After the infants' sixth week, both partners' tendencies to be apart increased together. Infants then began to spend longer away partly to interact with social companions other than their mother. Mothers restricted and followed their infants more up to week 4, but after week 8 decreases in these measures allowed infants to spend longer away. Similarities between the time courses of the time spent apart from their mothers by rhesus infants in this study and in field studies are pointed out. The similarities seem striking partly because differences between studies that do not use confidence intervals (or standard errors) cannot be shown easily. Conflict between parent and infant occurred, but how it appears, and how significant it is in each species at each infant age, remains to be discovered.     

Mating season effects on mother-infant conflict in Japanese macaques,Macaca fuscata

The impact of seasonal mating on the mother-infant relationship during the first year of the infant's life was documented in a confined troop of Japanese macaques. During the weeks in which the mothers were being mounted, negative behaviour directed towards the infants increased. As maternal rejections and punishments escalated, the infants displayed regressive behaviour (showing signs of distress more frequently). Infants also groomed their mothers at an increased rate at this time. Behaviour that indicated increased independence did not show increases during this time. Moreover, behaviour negatively associated with independence, such as ventral contact and proximity to the mother, remained stable throughout this time period. The mother-infant relationship undergoes a period of conflict during the mating season not because the mother is weaning her infant, but because it is to her reproductive advantage to regulate the times in which the infant is allowed to suckle.