Developmental trends in mother-infant interactions in Java macaques (Macaca fascicularis) during the first ten days of life

In this study on Java macaques themain characteristics of the mother-infant relationship during infants' first 10 days have been elaborated. Early mother and infant behaviour is described and early interactions between mothers and their young have been analyzed. Observations and trend analyses of early behaviours like ventro-ventral contact behaviour, being on nipple, and explorative behaviour, make it clear that Java macaque infants play an important role in the early development of mother-infant interactions. In contrast to the rhesus and the stumptailed infant, the young Java macaque appears to develop a great variety of behaviours in its first 10 days. Whereas the infant's behaviour gains in complexity and social initiative, the mother becomes increasingly more passive and self-oriented. Early mother-infant interaction can be characterized by mutual adjustment.     

Fatal attraction: interest in infants and infant abuse in rhesus macaques.

This study investigated whether infant abuse by female rhesus macaques (Macaca mulatta) is a phenomenon specific to their own offspring or reflects a general tendency to interact negatively with infants. Several aspects of the relationship between maternal behavior, infant handling, and infant harassment were also investigated. Study subjects were 20 group-living rhesus mothers with their infants observed during the first 12 weeks of lactation. The results of this study indicate that abusive mothers are highly attracted to infants in general but that infant abuse is a phenomenon specific to their own offspring. Infant harassment is not an accidental by-product of infant handling or the result of maternal inexperience but it is likely related to reproductive competition among lactating females. Maternal behavior and infant handling may be regulated by similar proximate mechanisms, but probably have different adaptive functions and evolutionary history across the Primate order. Am J Phys Anthropol 110:17-25.     

Infant Handling and Maternal Response in Japanese Macaques

We focused on the social interactions of infant Japanese macaques (Macaca fuscata) and on the protective response of their mothers to such interactions. Infant social interactions included: received allomaternal behavior (positive infant handling), hand touch and inspection (neutral handling), and aggression (negative handling) as well as social play. Maternal protective responses included aggression to the infant's interactant and restraining or retrieving the infant. All types of social interactions as well as the maternal response to such interactions showed clear developmental variations. Frequency of infant social interactions and maternal protective responses also showed large interindividual variability. Juvenile and subadult females without maternal experience were the most frequent infant handlers. Infants received positive handling primarily from their kin, while mothers were equally protective in response to positive handling received by kin and by non-kin. Conversely, kin showed higher levels of neutral handling and their interest was more easily tolerated by mothers compared to that of non-kin.     

Growth in colony living anubis baboon infants and its relationship with maternal activity budgets and reproductive status

Early growth is of interest because it is susceptible to maternal effects and linked to fitness components for a range of species. Here we present anthropometric measurements on 23 infant olive baboons born into a captive colony in order to describe growth over the first 2 years of life, to explore maternal influences on growth, and to assess the impact of growth profiles on maternal reproduction. Six main findings emerged: 1) Infant growth rates in our colony were higher than those reported for wild populations but comparable to those observed for food-enhanced animals. 2) The ratio of infant mass to maternal mass was positively associated with reproductive parameters, such as duration of post-partum amenorrhea and interbirth interval. 3) Mothers resumed cycling and reconceived when their infants attained a relatively consistent threshold mass. 4) Infant mass-for-age was associated with maternal rank and, independently, with maternal mass such that females of high dominance rank and heavy females had relatively large infants at their resumption of cycling. 5) Low-ranking and lighter females had longer investment periods but smaller infants. They continued investment in infant through prolonged lactation until their infants reached a mass similar to that of infants of high-ranking/heavy mothers, suggesting that the lengthening of investment is essentially compensatory for slow early growth. 6) There was no relationship between infant growth and maternal activity budgets. Maternal physical and social factors, not energetics, contributed to differences among infants in growth trajectories, and infant growth temporally influenced successive reproductive events.     

Control of nipple and body contact by mothers and infants in rhesus macaques.

While 3-month-old infant rhesus macaques (Macaca mulatta) were awake and active in social interactions away from their mothers, body and nipple contacts with their mothers were nevertheless made from time to time. In each dyad the proportions of contacts made by the mother nearly equalled those broken by her, suggesting a meshed interaction in which each partner accepted most of the other's contact initiations and terminations. Passive prevention of nipple contact by a mother reduced the frequency of nipple contact by her infant in the first 5 s after the infant had made body contact. Passive prevention occurred after fewer than 1 in 6 body contacts initiated by infants, and--even without its occurrence--most infants were less ready to take the nipple after their own initiatives than after maternal initiatives. Once nipple contact had been made, the probability of breaking body contact was reduced. The role of maternal rejection both in the control of nipple contact in the short term and in determining (through its effect on the sucking pattern) whether the mother gives birth in the next birth season or later is discussed. We suggest that, by the age of 3 months, the infants had already learned when and how often nipple contact with their mothers would be acceptable during their awake and active periods, and we suggest that subsequent decreases in the frequency of nipple contact were partly the results of maternal rejections which were accepted by the infants.     

Maternal antibodies against tetanus toxoid do not inhibit potency of antibody responses to autologous antigen in newborn rhesus monkeys

Background

Our previous study suggested newborns have competent immune systems with the potential to respond to foreign antigens and vaccines. In this study, we examined infant immune responses to tetanus toxoid (TT) vaccination in the presence of maternal antibody to TT.

Methods

We examined changes in plasma levels of tetanus toxoid‐specific IgG1 (anti‐TT IgG1) in a total of eight infant rhesus macaques from birth through 6 months of age using a commercial Monkey Anti‐TT IgG1 ELISA kit.

Results

A significant correlation between anti‐TT IgG1 levels in vaccinated dams and their paired newborn infants was detected in control (non‐vaccinated) infants as previously reported. Maternal anti‐TT IgG1 levels declined rapidly within 1 month of birth in non‐vaccinated infants (n=4). In four infants vaccinated with TT at birth, we found two had rapid and robust antibody responses to vaccination. Interestingly, the other two first showed declining TT antibody levels for 2 weeks followed by increasing levels without additional vaccine boosts, indicating all four had good antibody responses to primary TT vaccination at birth, despite the presence of high levels of maternal antibodies to TT in all four infants.

Conclusions

Our data indicate that newborn macaques have competent immune systems that are capable of generating their own primary antibody responses to vaccination, at least to tetanus antigens. Maternal antibodies thus do not significantly impair antibody response to the vaccination, even when received on the day of birth in infant rhesus macaques.     

Early maternal recognition of offspring vocalizations in rhesus macaques (Macaca mulatta)

This study investigated the development of maternal recognition of infant calls in rhesus macaques (Macaca mulatta). Fifteen mothers and their offspring, of age ranging from several hours to 28 days, served as subjects of an experiment in which the offspring's distress vocalizations were recorded and then played back to their mothers simultaneously with those of an age-matched control infant. The proportion of time looking at, but not the proportion of orientations to the speaker playing the offspring's vocalizations increased significantly as a function of infant age. Specifically, mothers of infants older than 1 week of age responded longer to the playback of their own infant's calls than did mothers of younger infants. These findings provide the firt evidence that offspring recognition in macaques develops between the first and second week of the infant's life and are consistent with the hypothesis that mothers need to be exposed to their infants' calls in order to learn their acoustic characteristics.     

Neonatal nipple preference and maternal cradling laterality in wild Taihangshan macaques (Macaca mulatta tcheliensis)

Lateralized behavior is considered an observable phenotype of cerebral functional asymmetry and has been documented in many mammalian species. In the present study, we examined evidence of lateralization in neonatal nipple contact, maternal cradling, and the relationship between these two behaviors during the first 12 weeks of life in wild Taihangshan macaques (Macaca mulatta tcheliensis). The results showed that across our sample of nine mother–infant dyads: (1) Seven of nine neonates exhibited a significant left-side nipple preference during the first 12 weeks of life, whereas eight of nine mothers displayed a significant right-side cradling preference; (2) at the population level, there was a significant preference for left nipple contact by neonatal Taihangshan macaques and a significant right-hand maternal cradling preference; (3) at the population level, there was a nonsignificant negative correlation between neonatal nipple preference and maternal cradling bias; and (4) the strength of individual neonatal nipple preference and maternal cradling laterality were not correlated. We conclude that asymmetry in nipple contact of Taihangshan macaques occurs early in behavioral development. Given that infant Taihangshan macaques are able to nurse and cling unassisted to their mothers within a few days after birth, it appears that the infant rather than its mother is responsible for determining a nipple-side preference. Our results indicating a left-side nipple bias in 78% of wild neonatal Taihangshan macaques are most consistent with the heartbeat hypothesis.     

Modeling the effects of maternal nutritional status and socioeconomic variables on the anthropometric and psychological indicators of Kenyan infants from age 0-6 months

This paper presents a comprehensive empirical analysis of the factors affecting growth and psychological development of over 100 infants from birth to age 6 months in the Embu region of Kenya. The analysis was divided into four parts. First, infants' birth weight, and length and head circumference as measured few days after birth, were modeled using multiple regression models. Maternal prepregnancy body mass index (BMI), gestation period, and parity were associated with infants' anthropometric measurements (P < 0.05). Second, the scores on seven clusters of the Brazelton Neonatal Behavioral Assessment Scale were explained by health and socioeconomic indicators. While the models had poor predictive power, the scores were comparable to those reported in the literature for Puerto Rican and African American infants. The third part of the analysis modeled infant growth between 1-6 months by analyzing longitudinal data on length, head circumference, and weight. Dynamic models were postulated for the effects of nutritional, socioeconomic, and environmental factors and morbidity on anthropometric variables. The results showed that infants' calcium intakes were positively associated with length (P < 0.05). Maternal BMI and hemoglobin concentration were positively associated with infant weight (P < 0. 05); infant morbidity was negatively associated with weight (P < 0. 05). Lastly, the infants' scores at 6 months on the Bayley Motor Scale and on eight items from the Bayley Infant Behavior Record were explained using anthropometric, socioeconomic, and psychological variables. The infants' arm circumference and intake of protein were significant predictors of scores on the Bayley Motor Scale. In addition, time spent by the mother talking to the infant was positively associated with the scores on the Bayley Infant Behavior Record. The empirical results have implications for identifying vulnerable children in developing countries.     

Change of nipple preference between successive offspring in Japanese macaques

Selective use of nipples among free-ranging infant Japanese macaques (Macaca fuscata) was studied. Each infant held only one of its mother's two nipples in the mouth during an average of 90.9% ± 1.5% (SEM) of total nipple contact time. The next offspring born to the same mother tended to use the nipple that its previous sibling had not used. Maternal behavior did not cause use of one nipple or the other.     

Species differences in the interest shown in infants by juvenile female macaques (Macaca radiata andM. mulatta)

Using a focal animal technique, 16 juvenile female rhesus and bonnet macaques (2–3 years old) were observed with respect to the frequency and duration of their contacts with infants (0–1 year old). Each of these subjects was a member of one of four seminatural groups of macaques housed in 0.5-acre field cages at the California Primate Research Center. Rhesus juvenile females became very interested in infants when the latter were quite young, and maintained that interest throughout the study. When the infants were approximately 3–4 months old, the rhesus juveniles spent, on the average, 3.9 min/hr with those infants. By the time the infants were yearlings, the time spent with infants was approximately 6 min/hr. Relative to the rhesus, the bonnet juveniles showed less interest (about 2.2 min/hr) in young (3- to 4- month-old) infants, although by the time the infants were yearlings, the bonnets spent about 5.6 min/hr with them. Rhesus juveniles preferred sibling over nonsibling infants, but the presence of a sibling was not a necessary requirement for infant-directed behavior. The two bonnet juveniles who had infant siblings showed no preference for the latter. These data were interpreted within the framework of Quiatt’s [(1979) Am. Anthropol. 81: 310–319 conclusions about allomaternal behavior. Specifically, it was argued that, to the extent that there are species differences in maternal behavior, there should also be species differences in allomaternal behavior. The species differences in the maternal styles of rhesus and bonnet macaques provide a basis for an examination of this hypothesis.     

Ecological constraints on the development of infant independence in rhesus

Mother-infant dyads were observed among three populations of rhesus monkeys (Macaca mulatta) in India and Nepal. This research had three purposes: 1) to examine the influences of maternal activities (ie, feeding, locomotion, and rest) and arboreality on the early development of infant independence; 2) to determine whether interpopulation differences in the development of infant independence can be accounted for by correlated differences in maternal time budgets and the amount of time infants spent on the ground; and 3) to explore how patterns of maternal care may or may not mitigate increased risk of infant mortality resulting from human harassment. Despite significant interpopulation differences in maternal time budgets, the amount of time infants spent on the ground, and the degree of harassment the animals experienced, few interpopulation differences in infant development could be found. The application of a multiple regression/ correlation analysis revealed that the development of infant independence was affected by the above factors but that those factors were acting in complementary ways to constrain development and to minimize the differences across populations.     

Do young rhesus macaques know what others see?: A comparative developmental perspective

Humans undergo robust ontogenetic shifts in the theory of mind capabilities. Are these developmental changes unique to human development or are they shared with other closely related non-human species? To explore this issue, we tested the development of the theory of mind capacities in a population of 236 infant and juvenile rhesus macaques (Macaca mulatta). Using a looking-time method, we examined what developing monkeys know about others’ perceptions. Specifically, we tested whether younger monkeys predict that a person will reach for an object where she last saw it. Overall, we found a significant interaction between a monkey's age and performance on this task (p = .014). Juvenile monkeys (between two and 5 years of age) show a nonsignificant trend towards human infant-like patterns of performance, looking longer during the unexpected condition as compared to the expected condition, though this difference is nonsignificant (p = .09). However, contrary to findings in human infants, infant rhesus macaques show a different trend. Infant monkeys on average look slightly longer on average during the expected condition than the unexpected condition, though this pattern was not significant (p = .06). Our developmental results in monkeys provide some hints about the development of the theory of mind capacities in non-humans. First, young rhesus macaques appear to show some interest in the perception of other agents. Second, young rhesus seems able to make predictions based on the visual perspective of another agent, though the developmental pattern of this ability is not as clear nor as robust as in humans. As such, though an understanding of others’ perceptions is early-emerging in human infants, it may require more experience interacting with other social agents in our non-human relatives.     

Primigravidity,body weight,and costs of rearing first offspring in rhesus macaques

Body size is associated with menarche and ovarian function, but the relationship to first conception is rarely examined. We conducted a longitudinal investigation of rhesus macaques, Macaca mulatta, to determine the effect of differences in body weight on both the age at first conception and survivorship of first progeny. Young females who became pregnant weighed significantly more than peers who remained barren, with weight changes for females who successfully raised offspring no different than those for females who did not produce offspring. Infant mortality among primiparae was not significantly greater than that among multiparae, although nearly twice as high. First-born males tended to have lower survivorship than first-born female offspring. We suggest that reproductive costs encountered by primiparous females are more likely to be modulated by immature neuroendocrine function than by inexperience, small body size, or infant suckling patterns. We conclude that body size influences probability of first conception, socioendocrine factors mediate the likelihood of infant survival, and primiparous production of male progeny seems to exert a greater reproductive cost than does production of female progeny. Am. J. Primatol. 46:135–144, 1998. © 1998 Wiley-Liss, Inc.     

Hormonal Correlates of Maternal Style in Captive Macaques (Macaca fuscata and M. mulatta)

Previous studies on nonhuman primate maternal styles showed that variation in infant-directed behavior falls along two dimensions, traditionally labeled as protectiveness and rejection. We investigated maternal styles in rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques living in analogous captive social groups, and correlated them with the levels of estrogen metabolites excreted in female feces during the perinatal period. We focally observed mother-infant pairs 3 hours per week during the first 12 weeks of infant life. We collected fecal samples twice a week from each mother, starting 4 weeks before delivery and ending 4 weeks after delivery. Three significant components were extracted by principal component analysis from 15 different infant directed behaviors, each reflecting a different aspect of mothering style: rejection is correlated with behavioral measures of maternal opposition to contact; protectiveness is correlated with maternal solicitude; and independence is correlated with time in contact, grooming and cradling. Levels of estrogen metabolites are significantly correlated to rejection but not to protectiveness or independence, indicating that, in nonhuman primates, individual endocrine changes related to maternal behavior might specifically affect the timing of contact interruption.     

Peer-rearing influences subsequent maternal behavior and infant survival in a newly formed herpes B-virus negative rhesus macaque group

The maternal behavior of primiparous rhesus macaques (Macaca mulatta), peer-reared since 1/2 years(s) of age as part of aHerpesvirus simiae (herpes B-virus) screening protocol, was examined and compared to a control group of conspecifics reared in their natal group. Infant survival was significantly higher in control groups as compared to the test group, a result attributed to the high incidence of infant kidnapping/abandonment in the test group. Among the test subjects, infant survival rate increased as the birth season progressed, thus it is possible that exposure to mothers/infants helped in the maternal success of those females who gave birth later in the season. Test group infants were touched by group members significantly more than the infants of control subjects, whereas these infants were groomed by their mothers and in a ventral position for a greater time relative to the infants of the test subjects. This study suggests that females, partially reared in peer groups, may be at early risk for maternal incompetence and consequent greater infant mortality, and that exposure to mother-infant dyads may augment the proficiency of maternal skills.     

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 development of behavioural sex differences in infant rhesus macaques (Macaca mulatta)

Studies of infant rhesus macaques have generally reported sex differences in the frequency of expression of some behaviour patterns, such as rough-and-tumble play and socio-sexual mounting. In contrast, sex differences in other behaviour patterns, such as proximity to the mother, have been less consistantly reported. Using data on the behavioural development of infant rhesus macaques living in captive social groups, we have attempted to provide further evidence for, or against, sex differences in behaviour and to investigate the possible influence of maternal rank and parity on sex differences in infant behaviour and mother-infant interactions. The behaviour of 14 male and 20 female infants and their mothers was studied during the first six months of life, including measures of play behaviour socio-sexual mounting, and mother-infant interactions. Our data reveal that, on average, male infants exhibited more rough-and-tumble play and mounting than female infants, and also exhibited stationary play, chasing play, and initiated play more frequently than females. Such sex differences appear to be robust in macaques and have been reported in a variety of housing conditions. male and female infants did not differ in the amount of time spent at particular distances from their mothers, and mothers were not found to behave differently towards sons and daughters, using measures of restraint, rejection, and grooming. These results are in contrast to previous studies on singly-housed mother-infant pairs but similar to those on free-ranging populations. Mothers did behave differently towards their infants depending upon the mother's rank and previous number of offspring. These maternal characteristics may have significant consequences for the behavioural development of both male and female infant primates.     

Effects of nonmaternal restraint on the vocalizations of infant rhesus monkeys (Macaca mulatta)

This study explored the effects of restraint by females other than the mother on the vocalizations of infant rhesus macaques (Macaca mulatta) in a captive social setting. In this species, females are very attracted to young infants and will frequently approach, groom, and hold the infant. Incompetent handling, abusive behavior, or extended periods away from the mother that prevent the infants from nursing represent potentially significant risks for infants. Vocal responses to such risky conditions appear to be the infants' only means to promote a return to their mothers. We examined the association between the severity of the threat posed to the infant and the nature of its vocal response to restraint, and whether the infants' calls influenced the behavior of their mothers or captors. The results suggest that situations posing greater risks for the infants, i.e., longer periods of restraint, were associated with a greater use of noisy screams. Furthermore, mothers' responding was associated with a greater use of noisy screams as well. The mothers' reactions, however, could be described as cautious, and consisted mostly of closer monitoring; such tempered response might be related to the risk of injury to the infant that could result from a more forceful and direct attempt at retrieval.