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.     

Infant cradling in a captive mother gorilla

The purpose of the study presented here was to investigate the handedness and cradling preferences of a mother gorilla (Gorilla gorilla) from the Metro Toronto Zoo. The study also examined preferences for handedness for each member of the captive group. Observational data were collected using scan sampling at 60‐sec intervals. Handedness was determined with a coordinated bimanual tube test using peanut butter spread on the interior of a PVC tube. Our findings were largely consistent with the literature on laterality in African apes by documenting a left‐side cradling bias for one apparently ambidextrous captive gorilla mother. This bias was associated with a left head positioning preference by her infant. Although based on a single mother/infant pairing, this study indicates that cradling bias is not always determined by maternal handedness. Zoo Biol 27:420–426, 2008. © 2008 Wiley‐Liss, Inc.     

秦岭川金丝猴雌性携抱偏好与婴儿吸乳偏好

为了揭示婴儿吸乳偏好以及母猴携抱偏好发育过程,对具有不同生育背景的出生一周的婴儿吸乳偏好和母亲携抱偏好进行了研究。采用扫描取样法,对32 对母婴(7 个初次生育雌性及其婴儿,25 个多次生育雌性及其婴儿)的雌性携抱婴猴偏好行为,及其婴猴的吸乳偏好行为进行了记录。经对比和相关分析检验,结果显示,初次生育雌性的婴儿在吸乳时出现群体水平上的左侧偏好(t₍₆₎ = - 3.731,P = 0.010),再次生育雌性的婴儿没有出现群体水平的吸乳偏好(t₍₂₄₎ = 0.854,P = 0.402);初次生育的雌性会出现群体水平上的左侧携抱偏好(t₍₆₎ = - 3.890,P = 0.008),再次生育的雌性没有群体水平的偏好方向存在(t₍₂₄₎ = 1. 955,P = 0.062);同母婴儿绝大部分(8/9)会出现相反方向的吸乳偏好(N1 = 8,N2 = 1,P = 0.039)。这表明,再次生育经历会影响秦岭川金丝猴新生婴儿的吸乳偏好进而影响雌性的携抱偏好。     

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.     

First wild evidence of neonate nipple preference and maternal cradling laterality in Old World monkeys: a preliminary study from Rhinopithecus roxellana

Although captive or free-ranging settings offer a more controlled environment for assessing non-human primate laterality, research on wild populations provides evidence of how laterality is affected by natural environmental conditions and, thus may yield potential insights into the evolution of laterality. This study of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) constitutes the first report on asymmetric patterns of early mother-infant interactions among Old World monkeys in the wild. It was found that neonate nipple preference and maternal cradling laterality are both evident on the individual level. Although there is no significant group-level preference direction, the group preference strength on both measures is evident. Moreover, neonate nipple preference is not significantly correlated with maternal cradling laterality on either LBI scores or the direction (LBI scores: r=0.174, p=0.632; direction: r=0.624, p=0.054). Taken together, it is possible to suggest that wild R. roxellana show independent orientation laterality from the first week of life.     

非人灵长类动物雌性携抱婴儿与婴儿吸乳偏好的研究进展

灵长类雌性动物在携抱婴儿时会表现出一种方向偏好,同时,婴儿在吸乳时也会表现出方向偏好.相关研究表明,这两类偏好与灵长类大脑不对称性及其功能的进化有着极其紧密的联系.此方面的研究作为灵长类偏好行为研究的重要关注点之一,在国外已得到了较好的发展,在国内尚处于萌芽阶段.由于多种影响因素的存在,非人灵长类已有的研究结果间存在一定差异.     

Scan and focal sampling: reliability in the laterality for maternal cradling and infant nipple preferences in olive baboons, Papio anubis

We compared measures of laterality obtained by two observational sampling procedures (a 15-min focal-dyad sampling with continuous recording, and a scan and instantaneous sampling), using 10 mother-infant dyads of captive olive baboons. The two measures of lateral biases for maternal cradling, infant nipple preference, infant head position and maternal carrying, but not those for infant retrieval, were positively and significantly correlated. Our results clearly show that the two sampling procedures produce equally sensitive measures of lateral bias for both the maternal and the infant behaviours. They also provide evidence of asymmetries in mean bout length and therefore suggest that recording bouts is not necessarily the best measure of lateral bias. Taken together, these results show empirically that the scan and instantaneous sampling procedure does not lead to a lack of independence of data points, as previously assumed.     

Mother-infant interactions of wild-born,individually-caged cynomolgus monkeys (Macaca fascicularis) during the first 14 weeks of infant life

This study documents age-related changes in the interactions of wild-born cynomolgus macaque mothers and their infants living in individual cages during the first 14 weeks of infant life. Body contact between mother and infant, maternal holding, and infant sucking were found to decrease, and the mothers showed an increased frequency of aggression toward their infants with age. These results were broadly similar to those reported for mother-infant interactions in other macaques living in social groups. Nevertheless, a clear difference between the present cynomolgus macaques and other macaques in social groups was apparent. The cynomolgus macaque mothers tended to permit their infants to move about freely without displaying maternal protectiveness such as restraint or retrieval, unlike other macaque mothers in social groups. Such maternal behaviors might derive from the experience of living in individual cages for many years and the relative safety of living in individual cages. The lack of maternal restraint and retrieval could be responsible for the observed sex differences in behavior: male infants moved more actively, and broke, and made contact with their mothers more frequently than did female infants. Moreover, mothers of female infants held and groomed them more frequently and were less aggressive toward them.     

Laterality in Maternal Cradling and Infant Positional Biases: Implications for the Development and Evolution of Hand Preferences in Nonhuman Primates

Left-sided maternal cradling has been widely reported in human populations. In this paper, I review the evidence of laterality in maternal cradling and infant positional biases in non-human primates. The review revealed some evidence of population-left sided cradling in great apes but little consistency in bias was found among Old and New World monkeys. Very little data have been reported in prosimians. I further describe how asymmetries in either maternal cradling or infant positional biases may explain individual and species differences in hand preference.     

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.     

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.     

Effects of six-day maternal separation on tonkean macaque infants

Maternal separation may induce a depressive state in infant macaques. However, this does not occur in all macaque species. From present hypotheses, it may be predicted that infants belonging to a species characterized by open and tolerant social relationships should not develop severe depressive symptoms. Tonkean macaques (Macaca tonkeana) stand as such a species. The goal of the study was to verify that the infant’s reaction to mother loss is related to the social environment. The mothers of eight 5- to 9-month-old infants were removed during 6-day experimental periods. Infants’ behavior was characterized by a mild initial protest stage, followed by a slight decrease in activity during later maternal separation, and quick recovery after the mother’s return. No despair stage occurred. During separation, group members compensated for mother’s absence by cradling the infants. That social networks determine the intensity of the infant’s response to separation has far-reaching implications with regard to the meaning of depression occurrence within social networks.     

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.     

Ear asymmetry and left-side cradling

Women and girls tend to cradle infants and dolls on the left side of the body. Left-sided cradling is found in chimpanzees and gorillas, is cross-cultural and present in historical works of art, and is transmitted down the human maternal line. One explanation for the left-cradling tendency is that it facilitates the flow of affective information from the infant via the left ear and eye to the center for emotional decoding, that is, the right hemisphere of the mother. We show that the developmental stability of the ear, as measured by ear asymmetry, is negatively correlated with the left-sided cradling tendency. Left-cradling English women holding infants and Jamaican girls holding dolls had a strong tendency to show lower ear asymmetry than right cradlers, whereas no such relationship was found in boys nor for various measures of asymmetry of the hand, with the possible exception of the wrist in Jamaican girls. Degree of handedness, as measured by the Annett peg-moving test, did not predict cradling preference in the Jamaican children, and the relationship between ear asymmetry and cradling preference was independent of hand preference. Our results suggest that developmental instability of the ear (including the pinna, external auditory meatus, and middle ear) may interfere with the flow of affective information to the right hemisphere. Ear asymmetry also showed evidence of strong maternal but not paternal transmission. It is suggested that between-individual variation of in utero stress may explain patterns of maternal transmission of lateral cradling tendencies.     

Infant development in the lion-tailed macaque,Macaca silenus (Linnaeus): The first eight weeks

Infant development in lion-tailed monkeys was observed during the first eight weeks after birth. A rapid decrease in the time spent in the closest association by the mother and the infant was seen between the first and second weeks. Between the second and fifth week there was a somewhat steady state with only marginal decrease in the time spent by the infant out of lap of the mother. However, during this time, a rapid decline in maternal cradling and restraining behaviour was seen. From the sixth week onwards, there was a rapid increase in the time spent by the infant out of contact with the mother. Independence of the infant during troop progression was seen only towards the eighth week, that too only marginal. Among the troop members the subadult females and the juvenile females showed the maximum interest in the infant. The former spent much more time than the juveniles interacting with the infant. The adult females showed only little interest in the infant while the adult male showed no interest at all. Infant snatching by subadult females and juvenile females was seen on many occasions. The infant remained in the possession of them from less than 1 min to more than 2 hr. This behaviour tended to decrease towards the sixth week.     

Explaining variation in maternal care in a cooperatively breeding mammal

Because of the necessity of lactation, mammalian mothers must perform at least a minimum amount of infant care. In cooperatively breeding species, other group members aid in all other aspects of infant care. However, some mothers continue to carry and nurse their infants more than others. The golden lion tamarin, Leontopithecus rosalia, is a small, communally breeding primate in the family Callitrichidae. We studied hormonal, individual, historical and social factors hypothesized to contribute to variation in levels of maternal care. We used neonatal weight as a measure of prenatal care, and carrying and nursing as measures of postnatal care. Greater neonatal weight was associated with smaller litter size, lower prepartum levels of oestrogen conjugates, and higher prepartum cortisol levels. Higher rates of carrying during weeks 2 and 3 were associated with higher maternal weight, larger litter size and smaller numbers of helpers per infant. Higher rates of nursing in weeks 2 and 3 were predicted by smaller group size and provisioning of the mother. The most important factors affecting postnatal maternal care were maternal weight, group size, litter size and provisioning status of the mother. Thus, females that display higher levels of maternal care do so either because they have to (they have fewer helpers) or because they can (they are in better condition).     

The social behavior of adult male-infant pairs of Rhesus macaques in a laboratory environment

Adult males in nonhuman primate societies exhibit a wide range of behaviors toward immature members of their social group, ranging from virtually continuous nurturance to systematic infanticide. Among macaques, rhesus monkey males in the wild display perhaps the least degree of paternalistic behavior toward conspecific infants. But adult male-infant rhesus attachments have not as yet been explored in a controlled longitudinal study, even though the mother-infant bond has received careful attention for several decades. In the present study two pairs of adult male and infant rhesus macaques were housed together without the mother for a period of at least seven months. To minimize the probability of physical harm to the infants, one adult male was present at the birth of the infant with whom it was paired and the other was visually familiarized with the infant for several weeks before being paired with it. Both pairs have shown much less ventral-ventral contact than mother-infant pairs and the infants have rarely attempted to gain nipple contact. The female infant now initiates and maintains ventral-ventral contact much more frequently than the male infant in spite of the higher degree of aggression directed toward her by the male. The adults frequently groom their infants and exhibit varying degrees of both tolerance and aggression. Rough-and-tumble play appeared quite early in both pairs and is much more vigorous than mother-infant play. Recently the male-male pair has exhibited reciprocal mounting and thrusting. Comparisons are made with data obtained in an earlier study of mother-infant pairs conducted under nearly identical experimental circumstances. The effects of separating the adult males and infants at seven months are also described.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

Male-infant relationships in semifree-ranging Barbary macaques (Macaca sylvanus) of affenberg salem/FRG: Testing the “male care” hypothesis

The infant-directed behavior of Barbary macaque males was analyzed in order to determine whether it is essential for an infant's survival during the first year and whether males interact selectively with closely related infants. Dyadic male-infant contacts were recorded in a large group of semifree-ranging Barbary macaques. Data collected during the first 12 weeks of life on each infant born in 1983 (n = 36) were analyzed. All adult and almost all subadult males established strong relationships with at least one infant. Almost two-thirds of the infants (22) had frequent contacts with one or several males. Males showed no preference for closely related infants. Sexual associations with an infant's mother during the preceding mating season had no significant effect. Natal males did not prefer infants of their own matrilineage. There was no evidence that contacts with males had a positive influence on infant survival or that other benefits to the infants resulted from these contacts. Instead, excessive carrying by males and females led to starvation of some very young infants and was a major cause of neonatal deaths in this population. Males interacted preferentially with infants that were born early in the birth season, had a high-ranking multiparous mother, and were male. Younger males established strong relationships with male infants only, while mother's rank was more important for older males. It is suggested that certain mothers prevented early contacts between their infants and males so that the observed preferences for certain infants were also a result of easier access to them. All results suggested that males interacted with infants for their own benefit.