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.     

Parity-related differences in suckling behavior and nipple preference among free-ranging Japanese macaques

Suckling behavior of primiparae in free-ranging Japanese macaques (Macaca fuscata) was compared with that of multiparae at Jigokudani Monkey Park, the Shiga Heights, Nagano Prefecture, Japan, from April 1984 to June 1994. The estimated rates of milk secretion in a single preferred nipple among primiparae were lower than those among multiparae from birth to 5 months of age. Milk secretion capabilities of primiparous mothers, hence, appear to be inferior to those of multiparous mothers. In nutritive sucking, although Japanese macaque infants preferred one single nipple, nipple preferences in primiparae were weaker than those in multiparae. With supplementary two-nipple use during sucking, however, the infants of primiparae appear to overcome a suckling flaw of their primiparous mothers. After infants were 5 months of age and after a drop (from approximately 10% to approximately 5%) in the rates of milk secretion, however, milk secretion rates in a single preferred nipple among primiparae were similar to those in multiparae and the supplementary two-nipple use in primiparous mother-infant dyads disappeared. Am. J. Primatol. 42:331–339, 1997. © 1997 Wiley-Liss, Inc.     

Nipple contact in captive black-faced chimpanzees (Pan t troglodytes [Blumenbach, 1779])

Three chimpanzee (Pan t troglodytes) mother-infant dyads were studied from months 3 to 11 of the infants' lives in order to obtain data on nipple contact. Three conclusions were obtained: (1) There were fluctuations in the time spent in nipple contact. (2) Both female offspring were in nipple position for less time than the male offspring. (3) Grooming of the infants by their mothers during nipple contact was observed more frequently in the mother-female offspring pairs.     

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.     

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.     

Development of infant twin Japanese monkeys (Macaca fuscata) in a free-ranging group

The behavioral development of infant twin Japanese monkeys in a free-ranging group during the first 12 months of life was reported and compared with that of single born infants. There were no clear differences in mother-infant interactions toward either twin or single infants, but the twins showed a clear nipple preference. The twins spent much time in contact with and proximity to each other and as their interactions were peaceful no dominance relations between them were assumed. Each twin interacted with other infants and juveniles less frequently than did the single infants.     

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。     

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.     

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.     

MOTHER-INFANT SPATIAL RELATIONS IN CAPTIVE BOTTLENOSE DOLPHINS,TURSIOPS TRUNCATUS

The prolonged nursing period and strong, extended mother-infant bond observed among bottlenose dolphins may reflect social and physical ontogeny critical for infant survival. This study was conducted to quantify ontogentic changes in mother-infant contact time and the amount of time infants spent in specific spatial states with their mothers from birth to age 12 mo. These behaviors were studied through a systematic, longitudinal study of six mother-infant pairs of captive bottlenose dolphins from three different social groups. There was a significant decrease in the time infants spent with their mothers (logistic regression, P < 0.001), following the general mammalian pattern of increasing independence with age. When with their mothers, the probability that infants would be found in “echelon” position, flanking the mother, decreased as the calf aged (logistic regression, P <0.001), possibly due to anatomical and hydrodynamic factors. The probability that infants would be found in “infant” position, underneath the mother, increased with calf age (logistic regression, P < 0.001). Results obtained in this study are consistent with similar studies of wild bottlenose dolphin mother-infant pairs, indicating a suite of ontogenetically comparable behaviors between wild and captive bottlenose dolphins.     

Discrimination of mother by infant among Japanese Macaques (Macaca fuscata)

Experiments on five mother-infant pairs of Japanese monkeys (Macaca fuscata)living together in a captive group were conducted during the first 12 weeks after birth in order to assess the time at which infants begin to discriminate their own mothers from other adult females. After removal from their social group, infants exposed to their mothers and three unfamiliar adult females at a distance of 150 cm failed to orient visually toward their mothers. However, when the infants were allowed to approach the four females, they responded preferentially to their mothers during the third month of life. We concluded that by 8–12 weeks of age, infant Japanese macaques are able to discriminate between their mothers and other adult females.     

Factors influencing nursing in Macaca fascicularis.

Nursing by two mother-infant pairs in a caged colony of Macaca fascicularis was monitored at 1-min intervals for 8 h beginning 8:30 a.m. BST, once a week for 3 months in the summer of 1973. Nursing occupied about 210 min in 8 daylight hours for the infants at 10 weeks of age, and the time spent nursing decreased at the average rate of 9.4 min per week until the infants were about 6 months old. The time spent nursing by the infants studied here resembles closely the times spent nursing by some other macaques and by baboons. In the course of a day the amount of time spent nursing varies significantly with a diurnal peak. If nursing by one mother-infant pair is independent of nursing by the other pair, then the time the two pairs spend nursing together would be a function of the product of the frequencies of nursing by each pair. The expected times for the pairs nursing together based on the hypothesis of independent events were significantly less than the observed times the pairs nursed together. Nursing, therefore, involves a positive influence or imitation of one nursing pair by the other. Nursing sessions involving both mother-infant pairs were longer on the average than sessions involving only one pair.     

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.     

Weaning Age,Infant Care,and Behavioral Development in <Emphasis Type="Italic">Trachypithecus leucocephalus</Emphasis>

Primate infants are born in an altricial state and rely on the care of their parents for a relatively long period of time. Parental investment is critical to offspring survival and thus to the reproductive success of the parent as well. However, mothers and infants may experience a conflict of interest, in that infants may benefit by receiving prolonged maternal care but mothers may curtail such care in a tradeoff between investment in current versus future offspring. Documenting life history characteristics, such as age at weaning, is important not only for understanding the conflicts of interest and tradeoffs; such information can also provide insights about female reproductive rates and be valuable for conservation efforts. Little is known about the life history of white-headed langurs (Trachypithecus leucocephalus), despite their endangered status. We were the first to investigate mother-infant relationships and infant behavioral development in the species. We studied 3 wild mother-infant pairs throughout infancy. We used data from >460 h of focal subject sampling to calculate the proportion of time individuals spent in different behavioral states and the frequency of instantaneous events, such as maternal rejection. White-headed langur infants depended on their mothers for 19–21 mo, at which time they were weaned. Maternal rejection facilitated infant independence in the early stages of infant development, and mothers stopped investing in their infants when they resumed estrus. The weaning age of the wild white-headed langurs we studied was dramatically longer than that of captives, possibly as a result of the nutritional differences between wild and captive populations. Weaning age was also longer than for most other Asian colobines, and may be attributable to the degradation and fragmentation of their natural habitat.     

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.     

神农架川金丝猴投食群的母婴关系

灵长类动物母亲的育婴行为不仅对后代的存活起着关键作用,而且对婴猴的发育和成年后的社会交往有着重大影响,因此母-婴关系一直是灵长类学研究的热点之一。为了解川金丝猴的母-婴关系,探讨川金丝猴母-婴关系个体差异的影响因素,我们于2013年3月至2014年10月,以母-婴间相对距离表示照料强度,对神农架川金丝猴的母-婴照料关系以及母亲照料强度个体差异的影响因素进行了定量研究。结果表明：母亲照料行为强度、母亲对阿姨行为的容忍与婴猴年龄相关,限制行为与婴猴年龄不相关。身体接触与婴猴年龄不相关;腹部接触以及母-婴相对距离小于1 m与婴猴年龄呈负相关;相对距离1 m至5 m、相对距离5 m至10 m和相对距离大于10 m与婴猴年龄呈正相关;母亲对阿姨行为的拒绝与婴猴年龄呈负相关;母亲对婴猴的限制行为与年龄不相关。总的来说,即随着婴猴成长,母婴间距离越来越远,母亲也逐渐减少对婴猴的保护。母亲的生育经验、婴猴性别、婴猴出生先后和社会单元大小对神农架川金丝猴母婴关系没有显著影响,补食群丰富的食物资源和群内雌性友好的关系可能是导致本结果的原因。     

Development of behaviors in a male spectacled langur (Presbytis obscurus)

An infant langur,Presbytis obscurus, was observed in a group setting, from birth until 1 year of age. Frequency or duration of 30 behaviors was recorded during 2 hour periods and plotted chronologically. Based on fluctuations and interrelations of these behaviors, age classes were designated. The Maternal Care Period (0–20 days) is characterized by close mother-infant contact, including a great deal of nipple contact and a high frequency of maternal behaviors. The Individuation Period (21–70 days) is typified by maternal restraint and retrieval, and independence and self-oriented behaviors like scratching, mouthing, and locomotory skills. The Socialization Period (71–240 days) is manifested by behavioral fluctuations, involving nipple contact, play, and care by other troop members and coincides with the molt from infant to juvenile pelage. Finally, during the Juvenile Period, the motherinfant distance increases and the mother interacts more with other troop members. Behavioral fluctuations observed in this infant langur are discussed with reference to other primates studied.     

Mother-infant interaction and rank order in Rhesus monkeys (Macaca mulatta)

Our research was made observing 6 infants for a period of 6 months in a group of 13 Macaca Rhesus in captivity conditions. We pointed out that mother-infant body contact behavior in Macaca Rhesus is strictly related to the mothers' rank order. In fact, as the infants of the same age grow up, the higher is the mother's rank order, the more frequent and varied are the infants' interactions with the other members of the group and the more frequently the body contact initiatives are taken by the infants. The behaviors observed in the first months of life can be also considered as the indispensable background of the subjects' future status in the group social structure.     

Maternal Behavior and Infant Congenital Limb Malformation in a Free-Ranging Group of <Emphasis Type="Italic">Macaca fuscata</Emphasis> on Awaji Island,Japan

We studied the relationship between maternal behavior and infant disability in 12 mother-infant dyads for the first 5 weeks of infant life in the free-ranging Japanese macaque (Macaca fuscata) group on Awaji Island, Japan, from May to September 2001. Congenital limb malformations are prevalent in this population, and as such carry implications for behavior and conservation. We did not detect any differences in maternal activity budgets, mother-infant physical contact, infant holding, and overall nursing and infant transport time between mothers of non-disabled infants, disabled infants that were able to cling to their mothers, and disabled infants whose limb structure prevented clinging. Mothers of infants with limb malformations severe enough to prevent normal clinging behavior manually supported their infants during nursing and locomotion significantly more than other mothers did theirs. Increased support-carrying and support-nursing, and higher frequencies of holding the infant to one's ventrum, suggest that mothers of extensively malformed infants may be investing more to facilitate the survival of their offspring and that infant disability appears to be influencing maternal behaviors in this population.     

Maternal fatness and viability of preterm infants

To investigate the effect of maternal fatness on the mortality of infants born preterm up to the corrected age of 18 months 795 mother-infant pairs were studied. Maternal fatness was defined by Quetelet''s index (weight/(height²)) and all infants weighed less than 1850 g at birth. In 771 mother-infant pairs maternal age, complications of pregnancy, mode of delivery, parity, social class, and the baby''s sex and gestation were analysed by a logistic regression model for associations with infant mortality (but deaths from severe congenital abnormalities and those occurring during the first 48 hours after birth were excluded). In a subgroup of 284 mother-infant pairs all infant deaths except those from severe congenital abnormalities were analysed in association with the infant''s birth weight and gestation and the mother''s height and weight; this second analysis included another 24 infants who had died within 48 hours after birth. In the first analysis mortality overall was 7% (55/771), rising from 4% (71/173) in thin mothers (Quetelet''s index <20) to 15% (6/40) in mothers with grades II and III obesity (Quetelet''s index >30). After adjusting for major demographic and antenatal factors, including serious complications of pregnancy, maternal fatness was second in importance only to length of gestation in predicting death of infants born preterm. In the second analysis mortality overall was 15% (44/284), rising from 9% (5/53) in thin mothers to 47% (8/17) in mothers with grades II and III obesity. In both analyses the relative risk of death by 18 months post-term was nearly four times greater in infants born to obese mothers than in those born to thin mothers. In addition, maternal fatness was associated with reduced birth weight, whereas it is associated with macrosomia in term infants.These data differ fundamentally from those reported in full term babies of obese mothers. It is speculated that the altered metabolic milieu in obesity may reduce the ability of the fetus to adapt to extrauterine life if it is born preterm.