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.     

Mother-infant relationships in Vervet Monkeys: Response to new adult males

The reaction of mothers to replacement of breeding adult males was studied in two captive groups of vervet monkeys. Mother-infant behavior for 15 infants born in the season following the introduction of new males was compared to mother-infant behavior for 35 infants born with adult males that had been resident in the group for more than a year. The mothers responded to the presence of new males by being more protective toward their infants in the first 3 months. Increased protectiveness disappeared in the second 3 months, and in the infant’s sixth month of life mothers with new males in the group became more rejecting than mothers with long-term resident males. The combination of increased protectiveness and increased rejection was unusual among the mothers with long-term resident males but was the most common mothering style used in the presence of new males. The rate of rejection was inversely correlated with the interbirth interval, and mothers with new males in the group conceived sooner and had significantly shorter inter-birth intervals compared to mothers with long-term resident males.     

Social and Demographic Influences on Mothering Style in Pigtail Macaques

This study represents the first investigation of variability in mothering styles in pigtail macaques, Macaca nemestrina nemestrina. Fifteen group-living mother-infant pairs were focally observed during the first 12 wk of infant life and several measures of maternal and infant behavior were recorded. Variability in mothering styles occurred along the three dimensions of maternal protectivencss, rejection, and warmth. Maternal parity and aggression received by mothers were the best predictors of variability in protectiveness and warmth, whereas variability in rejection was not predicted by any of the variables considered. This study provides clear evidence that aggression towards mothers and previous maternal experience have an important influence on mothering styles in pigtail macaques.     

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.     

Fission–Fusion Behavior in Yunnan Snub-Nosed Monkeys (Rhinopithecus bieti) in Yunnan, China

Several species of mammals live in relatively large social groups that temporarily fission or subgroup in response to changes in food availability, predation risk, foraging strategies, and mating competition. Although the dynamics of subgrouping are not well understood, evidence of facultative fission–fusion behavior in species that generally exhibit a highly cohesive group structure may help to clarify the set of ecological and social factors that constrain or affect group size in primates. We here examined patterns of subgrouping in Yunnan snub-nosed monkeys (Rhinopithecus bieti) inhabiting the Baimaxueshan National Nature Reserve in Yunnan, China. Rhinopithecus bieti lives in a large multilevel society consisting of 6–41 one-male, multifemale units (OMUs) and one all-male unit (AMU). Over a 5-yr period from 2003 through 2008, we tracked a group of >450 Rhinopithecus bieti. We recorded the location in the group’s home range where fission and fusion events occurred, the size and number of subgroups, days spent in subgroups, and food availability, and monitored predator sightings. The results indicate that the focal group underwent12 group fission events, all of which occurred between mid-June and July, and all in the same area of the group’s range. During these fissioning events, the AMU also showed subgrouping behavior. In all cases, the presence of bamboo shoots, an important seasonal component of the snub-nosed monkey diet, appeared to trigger subgrouping behavior. The subgroups reunited in other parts of their range after a period of 2–11?d. We found no evidence that the presence of predators had a direct affect on subgrouping behavior in Rhinopithecus bieti, as proposed in previous studies.     

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.     

Variability in the development of mother-infant relationships among free-ranging Japanese macaques

Mother-infant relationships were studied during the infant's first year in free-ranging Japanese macaques (Macaca fuscata). Three possible factors controlling the mother-infant relationships were examined using multivariate analysis. Parity was determined to exert the strongest influence on mother-infant relationships. Specifically, during month 1, multiparous mothers showed greater maternal suckling rejection than primiparous mothers, and primparae and multiparae differed in their responses to suckling behavior. During month 6, multiparous mothers prompted independence of their offspring more than primiparous mothers. By month 8, however, parity differences in maternal behavior were substantially reduced. Maternal rank was a less important factor, although during month 1, high-ranking mothers showed greater maternal restriction than low-ranking ones. In the present study, infant gender appeared to have no effect on mother-infant relationships. That most differences were due to parity indicates that mother-infant relations were largely determined by the mothers. This observation conflicts with the “learning-to-mother” hypothesis. Allo-mothering of neonates by nulliparae is rare among Japanese macaques. Primiparous mothers learned appropriate suckling care from handling their own infants.     

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.     

Identification of 13 Human Microsatellite Markers via Cross-species Amplification of Fecal Samples from Rhinopithecus bieti

Yunnan snub-nosed monkeys (Rhinopithecus bieti) are 1 of 3 snub-nosed monkey species endemic to China. Only ca. 1500 individuals remain in high-altitude forests 3000–4500 m above sea level on the Tibetan Plateau, making them the nonhuman primate living at the highest known elevation. It is one of the most endangered 25 primate species in the world. Proper knowledge of the population genetics and social system of Rhinopithecus bieti will contribute to more appropriate conservation management decisions. Cross-species amplification of human microsatellite loci has facilitated analysis of the population genetics and reproductive strategies of various primate species. We screened 72 human-derived markers to assess their utility in Yunnan snub-nosed monkeys. Thirteen of them produced reliable results and exhibited moderate levels of polymorphism.     

Comparison between wild-born mother-female infant interactions and laboratory-born mother-female infant interactions during the first 14 weeks after birth in individually caged cynomolgus macaques

In this study we compared mother-female infant interactions between primiparous and multiparous laboratory-born (F1) cynomolgus macaques (Macaca fascicularis) in individual cages at Tsukuba Primate Center (TPC), Japan, during the first 14 weeks of infant life. We also compared interactions between multiparousF1 mothers and their female infants with those between wild-born mothers and their female infants when mothers and their infants were housed in the same individual cages. PrimiparousF1 mothers showed significantly higher values for contact with and holding of their infants than multiparousF1 mothers. The primiparousF1 mothers also tended to behave aggressively toward their infants when the latter did not show any obviously irritating behaviors. Thus, the primiparousF1 mothers seemed to be inconsistent in terms of maternal behavior. Compared with multiparous wild-born mothers, multiparousF1 mothers moved more frequently, held their infants less frequently and acted aggressively toward their infants less frequently. However, infants ofF1 mothers, as well as infants of wild-born mothers, interacted with their mothers through approaching and playful contact with them. These findings indicate that the attitude of multiparousF1 mothers toward their infants was relatively passive. Possible reasons for the passive maternal style of multiparousF1 mothers are discussed.     

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.     

Nighttime Wakefulness Associated with Infant Rearing in Callithrix kuhlii

Parent-infant cosleeping occurs in human and nonhuman primates, yet studies on the impact of cosleeping on parental sleep patterns have been limited to human mothers. We examined the effects of cosleeping on the nighttime wakefulness of a biparental New World primate, Wied's black tufted-ear marmoset (Callithrix kuhlii). We compared the sleep patterns of marmoset parents caring for young infants to those without infants, using an 8 mm videocamera and timelapse VCR under infrared illumination. The presence of young infants significantly impacted the sleep of mothers but not fathers. In fact, mothers rearing young infants were awake >3 times as often as mothers without infants. We also examined the nighttime wakefulness of marmoset parents across the first 9 weeks of infant life (birth through weaning). Although callitrichid mothers tend to reduce their daytime investment in offspring very early in infant life by relinquishing the care of infants to fathers and alloparents, increased nighttime wakefulness was not limited to the early postpartum period for the mothers. Instead, mothers exhibited more nighttime wakefulness than fathers did across the first 9 weeks of infant life. Our results indicate that the presence of infants has a greater impact on the sleep patterns of Callithrix kuhlii mothers than fathers, suggesting that mothers are more involved in infant care than previously realized and that fathers are not nearly as involved in nighttime care as their behavior during the day would suggest.     

云南拉沙山黑白仰鼻猴对种子传播潜力的评估

灵长类是森林生态系统中植物种子的主要传播者,有助于森林植被的更新,然而受研究方法的限制,灵长类种子传播潜力常被低估。为全面评估温带灵长类动物的种子传播潜力,采用直接观察法和粪便分析法评估珍稀濒危灵长类动物黑白仰鼻猴的种子传播潜力。于2018年11月—2019年10月采用直接观察法(瞬时扫描取样法)收集云岭省级自然保护区拉沙山黑白仰鼻猴的活动时间分配数据,获取每月取食果实的比例;同时每月收集黑白仰鼻猴的粪便,采用粪便分析法分拣猴粪中残留的植物种子,统计有完整种子残留的月份和粪便比例,应用这两种方法评估黑白仰鼻猴种子传播潜力及其差异。结果表明：直接观察法收集到黑白仰鼻猴取食果实的月份数为6个月(7—12月),月均取食果实的比例为(15.31±20.15)%,共取食13种果实;而粪便分析法发现黑白仰鼻猴粪粒内全年都有完整种子残留,粪便中月均完整种子残留比例(35.19±35.43)%,其中9月至第二年1月粪便中种子残留比例都大于50%,共取食18种果实;综合两种方法发现云南拉沙山黑白仰鼻猴共取食20种植物果实,具有较高的种子传播潜力。直接观察法可确定黑白仰鼻猴取食果实的物种数,而粪便分析法能...     

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

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

Social dynamics and individual plasticity of infant care behavior in cooperatively breeding cotton‐top tamarins

Individual variation in infant caretaking behavior is prevalent among marmoset and tamarin monkeys. Although most group members participate in infant care, the timing and amount provided differs greatly. In this study, we quantified general trends in infant carrying behavior by using a longitudinal database that included 11 years of instantaneous scan observations following 80 births of cotton‐top tamarins. Using detailed focal observations on a subset of the same families (10 births) we identified influences that affected expression of infant care at the group and individual levels. Fathers were the primary carriers and paternal carry time gradually decreased with increasing infant age. Paternal carry time also decreased significantly with an increasing number of older sibling helpers. Most fathers began to carry on the first day postpartum. However, we report circumstances in which fathers delayed carrying until almost a month postpartum. Fathers retrieved infants the most, although adult brothers' rates of retrievals peaked and surpassed fathers' rates during week 4 postpartum. Fathers delayed rejection of infants until week 4, whereas mothers rejected infants immediately and throughout the eight weeks. Nonetheless, infants climbed onto their mothers more than onto any other family member. Mothers showed a high initial investment in carrying during the first two weeks, decreasing quickly thereafter. Maternal contributions to infant carrying remained low and relatively consistent regardless of group size. However, mothers dramatically increased their infant carrying behavior in families in which fathers were absent. Older siblings cared for infants more than did younger siblings, and brothers retrieved and carried infants more than did sisters. Individual expression of infant care changed to accommodate infant needs and changed according to varying social dynamics and circumstances across litters. Am. J. Primatol. 72:296–306, 2010. © 2009 Wiley‐Liss, Inc.     

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.     

Lactational programming? mother's milk energy predicts infant behavior and temperament in rhesus macaques (Macaca mulatta)

There are many aspects of “mothering” that may provide information to the mammalian infant about environmental conditions during critical periods of development. One essential element of mothering involves the quantity and quality of milk that mothers provide for their infants, but little is known about the consequences of variation in milk production. Mother's milk may affect infant behavior by contributing to brain development and to the development of behavioral dispositions. Here we present the first evidence for any mammal that natural variation in available milk energy (AME) from the mother is associated with later variation in infant behavior and temperament in rhesus macaques (Macaca mulatta, N=59). In the early postnatal period, heavier mothers with more reproductive experience produced greater AME, which is the product of milk energy density (kcal/g) and milk yield (g). Moreover, infants whose mothers produced greater AME in the early postnatal period showed higher activity levels and greater confidence in a stressful setting later in infancy. Our results suggest that the milk energy available soon after birth may be a nutritional cue that calibrates the infant's behavior to environmental or maternal conditions. These data provide new insight into potential mechanisms for the development of behavior and temperament and illuminate new directions for investigating maternal effects, nutritional programming, and developmental plasticity. Am. J. Primatol. 72:522–529, 2010. © 2010 Wiley‐Liss, Inc.     

Intraspecific Variability in Parenting Styles of Rhesus Macaques (Macaca mulatta): The Role of the Social Environment

This study tested the hypothesis that differences in parenting styles between two captive populations of rhesus macaques, one living in the UK (Madingley) and the other in the USA (Yerkes), are associated with differences in the degree to which social interactions with other group members pose a risk to infants. Twenty-eight mother–infant dyads, 17 living at Madingley and 11 at Yerkes, were observed for 24 h during the first 12 wks of infant life. Mother–infant dyads living at Madingley spent a higher percentage of time in contact than those living at Yerkes. The Madingley mothers also restrained and retrieved their infants more often, and rejected them less often than the Yerkes mothers. Consistent with the prediction, the protective parenting style of the Madingley mothers was associated with higher frequency of infant kidnapping and higher risk of infant harassment from other group members. Interpopulation differences in risks to infants and parenting styles are likely to be the result of differences in social density in the two environments rather than differences in the matrilineal structure of the two populations.     

Successful behavioral strategy to unite mother and infant rhesus monkeys (Macaca mulatta) after cesarean delivery

Developmental studies of pre‐ to postnatal continuities in rhesus monkeys sometimes require infants be reared with their mothers. However, complications during pregnancy or experimental designs may require cesarean delivery. Owing to lack of published information on this subject, strategies are needed to introduce mothers to their infants following cesarean delivery. Using positive and negative reinforcement techniques we attempted to unite six infant rhesus macaques, Macaca mulatta, to their mothers following c‐sections. For our seventh subject, we attempted to cross‐foster an infant onto an unrelated female after she had undergone a cesarean surgery for a late‐term spontaneous abortion. The mothers varied in age, parity, previous postnatal mothering experience with infants, housing earlier to delivery, and housing subsequent to introduction. Although there were large individual differences among the mother–infant pairs, all seven introductions were successful. The mothers learned to accept and care for their infants from the continuous application of operant conditioning techniques. These data suggest that mother‐rearing following cesarean section is a realistic possibility whether required for clinical reasons or for proper experimental control. Furthermore, the ability to successfully mother‐rear infants produced from cesarean delivery lessens the impact this potential confound of not being reared by their mothers exerts on many types of developmental studies. Am. J. Primatol. 71:510–522, 2009. © 2009 Wiley‐Liss, Inc.