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.     

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.     

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.     

Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: A comparison with captive pairs

The general course of mother-infant relationships among free-ranging rhesus monkeys (Macaca mulatta) on Cayo Santiago is remarkably similar both qualitatively and quantitatively to that observed in the socially living captive colony at the MRC Unit at Madingley, England. Nevertheless, small but consistent differences appear to be due to differences between mothers in the two environments rather than differences between infants. Captive mothers may be described as more protective and less encouraging of early independence in their infants than free-ranging mothers. Moreover, captive pairs have become more like free-ranging pairs over the years, perhaps as captive mothers have been allowed to raise their infants in the presence of kin. A unitary concept of environmental complexity is not useful in accounting for the results.     

Conditions of failure and recovery of maternal behavior in captive squirrel monkeys (Saimiri)

This paper deals with the functioning and malfunctioning of maternal behavior in relation to external and social conditions. During developmental studies in captive squirrel monkey groups, 49 mother-infant pairs were observed. There were several cases of maternal inadequacy subsequent to (1) postnatal transportation, (2) exaggerated social investigation by immatures,and (3) premature allomothering. Brief mother-infant separations by humans did not yield such failures. One female consistently prevented nursing with at least three of her five viable offspring. Complete or partial failure of maternal behavior did not preclude subsequent recovery and/or adequate allomothering. Dedicated to Prof. Dr. Med. Detlev Ploog on the occasion of his 60th birthday.     

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.     

Dyadic interactions of infant lowland gorillas in an outdoor exhibit compared to an indoor holding area

The behavior of two lowland gorilla mother-infant pairs living in a social group at Zoo Atlanta was compared in an indoor holding area vs. an outdoor exhibit. Focal animal data were collected for each pair during 30-min observation sessions over 24 days, alternating between indoors and outdoors. A variety of individual and social behaviors differed in the two conditions, particularly infant behaviors and infant-controlled behaviors. Mothers and infants spent more time closer together inside than outside, and infants left mothers more and mothers approached infants more outside than inside. Additional differences included more object examination and solitary play by the infants, and more feeding by the mothers, outside. Mothers autogroomed more and infants engaged in more self-manipulation inside. Additionally, there were significantly more aggressive display behaviors directed toward the mother-infant pairs inside than outside, and the adults engaged in coprophagy inside but not outside. A variety of other behaviors measured did not change between the two environments. There was a clear effect on behavior of the different housing conditions in which the gorillas were kept. © 1994 Wiley-Liss, Inc.     

Response to social challenge in young bonnet (Macaca radiata) and pigtail (Macaca nemestrina) macaques is related to early maternal experiences

Previous experience affects how young primates respond to challenging social situations. The present retrospective study looked at one aspect of early experience, the quality of the mother-infant relationship, to determine its relationship to young bonnet and pigtail macaques' responses to two social challenges: temporary maternal separation at 5-6 months and permanent transfer to an unfamiliar peer group at 16-17 months. Relationship quality was measured quantitatively on 30 macaque mother-infant pairs with the Relationship Quality Index (RQI), the ratio of relative affiliation to relative agonism as previously applied to capuchin monkeys. Infants with high RQI values had amicable mother-infant relationships and infants with low RQI values had agonistic mother-infant relationships. Young monkeys with amicable and agonistic relationships showed consistent differences in behavior before, during, and after each social challenge, supporting the hypothesis that juveniles from amicable mother-infant relationships based on the RQI coped more effectively with social challenges than did juveniles from agonistic mother-infant relationships. Results suggest 1) characteristic amicability or agonism in early mother-offspring macaque relationships has the potential to influence offspring behavior in tense social contexts and 2) the RQI is useful as one of a coordinated suite of methods for studying the development of social skills.     

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.     

Brief repot: Interactions with infants by full siblings,paternal half-siblings,and nonrelatives in a captive group of rhesus macaques (Macaca mulatta)

Six mother-infant pairs in a group of captive rhesus monkeys (Macaca mulatta) were observed for six months. “Infant grabs” by others and mothers' resistance to grabs were scored. More full siblings grabbed infants than either paternal half-siblings or nonrelatives. Mothers resisted grabbing by more nonrelatives than by paternal half-siblings. Although the maternal effect suggested by full sib-infant interactions is expected, the paternal effect revealed by mothers' tolerance of paternal half-sibs, but not full siblings, over nonrelatives is unexpected.     

Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages

Many scientists and colony managers assume that social housing is a beneficial living condition for all captive primates. Several older studies of primate development question the generality of this assumption. We recently tested this assumption by comparing the social development of pigtailed macaque infants raised in pairs and those that were raised in individual cages. All animals received 30 min of daily socialization in a playroom. Infants paired from postnatal week 3 through month 4 developed a playroom behavioral repertoire consisting largely of mutual clinging, fear, and social withdrawal. This was especially true of females. Unlike the singly caged infants, pair-reared monkeys did not successfully adapt to living in a large social group at 8–10 months of age. In this situation, pair-reared infants were subordinate and spent almost all of their time huddling on the pen floor. It was concluded that rearing macaque infants in pairs produces a behavioral repertoire that is maladaptive with respect to social development.     

Attacks on neonates by a male mangabey (Cercocebus atys)

Aggressive behavior by an adult male toward selected infants and their mothers was observed during a long-term study of reproduction in a captive social group of sooty mangabeys (Cercocebus atys). The highest-ranking adult male in this group was observed to attack and bite three neonates out of a total of 13 infants born in 1982. All three attacks were directed attacks in which infants were grabbed from their mothers and bitten in the head. The first infant was fatally injured; the other two probably would have sustained fatal wounds had the male's canines not been blunted beforehand and had observers not intervened. The attacks were preceded by a pattern in which the male persistently stalked or chased the mother-infant pairs, a behavior first observed in the hours immediately following parturition. Unlike attacks in wild baboon groups following male immigration, these attacks on infants occurred in a stable social group in which the male attacker had been a lifelong resident. This male, however, had gained alpha rank only 3 months before attacking the first infant. These attacks, in the context of other evidence of aggression and wounding, are discussed relative to current models of infanticide in primates.     

Development and mother-infant relations among captive patas monkeys

Generalizations about the rate of behavioral development and mother-infant relations in nonhuman primates are often based largely on observations of a few closely related species of macaques. Patas monkeys (Erythrocebus patas)are sufficiently distant phylogenetically and distinct in their social and ecological adaptations from the well-studied macaque species that observations of their patterns of infant development and mother-infant relations may indicate to what extent macaque patterns are typical of Old World monkey species. Eight patas infants living with their mothers in an established captive group were observed for 960 hr over the first year of life. These infants showed a rapid rate of behavioral development and attainment of independence from mothers. Patas also have one of the fastest rates of sexual maturation of any Old World monkey species. This pattern of rapid social and sexual development can be viewed as a response to a highly seasonal savannah environment in which there is a premium on ability to achieve nutritional, locomotor, and social self-sufficiency as quickly as possible and to reproduce as early and as often as developmental constraints will permit. Patterns of infant development and mother-infant relations may be best understood as an integral part of a species’ overall life history pattern.     

Psychobiological consequences of two different weaning methods in sheep.

Weaning is associated with a break in the mother-infant contact. In sheep, under natural conditions, the rupture of the social bond is progressive. In contrast, weaning imposed by breeders may result in psychobiological disturbances. The aim of this experiment was to measure the behavioural, hormonal and immune consequences of two types of sudden weaning: total separation (TS) and partial separation (PS), in 42 Ile-de-France ewes and their 60 lambs. TS animals (lambs and ewes) vocalized less frequently and for a shorter period of time than did the PS animals. Neither the plasmatic cortisol level in lambs nor the humoral response of dams and young were modified by the two weaning methods. In contrast, the excretion of coccidial oocysts increased significantly after weaning in TS lambs only and the growth rate of TS females was lower than that of the other lambs. These results suggest that these methods of rupture of mother-young social contact have only limited negative consequences on both partners in sheep, contrary to primates and rodents.     

How rhesus monkey infants budget their time between mothers and peers

Social play between two rhesus monkey (Macaca mulatta) infants takes place mainly when they are both not in body contact with their mothers. This suggests that social play and mother-infant body contact are potential competitors in the infants' time budgets. We investigated whether the presence of a playmate changed the duration of mother-infant body contact during the first 6 months of life. A decrease in contact would favour play opportunity. Mother-infant pairs were observed alternately alone and together with another pair. Resting, which always occurs during on-mother, was not reduced in the presence of a peer. Body contact during activity phases was reduced in most playing pairs, but only to a large extent in pairs which showed relatively high levels of contact in the situation without a peer. Play opportunity was further increased by synchronization of the rest-activity cycles of the two infants; this occurred without a reduction in mother-infant interactions. No influences by mothers on play opportunity were demonstrated, except that strong maternal interference with resting reduced activity synchronization.     

Maternal aggressive contact vocalizations in captive bottlenose dolphins (Tursiops truncatus): Wide-band,low-frequency signals during mother/aunt-infant interactions

The mother-infant bond in bottlenose dolphins is critical to infant survival and has been reported to last from 3-10 years in both captive and wild populations. Little information on mother-infant communication during early development has been collected. This paper reports on a newly discovered dolphin vocalization, termed thunk, which is predominantly used by mothers toward infants. Four mother-infant pairs and one aunt-infant pair were the subjects for this study. Methods included a focal animal sampling technique using 2.5 min interval and event/continuous sampling regimes on audio- or videotape. Results indicated that thunks are produced by mothers or aunting females during infant departures (distances greater than 5 feet) and are frequently followed by disciplinary activity by the mother or aunt. In addition, thunks appeared to cease at approximately 9-10 months after birth, concurrent with a decrease in infant dependence. Thunks also were analyzed acoustically for frequency and duration parameters. Thunks have a harmonic structure with an energy peak in the 273–350 Hz range and ranged from 129–5,556 Hz in frequency and from 21–171 ms in duration. They appear to function as aggressive contact vocalizations produced by mothers and other adult females toward infants in order to maintain infant proximity. © 1995 Wiley-Liss, Inc.     

Mother-infant interactions in captive slow lorises (Nycticebus coucang)

Information is presented about mother-infant interactions and infant development in a rarely studied prosimian primate, the slow loris (Nycticebus coucang). Four dyads were observed, by means of closed circuit TV, in a semi-natural environment for 1 hour per day three times a week. Infants were inactive for the first 6–8 weeks. Although mothers carried infants, they also left them alone for substantial periods of time after the 1st week. Over the 20-week study period, there was a significant decline in ventral contact but not in sitting within 12 inches or engaging in active social interactions. By the end of the study, infants were not yet fully independent. Three of the 4 were primarily responsible for maintaining physical closeness to the mother; they made most of the approaches and mothers made most of the departures. However, only 2 of the 4 infants had assumed responsibility for the initiation and maintenance of social interactions with the mother. By comparison with other nocturnal prosimians of similar size, the rate of development is relatively slow. Unlike many anthropoids, mothers were not strongly protective or rejecting. They did not bring infants back to a fixed location or try to prevent infants from leaving them; and the decline in ventral contact was not accompanied by fights between the pair. The 3 group-living mothers were more protective than the single individually housed mother, and it would seem advisable to isolate mother-infant pairs in laboratory breeding colonies.     

Circadian and Ultradian Time Patterns in Human Behavior: Part 2: Social Synchronisation During the Development of the Infant's Diurnal Activity-Rest Pattern

Individually developing patterns of activity-rest rhythms in infants and the influence of environmental factors in the tuning and synchronisation of parent-infant pairs have important implications for the health of both infant and parents. After discharge from the hospital newborn infants are exposed to patterned influences of maternal and environmental regularities of a family's daily life resulting in varying degrees of social synchronisation. Actigraphic monitoring was used in this longitudinal study to examine how activity patterns of the entire family agree or disagree with each other, and how the infant entrains to the environment. Activity data of 12 families (father, mother and infant) were continuously recorded using non-invasive Actiwatch units. Recordings of parental activity started at the beginning of the 37th week of gestation, and were continued in parallel with the infants' recordings in three series of 21 days each until four months after birth: 1st to 3rd week, 7th to 9th week and 13th to 15th week of life. Fast Fourier transformation and cross correlation techniques were used to determine frequencies of each family member and to quantify the synchronisation of activity between parents and infants. To elucidate differences in social synchronisation between human cultures, synchronisation of a Melanesian family was additionally compared. Results showed the existence of corresponding ultradian frequencies in the activity patterns of mother-infant pairs at 1, 2 and 4 months. Increases in the synchronisation of parental activity were found from prenatal to postnatal and for mother-infant pairs from the first to the second month. Synchronisation between mother and infant always exceeded that of father and infant. Transient mono-, bi- or polyphasic activity patterns emerged in the infants immediately after birth. Good correspondence of mother-infant activity patterns during the early postnatal period was correlated with a rapid development of an entrained daily pattern in the infant.     

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

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

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.