Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.     

Neonatal interactions in pig-tailed macque (M. nemestrina) dyads: Influence on rearing success,infant weight change and behavioral response to reunion with mother

This research assessed the significance of variation in dyadic neonatal interaction for subsequent infant development in pig-tailed macaques. Adult females were selected which differed in parity and reproductive risk. The 29 dyads were housed individually to reduce external environmental influences. Large variation was observed in maternal and neonatal behavior, but it was not significantly associated with maternal or infant risk variables and could not identify six unsuccessfully reared pairs. Among the 23 successfully reared dyads, variation in nutritional and behavioral measures hypothesized to be associated with infant growth were found to be independent of neonatal weight gain. These 23 infants were separated from their mothers after 30 days and their responses at reunion were observed. Some infants clung to the mother's ventrum (attached response) while others jumped away quickly (aloof response). Prior dyadic interactions were not significantly associated with this dichotomous response, nor were maternal and most infant variables. These results suggest that dyads at risk for neonate separation when living in captive groups are not necessarily at risk in individual housing conditions. Further, pig-tailed neonates appear unaffected by variations in mother-infant interactions that do not result in separation, but neonatal characteristics may show continuity across development.     

Mother-infant contact and maternal maintenance activities among free-ranging rhesus monkeys

Mother-infant dyads were observed among three populations of rhesus monkeys (Macaca mulatta) in India and Nepal. Physical contact between mothers and infants, essential for effective maternal care in rhesus, was found to be influenced by the mothers' feeding behavior. As early as the second week of life, infants exhibited a diminished probability of being in contact with their mothers if their mothers were feeding rather than resting. Rhesus mothers disproportionately rejected their infants within feeding contexts, indicating that mothers were actively discouraging contact attempts by their infants during feeding bouts—perhaps because an active infant, if it remained in contact, would diminish its mother's foraging efficiency. In contrast to the mothers' feeding behavior, mother-infant contact was found to be little influenced by maternal locomotion. Most infants were found to be neither disproportionately in, nor out of contact while their mothers were in motion. However, as the amount of time mothers spent walking increased, so did the probability that infants would be carried. These data suggest that rhesus mothers behave so as to minimize their energetic costs during locomotion.     

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

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

The hormonal costs of subtle forms of infant maltreatment

We show here that subtle forms of maltreatment during infancy (below 1 year of age) have potential consequences for the functioning of the child's adrenocortical response system. Infants who received frequent corporal punishment (e.g., spanking) showed high hormonal reactivity to stress (a repeated separation from mother, combined with the presence of a stranger). In addition, infants who experienced frequent emotional withdrawal by their mothers (either as a result of maternal depression, or mother's strategic use of withdrawal as a control tactic) showed elevated baseline levels of cortisol. It was suggested that there are hormonal "costs" when mothers show response patterns (intentionally or unintentionally) that limit their utility as a means of buffering the child against stress. The hormonal responses shown by infants may alter the functioning of the hypothalamic-pituitary-adrenal (HPA) axis in ways that, if continued, may foster risk for immune disorders, sensitization to later stress, cognitive deficits, and social-emotional problems.     

Location-restricted dyadic interactions and maternal patterns

The purpose of this study was to determine the impact of infant restraint on dyadic interactions and maternal foraging patterns. Five bonnet macaque (Macaca radiata) mother-infant dyads were observed under three conditions: high foraging demand for the mothers with nonrestrained contact between mothers and infants (HFD-NRC), high foraging demand with restrained contact (HFD-RC), and low foraging demand with restrained contact (LFD-RC). In the restrained contact conditions the infants lived in a nursery within the group pen that allowed dyadic nursing, contact, proximity, and grooming, but prevented the infants from being with their mothers in the remaining portions of the pen, including the foraging area. Observations began when the infants were a mean of 5.4 months old. HFD-RC resulted in decreased dyadic contact relative to HFD-NRC, but did not significantly affect foraging task engagement; there were, however, marked individual differences in the response patterns of the mothers. Dyadic contact was also decreased during the LFD-RC condition, but maternal patterns under low demand resulted in lower levels of infant contact initiation. This study demonstrated the feasibility of a nursery-restrained rearing paradigm in exploring the strategic patterns of coping with conflicting environmental and maternal demands in bonnet macaque mothers. © 1993 Wiley-Liss, Inc.     

The effects of twinning and maternal experience on maternal-filial social relationships in confined beef cattle

The objective of this investigation was to assess the maternal-filial social relationships of Hereford beef cattle as influenced by maternal experience of the dam (primiparous vs. multiparous) and number of offspring (one vs. two calves). Calves were temporarily separated from their dams during the first week after parturition, and the behavioral responses of mother and young were noted during and following separation.Contact and contact-seeking behaviors between twins and their mothers began to decline by the 5th or 6th day post-partum. Over the same period, contact behaviors exhibited by single calves and their dams remained stable or increased in frequency. Mothers of twins were less responsive to their calves than mothers of singles both during and following separation, and twins interacted with alien females more frequently than single-born young. It is proposed that insufficient milk production by Hereford dams bearing two calves provides an incentive for twins to parasitize the milk supply of alien mothers and, thus, become less dependent on their natural mothers. Social feedback between mother and twins may be further reduced by dams dividing their maternal attentiveness between two offspring.In general, experienced cows were more responsive to separation from their offspring than inexperienced heifers. Cows and their calves exhibited more frequent contact and contact-seeking behavior than heifers and their young.     

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.     

Empty Nest: A Case Study of Maternal Response to Separation From a Juvenile Offspring in a Captive Sumatran Orangutan (Pongo pygmaeus abelii)

Improving the welfare of captive nonhuman primates requires evaluating the stressors created by the captive environment and reducing their negative effects. Social separation, although sometimes necessary for managing the genetic diversity of captive populations of animals, causes both psychological and physiological stress in human and primate monkey infants. Few studies have examined the maternal response of great ape mothers to separation from their offspring. This article describes the behavioral changes of a mother orangutan (Pongo pygmaeus abelii) after separation from her juvenile daughter. We collected data on measures of proximity and social behavior before the separation of the mother-infant dyad and of locomotion, arboreality, abnormal behavior, solitary behavior, and vocalization both before and after separation. We observed no behavioral indications of protest but observed some indications of despair after separation: decreased locomotion, increased inactivity, and increased self-directed behavior. In addition, we observed increases in arboreality and object-oriented behavior during morning sessions. These findings suggest that mother-juvenile separation in orangutans might be less stressful for mothers than might be expected. Such research has implications for the welfare and management of captive animals.     

Empty Nest: A Case Study of Maternal Response to Separation From a Juvenile Offspring in a Captive Sumatran Orangutan (Pongo pygmaeus abelii)

Improving the welfare of captive nonhuman primates requires evaluating the stressors created by the captive environment and reducing their negative effects. Social separation, although sometimes necessary for managing the genetic diversity of captive populations of animals, causes both psychological and physiological stress in human and primate monkey infants. Few studies have examined the maternal response of great ape mothers to separation from their offspring. This article describes the behavioral changes of a mother orangutan (Pongo pygmaeus abelii) after separation from her juvenile daughter. We collected data on measures of proximity and social behavior before the separation of the mother-infant dyad and of locomotion, arboreality, abnormal behavior, solitary behavior, and vocalization both before and after separation. We observed no behavioral indications of protest but observed some indications of despair after separation: decreased locomotion, increased inactivity, and increased self-directed behavior. In addition, we observed increases in arboreality and object-oriented behavior during morning sessions. These findings suggest that mother-juvenile separation in orangutans might be less stressful for mothers than might be expected. Such research has implications for the welfare and management of captive animals.     

Parent-infant bed-sharing behavior

An evolutionarily informed perspective on parent-infant sleep contact challenges recommendations regarding appropriate parent-infant sleep practices based on large epidemiological studies. In this study regularly bed-sharing parents and infants participated in an in-home video study of bed-sharing behavior. Ten formula-feeding and ten breast-feeding families were filmed for 3 nights (adjustment, dyadic, and triadic nights) for 8 hours per night. For breast-fed infants, mother-infant orientation, sleep position, frequency of feeding, arousal, and synchronous arousal were all consistent with previous sleep-lab studies of mother-infant bed-sharing behavior, but significant differences were found between formula and breast-fed infants. While breast-feeding mothers shared a bed with their infants in a characteristic manner that provided several safety benefits, formula-feeding mothers shared a bed in a more variable manner with consequences for infant safety. Paternal bed-sharing behavior introduced further variability. Epidemiological case-control studies examining bed-sharing risks and benefits do not normally control for behavioral variables that an evolutionary viewpoint would deem crucial. This study demonstrates how parental behavior affects the bed-sharing experience and indicates that cases and controls in epidemiological studies should be matched for behavioral, as well as sociodemographic, variables.     

Adoption by captive parturient rhesus macaques: Biological vs. adopted infants and the cost of being a “twin” and rearing “twins”

Four rhesus macaque (Macaca mulatta) mothers each spontaneously adopted and reared an abandoned, unrelated neonate in addition to their own neonate. Data on relative time spent in maternal contact and who maintained proximity were collected for the biological and adopted “twins” and singleton control infants using focal animal sampling. Infant weight gain and the subsequent conception history for each mother were obtained for the following year. Biological infants spent more time in maternal contact than their adopted “twin” siblings. When in contact with their mothers, biological “twins” spent more time in the ventro-ventral position and more ventral time alone than adoptees. Mothers initiated more contacts with their biological infants than their adopted infants, suggesting these differences may be due to differential maternal behavior. “Twins” gained weight at a slower rate than singletons, and mothers rearing “twins” produced significantly fewer offspring the following season. Am. J. Primatol. 43:259–264, 1997. © 1997 Wiley-Liss, Inc.     

Comparative Network Analysis of Preterm vs. Full-Term Infant-Mother Interactions

Several studies have reported that interactions of mothers with preterm infants show differential characteristics compared to that of mothers with full-term infants. Interaction of preterm dyads is often reported as less harmonious. However, observations and explanations concerning the underlying mechanisms are inconsistent. In this work 30 preterm and 42 full-term mother-infant dyads were observed at one year of age. Free play interactions were videotaped and coded using a micro-analytic coding system. The video records were coded at one second resolution and studied by a novel approach using network analysis tools. The advantage of our approach is that it reveals the patterns of behavioral transitions in the interactions. We found that the most frequent behavioral transitions are the same in the two groups. However, we have identified several high and lower frequency transitions which occur significantly more often in the preterm or full-term group. Our analysis also suggests that the variability of behavioral transitions is significantly higher in the preterm group. This higher variability is mostly resulted from the diversity of transitions involving non-harmonious behaviors. We have identified a maladaptive pattern in the maternal behavior in the preterm group, involving intrusiveness and disengagement. Application of the approach reported in this paper to longitudinal data could elucidate whether these maladaptive maternal behavioral changes place the infant at risk for later emotional, cognitive and behavioral disturbance.     

Effects of age,rearing, and separation stress on immunoglobulin levels in rhesus monkeys

The study reported here examined the effect of different rearing conditions and psychological stress on immunoglobulin levels in rhesus monkey infants. In the first experiment, 24 rhesus neonates were placed in one of the three following rearing conditions: Separated from their mothers and reared in the laboratory nursery; kept with their biological mothers; or removed at birth from their biological mothers and cross-fostered to adoptive rhesus mothers. Plasma samples were obtained from the nursery-reared infants immediately after birth and at weekly intervals for the next 30 days. Samples were also obtained from mother-reared and foster-reared infants on days 15 and 29. All samples were tested for IgG and IgM levels. The results indicated that neither rearing nor diet affected Ig levels. IgG levels were highest at birth and decreased progressively for the first 30 days, suggesting that placental transfer of maternal IgG is the critical determinant of IgG levels in primate infants as in humans. IgM changes were also similar to those in human infants: Low levels at birth, a significant increase from birth to day 15, and a moderate decline from day 15 to day 30. When IgG levels and IgM levels were correlated across the first month, many significant correlations were found which were consistent with human data relating both infant IgG and IgM levels to infant maturation. In the second experiment, 11 of the previously tested nursery infants were subjected to four consecutive social separations from peer groups at 6 months of age. Plasma samples were obtained before and after the first and fourth weeks of separation and tested for IgG and IgM levels. Small but significant decreases in both immunoglobulins were detected after 4 days of separation, particularly on the fourth week.     

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.     

Behavioral and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment

The behavioral and adrenocortical responses of rhesus macaque mothers to a series of four consecutive 4-day separations from their 5-month old infants in an unfamiliar environment were examined. A biphasic behavioral response to separation was observed, with passive behavior, locomotion, and vocalization highest on Day 1 of separation, and self-directed behaviors and environmental exploration peaking during Days 2–4. Stereotyped locomotion increased, and passive behavior decreased, across successive weeks of separation. The rhesus mothers exhibited substantial cortisol elevations one and two hours postseparation, with cortisol decreasing on the fourth day of separation. The cortisol response was strongest during the first week of separation, but robust elevations occurred in response to repeated separations. No signs of behavioral depression were observed. The results indicate that infant separation combined with removal to a novel environment can be a potent stressor for rhesus macaque mothers.     

Aerobic Exercise during Pregnancy and Presence of Fetal-Maternal Heart Rate Synchronization

It has been shown that short-term direct interaction between maternal and fetal heart rates may take place and that this interaction is affected by the rate of maternal respiration. The aim of this study was to determine the effect of maternal aerobic exercise during pregnancy on the occurrence of fetal-maternal heart rate synchronization.

Methods

In 40 pregnant women at the 36^th week of gestation, 21 of whom exercised regularly, we acquired 18 min. RR interval time series obtained simultaneously in the mothers and their fetuses from magnetocardiographic recordings. The time series of the two groups were examined with respect to their heart rate variability, the maternal respiratory rate and the presence of synchronization epochs as determined on the basis of synchrograms. Surrogate data were used to assess whether the occurrence of synchronization was due to chance.

Results

In the original data, we found synchronization occurred less often in pregnancies in which the mothers had exercised regularly. These subjects also displayed higher combined fetal-maternal heart rate variability and lower maternal respiratory rates. Analysis of the surrogate data showed shorter epochs of synchronization and a lack of the phase coordination found between maternal and fetal beat timing in the original data.

Conclusion

The results suggest that fetal-maternal heart rate coupling is present but generally weak. Maternal exercise has a damping effect on its occurrence, most likely due to an increase in beat-to-beat differences, higher vagal tone and slower breathing rates.     

Serotonin transporter expression is predicted by early life stress and is associated with disinhibited behavior in infant rhesus macaques

Serotonin transporter (5-HTT) expression patterns may contribute to the risk for adverse psychological outcomes following early life stress. The present study investigated whether two types of early life stress, maternal and social aggression, and a serotonin transporter gene promoter polymorphism ( rh5-HTTLPR ) predicted lower post-stressor peripheral blood mononuclear cell (PBMC) 5-HTT expression in infant rhesus macaques. We further probed the relationships among these factors and infant behavioral disinhibition within a stressful situation. Fifty-three infants residing with mothers in large, complex social groups were observed over the first 12 postnatal weeks, during which time the rate of aggression received by the infant from their mothers and social group members was recorded. At 90–120 days of age, infants underwent a 25-h maternal separation/biobehavioral assessment, which included standardized behavioral assessments and blood sampling. Infants' rh5-HTTLPR genotypes were determined, and infant 5-HTT expression was quantified from PBMCs collected 8 h after separation. Receipt of aggression from the mother, but not from social group members, was associated with lower post-stressor 5-HTT expression. Lower post-stressor 5-HTT expression, but not receipt of aggression, was associated with disinhibited behavior during assessment. Rh5-HTTLPR genotype was unrelated to any measure. We conclude that 5-HTT regulation is linked with specific, presumably stressful early experiences in infant rhesus macaques. Further, 5-HTT expression predicted behavioral disinhibition, presumably via parallel processes that operate in the brain.     

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.     

The development of range of action in infant cynomolgus monkeys (Macaca fascicularis) reared by restrained mothers

In order to study the effects of the mothers' range of action on the development of their infants' range of action during the first year of life, mother cynomolgus monkeys were restrained in their range of action by penning them in a separation cage within the large cage of the harem group they belonged to. The infants, however, could leave their mothers' separation cage. The control group consisted of infants growing up with unrestrained mothers in the same group. It appeared that infants of restrained mothers were initially retarded in the development of their range of action but at the end of the first year they did not differ anymore from infants of unrestrained mothers. It is concluded that the maternal range of action only temporarily affects the development of the infant's range of action.