Mother-infant separation and reunion in the great apes

One mother-infant dyad of each species of great ape, orang-utan, chimpanzee and gorilla, with an additional conspecific cagemate, were studied for the effects of maternal separation and reunion. High levels of agitation were observed in all infants immediately upon separation, followed by a longer period of behavioral depression with continuing, intermittent agitation. A compatible cagemate seemed to attenuate, to some degree, the behavioral depression reaction. Initial detachment following reunion with the mother occurred for all the great ape infants studied. Subsequent intensification of mother-infant attachment occurred during reunion for all three species. The findings of intermittent agitation during separation and the initial detachment upon reunion with the mother are not generally reported for monkeys, but are reported for human children. These data suggest that certain responses to maternal separation and reunion occur, to some degree, among all primates that have been studied, whereas other responses seen among apes and humans are not generally reported for monkeys.     

The effect of peer separation in young chimpanzees (Pan troglodytes)

Ten chimpanzees (Pan troglogytes), aged 18–24 months, housed without mothers as two dyads and two triads, were subjected to social separation. Two issues were addressed: the effects of peer separation in chimpanzees; and differential responses by subjects living in dyads compared with those living in triads. Chimpanzees that were alone during separation reacted with high levels of “protest” alternating with “despair” throughout the separation period. The continued presence of one cagemate, during separation from a third, was a strong mitigating factor. Even when the primary attachment was formed with the absent cagemate, the remaining chimpanzees clung to each other and the levels of protest and despair, when present, were low. Upon reunion, neither “detachment” nor heightened levels of clinging were conspicuous, but there was increased social interaction. The data on separation of chimpanzees are intermediate between those of humans and monkeys separated from mothers or peers. The increased social interactions during reunion, including looking, are comparable to the visual vigilance reported for humans.     

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.     

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.     

Physiology of maternal separation in a bonnet macaque infant

A bonnet monkey infant (M. radiata) was monitored both physiologically and behaviorally during a separation experiment in which both its mother and other conspecifiecs were removed from its social group leaving the bonnet infant with three adult pigtailed females. The separated infant exhibited the characteristic slouched posture of depression and physiological changes including decreases in the heart rate and body temperature, increases in cardiac arrhythmias, and alterations in sleep patterns, as has been previously described in separated pigtailed infants. Persistent decreases in heart rate and body temperature were noted following reunion with the mother, possibly reflecting a disturbance in the mother-infant relationship secondary to the mother's having come into estrus during the period of separation. This study indicates that the physiological correlates of maternal separation previously described in pigtailed infants are not species specific.     

Behavioral responses of an infant gorilla to maternal separation in a captive social group of lowland gorillas (Gorilla gorilla gorilla)

The present report describes behavioral reactions of a 33-month-old female infant gorilla to maternal separation in a captive social group whose composition is similar to that of wild groups. The infant gorilla responded differently to two types of maternal separation. When she remained alone for a few hours, she cried repeatedly and moved restlessly, indicating protest. Upon reunion and also for a few days thereafter, an intensification of the mother-infant relationship occurred. On the other hand, when she was separated from her mother but remained with the other group members for nine days, she did not display any behaviors that could be characterized as protest, but rather showed clear behavioral depression. During the 9-day separation period, she hardly played with other group members but she developed affiliative relationships with the leading male. After the reunion from the 9-day separation, she spent as much time near her mother as before separation and played with other infants at a level similar to that before separation, while she sometimes displayed behavioral patterns demanding the maintenance of physical contact with her mother. The present findings are compared with other reports in great apes and human children.     

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.     

The behavior of the domestic dog (Canis familiaris) during separation from and reunion with the owner: A questionnaire and an experimental study

We have constructed a questionnaire to investigate the separation behavior in a sample of family dogs (Canis familiaris) (N = 45) and in parallel we have observed dogs’ separation-related behavior in a simple behavioral test (Separation and greeting test, S&G). We recorded the dogs’ behavior during the separation from and reunion (greeting) with the owner. We investigated whether owners’ report about their dogs’ separation behavior reflected the separation behavior under controlled testing conditions. Furthermore, we wanted to find out whether the duration of separation affected the behavior of dogs and whether there was some relationship between separation and greeting behavior.Dogs that were rated by their owner to be more “anxious” during separation and “happier” at reunion, showed more activity and stress-related behavior during separation, and more affection toward the owner during greeting. Dogs with owner-reported separation-related disorder (SRD) showed more stress-related behavior, they spent less time near the owner's chair during separation, and were more active during greeting than dogs without SRD. The two groups of dogs did not differ in affectionate behavior shown toward the owner. Non-affected dogs’ activity decreased with increasing separation duration, but dogs with SRD did not show this change in their separation behavior.Our results show that owners’ have a realistic view on their dogs’ separation behavior. In addition, dogs with SRD may not be “hyper-attached” to their owners because they do not show more affection during greeting. Moreover, dogs with SRD do not show preference for the owners’ objects left behind and they cannot be easily calmed by the returning owner.Our questionnaire and the Separation and greeting test could be used for screening dogs with suspected separation-related behavior problems.     

Reunion displays in captive male brown capuchins (Cebus apella)

Separation and subsequent reintroduction of brown capuchins (Cebus apella) can lead to reunion displays during which individuals will embrace and emit high-pitched, loud vocalizations. These displays were investigated in three male capuchins: two adults and one juvenile. These subjects were part of a larger captive social group held at the Capuchin Laboratory, Hiram College, OH, USA. We hypothesized that males would engage in reunion displays following separation regardless of the order of reintroduction, as evidence of an affiliative bond judged by concurrent social behavior. Sixty separations were conducted as part of weekly husbandry over a period of 13 months. Occurrence of reunion displays between the males was recorded with the initiator also noted. Reunion displays among males were found to occur only between the juvenile and alpha male, and all displays were initiated by the juvenile. Displays were highly influenced by the order of reintroduction. We suggest that reunion displays operate to reaffirm social relationships, particularly during situations of social tension.     

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.     

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.     

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.     

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.     

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.     

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.     

Behavioral and adrenocortical responses to mate separation and reunion in the zebra finch

The adaptive value of social affiliation has been well established. It is unclear, however, what endogenous mechanisms may mediate affiliative behavior. The Australian zebra finch (Taeniopygia guttata) breeds colonially and adults maintain lifelong pair bonds that may be disrupted in the wild due to high mortality rates. Many of its natural, social behaviors are maintained in laboratory conditions, making this species well suited for studying the mechanisms of affiliation. This study examines the behavioral and neuroendocrine responses to pair mate separation and reunion in zebra finches. We measured plasma corticosterone (CORT) and behavioral changes following separation from a pair bonded mate, and again upon reintroducing the mate or an opposite-sex cagemate. Plasma CORT concentrations were: (1). elevated during pair mate separation, even in the presence of other same-sex individuals, and (2). reduced to baseline upon reunion with the pair mate but not upon re-pairing with a new opposite-sex partner. These findings show that zebra finches exhibit hormonal responses to separation and reunion specifically with a bonded pair mate and not with other familiar conspecifics. In addition, alterations in behavior during separation and reunion are consistent with monogamous pair bond maintenance. This study presents evidence for adrenocortical involvement in avian pair bonding, and for hypothalamic-pituitary-adrenal activation in response to an ecologically relevant social stressor.     

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.     

Species-specific patterns of nonapeptide brain gene expression relative to pair-bonding behavior in grouping and non-grouping cichlids

Comparative studies have revealed that vasopressin–oxytocin pathways are associated with both pair bonding and grouping behavior. However, the relationship between pair bonding and grouping behavior remains unclear. In this study, our aim was to identify whether two species that differ in grouping behavior display a corresponding difference in their pair bonds, and in the underlying vasopressin–oxytocin hormonal pathways. Using two species of cichlid fishes, the highly social Neolamprologus pulcher and the non-social Telmatochromis temporalis, we measured proximity of pairs during pair bond formation, and then measured social behaviors (proximity, aggression, submission, affiliation) and brain gene expression of isotocin and arginine vasotocin (the teleost homologues of oxytocin and vasopressin, respectively), as well as their receptors, after a temporary separation and subsequent reunion of the bonded pairs. Pairs of the social species spent more time in close proximity relative to the non-social species. Rates of aggression increased in both species following the separation and reunion treatment, relative to controls that were not separated. Overall, whole brain expression of isotocin was higher in the social species relative to the non-social species, and correlated with proximity, submission, and affiliation, but only in the social species. Our results suggest that both a social and a non-social cichlid species have similar behavioral responses to a temporary separation from a mate, and we found no difference in the brain gene expression of measured hormones and receptors based on our separation–reunion treatment. However, our results highlight the importance of isotocin in mediating submissive and affiliative behaviors in cichlid fishes, and demonstrate that isotocin has species-specific correlations with socially relevant behaviors.