An experimental study of vocal communication between mother and infant monkeys (Macaca nemestrina)

Vocal communication was studied in six feral-born mother monkeys (Macaca nemestrina) and their three- to four-month-old infants in tests which employed two sound-shielded rooms equipped with microphones and speakers. The mothers' locomotor activity levels were measured as activity counts, and vocalizations of mothers and infants were recorded under three conditions: mothers in two-way auditory communication with their own infants, in two-way auditory communication with other infants of matched sex and age, and without communication. Mothers' vocalizations and activity counts during auditory access were correlated with the number of infants' vocalizations in the same tests. Mothers' activity counts were higher with auditory access to an infant. However, neither activity counts nor vocalizations of mothers differed when in communication with their own infants from the same measures when in communication with matched infants. Neither mothers nor infants vocalized differently, either qualitatively or quantitatively, in the three conditions.     

Intended Receivers and Functional Significance of Grunt and Girney Vocalizations in Free-Ranging Female Rhesus Macaques

We investigated the intended receivers and contexts of occurrence of grunt and girney vocalizations in rhesus macaques (Macaca mulatta) to assess whether these calls are best interpreted as signals of benign intent or as calls that may function to attract the attention of other individuals or induce arousal. We focally observed 19 free‐ranging adult female rhesus macaques. Female calls increased dramatically after infants were born, and most were directed toward mother–infant dyads. When infants were physically separated from their mothers, callers visually oriented toward infants in over 90% of the cases, suggesting that infants were the intended receivers of grunts and girneys. Approaches followed by vocalizations were more likely to lead to the caller grooming the mother, less likely to elicit a submissive response, and more likely to result in infant handling than approaches without calls. Infant handling, however, was not necessarily benign. Vocalizations were often emitted from a distance >1 m and were rarely followed by approaches or social interactions. Our results suggest that grunts and girneys are unlikely to have evolved as signals that encode information about the caller's intention or subsequent behavior. Whereas girneys may be acoustically designed to attract infants’ attention and elicit arousal, grunts may have no adaptive communicative function. Mothers, however, may have learned that other females’ grunts and girneys are unlikely to be associated with significant risk and, therefore, are generally tolerant of the caller's proximity and behavior.     

Maternal discrimination of infant vocalizations in squirrel monkeys

Responses of mother squirrel monkeys to vocalizations of their own and other infants were examined to determine whether mothers could discriminate their infants on the basis of auditory cues. Thirty mothers, whose infants ranged in age from one to seven months were tested in three conditions in which their own infant, a different infant, and no infant served as the stimulus. Mothers were tested in an enclosed alleyway with opaque end panels behind which stimuli were placed. The quantity and quality of maternal responses clearly differed in the three conditions and indicated that mothers recognized their own infants. Differences in maternal vocalizations were the most pronounced. All but one type of vocalization increased in the own-infant condition; the exception, a high-pitched shrill, decreased. Mothers also spent more time near the stimulus and were more active when tested with their own infants.     

Infant response to mother call patterns in Otolemur garnettii

Garnett's greater bushbaby infants vocalize in apparent response to their mother's contact calls. However, it remains unclear whether specific vocal or behavioral patterns by a mother elicit this vocal response. We video-recorded the behaviors and vocalizations of 4 individual mother-infant groups (mother with twins), analyzed vocalizations via spectrography and documented behaviors of mothers and infants. Initial analyses of all groups revealed that short growls and short growl bouts (or chains), but not long growls, emitted by mothers, were followed by infant clicks within 5 s. Further statistical examination of 1 mother-infant group revealed that an infant's vocal response is conditional on the sequencing of the mother's short growls and somewhat conditional on the mother's behavior before or after the short growls.     

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.     

Costs and benefits of maternal aggression in lactating female rhesus macaques

Data from over 400 hr of observation of mother-infant rhesus macaques indicate that during the first 12 weeks of lactation infants are at risk from other group members and that mothers use aggression as well as restraining to protect them. Maternal aggression was negatively correlated with infant restraining. High-ranking mothers reacted aggressively to individuals handling their infants more than did middle- and low-ranking mothers. Conversely, middle- and low-ranking mothers restrained their infants more than did high-ranking mothers. Maternal aggression did not vary with infant age. Maternal aggression was directed toward a higher proportion of higher-ranking adult females and their immature offspring and was more likely to be followed by counter-aggression than nonmaternal aggression, i.e. aggression not related to interactions involving the infant. Middle-and low-ranking mothers suffered higher costs in terms of retaliation than high-ranking mothers. It is argued that the occurrence and distribution of maternal aggression among species and individuals should depend on the risk posed to infants by conspecifics as well as on the characteristics of the social structure (e.g. degree of asymmetry of agonistic contests) and of the mother (e.g. her dominance rank) which may affect the probability of retaliation.     

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.     

Early maternal recognition of offspring vocalizations in rhesus macaques (Macaca mulatta)

This study investigated the development of maternal recognition of infant calls in rhesus macaques (Macaca mulatta). Fifteen mothers and their offspring, of age ranging from several hours to 28 days, served as subjects of an experiment in which the offspring's distress vocalizations were recorded and then played back to their mothers simultaneously with those of an age-matched control infant. The proportion of time looking at, but not the proportion of orientations to the speaker playing the offspring's vocalizations increased significantly as a function of infant age. Specifically, mothers of infants older than 1 week of age responded longer to the playback of their own infant's calls than did mothers of younger infants. These findings provide the firt evidence that offspring recognition in macaques develops between the first and second week of the infant's life and are consistent with the hypothesis that mothers need to be exposed to their infants' calls in order to learn their acoustic characteristics.     

Domestic Calves (Bos taurus) Recognize their Own Mothers by Auditory Cues

The goal of this study was to determine if auditory cues are important in maternal recognition by domestic cattle calves, Bos taurus. Cows and their calves were separated and the vocalizations of the mothers were recorded. During experimental playbacks in a test enclosure, each calf (n = 9) was given a choice between a tape-recorded vocalization of its mother and that of a strange mother. Calves significantly preferred their own mother's vocalization as compared to the vocalization of the unfamiliar mother. Calves spent significantly more time near the speaker that played their own mother's call, and approached significantly closer to their mother's speaker. These results demonstrate that 3–5-wk-old calves can recognize their mothers by auditory cues alone. Visual inspection of audiospectrograms of the cows' vocalizations suggests that there are individual differences among cows.     

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.     

Effects of nonmaternal restraint on the vocalizations of infant rhesus monkeys (Macaca mulatta)

This study explored the effects of restraint by females other than the mother on the vocalizations of infant rhesus macaques (Macaca mulatta) in a captive social setting. In this species, females are very attracted to young infants and will frequently approach, groom, and hold the infant. Incompetent handling, abusive behavior, or extended periods away from the mother that prevent the infants from nursing represent potentially significant risks for infants. Vocal responses to such risky conditions appear to be the infants' only means to promote a return to their mothers. We examined the association between the severity of the threat posed to the infant and the nature of its vocal response to restraint, and whether the infants' calls influenced the behavior of their mothers or captors. The results suggest that situations posing greater risks for the infants, i.e., longer periods of restraint, were associated with a greater use of noisy screams. Furthermore, mothers' responding was associated with a greater use of noisy screams as well. The mothers' reactions, however, could be described as cautious, and consisted mostly of closer monitoring; such tempered response might be related to the risk of injury to the infant that could result from a more forceful and direct attempt at retrieval.     

The response of some prosimian primate mothers to their own anesthetized infants

Six lemur mothers of three different species and oneGalago crassicaudatus mother were observed in the presence of their own anesthetized infants. Two of the lemur mothers spent only very brief periods sitting near their infants and seldom groomed them; the other four spent over half of the infant immobility period in close proximity to their infants and groomed them frequently. Four lemur mothers groomed the ano-genital region of their infant at least once. None of the lemur mothers picked up or carried her immobilized infant, as has been reported for some higher primate mothers, although one lemur mother used her hands to pull the infant toward her ventrum while sitting on the floor. Five lemur mothers rejected their infants when the infants displayed disoriented behavior while emerging from anesthesia. The galago mother retrieved her anesthetized infant in her jaws but dropped the infant several times while attempting to groom it. These results suggest very tentatively that prosimian mothers lack the ability shown by mothers of some higher primate species to improvise protective ways of behaving toward helpless infants.     

Maternal and fetal nutrition in south India.

The relation between the nutrition of the mother and that of her baby was assessed in a south Indian community where malnutrition is common and women do not smoke. Unselected mothers and their infants of over 37 weeks'' gestation were studied in two groups: those who paid for their care (150) and a poorer group who did not (172). There were significnat differences between the paying and non-paying groups in maternal triceps skinfold thickness, infant weight, and infant length. Overall there was a significant positive correlation between maternal triceps thickness and infant weight, length, and triceps and subscapular skinfold thickness. The correlation with the infant head circumference was less significant. These findings are further evidence that the nutrition of the mother has an important effect on the nutrition of her baby and that malnutrition is an important reason why Indian babies are lighter than European ones.     

The impact of paternity on male–infant association in a primate with low paternity certainty

In multimale groups where females mate promiscuously, male–infant associations have rarely been studied. However, recent studies have shown that males selectively support their offspring during agonistic conflicts with other juveniles and that father's presence accelerates offspring maturation. Furthermore, it was shown that males invest in unrelated infants to enhance future mating success with the infant's mother. Hence, infant care might provide fitness gain for males. Here, we investigate male–infant associations in rhesus macaques (Macaca mulatta), a primate with low paternity certainty as females mate with multiple partners and males ensure paternity less efficiently through mate‐guarding. We combined behavioural data with genetic paternity analyses of one cohort of the semi‐free‐ranging population of Cayo Santiago (Puerto Rico) and recorded affiliative and aggressive interactions between focal subjects and adult males from birth to sexual maturation (0–4 years) of focal subjects. Our results revealed that 9.6% of all interactions of focal subjects involved an adult male and 94% of all male–infant interactions were affiliative, indicating the rareness of male–infant aggression. Second and most interestingly, sires were more likely to affiliate with their offspring than nonsires with unrelated infants. This preference was independent of mother's proximity and emphasized during early infancy. Male–infant affiliation rose with infant age and was pronounced between adult males and male rather than female focal subjects. Overall, our results suggest that male–infant affiliation is also an important component in structuring primate societies and affiliation directed towards own offspring presumably represent low‐cost paternal care.     

Male-infant relationships in semifree-ranging Barbary macaques (Macaca sylvanus) of affenberg salem/FRG: Testing the “male care” hypothesis

The infant-directed behavior of Barbary macaque males was analyzed in order to determine whether it is essential for an infant's survival during the first year and whether males interact selectively with closely related infants. Dyadic male-infant contacts were recorded in a large group of semifree-ranging Barbary macaques. Data collected during the first 12 weeks of life on each infant born in 1983 (n = 36) were analyzed. All adult and almost all subadult males established strong relationships with at least one infant. Almost two-thirds of the infants (22) had frequent contacts with one or several males. Males showed no preference for closely related infants. Sexual associations with an infant's mother during the preceding mating season had no significant effect. Natal males did not prefer infants of their own matrilineage. There was no evidence that contacts with males had a positive influence on infant survival or that other benefits to the infants resulted from these contacts. Instead, excessive carrying by males and females led to starvation of some very young infants and was a major cause of neonatal deaths in this population. Males interacted preferentially with infants that were born early in the birth season, had a high-ranking multiparous mother, and were male. Younger males established strong relationships with male infants only, while mother's rank was more important for older males. It is suggested that certain mothers prevented early contacts between their infants and males so that the observed preferences for certain infants were also a result of easier access to them. All results suggested that males interacted with infants for their own benefit.     

Food transfer between mother and infant chimpanzees of the Mahale Mountains National Park,Tanzania

We studied food transfer between chimpanzee mothers and infants in the Mahale Mountains National Park, Tanzania. The rate of infant solicitation for food dramatically increased in the second year of life, then gradually decreased and, in the seventh year, virtually disappeared. The pattern of the ontogeny of food sharing precisely followed that of solicitation because mothers shared food only when requested to do so by their infants. The success rate of solicitation, however, did not display extreme changes across ages. Food that was difficult to process was shared more frequently because it was more likely to be demanded by infants. We defined food retrieval as an infant’s recovery of leftovers discarded by its mother. Food types retrieved were often those that are difficult to process and were also likely to be shared by mothers. However, infants tended to solicit small, difficult food types for sharing while they often retrieved the remains of large, difficult food types. The function of food sharing and food retrieval lies in an infant’s learning food types that it cannot easily obtain or process by itself. The level of competition for food between mothers and infants remained low throughout infancy. We noted no particular characteristic about foods from which infants were displaced by mothers. As infants grew older, they increased the distance between themselves and mothers that became more aggressive.     

Bystanders affect the outcome of mother–infant interactions in rhesus macaques

Animal communication involves the transfer of information between a sender and one or more receivers. However, such interactions do not happen in a social vacuum; third parties are typically present, who can potentially eavesdrop upon or intervene in the interaction. The importance of such bystanders in shaping the outcome of communicative interactions has been widely studied in humans, but has only recently received attention in other animal species. Here, we studied bouts of infant crying among rhesus macaques (Macaca mulatta) in order to investigate how the presence of bystanders may affect the outcome of this signalling interaction between infants and mothers. It was hypothesized that, as crying is acoustically aversive, bystanders may be aggressive to the mother or the infant in order to bring the crying bout to a close. Consequently, it was predicted that mothers should acquiesce more often to crying if in the presence of potentially aggressive animals. In line with this prediction, it was found that mothers gave infants access to the nipple significantly more often when crying occurred in the presence of animals that posed a high risk of aggression towards them. Both mothers and infants tended to receive more aggression from bystanders during crying bouts than outside of this time, although such aggression was extremely rare and was received by less than half of the mothers and infants in the study. Mothers were also found to be significantly more aggressive to their infants while the latter were crying than outside of crying bouts. These results provide new insight into the complex dynamics of mother–offspring conflict, and indicate that bystanders may play an important role in shaping the outcome of signalling interactions between infants and their mothers.     

Control of nipple and body contact by mothers and infants in rhesus macaques.

While 3-month-old infant rhesus macaques (Macaca mulatta) were awake and active in social interactions away from their mothers, body and nipple contacts with their mothers were nevertheless made from time to time. In each dyad the proportions of contacts made by the mother nearly equalled those broken by her, suggesting a meshed interaction in which each partner accepted most of the other's contact initiations and terminations. Passive prevention of nipple contact by a mother reduced the frequency of nipple contact by her infant in the first 5 s after the infant had made body contact. Passive prevention occurred after fewer than 1 in 6 body contacts initiated by infants, and--even without its occurrence--most infants were less ready to take the nipple after their own initiatives than after maternal initiatives. Once nipple contact had been made, the probability of breaking body contact was reduced. The role of maternal rejection both in the control of nipple contact in the short term and in determining (through its effect on the sucking pattern) whether the mother gives birth in the next birth season or later is discussed. We suggest that, by the age of 3 months, the infants had already learned when and how often nipple contact with their mothers would be acceptable during their awake and active periods, and we suggest that subsequent decreases in the frequency of nipple contact were partly the results of maternal rejections which were accepted by the infants.     

Mother-offspring conflict and interference at mother's mating inMacaca fascicularis

Theory suggests that it is in the interest of an infant to garner more care than its mother is selected to provide and that a rival sibling would curtail care from the mother. Thus delayed conception in the mother would be of advantage to the infant. One method of achieving this result would be to interfere with the mother's potential matings. To test this theory, the conflict between mothers and their infants in relation to maximizing inclusive fitness has been studied inMacaca fascicularis and infant interference has been observed. Focal animal samples were taken on 8 mothers and their 13 infants. Interactions analyzed were those between the mother and (1) an adult male, (2) her infant, (3) an adult female, (4) her infant and an adult male, (5) her infant and an adult female. Only explicit behaviours were analyzed. The infant's interference was found to be significantly related to its mother's mating, and this produced a deterring effect on the male. Infants did not interfere with any female's matings other than those of their mother. The interference was related to the number of mother-male contacts. In mothers that did subsequently conceive, infant interference at mating increased up to the mother's conception date and decreased thereafter. By contrast to the infants direct method, mothers approached the conflict indirectly. There were significantly more contacts and mounts with males in their infant's absence, they reacted negatively to their infant only when it had interfered, they were more lenient in the presence of an adult female than with an adult male, and they avoided their infant's presence at mother-male contacts. No significant sex bias in interference or the number of contacts with mother-male pairs has been found. There are indications of a sibship pattern of interference.     

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.