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.     

Maternal Attachment Representation and Neurophysiological Processing during the Perception of Infants’ Emotional Expressions

The perception of infant emotions is an integral part of sensitive caregiving within the mother-child relationship, a maternal ability which develops in mothers during their own attachment history. In this study we address the association between maternal attachment representation and brain activity underlying the perception of infant emotions. Event related potentials (ERPs) of 32 primiparous mothers were assessed during a three stimulus oddball task presenting negative, positive and neutral emotion expressions of infants as target, deviant or standard stimuli. Attachment representation was assessed with the Adult Attachment Interview during pregnancy. Securely attached mothers recognized emotions of infants more accurately than insecurely attached mothers. ERPs yielded amplified N170 amplitudes for insecure mothers when focusing on negative infant emotions. Secure mothers showed enlarged P3 amplitudes to target emotion expressions of infants compared to insecure mothers, especially within conditions with frequent negative infant emotions. In these conditions, P3 latencies were prolonged in insecure mothers. In summary, maternal attachment representation was found associated with brain activity during the perception of infant emotions. This further clarifies psychological mechanisms contributing to maternal sensitivity.     

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.     

Responses of mother squirrel monkeys to dead infants

The responses of mother squirrel monkeys to infants were examined by testing the mothers with bodies of their own and other infants. Mothers whose infants were stillborn or died at one day of age showed strong and equivalent maternal responses to all the bodies with which they were presented, while those whose infants died after two weeks of age responded mainly to the body of their own infant. These results suggest that the female squirrel monkey becomes more selective in responding to the body of a dead infant with the passage of time after parturition. The female's post-parturient condition appears to be the prime cause for changes in her responsiveness, although other factors related to the infant's growth and development might also be important.Supported by Grant HD 04905 from the National Institute of Child Health and Human Development.     

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.     

Early Interactions Between Mothers and Their Medically Fragile Infants

The purpose of this study was to examine the interactions of 56 medically fragile infants and their mothers and to determine the influence of infant age, neurological status, maternal education, ethnicity, and observation location on these interactions. The interactions were observed for about 1 hr every 2 months while in the hospital, 1 month after hospital discharge, and at 6 months corrected age. The age of the infants had the greatest effect on the interaction. As infants grew older, mothers spent less time feeding, involved, holding, in body contact, looking, rocking, gesturing, and touching. However, mothers talked more, and played more with older infants. Older medically fragile infants were alert more, vocalized more, and slept less. Only one variable was directly affected by neurological status: Mothers moved neurologically normal infants more often. The neurologically normal and compromised groups were also more similar at older ages than younger ages in the percentage of time the mother was involved and the infant vocalized. Mothers with more years of education fed their infants more and looked at them more often, and minority mothers talked to their infants less and moved them more.     

Maternal recognition of individual infant squirrel monkeys from isolation call playbacks

Responses of six squirrel monkey (Saimiri sciureus) mothers to playback of a single call type, the “isolation peep,” made by their own infants were tested after mothers and infants had been separated for more than a week. The playback tapes were edited from tapes containing mixed vocal material recorded when infants and mothers could see but not touch each other. Mothers showed recognition of their own infants compared to other familiar infants by increases in four measures of proximity to the speaker. These data provide evidence that maternal recognition of infants by means of acoustic cues is possible when the test stimuli consist of examples of a single call type with demonstrated individuality.     

Effects of placental malaria on mothers and neonates from Zaire

Of one hundred placentas collected consecutively in the Ubangi district, Zaire, 64 had falciparum malaria. Mothers and infants of the 64 malarious and 36 non-malarious placentas were compared. The malarious placentas had no consistent relationship to infant length or head circumference, APGAR score, birthweight, maternal anemia, splenomegaly or hydramnios. The rate of hydramnios, in fact, was higher in the mothers with non-malarious placentas. Mothers with malarious placentas were younger (means 24) than mothers with non-malarious placentas (means 29). Mothers with fewer pregnancies were more likely to have malarious placentas than older multiparous mothers. There were 7 stillbirths, 4 from mothers with malarious placentas. Infants born to mothers with malarious placentas averaged 100 g less than those from mothers with non-malarious placentas. This study shows that mothers with falciparum malaria from the Ubangi district deliver normal and apparently unaffected infants.     

Natal Attraction in Adult Female Baboons (Papio cynocephalus ursinus) in the Moremi Reserve, Botswana

Mammalian females are strongly attracted to infants and interact regularly with them. Female baboons make persistent attempts to touch, nuzzle, smell and inspect other females’ infants, but do not hold them for long periods, carry them, or provide other kinds of care for them. Mothers generally tolerate these interactions, but never initiate them. The function of these brief alloparental interactions is not well understood. Infant handling might be a form of reproductive competition if females’ interest in infants causes distress to mothers or harm to their infants. Alternatively, infant handling might be the product of selection for appropriate maternal care if females who are highly responsive to infants are the most successful mothers. We test several predictions derived from these hypotheses with data collected in a free‐ranging group of baboons (Papio cynocephalus ursinus) in the Moremi Reserve of Botswana. Infants were most attractive when they were very young. Mothers of young infants were approached by other adult females on average once every 6 min, and other females attempted to handle their infants approximately once every 9 min. By the time infants were a year old, their mothers were being approached only once every 30 min and infants were being handled only once every 5 h. Females were more strongly attracted to other females’ infants when they had young infants of their own, and their interest in other females’ infants declined as their own infants matured. Females seemed to be equally attracted to all infants, but had greater access to offspring of their relatives and subordinate females. Females nearly always grunted as they handled infants. As in other contexts grunts are a reliable predictive signal that non‐aggressive behavior will follow, the use of grunts before handling suggests that these interactions were not a form of deliberate harassment.     

Development in Japanese macaques (Macaca fuscata): Sexually dimorphic behavior during the first year of life

We have documented several sexually dimorphic patterns of behavior that develop during the first year of life in infant Japanese macaques and their mothers. Mothers treated their infants differently by sex—mothers of males broke contact with them and retrieved them more frequently than did mothers of females. And mothers of male infants moved more frequently than did mothers of female infants. Male infants played more, played in larger groups, and mounted more frequently; female infants groomed and spent more time close to other monkeys in larger social groups than did males. Female infants were also punished by other group members more frequently than were male infants. We conclude that male and female Japanese macaque infants receive differential treatment early in life by both their own mothers and other animals, and males and females in turn treat their mothers and other animals differently. There appears to be a reciprocal relationship between the behavior of infants, mothers and other social partners that contributes to the development of sexually dimorphic patterns of behavior.     

Sex differences in infant rhesus macaque separation-rejection vocalizations and effects of prenatal androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation-rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

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.     

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.     

Fatal attraction: interest in infants and infant abuse in rhesus macaques.

This study investigated whether infant abuse by female rhesus macaques (Macaca mulatta) is a phenomenon specific to their own offspring or reflects a general tendency to interact negatively with infants. Several aspects of the relationship between maternal behavior, infant handling, and infant harassment were also investigated. Study subjects were 20 group-living rhesus mothers with their infants observed during the first 12 weeks of lactation. The results of this study indicate that abusive mothers are highly attracted to infants in general but that infant abuse is a phenomenon specific to their own offspring. Infant harassment is not an accidental by-product of infant handling or the result of maternal inexperience but it is likely related to reproductive competition among lactating females. Maternal behavior and infant handling may be regulated by similar proximate mechanisms, but probably have different adaptive functions and evolutionary history across the Primate order. Am J Phys Anthropol 110:17-25.     

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.     

Sex Differences in Infant Rhesus Macaque Separation–Rejection Vocalizations and Effects of Prenatal Androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation–rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

Rhesus macaque milk: magnitude, sources, and consequences of individual variation over lactation

Lactation represents the greatest postnatal energetic expenditure for mammalian mothers, and a mother's ability to sustain the costs of lactation is influenced by her physical condition. Mothers in good condition may produce infants who weigh more, grow faster, and are more likely to survive than the infants of mothers in poor condition. These effects may be partially mediated through the quantity and quality of milk that mothers produce during lactation. However, we know relatively little about the relationships between maternal condition, milk composition, milk yield, and infant outcomes. Here, we present the first systematic investigation of the magnitude, sources, and consequences of individual variation in milk for an Old World monkey. Rhesus macaques produce dilute milk typical of the primate order, but there was substantial variation among mothers in the composition and amount of milk they produced and thus in the milk energy available to infants. Relative milk yield value (MYV), the grams of milk obtained by mammary evacuation after 3.5-4 h of maternal-infant separation, increased with maternal parity and was positively associated with infant weight. Both milk gross energy (GE) and MYV increased during lactation as infants aged. There was, however, a trade-off; those mothers with greater increases in GE had smaller increases in MYV, and their infants grew more slowly. These results from a well-fed captive population demonstrate that differences between mothers can have important implications for milk synthesis and infant outcome.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

Emergence of individual recognition in young macaques

Few studies have addressed the development of nonhuman primate infants' responses to conspecific vocalizations. Previous studies showed that the appropriate response to alarm, intergroup and long-distance contact calls emerged at about 6 months of age. It remained unclear whether this age constitutes a watershed in terms of infants' sociocognitive development or whether it was due to the types of stimuli used in the experiments. I therefore examined the development of infant Barbary macaque, Macaca sylvanus, responses to maternal calls, under the assumption that recognition of the mother is one of the tasks that infants should master as early as possible. I presented infants of different age categories with short bouts of screams recorded from their mothers or another female of the same social group. Experiments on yearlings confirmed the suitability of the experimental approach: yearlings responded significantly more strongly to maternal calls than to calls from unrelated females. Infants were tested at 4, 10 and 16 weeks of age. In the youngest age group, they failed to respond to the playbacks, whereas from 10 weeks of age on they responded significantly more strongly to maternal calls, suggesting that by this age they recognized their mothers by voice. These results suggest that the developmental trajectories in the domain of comprehension learning may be flexible, in the sense that infant responses may depend on the salience of, and the exposure to, the call type under study. The experiments also show that screams may transmit individual-specific characteristics that are perceptually salient to the listeners.     

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.