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.     

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.     

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.     

Genetic analysis of human immunodeficiency virus type 1 envelope V3 region isolates from mothers and infants after perinatal transmission.

The human immunodeficiency virus type 1 (HIV-1) sequences from variable region 3 (V3) of the envelope gene were analyzed from seven infected mother-infant pairs following perinatal transmission. The V3 region sequences directly derived from the DNA of the uncultured peripheral blood mononuclear cells from infected mothers displayed a heterogeneous population. In contrast, the infants' sequences were less diverse than those of their mothers. In addition, the sequences from the younger infants' peripheral blood mononuclear cell DNA were more homogeneous than the older infants' sequences. All infants' sequences were different but displayed patterns similar to those seen in their mothers. In the mother-infant pair sequences analyzed, a minor genotype or subtype found in the mothers predominated in their infants. The conserved N-linked glycosylation site proximal to the first cysteine of the V3 loop was absent only in one infant's sequence set and in some variants of two other infants' sequences. Furthermore, the HIV-1 sequences of the epidemiologically linked mother-infant pairs were closer than the sequences of epidemiologically unlinked individuals, suggesting that the sequence comparison of mother-infant pairs done in order to identify genetic variants transmitted from mother to infant could be performed even in older infants. There was no evidence for transmission of a major genotype or multiple genotypes from mother to infant. In conclusion, a minor genotype of maternal virus is transmitted to the infants, and this finding could be useful in developing strategies to prevent maternal transmission of HIV-1 by means of perinatal interventions.     

Mother-infant interactions of wild-born,individually-caged cynomolgus monkeys (Macaca fascicularis) during the first 14 weeks of infant life

This study documents age-related changes in the interactions of wild-born cynomolgus macaque mothers and their infants living in individual cages during the first 14 weeks of infant life. Body contact between mother and infant, maternal holding, and infant sucking were found to decrease, and the mothers showed an increased frequency of aggression toward their infants with age. These results were broadly similar to those reported for mother-infant interactions in other macaques living in social groups. Nevertheless, a clear difference between the present cynomolgus macaques and other macaques in social groups was apparent. The cynomolgus macaque mothers tended to permit their infants to move about freely without displaying maternal protectiveness such as restraint or retrieval, unlike other macaque mothers in social groups. Such maternal behaviors might derive from the experience of living in individual cages for many years and the relative safety of living in individual cages. The lack of maternal restraint and retrieval could be responsible for the observed sex differences in behavior: male infants moved more actively, and broke, and made contact with their mothers more frequently than did female infants. Moreover, mothers of female infants held and groomed them more frequently and were less aggressive toward them.     

Playback experiment to test maternal responses of Japanese macaques (Macaca fuscata) to their own infant's call when the infants were four to six months old

Calls emitted by infants when the infant loses sight of its parents are useful to estimate the infant's requirement for parental care. When an Old World monkey infant loses sight of its mother it emits whistles. Therefore, it would be interesting to determine whether mothers could distinguish their own infant's whistles from the whistles of other infants. The response of each of seven Japanese macaque (Macaca fuscata) mothers to her own infant's whistle was compared with their responses to another infant's whistle. Matched control playback experiments were performed when the infants were four to six months old. The results showed that each mother could distinguish her own infant's whistle from that of another infant when the infants were four to six months old. Although a stricter experimental plan is required to further examine the issue, we found that the dominance rank of the infant's mother was another important factor in the female response to the infant's call. The finding suggests that females can associate a call emitted by an infant with its mother's rank, even before the infant begins to wander far from its mother.     

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.     

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.     

Effects of group environment on the mother-infant relationship in pigtailed monkeys (Macaca nemestrina)

Behavior of sixMacaca nemestrina mother-infant pairs was observed in two different environments; three pairs were part of a large group in a compound and three pairs were housed in individual laboratory cages. At weeks 14–15 of the infants' lives, group mothers were more retentive of their infants than caged mothers; group infants spent more time in ventral contact with mother and nursed more than did caged infants. The authors conclude that the greater dependence of an infant raised in a potentially dangerous group setting is due to a more protective mother rather than to a more fearful infant.This work was supported by grant no. FR 00166 from the National Institutes of Health, U. S. Public Health Service.Reprints may be obtained from:Primate Information Center, I-321 Health Sciences Building, University of Washington, Seattle, Washington 98105, U.S.A.     

Rate of growth in length of Bangladeshi infants as a function of attained length.

We examine variation in the rate of growth in length of breast-feeding infants from rural Bangladesh. These data were collected between November 1985 and February 1986 from two rural sites. Eighty-eight infants, ranging from birth to 4 months of age at the start of the study and their mothers were measured monthly for 4 months. Length increased linearly with age over this 4-month period (infants' average bias-adjusted R2 = 0.90). The relationship between infant rate of growth in length and attained length was analyzed by two different methods: Oldham's (1962) method of regressing rate of growth on mean length and Blomqvist's (1977) method of regressing rate of growth on estimated initial length. The methods gave similar results. The rate of growth was negatively associated with mean infant length over the 4-month period (p less than 0.001); that is, shorter infants grew at a faster rate than longer infants. For every centimeter shorter the infant was, the rate of growth was 0.1 cm/mo faster on average; the effect was greater among males than among females. The average rate of growth was greater for males than for females and greater in financially solvent households and varied by site. Infant growth rate was slower among older infants than among younger infants, as expected. However, after adjusting for mean infant length, age was no longer significantly associated with infant growth rate, although mean infant length remained highly significant. Forty-one percent of the variation in infant rate of growth in length was explained by mean infant length, sex, sex by length interaction, household financial solvency, and site.     

Patterns of food sharing among mother and infant chimpanzees at Gombe National Park, Tanzania

The patterns of food sharing among mother and infant chimpanzees at the Gombe National Park, Tanzania, are primarily influenced by the infants' ability to procure and process foods independently. Foods infants could find and process on their own were not shared by mothers as frequently as foods infants could not obtain independently. Temporal changes were observed in the patterns of interactions as infants matured. It is suggested that food sharing may be considered a behavioral strategy which facilitates the infant's transition from dependent suckling to independent foraging.     

Lactational programming? mother's milk energy predicts infant behavior and temperament in rhesus macaques (Macaca mulatta)

There are many aspects of “mothering” that may provide information to the mammalian infant about environmental conditions during critical periods of development. One essential element of mothering involves the quantity and quality of milk that mothers provide for their infants, but little is known about the consequences of variation in milk production. Mother's milk may affect infant behavior by contributing to brain development and to the development of behavioral dispositions. Here we present the first evidence for any mammal that natural variation in available milk energy (AME) from the mother is associated with later variation in infant behavior and temperament in rhesus macaques (Macaca mulatta, N=59). In the early postnatal period, heavier mothers with more reproductive experience produced greater AME, which is the product of milk energy density (kcal/g) and milk yield (g). Moreover, infants whose mothers produced greater AME in the early postnatal period showed higher activity levels and greater confidence in a stressful setting later in infancy. Our results suggest that the milk energy available soon after birth may be a nutritional cue that calibrates the infant's behavior to environmental or maternal conditions. These data provide new insight into potential mechanisms for the development of behavior and temperament and illuminate new directions for investigating maternal effects, nutritional programming, and developmental plasticity. Am. J. Primatol. 72:522–529, 2010. © 2010 Wiley‐Liss, Inc.     

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.     

Maternal Investment and Infant Survival in Gray-Cheeked Mangabeys (Lophocebus albigena)

Differences among females in infant survival can contribute substantially to variance in fitness. Infant survival is a product of external risk factors and investment by kin, especially the mother, and is thus closely tied with the evolution of behavior and life history. Here we present a 9-yr study (2004–2012) of infant survival and sex ratio relative to age and dominance ranks of mothers and the presence of immigrant males in a free-ranging population of gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda. We consider immigrant males because they are known to increase infant mortality in several other species. We found that infants of older mothers had higher survival than those of younger mothers but that high rank did not confer a significant benefit on infant survival. Female infants had higher survival than male infants. Young, low-ranking females had more male infants than young, high-ranking females, which had slightly more daughters, but this difference declined as females aged because low-ranking females had more daughters as they aged. With limited data, we found a significant relationship between the presence of male immigrants and infant mortality (falls and unexplained disappearances) to 18 mo. Our results suggest that infant survival in gray-cheeked mangabeys is most precarious when mothers must allocate energy to their own growth as well as to their infants, that sons of young mothers are at greatest risk, and that immigrant males can negatively affect infant survival.     

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.     

Tactics of care for young infants by forest-living ruffed lemurs (Varecia variegata variegata): Ground nests,parking, and biparental guarding

Over a 4 month period, systematic and ad libitum observations were conducted on two adult female black-and-white ruffed lemurs (Varecia variegata variegata) and their infants in a 3.5 ha forest enclosure. The females were mother and daughter, members of a family group that had been semifree-ranging for 2 years and 3 months at the time of the births. One to two weeks before parturition, the females independently constructed nests, in which they kept their infants during the first few weeks following parturition. The older mother, cage-reared herself, prepared at least one nest. Her daughter, who has lived in the forest since late juvenescence, prepared at least four. Two to three weeks after parturition, the mothers moved their infants high into trees. During periods of maternal absence, the infants were often alone, and they rarely or never moved, vocalized, or groomed themselves. The mothers often kept their infants together after nests were no longer used. Each infant nursed freely from both lactating females. The infants were carried orally only by their mothers and were never transported by clinging to the pelage of any group members. Previously, researchers suggested that ruffed lemurs build nests for care of infants high up in trees. The present observations, however, suggest that two major modes of neonate care in Varecia exist: serial use of multiple ground nests and “parking” of infants high in trees. Advance preparation of several nest sites, relative lack of large predators, alternate maternal and paternal guarding of infants, infant immobility during absence of mother, and rapid infant development make this tactic of care for neonates plausible.     

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.     

Aunts and Mothers: Adaptive Implications of Allomaternal Behavior of Nonhuman Primates

Explanations of the function of behavior directed toward young primates by conspecifc females other than the mother have emphasized variow outcomes beneficial to "aunts, I' mothers, infants, or some combination thereof. There is little evidence, however, that allomothering benefits mothers or infants to any signifcant degree; allomothering is selfish behavior with highly variable consequences roughly predzctable on the basis of genealogical ties between participants. Selective consequences of infant kidnapping and aunting-to-death are examined, and a hypothesis is suggested concerning the adaptive significance for mothering of allomothering. [adoption, infant-stealing, behavioral selection]     

Post-conception reproductive competition in cooperatively breeding common marmosets

Common marmosets are cooperatively breeding monkeys that exhibit high female reproductive skew. Subordinate females usually fail to breed as a consequence of ovulation suppression and inhibition of sexual behavior, and, even when they do breed, typically rear fewer infants than dominants. We evaluated possible mechanisms of post-conception reproductive competition by comparing hormonal profiles across pregnancy, pregnancy outcomes, infant survivorship, and behavior in laboratory-housed families containing one (N=9) or two (N=7) breeding females. Breeding females in plurally breeding groups did not exhibit well-defined dominance relationships and rarely engaged in escalated aggression with one another. No significant differences were found among singly breeding mothers, plurally breeding mothers, and plurally breeding daughters in urinary chorionic gonadotropin or estradiol sulfate concentrations during pregnancy, fetal biparietal diameter, frequency of spontaneous abortion, frequency of stillbirths, number of live-born infants per litter, or infant mortality rates. When females gave birth while another female in the family was pregnant, however, their infants were highly likely to be killed. The perpetrator was definitively identified in only one family, in which a pregnant female killed her daughter's infant. These results are consistent with observations of free-living common marmosets and suggest that breeding females do not regularly influence one another's pregnancy outcomes, but that they may commonly kill each other's infants, especially during their own pregnancy. Our findings further suggest that infanticide by breeding females may have selected for the evolution of reproductive restraint in subordinate female marmosets.     

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.