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.     

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.     

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.     

Ontogeny of conspecific and heterospecific alarm call recognition in wild Verreaux's sifakas (Propithecus verreauxi verreauxi)

The production of vocalizations in nonhuman primates is predominantly innate, whereas learning influences the usage and comprehension of vocalizations. In this study, I examined the development of alarm call recognition in free-ranging infant Verreaux's sifakas. Specifically, I investigated their ability to recognize conspecific alarm calls as well as those of sympatric redfronted lemurs (Eulemur fulvus rufus) in Kirindy forest, western Madagascar. Both species have functionally referential alarm calls for aerial predators and give general alarm calls for both aerial and general predators and also other kinds of threats, such as intergroup encounters with conspecifics. I conducted playback experiments with members of two birth cohorts (nine and ten individuals) to determine the age at which infant Verreaux's sifakas discriminate between conspecific alarm calls, heterospecific alarm calls, and non-alarm vocalizations (parrot song). Most 3-4 months old infants fled toward adults after hearing any playback stimuli, whereas 4-5-month-old infants did so only after presentation of alarm calls. Moreover, all infants of these age classes showed a longer latency to flee after the parrot song indicating their emerging ability to discriminate between alarm calls and non-alarm stimuli. At an age of about 6 months, infants switched from fleeing toward adults to performing adult-like escape responses after presentation of conspecific and heterospecific alarm calls. Thus, the ability to discriminate between alarm from non-alarm stimuli precedes the appearance of adult-like responses. The transition to adult-like escape behavior was coincident with the physical independence of infants from their mothers.     

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 discrimination of offspring vocalizations in Barbary macaques (Macaca sylvanus)

The response of Barbary macaque (Macaca sylvanus) females to vocalizations of their offspring was studied in a semi-free ranging population. The results of both facal observations and playback experiments demonstrated that mothers preferentially turned to their offspring's vocalizations over those of other young, providing evidence that mothers are able to recognize their offspring by acoustic signals alone. We assume that they may use this ability to monitor their infants' activities.     

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.     

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.     

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.     

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.     

Mother goats do not forget their kids' calls

Parent-offspring recognition is crucial for offspring survival. At long distances, this recognition is mainly based on vocalizations. Because of maturation-related changes to the structure of vocalizations, parents have to learn successive call versions produced by their offspring throughout ontogeny in order to maintain recognition. However, because of the difficulties involved in following the same individuals over years, it is not clear how long this vocal memory persists. Here, we investigated long-term vocal recognition in goats. We tested responses of mothers to their kids' calls 7-13 months after weaning. We then compared mothers' responses to calls of their previous kids with their responses to the same calls at five weeks postpartum. Subjects tended to respond more to their own kids at five weeks postpartum than 11-17 months later, but displayed stronger responses to their previous kids than to familiar kids from other females. Acoustic analyses showed that it is unlikely that mothers were responding to their previous kids simply because they confounded them with the new kids they were currently nursing. Therefore, our results provide evidence for strong, long-term vocal memory capacity in goats. The persistence of offspring vocal recognition beyond weaning could have important roles in kin social relationships and inbreeding avoidance.     

Grooming and Infant Handling Interchange in <Emphasis Type="Italic">Macaca fascicularis</Emphasis>: The Relationship Between Infant Supply and Grooming Payment

Female long-tailed macaques are attracted to infants and frequently groom mothers bearing them. Such grooming often involves the groomer contacting the infant and may be a trade of grooming for infant handling. To identify if grooming and infant handling are directly traded, I collected samples on times after female-to-mother grooming and on interactions in which a female groomed a mother and contacted her infant. I determined that grooming tended to promote an exchange with infant handling and that the supply of available infants was related to how long a female groomed a mother. Grooming interactions were longer when infants were scarce in the surrounding social environment than when they were abundant, indicating a possible supply-and-demand effect. This supports that grooming may be payment for infant handling. Grooming-infant handling interchanges tended to be unidirectional as mothers usually did not reciprocate grooming. Instead, infant contact occurred. A larger proportion of grooming-infant handling interchanges involved younger infants, but infant age did not seem to influence grooming durations. The length of female-to-mother grooming had no observable effect on handling time. Lower-ranked females groomed higher-ranked mothers and their infants longer than vice versa. Moreover, it was possible to predict up-rank grooming via supply and demand better than down-rank grooming. There was no observable influence of kinship on grooming-infant handling interchange. These results support the conclusion that grooming and infant handling may be traded. Grooming promoted infant handling, while supply and rank predicted the grooming payment a female would offer to access an infant.     

Weaning Age,Infant Care,and Behavioral Development in <Emphasis Type="Italic">Trachypithecus leucocephalus</Emphasis>

Primate infants are born in an altricial state and rely on the care of their parents for a relatively long period of time. Parental investment is critical to offspring survival and thus to the reproductive success of the parent as well. However, mothers and infants may experience a conflict of interest, in that infants may benefit by receiving prolonged maternal care but mothers may curtail such care in a tradeoff between investment in current versus future offspring. Documenting life history characteristics, such as age at weaning, is important not only for understanding the conflicts of interest and tradeoffs; such information can also provide insights about female reproductive rates and be valuable for conservation efforts. Little is known about the life history of white-headed langurs (Trachypithecus leucocephalus), despite their endangered status. We were the first to investigate mother-infant relationships and infant behavioral development in the species. We studied 3 wild mother-infant pairs throughout infancy. We used data from >460 h of focal subject sampling to calculate the proportion of time individuals spent in different behavioral states and the frequency of instantaneous events, such as maternal rejection. White-headed langur infants depended on their mothers for 19–21 mo, at which time they were weaned. Maternal rejection facilitated infant independence in the early stages of infant development, and mothers stopped investing in their infants when they resumed estrus. The weaning age of the wild white-headed langurs we studied was dramatically longer than that of captives, possibly as a result of the nutritional differences between wild and captive populations. Weaning age was also longer than for most other Asian colobines, and may be attributable to the degradation and fragmentation of their natural habitat.     

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.     

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.     

Individual variation in pup vocalizations and absence of behavioral signs of maternal vocal recognition in Weddell seals (Leptonychotes weddellii)

Individually stereotyped vocalizations often play an important role in relocation of offspring in gregarious breeders. In phocids, mothers often alternate between foraging at sea and attending their pup. Pup calls are individually distinctive in various phocid species. However, experimental evidence for maternal recognition is rare. In this study, we recorded Weddell seal (Leptonychotes weddellii) pup vocalizations at two whelping patches in Atka Bay, Antarctica, and explored individual vocal variation based on eight vocal parameters. Overall, 58% of calls were correctly classified according to individual. For males (n= 12) and females (n= 9), respectively, nine and seven individuals were correctly identified based on vocal parameters. To investigate whether mothers respond differently to calls of familiar vs. unfamiliar pups, we conducted playback experiments with 21 mothers. Maternal responses did not differ between playbacks of own, familiar, and unfamiliar pup calls. We suggest that Weddell seal pup calls may need to contain only a critical amount of individually distinct information because mothers and pups use a combination of sensory modalities for identification. However, it cannot be excluded that pup developmental factors and differing environmental factors between colonies affect pup acoustic behavior and the role of acoustic cues in the relocation process.     

The ontogeny of social play in a feral troop of vervet monkeys (Cercopithecus aethiops sabaeus): The function of early play

We describe the ontogeny of social play over the first 30 weeks of age in a troop of feral vervet monkeys (Cercopithecus aethiops sabaeus) in Barbados. Play time increased rapidly for the first 10 weeks but remained relatively constant thereafter. The form of play changed with infant age; bouts became more frequent but of shorter duration. Play time, bout frequency, and bout duration at a given age differed between infants; younger infants altered their play patterns to complement those of older infants. All infants played more within their own year class than with older juveniles; play time increased with decreasing age difference between the infant and the play partner. Infants terminated a higher proportion of their play bouts the greater the age difference between themselves and their play partners. Preferred play partners are therefore individuals of similar age that will be similar in size and have matched motivation to play and form of play. Neither play time nor proportion of bouts initiated or terminated was correlated with the social rank of the play partner, which suggests that play is not directed toward individuals that may be high-value alliance partners. Maternal intervention in play occurred primarily when infants were<10 weeks old. It was not correlated with the age or social rank of the mother or with the age or social rank of her infant's play partner. Infants played more and terminated a lower proportion of their play bouts in the absence of their mothers than in their presence. Our results are consistent with the hypothesis that the primary function of early play is to enhance physical fitness and to develop coordination and other fighting skills, with minimal risk of injury.     

Maternal care and infant development in <Emphasis Type="Italic">Callimico goeldii</Emphasis> and <Emphasis Type="Italic">Callithrix jacchus</Emphasis>

Callimico goeldii gives birth to single offspring, whereas other callitrichids, including Callithrix jacchus, twin. This study compares maternal effort and infant development in C. goeldii and C. jacchus; it is the first study to look at nursing frequency. Infants were observed from birth for 7 weeks in two captive groups each of C. goeldii and C. jacchus. C. goeldii mothers physiologically invested the same or less than C. jacchus mothers. C. goeldii mothers gained the same amount of weight during pregnancy in absolute terms as did the smaller C. jacchus. This results in a smaller gain in proportion to maternal weight but an equivalent proportional gain on a per fetus basis. C. goeldii mothers nursed their infants less based on duration of nursing bouts compared with C. jacchus mothers. C. goeldii mothers transported their infants exclusively through the first 2 weeks of life, which is longer than C. jacchus mothers, who exclusively transported infants only during the first week of life. As maternal infant carriage declined, other group members transported offspring in both species. C. goeldii infants engaged in independent locomotive sequences later in development and tasted solid foods less frequently than C. jacchus infants when compared at equivalent ages. A single, opportunistic milk sample obtained from a C. goeldii mother when her infant was 48 days old indicates that C. goeldii milk contains gross energy from crude protein within the range of variation observed in Callithrix milk. Despite the similarities in milk quality and prenatal effort in individual fetuses, C. goeldii infants gain weight faster from 0 to 18 months than do C. jacchus infants. A reduction in litter size allows C. goeldii mothers to spend more time carrying their infant and to delay weaning, thereby allowing accelerated infant and juvenile growth rates compared with C. jacchus.