Spectrographic Description of Vocalizations in Captive Otolemur garnettii

To advance knowledge of the vocal communication associated with close proximity social interactions in Garnett's greater bush baby (Otolemur garnettii), we measured acoustic and temporal properties of vocalizations from videotaped recordings of captives in two main social contexts: mother-infant interactions and adult male-female pair introductions and reintroductions. We used a real-time sonagraph or software program to display, edit, and analyze vocal waveforms, and to provide wideband and narrowband spectrograms. Vocalization characteristics measured include fundamental frequency (via inspection of harmonics) and spectral features such as formant frequency, intensity, and duration. The vocal repertoire contained 4 major types of vocalizations: 1) barks and complex multiple bark sequences, 2) low frequency flutter/hums and growls, 3) high frequency clicks and spits, and 4) noisy shrieks. We describe several vocalizations for the first time and provide a clear classification of some of them on the basis of call durations (long/short growls). Complex bark sequences, previously described as distant communication calls, were invariant and were not often emitted by individuals when in close proximity. When classified spectrographically, the remaining 3 call types, which occurred when individuals were in close proximity, were less stereotypical, and gradations within call types were apparent. Our results show that although nocturnal and non-gregarious, complex communicatory signals of bush babies constitute a vocal repertoire formerly thought to be characteristic only of diurnal, gregarious primates.     

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.     

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 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.     

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.     

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.     

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.     

Behavioral changes during weaning in captive chimpanzees

Behavioral changes during weaning of chimpanzee infants in captive social groups were compared with those of infants in the natural habitat. Results of the weaning process were the same for the mother-infant pairs in captivity and the natural habitat, i.e., an infant independent of suckling, regular maternal transport and sleeping with the mother. The captive infants, however, did not respond to weaning with depression or regression to infantile behaviors as did infants in the natural habitat. Quite probably the social and physical environmental differences between the two habitats faciliated a less stressful weaning period for the captive mother-infant pairs.     

Saccular potentials of the vocal plainfin midshipman fish, <Emphasis Type="Italic">Porichthys notatus</Emphasis>

The plainfin midshipman fish, Porichthys notatus, is a vocal species of teleost fish that generates acoustic signals for intraspecific communication during social and reproductive behaviors. All adult morphs (females and males) produce single short duration grunts important for agonistic encounters, but only nesting males produce trains of grunts and growls in agonistic contexts and long duration multiharmonic advertisement calls to attract gravid females for spawning. The midshipman fish uses the saccule as the main acoustic endorgan for hearing to detect and locate vocalizing conspecifics. Here, I examined the response properties of evoked potentials from the midshipman saccule to determine the frequency response and auditory threshold sensitivity of saccular hair cells to behaviorally-relevant single tone stimuli. Saccular potentials were recorded from the rostral, medial and caudal regions of the saccule while sound was presented by an underwater speaker. Saccular potentials of the midshipman, like other teleosts, were evoked greatest at a frequency that was twice the stimulus frequency. Results indicate that midshipman saccular hair cells of non-reproductive adults had a peak frequency sensitivity that ranged from 75 (lowest frequency tested) to 145 Hz and were best suited to detect the low frequency components (≤105 Hz) of midshipman vocalizations.     

Serotonin transporter allelic variation in mothers predicts maternal sensitivity, behavior and attitudes toward 6-month-old infants

Maternal behavior in the new mother is a multidimensional set of responses to infant cues that are influenced by the mother's early life experiences. In this study, we wanted to test if mothers' early life experiences and mothers' genotype have interactive effects on maternal behaviors and attitudes, something which has not been previously explored. In a sample of 204 mothers, we assessed maternal genotype at the serotonin transporter-linked polymorphic region (5-HTTLPR) and an adjacent upstream polymorphism (rs25531), together giving rise to three alleles: short (S), L(G) and L(A). Controlling for maternal age and parity, we showed that this genotype can predict differences in maternal sensitivity at 6 months postpartum: mothers with an S (or the functionally similar L(G)) allele were more sensitive than mothers who lacked the allele during a 30-min recorded mother-infant interaction (F (4,140) = 3.43; P = 0.01). Furthermore, we found highly significant gene-environment interactions in association with maternal behavior, such that mothers with no S or L(G) alleles oriented away more frequently from their babies if they also reported more negative early care quality (F (5,138) = 3.28; P = 0.008). Finally, we found significant gene-environment associations with maternal attitudes; mothers with the S allele and with greater early care quality scored higher on ratings of their perceived attachment to their baby (F (5,125) = 3.27; P = 0.008). The regression results show significant interactions between the reported quality of care mothers received from their own parents and genotype on both their frequency of orienting away from the infant during the interaction (F(5, 138) = 3.28; P = 0.008, Fig. 1a) and their perceived attachment feelings to the infant (F(5, 125) = 3.27; P = 0.008, Fig. 1b); however the direction of the effects for these two outcome measures were different from one another. With increasing care quality, mothers with the L(A)L(A) genotype (no S or L(G) allele) oriented away less frequently, while S or L(G) allele carriers showed no significant change. In contrast, with increasing early care quality. L(A)L(A) (no S or L(G) allele) mothers scored lower on perceived attachment to their infants, whereas S or L(G) allele carrying mothers scored higher. [corrected].     

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.     

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.     

Mother-infant interactions in captive slow lorises (Nycticebus coucang)

Information is presented about mother-infant interactions and infant development in a rarely studied prosimian primate, the slow loris (Nycticebus coucang). Four dyads were observed, by means of closed circuit TV, in a semi-natural environment for 1 hour per day three times a week. Infants were inactive for the first 6–8 weeks. Although mothers carried infants, they also left them alone for substantial periods of time after the 1st week. Over the 20-week study period, there was a significant decline in ventral contact but not in sitting within 12 inches or engaging in active social interactions. By the end of the study, infants were not yet fully independent. Three of the 4 were primarily responsible for maintaining physical closeness to the mother; they made most of the approaches and mothers made most of the departures. However, only 2 of the 4 infants had assumed responsibility for the initiation and maintenance of social interactions with the mother. By comparison with other nocturnal prosimians of similar size, the rate of development is relatively slow. Unlike many anthropoids, mothers were not strongly protective or rejecting. They did not bring infants back to a fixed location or try to prevent infants from leaving them; and the decline in ventral contact was not accompanied by fights between the pair. The 3 group-living mothers were more protective than the single individually housed mother, and it would seem advisable to isolate mother-infant pairs in laboratory breeding colonies.     

Neonatal interactions in pig-tailed macque (M. nemestrina) dyads: Influence on rearing success,infant weight change and behavioral response to reunion with mother

This research assessed the significance of variation in dyadic neonatal interaction for subsequent infant development in pig-tailed macaques. Adult females were selected which differed in parity and reproductive risk. The 29 dyads were housed individually to reduce external environmental influences. Large variation was observed in maternal and neonatal behavior, but it was not significantly associated with maternal or infant risk variables and could not identify six unsuccessfully reared pairs. Among the 23 successfully reared dyads, variation in nutritional and behavioral measures hypothesized to be associated with infant growth were found to be independent of neonatal weight gain. These 23 infants were separated from their mothers after 30 days and their responses at reunion were observed. Some infants clung to the mother's ventrum (attached response) while others jumped away quickly (aloof response). Prior dyadic interactions were not significantly associated with this dichotomous response, nor were maternal and most infant variables. These results suggest that dyads at risk for neonate separation when living in captive groups are not necessarily at risk in individual housing conditions. Further, pig-tailed neonates appear unaffected by variations in mother-infant interactions that do not result in separation, but neonatal characteristics may show continuity across development.     

Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism

BTBR T+ tf/J (BTBR) is an inbred mouse strain that displays social abnormalities and repetitive behaviors analogous to the first and third diagnostic symptoms of autism. Here we investigate ultrasonic vocalizations in BTBR, to address the second diagnostic symptom of autism, communication deficits. As compared to the commonly used C57BL/6J (B6) strain, BTBR pups called more loudly and more frequently when separated from their mothers and siblings. Detailed analysis of ten categories of calls revealed an unusual pattern in BTBR as compared to B6. BTBR emitted high levels of harmonics, two-syllable, and composite calls, but minimal numbers of chevron-shaped syllables, upward, downward, and short calls. Because body weights were higher in BTBR than B6 pups, one possible explanation was that larger thoracic size was responsible for the louder calls and different distribution of syllable categories. To test this possibility, we recorded separation calls from FVB/NJ, a strain with body weights similar to BTBR, and 129X1/SvJ, a strain with body weights similar to B6. BTBR remained the outlier on number of calls, displaying low numbers of complex, upward, chevron, short, and frequency steps calls, along with high harmonics and composites. Further, developmental milestones and growth rates were accelerated in BTBR, indicating an unusual neurodevelopmental trajectory. Overall, our findings demonstrate strain-specific patterns of ultrasonic calls that may represent different lexicons, or innate variations in complex vocal repertoires, in genetically distinct strains of mice. Particularly intriguing is the unusual pattern of vocalizations and the more frequent, loud harmonics evident in the BTBR mouse model of autism that may resemble the atypical vocalizations seen in some autistic 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.     

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.     

Dyadic interactions of infant lowland gorillas in an outdoor exhibit compared to an indoor holding area

The behavior of two lowland gorilla mother-infant pairs living in a social group at Zoo Atlanta was compared in an indoor holding area vs. an outdoor exhibit. Focal animal data were collected for each pair during 30-min observation sessions over 24 days, alternating between indoors and outdoors. A variety of individual and social behaviors differed in the two conditions, particularly infant behaviors and infant-controlled behaviors. Mothers and infants spent more time closer together inside than outside, and infants left mothers more and mothers approached infants more outside than inside. Additional differences included more object examination and solitary play by the infants, and more feeding by the mothers, outside. Mothers autogroomed more and infants engaged in more self-manipulation inside. Additionally, there were significantly more aggressive display behaviors directed toward the mother-infant pairs inside than outside, and the adults engaged in coprophagy inside but not outside. A variety of other behaviors measured did not change between the two environments. There was a clear effect on behavior of the different housing conditions in which the gorillas were kept. © 1994 Wiley-Liss, Inc.