Reproduction in wild female olive baboons

The purpose of this paper is to evaluate several factors that influence female reproduction in a large troop of wild olive baboons (Papio cynocephalus anubis) based on 4 consecutive years of demographic data. Interbirth intervals were significantly shorter for females whose infants died before their next conception than for females whose infants survived. High-ranking mothers of surviving infants had significantly shorter birth intervals than comparable low-ranking mothers, independent of maternal age. This occurred mainly because the interval from resumption of cycling to conception was significantly shorter for high-vs. low-ranking females. Dominance rank did not influence sex ratio at birth, infant survival in the first 2 years, or adult female mortality. Age was also significantly related to interbirth intervals, with older females having shorter intervals. Primiparous females had consistently longer reproductive intervals than did multiparous females, but this difference reached statistical significance only for females whose infants died before the next conception. Primiparous females also experienced significantly higher infant mortality. Data on body size and estrous cycle length indicated no differences between high- and low-ranking females. Nutritional and stress-related mechanisms that may underlie the reproductive advantages of high rank are discussed.     

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.     

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.     

Effects of rearing on aggression and subordination in papio monkeys

The objective of this study is to assess the effects of short-term maternal deprivation (birth to 12 weeks) followed by peer group rearing on the development of aggressive and subordinate behaviors in papio monkeys (superspecies – Papio cynocephalus). Nursery reared monkeys (34 males and 30 females) were compared with mother-peer reared monkeys (11 males and 12 females) in late infancy (6 to 12 months of age) and at the end of their juvenile stage (36 to 42 months of age) in social groups composed of 75% nursery reared subjects and 25% mother reared subjects. Focal animal data were analyzed with a repeated measure ANOVA model. In general, the nursery reared infants tended to be less aggressive than mother-peer reared infants and performed less dominance behaviors, such as displace. Significant sex differences were present in the performance of aggressive (♂ > ♀) and subordinate (♂ > ♀) behaviors. Significant age differences were observed, with infants having consistently higher rates of performance.     

Differences in fertility and suckling patterns between primiparous and multiparous rhesus mothers (Macaca mulatta)

Primiparous females gave birth around the same time as multiparous nonlactating females, and earlier than did multiparous lactating females. No differences in birth sex ratio were found between primiparous and multiparous females. During the breeding season following birth, primiparous mothers returned to oestrus later than did multiparous mothers, and while few primiparous mothers conceived successfully during that season, most multiparous mothers did. Primiparous females suckled their infants more frequently than did multiparous females at all ages; infants of primiparous females also made more nipple contacts per bout, and had shorter sucking bouts. When mothers came into oestrus, suckling frequency drastically increased for primiparous females, but not for multiparous females, magnifying the differences between the two groups. After the first oestrus, suckling frequency declined for all mothers, but multiparous mothers had consistently lower suckling frequencies than did primiparous mothers. The high suckling frequency, and numerous nipple contacts per bout, found among primiparous mothers are likely to be related to the low reproductive chances that these females faced during the breeding season. Multiparous mothers seemed to compensate for their low suckling frequency by lengthening the suckling bouts, and this suckling pattern did not hinder their reproduction. It is argued that primiparous mothers might have to suckle their infants more frequently because they can only produce milk at slow rates, being in this way forced into a reproductively inhibiting suckling pattern. However, the delay in subsequent reproduction could be ultimately advantageous for primiparous mothers if it enhanced infant survival, and allowed the mothers to regain physical condition before reproducing again.     

Impact of Male Takeovers on Infant Deaths,Births and Conceptions in Cebus capucinus at Santa Rosa,Costa Rica

Male takeovers are associated with infant wounding and death in 3 of 4 capuchin species. In this paper, I analyze the effects of male takeovers on infant mortality and the subsequent conceptions and interbirth intervals of their mothers over an 18-yr period and test predictions of the sexual selection model of infanticide for white-faced capuchins, (Cebus capucinus). Major findings are that infants are significantly more likely to die in the 3- and 12-mo periods following a takeover than in times of peace and that a female whose infant dies experiences a significantly shorter interbirth interval before her next infant is born than she would have had the former infant survived. In the vast majority of cases, the invading males become resident in the group and are present during the subsequent conceptions of the females in the group. However, overall conception rates do not rise significantly in the year after a takeover, there is no relationship between the age of the infant at death and the length of the mother's subsequent interbirth interval, and it is not yet clear if male infants are preferentially targeted by invading males. Most takeovers occur during the 6-mo dry season and most conceptions occur in the wet season, 3–6 mo later. My findings support the major predictions of the sexual selection model of infanticide in primates and demonstrate that male takeovers of social groups have substantial effects on infant survival and maternal parturition patterns in Cebus capucinus.     

Life history traits, maternal behavior and infant development of blue-eyed black lemurs (Eulemur flavifrons)

An understanding of recruitment is important for estimating population growth and viability, and their implications for conservation. We present the first results regarding the life history, maternal behavior and infant development of the critically endangered blue-eyed black lemur (Eulemur flavifrons) of Madagascar. The species breeds seasonally, with births occurring at the end of the dry season, between late August and October. Over two successive birth seasons in 2006 and 2007, we observed a total of 13 lactating females and 22 infants from six groups. We inferred age at first reproduction as 3 years, and calculated the birth rate as 1.0 infant per female per year with a mean inter-birth interval of 358 ± 24.81 days (319-410 days). Infants spent the first 3 weeks of life constantly with their mothers; locomotor independence and ingestion of solid food began at week 10, and the infants were weaned by week 25. After week 28, infants spent less than 20% of their time in contact with their mothers. Over the study period infant mortality was 22.7%, with predation and sickness observed as causes. Our results suggest that overall recruitment is relatively slow, which has implications for the species' survival, particularly given their restricted and threatened habitat.     

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.     

Discrimination of mother by infant among Japanese Macaques (Macaca fuscata)

Experiments on five mother-infant pairs of Japanese monkeys (Macaca fuscata)living together in a captive group were conducted during the first 12 weeks after birth in order to assess the time at which infants begin to discriminate their own mothers from other adult females. After removal from their social group, infants exposed to their mothers and three unfamiliar adult females at a distance of 150 cm failed to orient visually toward their mothers. However, when the infants were allowed to approach the four females, they responded preferentially to their mothers during the third month of life. We concluded that by 8–12 weeks of age, infant Japanese macaques are able to discriminate between their mothers and other adult females.     

The influence of birth timing upon infant growth and survival in Captive Rhesus Macaques (Macaca mulatto)

Weights, growth rates, and mortality data of 815 captive-born Macaca mulattainfants were studied to determine if date of birth influences infant growth and survival. The six groups studied displayed a unimodal spring-summer birth season that has become systematically more restricted since 1977. Males exhibited higher rates of stillbirth and neonatal death and were more frequently born outside the normal birth season, when infant mortality was more common. Within the normal birth season, infant weight increased linearly with birth date, and infant growth rate declined linearly with birth date. Female infants with weights and growth rates near the developmental norm, especially those born in the middle of the birth season, have the greatest probability of survival. Males are more likely to survive if their weights and growth rates exceed the developmental norm, and thus male infants might be initially more costly to produce than female infants. These results are inconsistent with the hypothesis that offspring of high-ranking males, which conceived predominantly in the first third of the breeding season, enjoy a selective advantage.     

Birth sex ratios and maternal social rank in a captive colony of rhesus monkeys (Macaca mulatta)

Data from a 35-year study of rhesus macaques (Macaca mulatta) at Madingley, Cambridge, were used to investigate sex ratio biases associated with maternal rank. Data were available from two colonies, the Old colony (1960–81) and New colony (1982–93). Overall, top-ranking mothers gave birth to 30.9% sons, while non-top mothers gave birth to 58.4% sons. Among non-top mothers, middle- and bottom-ranking ones had 59.0 and 55.0% sons, respectively. Top mothers' daughter biases were strongest in matrilines with two adult females in the year the infants were conceived (15.4 sons and 14.3% sons in Old and New colonies). Non-top mothers' son biases (88.9 and 71.0% in Old and New colonies) were strongest in matrilines with 3 females. The findings are discussed in relation to the colonies' small matriline sizes and data on breeding performance and infant survival, which indicate the costs to mothers of different rank of having different sex infants. Overall, top-ranking mothers were more likely to breed in two successive years (78.6%) than non-top mothers (56.7%). Infant survival to 7 days was significantly higher in the New colony (89.0%) than the Old colony (75.3%), with daughters born to Old colony mothers doing especially poorly. We point out that between-group and between-species comparisons of sex ratio effects depend critically on how females are assigned to rank categories, and require information about divergences of sex ratios from 50:50 in each category. © 1996 Wiley-Liss, Inc.     

The roles of DNA methylation of NR3C1 and 11β-HSD2 and exposure to maternal mood disorder in utero on newborn neurobehavior

Exposure to maternal mood disorder in utero may program infant neurobehavior via DNA methylation of the glucocorticoid receptor (NR3C1) and 11β-hydroxysteroid dehydrogenase type 2 (11β-HSD-2), two placental genes that have been implicated in perturbations of the hypothalamic pituitary adrenocortical (HPA) axis. We tested the relations among prenatal exposure to maternal depression or anxiety, methylation of exon 1F of NR3C1 and 11β-HSD-2, and newborn neurobehavior. Controlling for relevant covariates, infants whose mothers reported depression during pregnancy and showed greater methylation of placental NR3C1 CpG2 had poorer self-regulation, more hypotonia, and more lethargy than infants whose mothers did not report depression. On the other hand, infants whose mothers reported anxiety during pregnancy and showed greater methylation of placental 11β-HSD-2 CpG4 were more hypotonic compared with infants of mothers who did not report anxiety during pregnancy. Our results support the fetal programming hypothesis and suggest that fetal adjustments to cues from the intrauterine environment, in this case an environment that could be characterized by increased exposure to maternal cortisol, may lead to poor neurodevelopmental outcomes.     

Birth rate and mortality rate of infants with congenital malformations of the limbs in the Awajishima free-ranging group of Japanese monkeys (Macaca fuscata)

The birth rate and mortality rate of infants with congenital malformations of the limbs were examined in the Awajishima free-ranging group of Japanese macaques (Macaca fuscata). Of the 606 infants born between 1978 and 1995, 86 (14.2%) were malformed. The male-female ratio did not differ between malformed and normal infants. Most kin-groups included females who gave birth to malformed infants at least once. The mortality rate within the first year after birth for malformed infants (28.2%) was significantly higher than that for normal infants (10.0%). However, this indicates that more than 70% of malformed infants were able to survive for the first year of life, even though they were unable to cling to their mothers ventrum due to their limb deformities. This finding indicates that maternal care-taking is sufficient to enable malformed infants to survive during the early stages of development and that clinging by the infant is not necessary for the display of maternal care. Am. J. Primatol. 42:225–234, 1997. © 1997 Wiley-Liss, Inc.     

Maternal Infant Monitoring in a Free-ranging Group of Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

In nonhuman primates, females with infants visually monitor their infants from a distance to detect and consequently avoid potential threats to their infants. We recorded maternal visual monitoring of infants (infant monitoring) ages 7–18 wk in a free-ranging, provisioned group of Japanese macaques (Macaca fuscata). The infant monitoring rate declined as a function of infants’ ages in weeks and increased when the infants were beyond their mother’s reach, indicating that infant monitoring reflects the vulnerability of infants. Females with infants increased infant monitoring when their infants were handled by other group members but not when their infants moved alone. This suggests that intragroup threats (harassment/mishandling or kidnapping) have a relatively stronger influence on infant monitoring than external threats (predation or infanticide) under the condition of this study. Infant monitoring of middle-/low-ranking females was more frequent than that of high-ranking females when their infants were handled by other individuals. This may reflect greater intragroup threats to infants of middle-/low-ranking females; however, further study is needed to confirm this. During important activities (feeding or grooming), the infant monitoring rate was lower than that during other activities (resting or self-directed behavior). However, even during important activities, females with infants increased infant monitoring when infants were handled. This indicates that females with infants face a trade-off between infant monitoring and other important activities, and even if females have to reduce the time spent on important activities, they increase infant monitoring when their infants face greater potential intragroup threats.     

Sex differences in infant integration in a semifree-ranging group of Barbary macaques (Macaca sylvanus,L. 1758) at Salem,Germany

Sixteen multiparous Barbary macaque females with newborns were studied over a 16 month period within the context of their naturally formed group. Analysis of their social behavior revealed 1) triadic interactions involving focal females, their newborns, and other group members occurred mainly with other females; and 2) mothers with female newborns interacted mainly with females of their own matriline, while mothers with male newborns interacted mainly with nonmatriline females. Observed in two successive birth seasons, this pattern indicates that partners of maternal interactions chose each other according to the sex of the newborn. Measures of distance from the mother also reflected differences between infants of different sex. At about five months of age, female infants were observed close to their mothers significantly more often than males. This finding follows the pattern of a sex-specific infant socialization process which integrates female infants into the network of their matrilines and male infants into the broader group. This sex-specific integration pattern is interpreted as supporting female philopatry and male dispersal. © 1995 Wiley-Liss, Inc.     

Proximity of residence to trichloroethylene-emitting sites and increased risk of offspring congenital heart defects among older women

BACKGROUND: Previous studies suggest that trichloroethylene (TCE) is a selective cardiac teratogen. We tested the hypothesis that the odds of maternal residence close to TCE-emitting sites would be greater among infants with congenital heart defects (CHDs) than among infants without CHDs. METHODS: We conducted a case-control study of 4025 infants, identified from hospital and birth records, born from 1997 to 1999 to Milwaukee, Wisconsin mothers. A geographic information system was used to calculate distances between maternal residences and TCE sites. We used classification tree analysis to determine appropriate values by which to dichotomously categorize mothers by TCE exposure (exposed: residence within 1.32 miles of at least one TCE site) and age (older: >/=38 years), and logistic regression to test for CHD risk factors. RESULTS: The proportion of mothers who were both older and had presumed TCE exposure was more than six-fold greater among case infants than among control infants (3.3% [8/245] versus 0.5% [19/3780]). When adjusted for other variables, CHD risk was over three-fold greater among infants of older, exposed mothers compared to infants of older, nonexposed mothers (adjusted OR, 3.2; 95% CI, 1.2-8.7). Older maternal age, alcohol use, chronic hypertension, and preexisting diabetes were each associated with CHDs (adjusted ORs, 1.9, 2.1, 2.8, 4.1; 95% CIs, 1.1-3.5, 1.1-4.2, 1.2-6.7, 1.5-11.2, respectively), but residence close to TCE sites alone was not. CONCLUSIONS: Our findings suggest that maternal age and TCE exposure interact to increase CHD risk, although the mechanism by which this occurs is unknown. A prospective study is underway to confirm this finding.     

Lactation and care for unrelated infants in forest-living ringtailed Lemurs

An adult female ringtailed lemur (Lemur catta) known not to have been pregnant showed spontaneous lactation in response to twin infants born to an unrelated female. The females had met only 7 months earlier, when they and two other unrelated adult females were released from separate locations in a forest enclosure to form a new social group. Three months after release, an adult male from an adjacent enclosure gained access to the new group for 1 day, the day of one female's estrus. No males had access to the females throughout the remainder of the breeding season. Within 2 weeks of the birth of the twins, one of the other adult females began carrying the infants frequently, typically one at a time. All three females were checked for lactation when the infants were two months old. Both their mother and the unrelated adult who had been carrying the infants were producing milk. The third adult female, who never carried either infant, had no milk. The third adult female, who never carried either infant, had no milk. This female, however, like the two maternal females, frequently attacked unfamiliar immigrating adult males when the males approached the infants. Potential implications of these observations concerning the social organization of ringtailed lemurs are discussed.     

A test of the randomness of paternity of members of maternal sibships in six captive groups of rhesus monkeys (Macaca mulatta)

Results of previous studies have shown that in captive groups of rhesus monkeys (Macaca mulatto)fathers associate more frequently with their own offspring than with those of other males and that mothers are most permissive of physical contact between their own infant and a juvenile when that juvenile shares the same father with her infant. These two observations suggest that the identity of offspring born in captive groups of rhesus monkeys is recognized by at least some adult members of the group. Consistent patterns of mating among mating seasons might explain this apparent recognition of offsprings’ paternity. Fathers, for example, might regularly associate with young who maintain a close relationship with females with whom they have previously mated, and mothers might selectively permit juveniles who maintain a close relationship with males with whom they have previously mated to associate with their infants. This hypothesis is tested in this paper by comparing the observed distribution of 70 maternal sibships, members of which were fathered by the same or by different adult males over a 4-year period in six captive groups of rhesus monkeys, with that distribution expected based on random mating from season to season. Seasonal mating patterns were found to be random. Preparations are now underway to test this hypothesis in several free-ranging groups.     

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.     

Birth-season interactions of adult female Japanese Macaques(Macaca fuscata) without newborn infants

The affiliative interactions of 11 adult female Japanese macaques that did not deliver an infant during the 1981 birth season of the Arashiyama West troop were examined. Consideration was given to the effects of kinship as a structuring element in these birth-season interactions and to the degree of association with various categories of troop members based on age, sex, and (in the case of adult females) whether or not the females were new mothers. Females without infants interacted predominantly with their yearling off-spring, although it was the behavior of the offspring that precipitated the interaction. These females were active in soliciting affiliation with nonkin new mothers, whereas female matrilineal relatives with new infants approached and remained in proximity to them more than did nonrelated new mothers. Females without newborns groomed and approached nonkin infants more than infants within their own matriline, and these infants were predominantly those of females in the highest-ranking matriline of the troop. Adult males were responsible for 40% of all grooming received from nonkin by the females without newborns, and these males approached them significantly more than did other adult females without infants. These patterns demonstrate that the structure of social relationships is influenced by the particular dynamics of troop contexts such as birth seasons, as well as by enduring, broad-based affinities which are less affected by cyclic changes in troop context.