Infant Development and Parental Care in Free-Ranging <Emphasis Type="Italic">Aotus azarai azarai</Emphasis> in Argentina

Studies of infant development and parental behavior in free-ranging owl monkeys have been constrained by their nocturnal habits. Taking advantage of the cathemeral activity pattern of Aotus azarai azarai in the Argentinean Chaco, we describe the development of a cohort of free-ranging infants born in an owl monkey population in Formosa Province. We observed 7 infants, whose birth dates are known to the nearest week, to record details of their development and care between October 1999 and March 2000. We collected 92 h of behavioral data in 76 sessions. The infants were almost never off the parents during the first 4 wk of life, and we observed no infant being transported by a nonadult. The parent carrying the infant traveled most frequently in the middle of the group, sometimes first, but rarely last. The mean duration of 33 nursing episodes is 69 sec. After nursing, the infant was more likely to return to the nonnursing adult than to remain with the mother suggesting that in owl monkeys the infant may be primarily attached to the adult male in the group. Infants began to explore, to manipulate and to consume solid foods during the second month. Our observations are comparable to ones on captive breeding groups of Colombian owl monkeys (Aotus lemurinus) and Bolivian owl monkeys (A. azarai boliviensis) under controlled conditions of temperature, illumination and food availability.     

Infant Carrying Behavior in Callitrichid Primates: Callithrix and Leontopithecus

Care of offspring by individuals other than the mother is ubiquitous in callitrichid primates. In spite of its widespread occurrence, however, there is considerable taxonomic variation in the timing and intensity of parental effort by breeding males and nonbreeding juvenile group members. These differences may be attributable to generic and specifies differences in the costs of reproduction for females or in ecological constraints on travel and foraging. We present data on patterns of infant carrying in social groups of two taxa of callitrichid primates (Callithrix and Leontopithecus) throughout the first 3 months of infant life. We evaluated patterns of care in small groups (two or fewer juvenile or subadult helpers) and in large groups (three or more helpers in addition to the breeding adult male and female). Group size had little effect on levels of maternal carrying effort in either marmosets or lion tamarins, and mothers ceased carrying infants by 3 months of age. Carrying efforts by fathers were significantly reduced in groups with many helpers relative to small groups. Helpers carried at consistent rates during the second and third months of infant life in Leontopithecus, while in Callithrix, carrying by helpers peaked during the second month. These results suggest that if helpers reduce energetic demands on lactating females, the mechanism by which helpers reduce these burdens is independent of maternal carrying effort.     

Nighttime Wakefulness Associated with Infant Rearing in Callithrix kuhlii

Parent-infant cosleeping occurs in human and nonhuman primates, yet studies on the impact of cosleeping on parental sleep patterns have been limited to human mothers. We examined the effects of cosleeping on the nighttime wakefulness of a biparental New World primate, Wied's black tufted-ear marmoset (Callithrix kuhlii). We compared the sleep patterns of marmoset parents caring for young infants to those without infants, using an 8 mm videocamera and timelapse VCR under infrared illumination. The presence of young infants significantly impacted the sleep of mothers but not fathers. In fact, mothers rearing young infants were awake >3 times as often as mothers without infants. We also examined the nighttime wakefulness of marmoset parents across the first 9 weeks of infant life (birth through weaning). Although callitrichid mothers tend to reduce their daytime investment in offspring very early in infant life by relinquishing the care of infants to fathers and alloparents, increased nighttime wakefulness was not limited to the early postpartum period for the mothers. Instead, mothers exhibited more nighttime wakefulness than fathers did across the first 9 weeks of infant life. Our results indicate that the presence of infants has a greater impact on the sleep patterns of Callithrix kuhlii mothers than fathers, suggesting that mothers are more involved in infant care than previously realized and that fathers are not nearly as involved in nighttime care as their behavior during the day would suggest.     

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.     

Relationship Between Infant and Mother Circadian Rest-Activity Rhythm Pre- and Postpartum,in Comparison to an Infant With Free-Running Rhythm

Some infants show a free-running rhythm in their rest-activity. We do not know why, nor do we know exactly what the entrainment factors are for the development of the normal 24-h rest-activity rhythm. Actigraphic recordings on 10 primiparae during late pregnancy and these mothers and their infants during the 2nd, 6th, and 12th wks after birth were made over 3–5 continuous days to investigate maternal and infant entrainment. One infant showed a free-running rest-activity circadian rhythm. In late pregnancy, the period in the autocorrelogram of the mother with the free-running infant was longer than the significant period of the mean autocorrelogram of the mothers with non-free-running infants. The finding of this study indicates the free-running rhythm of infant is not reset by maternal entrainment factors. (Author correspondence: nishihara-kk@igakuken.or.jp)     

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.     

It’s All in the Timing: Birth Seasonality and Infant Survival in <Emphasis Type="BoldItalic">Eulemur rubriventer</Emphasis>

Highly seasonal breeding has been considered one of the keys to understanding Malagasy primate socioecology. Strict seasonal breeding may be particularly critical for Malagasy primates because they live in such energetically challenging seasonal environments. Lemurs also live in highly unpredictable environments, and there is growing evidence that reproductive timing may be mediated by additional factors, suggesting that more relaxed breeding seasonality is adaptive in some cases. I tested the adaptive breadth of the birth peak in Eulemur rubriventer, which breed in several different months. I describe reproduction in the species by determining the timing and extent of the birth season (period in which all births occur) and birth peak (period in which the majority of births occur); test whether relaxed reproductive seasonality might increase reproductive success by comparing infant mortality within and outside the birth peak; and model the extent to which fruit availability has an influence on the timing of reproduction. I collected birth data on 5 groups in 2003–2005, which I combined with demographic data that D. Overdorff collected from 5 focal groups and additional censused groups between 1988 and 1996. Thirty births occurred in 8 different months. Births were significantly seasonal, with a unimodal birth peak in late August/September/October, and a mean birth date of October 11. Twenty-three births (76.7%) occurred within 54 d (14.79%) of the year. No births occurred May–July, indicating that conceptions did not occur from late December through late February, and cycling (estimated using gestation length) did not occur until ca. 101 d after the austral summer solstice (December 21). Of 22 infants followed regularly, 18 were born in the birth peak, of which 2 died (11%). All 4 infants born out of season died. Based on fruit availability, I calculated a Theoretical Overlap index (T), which indicated a 3-mo window with optimal food conditions for reproduction. This window corresponded to the timing and breadth of the birth peak in Eulemur rubriventer. These results indicate that a breeding season >3 mo within a given year is not adaptive in the species, likely due in large part to the availability of fruit during key reproductive stages, particularly before breeding.     

Observation of a birth among wild toque macaques (Macaca sinica)

Most toque macaques give birth to their infants during the night when resting arboreally. Here we report on a birth that occurred in daytime (at 0916 hr) and on the ground. The mother was 7.6 years old; the birth was her second. Prepartum behaviors included lordosis, arching of the back, stretching, squatting, rolling on the ground, and anogenital self-examination. During the birth the female was isolated about 100 m from the rest of her group. The mother stood bipedally during parturition and assisted delivery with her hands. The infant was born within 2 min after first appearing at the vulva. It immediately clung to the mother’s leg and vocalized. The mother licked the infant and oriented it toward her ventrum. She resumed foraging behavior within 20 min after parturition. The infant nursed for the first time 2.25 hr after being born. The mother ate part of the placenta, but the alpha female of the group usurped and also ate a portion of it. Curious group members sniffed and looked at the infant but did not touch it.     

Reproductive parameters of wild Trachypithecus leucocephalus: seasonality,infant mortality and interbirth interval

Understanding the reproductive parameters of endangered primate species is vital for evaluating the status of populations and developing adequate conservation measures. This study provides the first detailed analysis of the reproductive parameters of wild white‐headed langurs (Trachypithecus leucocephalus), based on demographic data collected over an 8‐year period in the Nongguan Karst Hills in Chongzuo County, Guangxi, China. From 1998 to 2002, a total of 133 live births were recorded in the population based on systematic censuses. Births occurred throughout the year, but the temporal pattern was highly correlated with seasonal variation in temperature and rainfall, with the birth peak coinciding with the dry and cold months of November–March. The average birthrate was 0.47±0.13 births per female per year and mortality for infants younger than 20 months was 15.8%. From 1998 to 2006, 14 females gave birth to 41 infants in four focal groups. The average age at first birth for female langurs was 5–6 years (n=5) and the interbirth interval (IBI) was 23.2±5.2 months (median=24.5 months, n=27). Infants are weaned at 19–21 months of age. The IBI for females with infant loss before weaning was significantly shorter than those for females whose infants survived. It appears that birth seasonality in the white‐headed langurs is influenced by seasonal changes in food availability. The timing of conceptions was found to coincide with peak food availability. The reproductive parameters for white‐headed langurs reported here are quite similar to those reported for other colobine species. One major difference is our observation of lower infant mortality in Trachypithecus. Am. J. Primatol. 71:558–566, 2009. © 2009 Wiley‐Liss, Inc.     

Daughter dearest: Sex‐biased calcium in mother's milk among rhesus macaques

Mother's milk provides building blocks necessary for infant development and growth postnatally. Minerals in milk are particularly important for infant skeletal development and may reflect maternal characteristics that are associated with the capacity to synthesize milk and sex‐specific developmental priorities of the infant. Using a large sample of mother–infant dyads assigned to the outdoor breeding colony at the California National Primate Research Center (N=104), we investigated the relationship of milk calcium (Ca) and phosphorus (P) concentrations and the ratio of Ca/P to maternal and infant characteristics and to other milk variables. Ca and P are largely associated with casein micelles, and as expected, both Ca and P were positively correlated with protein concentrations in milk. Neither Ca nor P concentrations were associated with maternal parity. Mothers rearing daughters tended to produce higher mean Ca concentration in milk, and consequently a higher Ca/P ratio, than did mothers rearing sons, even though protein concentration was not elevated. These results suggest that the Ca/P ratio in rhesus milk may have been under separate selective pressure from protein content to facilitate the accelerated rate of skeletal calcification that has been observed in female Macaca mulatta infants. Am J Phys Anthropol 151:144–150, 2013. © 2013 Wiley Periodicals, Inc.     

A method for encouraging maternal care in the giant panda

We developed a method to facilitate maternal care in a giant panda (Ailuropoda melanoleuca) female that rejected her cub immediately after parturition. After removal of the cub, the female was systematically exposed to a regime of infant‐related stimuli, including a surrogate toy panda, accompanied by infant vocalizations and urine, and the mother's own milk. The female displayed several measures of maternal behavior toward the surrogate, for example, spending 61% of her time holding the surrogate in positions typical for the species. There was some evidence that maternal proficiency increased across the 4 weeks of the experiment. Results also indicate that the female was responsive to both infant vocalizations and urine, but not milk. After a transitional period in which we assisted the female in her efforts to nurse and groom the infant, all maternal care‐giving responsibilities were returned to the mother. Over the next 3 months, the pattern of maternal care followed the species‐typical course of declining mother‐infant contact, grooming, overall interaction time, and responsiveness to the cub's vocalizations. This study marks the first successful reunification of a giant panda mother with an infant separated at birth and, it is hoped, will serve as a model for similar efforts elsewhere. Zoo Biol 19:53–63, 2000. © 2000 Wiley‐Liss, Inc.     

Attachment and social preferences in cooperatively-reared cotton-top tamarins

In many primate species a close attachment between mother and infant provides a secure base for the infant when the infant is frightened or under stress. In cooperatively breeding primates infant carrying is divided among several individuals in the group, with the mother often doing little more than nursing. In these species it is not clear which individual would best serve as a secure base for the infant. We studied eight infant cotton-top tamarins from birth through 20 weeks of age, noting who carried the infant during the first 100 days, who transferred food with the infants, and, as infants became independent, with whom they associated during social play and affiliative behavior. From week 9 to week 20, when infants were independent of carriers most of the time, we presented families with six trials (once every 2 weeks) with a threatening stimulus (a human dressed in a lab coat and wearing an animal mask). Infants played primarily with their twin or youngest sibling and had affiliative interactions with many family members. However, in fearful situations, infants ran to those who had carried them and transferred food with them the most-their father or oldest brother (never to the mother). Although adults increased rates of mobbing calls in response to the threat, infants significantly reduced their vocalization rate. For these cooperatively breeding monkeys, the attachment object for infants is the family member that invested the most effort in carrying the infant and transferring food with the infant. These results parallel and extend results from bi-parental infant care species in which the father serves as the primary attachment figure.     

Neonatal nipple preference and maternal cradling laterality in wild Taihangshan macaques (Macaca mulatta tcheliensis)

Lateralized behavior is considered an observable phenotype of cerebral functional asymmetry and has been documented in many mammalian species. In the present study, we examined evidence of lateralization in neonatal nipple contact, maternal cradling, and the relationship between these two behaviors during the first 12 weeks of life in wild Taihangshan macaques (Macaca mulatta tcheliensis). The results showed that across our sample of nine mother–infant dyads: (1) Seven of nine neonates exhibited a significant left-side nipple preference during the first 12 weeks of life, whereas eight of nine mothers displayed a significant right-side cradling preference; (2) at the population level, there was a significant preference for left nipple contact by neonatal Taihangshan macaques and a significant right-hand maternal cradling preference; (3) at the population level, there was a nonsignificant negative correlation between neonatal nipple preference and maternal cradling bias; and (4) the strength of individual neonatal nipple preference and maternal cradling laterality were not correlated. We conclude that asymmetry in nipple contact of Taihangshan macaques occurs early in behavioral development. Given that infant Taihangshan macaques are able to nurse and cling unassisted to their mothers within a few days after birth, it appears that the infant rather than its mother is responsible for determining a nipple-side preference. Our results indicating a left-side nipple bias in 78% of wild neonatal Taihangshan macaques are most consistent with the heartbeat hypothesis.     

Factors affecting weaning weight in Antarctic fur seals Arctocephalus gazella at South Georgia

Summary Relationships between size, body condition, age and feeding-attendance patterns during pup rearing of female Antacrtic fur seals Arctocephalus gazella and their effects on the timing of birth and weaning, pup weight, growth and condition were studied at South Georgia in 1981–1982. Twenty-seven (6 male, 21 female) mother-pup pairs were followed from birth to weaning. The analysis of maternal effects was limited to female pups because of the small sample size of male weaners. High weaning weight was associated with those female pups whose mothers spent more time ashore attending their offspring. Weaning weight showed no relationship with perinatal duration, number of feeding trips to sea, days at sea or date of weaning. A further 63 mother-pup pairs were analysed for the effects of maternal body condition (weight/length), age and timing of birth on offspring body weight and condition. Pup weight and condition were weakly correlated with maternal age in female pups. Male pups born earlier in the season were heavier and in better condition. Maternal and offspring body weight and condition were unrelated. For the Antarctic fur seal population at South Georgia where the food supply was apparently not limiting in summer, maternal condition and foraging time were subordinate to maternal care on land (as expressed by attendance duration) in determining offspring weight at weaning.     

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.     

Infant abuse associated with psychosocial stress in a group-living pigtail macaque ( Macaca nemestrina) Mother

This study reports a case of infant abuse by a pigtail macaque mother living in a captive social group. Patterns of abusive behavior appeared three weeks after the birth of the infant and were in strict temporal as sociation with the repeated kidnapping and severe harassment of the infant by the alpha-female in the group. Before and after the period of social stress, the mother exhibited proper caregiving behavior towards her infant. The analysis of the abusive mother's style of interaction with her infant relative to three control mothers indicated that she was an extremely permissive mother. It is argued that the mother's failure to adapt her mothering style to better protect her infant during the period of repeated kidnappings and the resulting lack of control over the situation may be the mechanism by which stress precipitated infant abuse. © 1994 Wiley-Liss, Inc.     

Synchronization of weaning time with peak fruit availability in squirrel monkeys (Saimiri collinsi) living in Amazonian Brazil

Many mammals coincide their reproductive activities with factors such as ambient temperature, rainfall, and food availability. In primates that invest immediate food intake into reproduction, the periods of maximum fruit production often coincide with the peak of lactation (to maximize maternal survival) or the occurrence of weaning (to maximize infant survival). This study investigates the relationship between reproductive periods and the availability of ripe fruit in the habitat of a population of wild squirrel monkeys (Saimiri collinsi) in Amazonian Brazil. We combine data from several years (2002–2003; 2011–2015) during which we followed the monkeys and quantified the occurrence of matings, gestations, births, and the number of lactating females. We also collected rainfall and plant phenological data for 24 months. Our results confirm that reproductive events are highly seasonal in S. collinsi. The period of weaning corresponded to the peak in the abundance of ripe fruits consumed by the monkeys. This indicates that the period of infant nutritional independence is optimally timed to coincide with periods of greater food production in this habitat. We suggest that seasonal breeding in these primates does not necessarily reduce maternal energetic stress, but likely improves infant survivorship.     

感染与早产儿脑损伤临床关系探讨

目的:探讨感染与早产儿脑损伤(HIE,ICH,CWMD)的临床表现,治疗,预后和预防的关系。方法:对2000年1月-2006年10月214例早产儿进行临床分析。结果:胎膜早破32例,母亲妊高症23例,胎儿宫内窘迫33例,脐带扭转打结7人,母亲妊娠糖尿病4人,胎儿畸形4人;早产儿肺炎101人,早产儿寒冷损伤综合征7人,早产儿急性坏死性小肠结肠炎5人,低血糖症27人,低血钙症13人,早产儿缺氧缺血性脑病(HIE)76人,早产儿颅内出血(ICH)21人,早产儿脑白质损伤(CWMD)3人。早期诊断、合理抗感染治疗可减少早产儿HIE及ICH以及CWMD患儿的神经系统后遗症。结论:早产儿感染与HIE及ICH以及CWMD的关系密切,预防产前、产时、产后感染对减少或减轻早产儿脑损伤至关重要。     

Relationship of early infant state measures to behavior over the first year of life in the tufted capuchin monkey (Cebus apella)

Data on activity states were collected from 29 group-housed capuchin monkey (Cebus apella) infants for 3 h each week from birth to 11 weeks of age. The amounts of time spent in sleeping/drowsy, alert–quiet, and alert–active states were measured in these subjects. Videotaped observations of these infants were recorded 3 times/week in the home cage over the first year of life and were scored for a number of social and exploratory behaviors. The extent to which early infant activity state scores predicted later behavior in the home cage was examined. Infant state measures correlated significantly with home cage behavior during months 2–6 in that infants that had been more active in early infancy spent more time alone, with other animals, and in exploration and play and less time with mothers than did quieter infants. Early state measures were less successful in predicting home cage scores beyond 8 months of age, whereas differences in behavior attributable to housing variables became more salient in the latter part of the first year. There was also a negative correlation between mother and infant activity in months 2 and 3, in that more sedentary mothers tended to have more active infants. Am. J. Primatol. 44:43–56, 1998. © 1998 Wiley-Liss, Inc. This article is a U.S. Government work, and, as such, is in the public domain in the United States of America.     

Growth and development of infant giant pandas (Ailuropoda melanoleuca) at the Wolong Reserve,China

From 1991 to 1993 inclusive, seven infant giant pandas (Ailuropoda melanoleuca) were born at the China Conservation and Research Center for the Giant Panda. Average daily weight gain in the first 6 months for mother-reared infants (n = 5) was 71.3 g/day; for one partially mother-reared and partially hand-reared infant, 41.5 g/day; and for one completely hand-reared infant, 50.3 g/day. There was a significant difference in growth rates across the first 6 months in all methods of rearing. In addition, a comparison of growth rates across the three rearing methods showed significant differences in the first, second, third, fifth, and sixth months. Average daily body length increase for mother-reared infants was 4.1 mm/day; for partially mother-reared/partially hand-reared infants, 4.0 mm/day; and for the completely hand-reared infant, 2.8 mm/day. In mother-reared infants, body length increase during the first month was significantly greater than during the following months, and was slowest during the sixth month. At birth, infants were all pink in color with a light white coat of lanugo. Black pigmentation was first noted at 7–10 days of age, which was also the time that initial hair coat growth was seen. Eyes opened at 35–48 days of age. Ears opened at 31–50 days of age. Deciduous dentition was first seen at 82–121 days of age, while permanent dentition began to erupt at 350 days of age. © 1996 Wiley-Liss, Inc.