Rhesus macaque milk: magnitude, sources, and consequences of individual variation over lactation

Lactation represents the greatest postnatal energetic expenditure for mammalian mothers, and a mother's ability to sustain the costs of lactation is influenced by her physical condition. Mothers in good condition may produce infants who weigh more, grow faster, and are more likely to survive than the infants of mothers in poor condition. These effects may be partially mediated through the quantity and quality of milk that mothers produce during lactation. However, we know relatively little about the relationships between maternal condition, milk composition, milk yield, and infant outcomes. Here, we present the first systematic investigation of the magnitude, sources, and consequences of individual variation in milk for an Old World monkey. Rhesus macaques produce dilute milk typical of the primate order, but there was substantial variation among mothers in the composition and amount of milk they produced and thus in the milk energy available to infants. Relative milk yield value (MYV), the grams of milk obtained by mammary evacuation after 3.5-4 h of maternal-infant separation, increased with maternal parity and was positively associated with infant weight. Both milk gross energy (GE) and MYV increased during lactation as infants aged. There was, however, a trade-off; those mothers with greater increases in GE had smaller increases in MYV, and their infants grew more slowly. These results from a well-fed captive population demonstrate that differences between mothers can have important implications for milk synthesis and infant outcome.     

No evidence for sex biases in milk macronutrients,energy, or breastfeeding frequency in a sample of filipino mothers

Maternal reproductive investment includes both the energetic costs of gestation and lactation. For most humans, the metabolic costs of lactation will exceed those of gestation. Mothers must balance reproductive investment in any single offspring against future reproductive potential. Among mammals broadly, mothers may differentially invest in offspring based on sex and maternal condition provided such differences investment influence future offspring reproductive success. For humans, there has been considerable debate if there are physiological differences in maternal investment by offspring sex. Two recent studies have suggested that milk composition differs by infant sex, with male infants receiving milk containing higher fat and energy; prior human studies have not reported sex‐based differences in milk composition. This study investigates offspring sex‐based differences in milk macronutrients, milk energy, and nursing frequency (per 24 h) in a sample of 103 Filipino mothers nursing infants less than 18 months of age. We found no differences in milk composition by infant sex. There were no significant differences in milk composition of mothers nursing first‐born versus later‐born sons or daughters or between high‐ and low‐income mothers nursing daughters or sons. Nursing frequency also showed no significant differences by offspring sex, sex by birth order, or sex by maternal economic status. In the Cebu sample, there is no support for sex‐based differences in reproductive investment during lactation as indexed by milk composition or nursing frequency. Further investigation in other populations is necessary to evaluate the potential for sex‐based differences in milk composition among humans. Am J Phys Anthropol 152:209–216, 2013. © 2013 Wiley Periodicals, 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.     

Growth in colony living anubis baboon infants and its relationship with maternal activity budgets and reproductive status

Early growth is of interest because it is susceptible to maternal effects and linked to fitness components for a range of species. Here we present anthropometric measurements on 23 infant olive baboons born into a captive colony in order to describe growth over the first 2 years of life, to explore maternal influences on growth, and to assess the impact of growth profiles on maternal reproduction. Six main findings emerged: 1) Infant growth rates in our colony were higher than those reported for wild populations but comparable to those observed for food-enhanced animals. 2) The ratio of infant mass to maternal mass was positively associated with reproductive parameters, such as duration of post-partum amenorrhea and interbirth interval. 3) Mothers resumed cycling and reconceived when their infants attained a relatively consistent threshold mass. 4) Infant mass-for-age was associated with maternal rank and, independently, with maternal mass such that females of high dominance rank and heavy females had relatively large infants at their resumption of cycling. 5) Low-ranking and lighter females had longer investment periods but smaller infants. They continued investment in infant through prolonged lactation until their infants reached a mass similar to that of infants of high-ranking/heavy mothers, suggesting that the lengthening of investment is essentially compensatory for slow early growth. 6) There was no relationship between infant growth and maternal activity budgets. Maternal physical and social factors, not energetics, contributed to differences among infants in growth trajectories, and infant growth temporally influenced successive reproductive events.     

Peer interaction in infant chimpanzees

The peer interactions of 6 infant chimpanzees (Pan troglodytes) ranging in age from 18 to 50 months were observed in a seminatural context. The infants and their mothers lived as members of a captive social group at the Yerkes Regional Primate Research Center. An analysis of contact initiations between infants indicated that the most preferred peer interactant was the youngest and the least preferred was the oldest infant. Infants also initiated more interactions with the offspring of adults that had the closest relationships with both themselves and their mothers. These results indicate that a number of factors may influence the peer affiliations of infant chimpanzees, including the age of the infant and the mother's social relationships.     

A physiological role of breast milk leptin in body weight control in developing infants

Objective: Leptin, a hormone that regulates food intake and energy metabolism, is present in breast milk. The aim of this study was to determine whether milk leptin concentration is correlated with maternal circulating leptin and BMI and with body weight gain of infants. Research Methods and Procedures: A group of 28 non‐obese women (BMI between 16.3 and 27.3 kg/m²) who breast‐fed their infants for at least 6 months and their infants were studied. Venous blood and milk samples were obtained from mothers at 1, 3, 6, and 9 months of lactation, and leptin concentration was determined. Infant body weight and height were followed until 2 years of age. Results: During the whole lactation period, milk leptin concentration correlated positively with maternal plasma leptin concentration and with maternal BMI. In addition, milk leptin concentration at 1 month of lactation was negatively correlated with infant BMI at 18 and 24 months of age. A better negative correlation was also found between log milk leptin concentration at 1 and at 3 months of lactation and infant BMI from 12 to 24 months of age. Discussion: We concluded that, in a group of non‐obese mothers, infant body weight during the first 2 years may be influenced by milk leptin concentration during the first stages of lactation. Thus, moderate milk‐borne maternal leptin appears to provide moderate protection to infants from an excess of weight gain. These results seem to point out that milk leptin is an important factor that could explain, at least partially, the major risk of obesity of formula‐fed infants with respect to breast‐fed infants.     

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.     

Fatal attraction: interest in infants and infant abuse in rhesus macaques.

This study investigated whether infant abuse by female rhesus macaques (Macaca mulatta) is a phenomenon specific to their own offspring or reflects a general tendency to interact negatively with infants. Several aspects of the relationship between maternal behavior, infant handling, and infant harassment were also investigated. Study subjects were 20 group-living rhesus mothers with their infants observed during the first 12 weeks of lactation. The results of this study indicate that abusive mothers are highly attracted to infants in general but that infant abuse is a phenomenon specific to their own offspring. Infant harassment is not an accidental by-product of infant handling or the result of maternal inexperience but it is likely related to reproductive competition among lactating females. Maternal behavior and infant handling may be regulated by similar proximate mechanisms, but probably have different adaptive functions and evolutionary history across the Primate order. Am J Phys Anthropol 110:17-25.     

Neonatal abandonment in Japanese macaques

This study analyzed long-term demographic data relative to a captive colony of Japanese macaques (Macaca fuscata) in order to evaluate factors predicting increased probability of infant neonatal abandonment. Overall, 7.7% of liveborn infants were abandoned at birth. Probability of abandonment was significantly increased in primiparous and, to a lesser extent, low-ranking mothers. Primiparous mothers abandoned about 40% of their infants at birth. Mother age and infant sex had no independent effects on the probability of neonatal abandonment. Primiparous mothers that did not abandon their infants suffered increased infant mortality and showed longer interbirth intervals compared to same-age multiparous mothers. These results are partially consistent with adaptive hypotheses predicting maternal divestment under unfavorable conditions, and with proximate explanations linking abandonment to inexperience and stress.     

Milk Composition during Lactation Suggests a Mechanism for Male Biased Allocation of Maternal Resources in the Tammar Wallaby (Macropus eugenii)

Recent research has found empirical evidence in support of the Trivers-Willard Hypothesis that offspring sex allocation is correlated with maternal investment. Tammar wallabies birthing sons have higher investment ability; however a mechanism for sex specific differential allocation of maternal resources in wallabies remains elusive. In metatherians the majority of maternal investment is during lactation. To examine if differential allocation occurs during lactation, we measured total milk protein, lipid and carbohydrates, from mothers with male and female pouch young, during phase 2B (100–215 days post partum) and phase 3 (215–360 days post partum) of lactation. Mothers of sons allocated significantly higher levels of protein than mothers of daughters during phase 2B of lactation, however no sex specific difference in maternal allocation was found for lipids, carbohydrates, or any milk component during phase 3 of lactation. We were unable to measure milk production to establish any differences in the amount of milk allocated. However, with the production of more milk comes a dilution effect on milk components. Given that we find no apparent dilution of milk components may suggest equality in milk production. Offspring body weight at 14 months of age was related to protein allocation during phase 2B of lactation, providing a maternal mechanism for differential allocation with fitness consequences. We believe collection of earlier phase 2A (0–100 days post partum) milk may yield important results given that differential investment in metatherians may be most apparent early in lactation, prior to any significant maternal investment, when a decision on termination of investment can be made with very little energetic loss to the mother. Interestingly, small mothers did not birth sons and better maternal condition was associated with raising sons. These data are in support of TWH and demonstrate a potential mechanism through which condition dependent and sex specific maternal investment may occur.     

Changes in maternal postpartum adiposity and infant feeding patterns

The relationship between maternal fatness and infant feeding practices was studied in 46 healthy Caucasian women from parturition to 6 months postpartum. Mothers reported infant feeding practices in diary form throughout the study. Weight, triceps and subscapular skinfolds, and midarm circumference were measured on seven occasions. Upper arm fat area was computed. All women breast fed their infants for at least 5 months, with no nonbreast milk food introduced for at least 2 months. All women had declining or stable postpartum weights. Linear regressions of upper arm fat area on days since parturition were used to ascertain overall direction of change in adiposity for each woman. Declining fat area occurred in 17 cases and was associated with a breast-feeding pattern of short frequent feeds. In the remaining 29 cases, increasing fat area was associated with significantly longer and less frequent feeds. It is hypothesized that these different fat change patterns result from differential activity of adipose tissue lipoprotein lipase, which is itself mediated by serum prolactin concentration. Relevance of these findings for resolution of the controversy surrounding the critical body composition hypothesis and lactation amenorrhea is discussed.     

Rapid Postnatal Weight Gain and Visceral Adiposity in Adulthood: The Fels Longitudinal Study

Rapid infant weight gain is associated with increased abdominal adiposity, but there is no published report of the relationship of early infant growth to differences in specific adipose tissue depots in the abdomen, including visceral adipose tissue (VAT). In this study, we tested the associations of birth weight, infant weight gain, and other early life traits with VAT, abdominal subcutaneous adipose tissue (ASAT), and other body composition measures using magnetic resonance imaging (MRI) and dual‐energy X‐ray absorptiometry in middle adulthood (mean age = 46.5 years). The sample included 233 appropriate for gestational age singleton white children (114 males) enrolled in the Fels Longitudinal Study. Multivariate‐adjusted general linear models were used to test the association of infant weight gain (from 0 to 2 years), maternal BMI, gestational age, parity, maternal age, and other covariates with adulthood body composition. Compared to infants with slow weight gain, rapid weight gain was associated with elevated risk of obesity (adjusted odds ratio = 4.1, 95% confidence interval = 1.4, 11.1), higher total body fat (+7 kg, P = 0.0002), percent body fat (+5%, P = 0.0006), logVAT mass (+0.43 kg, P = 0.02), logASAT mass (+0.47 kg, P = 0.001), and percent abdominal fat (+5%, P = 0.03). There was no evidence that the increased abdominal adipose tissue was due to a preferential deposition of VAT. In conclusion, rapid infant weight gain is associated with increases in both VAT and ASAT, as well as total adiposity and the risk of obesity in middle adulthood.     

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.     

Innate protection conferred by fucosylated oligosaccharides of human milk against diarrhea in breastfed infants

To test the hypothesis that human milk fucosyloligosaccharides are part of an innate immune system, we addressed whether their expression (1) depends on maternal genotype and (2) protects breastfed infants from pathogens. Thus the relationship between maternal Lewis blood group type and milk oligosaccharide expression and between variable oligosaccharide expression and risk of diarrhea in their infants was studied in a cohort of 93 Mexican breastfeeding mother-infant pairs. Milk of the 67 Le(a-b+) mothers contained more LNF-II (Le(a)) and 3-FL (Le(x)) (oligosaccharides whose fucose is exclusively alpha 1,3- or alpha 1,4-linked) than milk from the 24 Le(a-b-) mothers; milk from Le(a-b-) mothers contained more LNF-I (H-1) and 2'-FL (H-2), whose fucose is exclusively alpha 1,2-linked. The pattern of oligosaccharides varied among milk samples; in each milk sample, the pattern was summarized as a ratio of 2-linked to non-2-linked fucosyloligosaccharides. Milks with the highest ratios were produced primarily by Le(a-b-) mothers; those with the lowest ratios were produced exclusively by Le(a-b+) mothers (p<0.001). Thus maternal genetic polymorphisms expressed as Lewis blood group types are expressed in milk as varied fucosyloligosaccharide ratios. The four infants who developed diarrhea associated with stable toxin of Escherichia coli were consuming milk with lower ratios (4.4 +/- 0.8 [SE]) than the remaining infants (8.5 +/- 0.8; p<0.001). Furthermore, the 27 infants who developed moderate to severe diarrhea of any cause were consuming milk with lower ratios (6.1 +/- 0.9) than the 26 who remained healthy (10.5 +/- 1.9; p = 0.042). Thus, milk with higher 2-linked to non-2-linked fucosyloligosaccharide ratios affords greater protection against infant diarrhea. We conclude that specific oligosaccharides constitute a major element of an innate immune system of human milk.     

Maternal Time Allocation in Two Cooperative Childrearing Societies

This paper examines maternal trade-offs between subsistence/economic activities and caregiving, and it explores the effect of allomaternal investment on maternal time allocation and child care. I examine how nonmaternal investment in two multiple caregiving populations may offset possible risk factors associated with reductions in maternal caregiving. Behavioral observations were conducted on 8- to 12-month-old infants and their caregivers among the Aka tropical forest foragers and Ngandu farmers of Central Africa. Analysis demonstrates that mothers face trade-offs between subsistence/economic activities and infant care. Infants receive less investment when their mothers engage in subsistence/economic activities, indicating a potential risk to those infants. However, results indicate that allomothers target their assistance during times when mothers are engaged in work activities, partially offsetting potential risks associated with the maternal trade-off. The effects of intercultural variability on maternal time allocation and allomaternal investment are also explored as a means of examining the potential impact of their behaviors on infant care.     

妊娠期糖尿病妇女体重指数对新生儿体脂的影响

本研究旨在通过评估新生儿的精确磁共振成像,确定妊娠期糖尿病(GDM)、肥胖母亲的后代与正常体重女性的后代相比,新生儿脂肪沉积模式是否存在早期影响。对正常体重母亲(n=13)和肥胖母亲(GDM)(n=12)的25名新生儿进行磁共振成像测量皮下和腹部脂肪和磁共振波谱,以测量1~3岁时肝内脂质(IHCL)脂肪的含量。结果表明,与正常体重母亲所生的婴儿相比,肥胖/妊娠糖尿病母亲所生婴儿的IHCL平均增加了68%。对于所有婴儿,IHCL与孕妇体重指数相关,但与皮下脂肪无关。新生儿肝脏沉积物与母亲体重指数高度相关。这一发现可能有助于了解儿童非酒精性脂肪肝的发病起源。     

Excess iodinuria in infants and its relation to the iodine in maternal milk

ObjectiveIodine is an essential micro nutrient, and a deficiency or excessive intake of this mineral is related to changes in thyroid function. In Brazil, both deficiency and excessive intake of iodine are common; however, excessive intakes have recently been observed. Thus, the objective of the present study was to assess the iodine concentration in maternal milk, taking into account the salt iodine concentration of the participating households and in the infants’ urine.MethodUrine samples from 33 infants (less than 6 months of age), maternal milk samples and samples of the kitchen salt used by the mothers were collected. The iodine levels in the urine and maternal milk were assessed by ICP-MS; the iodine levels in the salt were assessed by titration.ResultThe median iodinuria value in the infants was 293 μg/L; the mean iodine concentration was 206 μg/L in the maternal milk and 39.9 mg I/kg in the salt. There was a positive correlation between the iodine concentration in the maternal milk and the infant iodinuria value.ConclusionThe median infant iodinuria was elevated due to the high iodine concentration present in the maternal milk. High iodine values were caused by high salt iodine levels, which should be reduced.     

Hematological and serum biochemical effects of nursing on the mother in cynomolgus monkeys (Macaca fascicularis)]

The effects of nursing on maternal hematological and serum biochemical values were analyzed in cynomolgus monkeys reared in indoor cages at Tsukuba Primate Center. In our breeding system, infants are usually separated from their mothers at the age of 121 to 180 days. Mother monkeys of such infants were studied hematologically and biochemically (Group B), as were mother monkeys who happened to have nursed their infants past 181 days after parturition (Group A). During the period with their infants, mother monkeys in the latter group showed lower white blood cell counts (WBC) and higher red blood cell counts (RBC), hematocrit values (Ht) and blood urea nitrogen concentrations (BUN) than the mother monkeys who had been separated from their infants. Also, serum calcium concentrations (Ca) were decreased with prolonged nursing periods, indicating that lactation by the mother monkey probably continues even for a period from 181 days to about one year after parturition if she nurses her infant. Lactation during this period may accelerate hematogenesis and protein metabolism in the mother monkey.     

Procedures for improving maternal behavior in captive chimpanzees

Captive female chimpanzees who have had no opportunity to observe mothers with infants or to interact with infants often show inappropriate maternal behavior, particularly with their first-born infant, and this usually results in the removal of the infant to be human-reared. The present study used two techniques to encourage appropriate maternal behavior in ten pregnant female chimpanzees. These females were housed together with unrelated infant chimpanzees to adopt, or with lactating female chimpanzees and infants to observe. In five cases both techniques were used, in two cases only the first technique was used, and in three cases only the second technique was used. All ten female chimpanzees showed appropriate maternal behavior when their infants were born, in contrast to a group of eight female chimpanzees who had no such experience whose infants had to be removed for human-rearing. It is suggested that these techniques, or adaptations of them, could be applied to many other captive female chimpanzees with similar results.     

Social rank and sex-biased maternal investment in captive japanese macaques: behavioural and reproductive data

This study investigated the relationship between social rank and sex-biased maternal investment in captive Japanese macaques (Macaca fuscata) using reproductive and behavioural data. High-ranking mothers showed a significantly male-biased secondary sex ratio, spent more time in contact with and carried male infants for longer than female infants. Low-ranking mothers showed no bias in secondary sex ratio nor in the time spent in contact with male and female infants, but carried female infants for longer. No differences were observed in the interbirth intervals following male and female infants nor in the frequency and intensity of aggression received by mothers with male and female infants, either in high-ranking or in low-ranking mothers. These results show that Japanese macaque mothers can adopt flexible and rank-dependent rearing strategies.