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.     

Milk secretion in pregnancy among free-ranging Japanese macaques

Milking under anesthesia in pregnant free-ranging Japanese macaques (Macaca fuscata) directly revealed lactation in gestation at Jigokudani Monkey Park, the Shiga Heights, Nagano Prefecture, Japan, from 12 to 14 February 1992. Multiparae secreted milk at 76–97 days of estimated fertilization age when the birth intervals to the next offspring were 2 years. The observation of sucking behavior from February 1991 to March 1992 indicated that concurrent suckling by these multiparae terminated approximately 70 days before the next parturition after the growth of fetuses had accelerated and the embryos survived the crisis of abortion. Thus, Japanese macaque mothers appear to hedge maternal investment with concurrent lactation against possible miscarriage. Two nulliparous pregnant females secreted milk 3 months before the first parturition although they had no suckers. The first preparation of lactation appears to require the duration of longer than 3 months in nulliparae although worked mammary glands appear to be able to resume within 1 month in multiparae. © 1993 Wiley-Liss, Inc.     

Lactation in the Japanese monkey (Macaca fuscata): Yield and composition of milk and nipple preference of young

Changes in the yield and chemical composition of milk, together with those in the nipple preferences and suckling behavior of infants, were followed in three lactating Japanese monkeys rearing single infants under laboratory conditions at monthly intervals for six months after their paturition. Milk accumulating in the mammary glands during a 4-hr separation of the infant was collected by milking under anesthesia with the aid of a physiological dose of oxytocin. The stage of full lactation appeared to last for about two or three months after parturition. The milk at this stage contained 14.0% of total solids, 4.2% of lipids, 1.6% of proteins, and 6.2% of lactose, and the concentrations of Na, Cl, and K in the milk water were 7.4, 15.1, and 5.9 mM, respectively. From the 9th or 13th week of lactation onwards, according to the individual, the milk composition changed appreciably and the time during which the young left hold of the mother's nipple also increased. The weaning of young in the Japanese monkey appears to begin during the 3rd or 4th month of age. The milk production then wanes and almost ceases by the end of the 6th month. The nipple preference of the young was generally established completely by the 3rd, or the 8th at latest, week of age. However, no difference in either the yield or composition of the milk secreted was found between the mammary glands of the preferred and non-preferred sides. Without regard to the apparent nipple preference, infants seem to ingest milk from the mother's breasts of both sides. Accurate estimation of the rate of milk production could not be achieved, but the rate was expected to be 150–200 g/day at the height of lactation based on the relation between the mother's body weight and the milk production rates of other primate species. A disparity was noted between the observed and estimated values for the milk yield, and a diurnal fluctuation in the milk secretion of the Japanese monkey was inferred. This study was conducted through the official system of the Primate Research Institute, Kyoto University, for cooperative research work with other institutions.     

Variability in the development of mother-infant relationships among free-ranging Japanese macaques

Mother-infant relationships were studied during the infant's first year in free-ranging Japanese macaques (Macaca fuscata). Three possible factors controlling the mother-infant relationships were examined using multivariate analysis. Parity was determined to exert the strongest influence on mother-infant relationships. Specifically, during month 1, multiparous mothers showed greater maternal suckling rejection than primiparous mothers, and primparae and multiparae differed in their responses to suckling behavior. During month 6, multiparous mothers prompted independence of their offspring more than primiparous mothers. By month 8, however, parity differences in maternal behavior were substantially reduced. Maternal rank was a less important factor, although during month 1, high-ranking mothers showed greater maternal restriction than low-ranking ones. In the present study, infant gender appeared to have no effect on mother-infant relationships. That most differences were due to parity indicates that mother-infant relations were largely determined by the mothers. This observation conflicts with the “learning-to-mother” hypothesis. Allo-mothering of neonates by nulliparae is rare among Japanese macaques. Primiparous mothers learned appropriate suckling care from handling their own infants.     

Control of nipple and body contact by mothers and infants in rhesus macaques.

While 3-month-old infant rhesus macaques (Macaca mulatta) were awake and active in social interactions away from their mothers, body and nipple contacts with their mothers were nevertheless made from time to time. In each dyad the proportions of contacts made by the mother nearly equalled those broken by her, suggesting a meshed interaction in which each partner accepted most of the other's contact initiations and terminations. Passive prevention of nipple contact by a mother reduced the frequency of nipple contact by her infant in the first 5 s after the infant had made body contact. Passive prevention occurred after fewer than 1 in 6 body contacts initiated by infants, and--even without its occurrence--most infants were less ready to take the nipple after their own initiatives than after maternal initiatives. Once nipple contact had been made, the probability of breaking body contact was reduced. The role of maternal rejection both in the control of nipple contact in the short term and in determining (through its effect on the sucking pattern) whether the mother gives birth in the next birth season or later is discussed. We suggest that, by the age of 3 months, the infants had already learned when and how often nipple contact with their mothers would be acceptable during their awake and active periods, and we suggest that subsequent decreases in the frequency of nipple contact were partly the results of maternal rejections which were accepted by the infants.     

Variability of breast sucking, associated milk transfer and the duration of lactational amenorrhoea.

Quantitative relationships between physical parameters of sucking, milk transfer and the duration of amenorrhoea were examined in normal mother-baby pairs under exclusive breastfeeding. Sucking pressures were recorded twice on the second and once on the fifth month after birth, during complete breastfeeding episodes, by means of a catheter attached to the nipple and connected to a pressure transducer, the signals of which were analysed by computer. Babies were weighed before and after each sucking episode to estimate milk transfer. In the first nursing episode after noon, 2-month-old babies sucked from 140 to > 800 times during 4-15 min from the first breast, obtaining from 20 to > 100 g milk. The physical parameters of sucking and milk transfer exhibited high inter-individual but low intra-individual variabilities. There were significant differences in the physical parameters of sucking and milk transfer efficiency between first and second breast and between the second and fifth months after birth. Milk transfer efficiency was inversely correlated with time occupied by non-sucking pauses > or = 1.5 s, and was directly correlated with mean intersuck intervals in the first breast and with duration of the sucking episode, number of sucks, mean pressure and area under the pressure curve in the second breast. There was no correlation between the physical parameters of sucking and duration of lactational amenorrhoea (n = 62). However, significantly more mothers had amenorrhoea lasting > 180 days among those whose babies spent a longer proportion of the nursing episode in non-sucking pauses > or = 1.5 s. This finding indicates that sensory stimulation of the nipple produced during a nursing episode by stimuli other than sucking itself may have an important role in sustaining lactational amenorrhoea. It is concluded that nursing episodes have a complex structure that allows the development of a breastfeeding phenotype in each mother-baby pair, exhibiting important inter-individual variability. The present analysis does not support the contention that this source of variability accounts for the variability in the duration of lactational amenorrhoea.     

Maternal regulation of milk composition,milk production,and pouch young development during lactation in the tammar wallaby (Macropus eugenii )

Specific changes in milk composition during lactation in the tammar wallaby (Macropus eugenii) were correlated with the ages of the developing pouch young (PY). The present experiment was designed to test the hypothesis that the sucking pattern of the PY determines the course of mammary development in the tammar wallaby. To test this hypothesis, groups of 60-day-old PY were fostered repeatedly onto one group of host mothers so that a constant sucking stimulus on the mammary gland was maintained for 56 days to allow the lactational stage to progress 42 days ahead of the age of the young. Analysis of the milk in fostered and control groups showed the timing of changes in the concentration of protein and carbohydrate were essentially unaffected by altering the sucking regime. The only change in milk protein secretion was a small delay in the timing of down-regulation of the secretion of whey acidic protein and early lactation protein in the host tammars. In addition, the rates of growth and development of the foster PY were significantly increased relative to those of the control PY because of ingesting more milk with a higher energy content and different composition than normal for their age. The present study demonstrates that the lactating tammar wallaby regulates both milk composition and the rate of milk production and that these determine the rates of PY growth and development, irrespective of the age of the PY.     

A comparison of primiparous and multiparous mother-infant dyads inMacaca mulatta

The relationships of 42 rhesus monkey mother-infant dyads were examined to investigate the effects of the mothers' parity. Primiparous mothers were found to be younger, more excitable and less confident than the multiparous mothers. They also received more aggression from other adult females living in their social group and were more anxious about their infants, approaching and leaving them more frequently. The primiparous mothers protected their daughters more than the multiparous mothers and their daughters correspondingly spent more time in the ventro-ventral position and more time on the nipple. Their sons however spent less time in contact with their mothers than did the sons of the multiparous mothers. Although the primiparous mothers protected their daughters more than their sons, for the multiparous mothers the converse was true and sons received more maternal protection. It is suggested that the greater protectiveness of the multiparous mothers towards male infants may be a consequence of the interest siblings have in males, whereas the greater protectiveness of primiparous mothers to daughters may stem from their greater vulnerability to attacks from adult females. The importance of mother-mediated sibling influences may explain the lack of strong parity differences in previous studies.     

Behavior of Japanese monkey (Macaca fuscata) mothers and neonates at parturition

Parturitional behavior in 12 caged Macaca fuscatawas analyzed. Wild-caught mothers showed adequate maternal behaviors immediately following the neonate’s expulsion. Parity differences existed in the behaviors; primiparae were more idiosyncratic than were multiparae. Among multiparae, those with two or more offspring were uniformly adequate, but those with a single birth experience varied in the adequacy of the maternal care they provided at parturition. Mothers embraced and licked their neonates and had ventroventral contact with them frequently immediately after parturition but decreased these behaviors after expulsion of the placenta. In contrast, mothers showed allogrooming after consuming the placenta. Placentophagy was correlated with the level of orality represented by maternal licking behaviors. An isolation-reared primipara reacted to her newborn in a basically negative manner, although she showed little actual aggression. She showed a rapid shift in her negative behavior during the immediate postpartum period. This mother’s newborn sought contact with her, indicating the neonate’s active role in establishing a stable mother-neonate bond.     

Effect of milkflow rate and presence of a floating nipple on abnormal sucking between dairy calves

The aim of this study was to investigate if access to an artificial teat compared to an open bucket would decrease abnormal sucking in calves held in pairs, and if the calves would perform less abnormal sucking if they spent more time drinking or sucking the milk. In total 16 calves of Swedish Red and White cattle housed in pairs were used. The eight groups were given 2.5l of whole milk per calf, twice a day in one of the following treatments; bucket with fast flow (control), bucket with slow flow, floating nipple with fast flow and floating nipple with slow flow. All groups were subjected to the four different treatments in a random balanced order. Two buckets were connected with a rubber pipe in order to control the milk flow. In the fast treatments, the milk poured from one bucket to the other in 40s, and in the slow treatments the milk poured from one bucket to the other in 10min. Each group had the treatment for 6 days before behavioural observations were done on day 7. These were made by instantaneous recordings at 20s intervals for 30min, starting when the calves received their milk in the morning and afternoon. The number of recordings of abnormal sucking was lower than the control in all treatments (P<0.001). The lowest recording of abnormal sucking was found, when the calves had both a floating nipple and a slow flow. Sucking on other objects in the pen had the highest number of recordings, when they had a nipple and a fast flow (P<0.01), but the sucking on the empty nipple represented 95% of this category. The calves tended to lick and bite more on the bucket, the nipple and pen fittings in the two treatments with fast flow (P<0.1) than in the slow treatment with nipple. It is concluded that both the performance of sucking and the time taken to ingest milk are important in order to decrease abnormal sucking between calves.     

Primigravidity,body weight,and costs of rearing first offspring in rhesus macaques

Body size is associated with menarche and ovarian function, but the relationship to first conception is rarely examined. We conducted a longitudinal investigation of rhesus macaques, Macaca mulatta, to determine the effect of differences in body weight on both the age at first conception and survivorship of first progeny. Young females who became pregnant weighed significantly more than peers who remained barren, with weight changes for females who successfully raised offspring no different than those for females who did not produce offspring. Infant mortality among primiparae was not significantly greater than that among multiparae, although nearly twice as high. First-born males tended to have lower survivorship than first-born female offspring. We suggest that reproductive costs encountered by primiparous females are more likely to be modulated by immature neuroendocrine function than by inexperience, small body size, or infant suckling patterns. We conclude that body size influences probability of first conception, socioendocrine factors mediate the likelihood of infant survival, and primiparous production of male progeny seems to exert a greater reproductive cost than does production of female progeny. Am. J. Primatol. 46:135–144, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Reproductive parameters of female Japanese macaques: Thirty years data from the arashiyama troops,Japan

Over a 30-year period from 1954 to 1983, 975 live births were recorded for Japanese macaque females at the Iwatayama Monkey Park, Arashiyama, Japan. Excluding unknown birth dates, primiparous mothers gave birth to 185 infants (182 cases with age of mother known) and multiparous mothers gave birth to 723 infants (603 cases with age of mother known). The peak month of birth was May with 52.3% of the total births occurring during the period. Multiparous females who had not given birth the previous year did so earlier than multiparous females who had given birth the previous year and also earlier than primiparous females. Among the females who had given birth the previous year, females whose infant had died gave birth earlier than females who had reared an infant the previous year. The offspring sex ratio (1:0.97) was not significantly different from 1:1, and revealed no consistent association with mother's age. Age-fecundity exhibited a humped curve. The annual birth rate was low at the age of 4 years but increased thereafter, ranging between 46.7% and 69.0%, at between 5 and 19 years of age, but again decreased for females between 20 and 25 years of age. Some old females displayed clear reproductive senescence. The infant mortality within the first year of age was quite low (10.3%) and the neonatal (less than 1 month old) mortality rate accounted for 49.0% of all infant deaths. There was no significant difference between the mortality rates of male and female infants. A female's rank-class had no apparent effect on the annual birth rate, infant mortality, and offspring sex ratio. These long-term data are compared with those from other primate populations.     

Analysis of ethnic differences in perinatal statistics.

The 3996 mothers delivered at Dudley Road Hospital, Birmingham, in 1979 were analysed for their ethnic origins. Social classes IV and V predominated in all groups. A high proportion of Indian mothers fell into the low-risk group based on age and parity but had the highest stillbirth and perinatal mortality rates (15.1 and 27.5/1000 respectively) and infants of low mean birth weight (2986 g). Elderly and multiparous mothers were characteristic of the Pakistani and Bangladeshi groups. Young, primiparous mothers were more common among the West Indians and Europeans, in whom the stillbirth and perinatal mortality rates were low; infants in the European group had a mean birth weight higher than in any other group (3231 g). From these findings ethnic origin of the mother is apparently an important factor in perinatal mortality.     

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.     

Zinc and copper in human milk

Studies of zinc and copper contents of breast milk were performed in 34 mothers during their lactation period until 5 days postpartum. They experienced no problems during pregnancy and delivery. All women had full term healthy infants, 22 were multiparous and 12 primiparous. The highest zinc concentration was found in the colostrum, and subsequently the concentration declined. Copper content was stable during the 5 days of lactation. Significantly lower zinc concentration and higher copper concentration were found in the serum of lactating women 3 days post partum, when compared with non-lactating women. Factors including lactation history, age of lactating women, serum levels of zinc and copper did not affect the contents of these trace minerals in breast milk.     

The influence of rearing conditions on maternal behavior in cynomolgus macaques (Macaca fascicularis)

We studied the influence of rearing on the adequacy of maternal behavior by comparing 20 harem-reared and 15 peer-reared primiparous cynomolgus monkeys. We used them plus 11 wild-caught females to extend this comparison to multiparous subjects and also to compare primiparae with multiparae. We observed no behavioral effect of rearing and parity. Primiparous maternal adequacy amounted to 93% in peer-reared subjects and to 95% in harem-reared monkeys. We extensively discuss theories concerning rearing effects. Leitmotifs throughout the discussion are survival value of maternal behavior immediately after parturition and predictive value of this behavior for the further course of maternal behavior. Support is accumulated for the hypothesis that certain tactile and visual experiences suffice for the development of adequate maternal behavior.     

Zinc and Copper Concentrations in Human Preterm Milk

Zinc and copper are important trace elements in the nutrition of preterm infants. This study determined and compared the concentrations of zinc and copper in preterm milk of mothers receiving and not receiving zinc supplementation diets. The effects of maternal supplementation on the blood levels and anthropometric parameters were evaluated. Thirty-eight mothers and their preterm infants were enrolled in the study. Eighteen mothers were given a daily supplementation of 50 mg zinc, whereas the other 20 were not. Zinc and copper levels in milk were determined at 15-day intervals, as were blood zinc levels along with anthropometric parameters. Zinc and copper contents were determined by atomic absorption spectrophotometry. No significant differences were found between groups either for zinc values in maternal milk and infant blood or for anthropometric measurements. A pronounced decrease in copper levels was observed in mothers receiving supplemental zinc. Zinc supplementation given to mothers who were breastfeeding preterm infants had no significant effect on zinc secretion in milk.