Some reproductive parameters of stumptailed macaques (Macaca arctoides)

Reproductive records kept from 1969 to 1981 were used to study menstrual cycles, pregnancies and births of eight colony-housed stumptailed macaques. The findings for annual distribution of births, pregnancy duration and infant sex ratio were consistent with previous reports. The interbirth interval after infant loss was significantly shortened from the interbirth interval when infants were maintained with their mothers. Vaginal bleeding during early lactation indicates that stumptails are not necessarily characterized by a prolonged period of postpartum amenorrhea. Complete copulation was observed prior to six months postpartum, but interbirth intervals indicate that conception did not occur prior to that time. Interbirth intervals tended to be shorter for dominant than for subordinate females and to lengthen as a function of increasing age.     

Aetiological approach of female reproductive physiology in lactational amenorrhoea.

The duration of postpartum amenorrhea and return of ovulation varies on an individual and population basis. In 1980, in Senegal, the relationship of chronic malnutrition and female fertility was investigated for 2 years. The stability of the female body regarding weight and arm circumference despite a heavy annual workload was a surprising finding. The mean female body mass index was higher for lactating women in amenorrhea than required for restoring menstruation in European women. The mean duration of postpartum amenorrhea was 18.2 +or- .6 months. The difference between those who resumed menstruation (20.9 +or- .9 months) and who still had amenorrhea (25.4 +or- 2.2 months) was significant. The duration of breast feeding determined the duration of amenorrhea. Studies have found a link between ovarian dysfunction and women in harsh third world environments and sportswomen under intensive training with both showing irregular menstruation and amenorrhea. Long duration of cycles in New Guinean women, high amount of anovulation in Zairian forest women, and suppression of testosterone and estradiol levels in hunter-gatherers were found. In affluent Europeans and urbanized women in developing countries postpartum amenorrhea dropped drastically. Long distance runners are often vegetarians with low calorie consumption and with a high degree of menstrual trouble owing to low body fat and weight-for-height. The role of beta-endorphins in the hypothalamic blockade of the gonadotropin releasing hormone pulse generator and high stress or physical training is proven. The functioning of the hypothalamo-pituitary-ovarian axis can be hurt by intensive training. Short-term fasting also suppressed the pulsatile luteinizing hormone and testosterone secretion. The protocol and methodology of an etiological study is outlined regarding the factors of this hypothesis on amenorrhea.     

Synchronization of Menstrual Cycles in Pigtailed Macaques Using Photoperiod

Periods of artificial light were manipulated to induce synchronous ovulation in a group of pigtailed macaques. Treatments consisted of constant light exposure over diminishing periods of 9,7,5,3 and 3 days. Ovulation was assessed externally and assumed to have occurred on the first day of perineal detumescence. The results demonstrate that manipulation of light exposure affects reproductive cycling.     

Sexual Maturation of Female Japanese Macaques Under Poor Nutritional Conditions and Food-Enhanced Perineal Swelling in the Koshima Troop

Provisioned food was severely restricted for 5 years, from 1972 until June 1977, in the insular Koshima troop of Japanese macaques. The monkeys experienced very poor nutritional conditions during this period. The feeding policy was changed in 1977 and food conditions improved, but only in summer. A remarkable consequence of intensive provisioning in summer was the occurrence of perineal swelling in many young females outside of the mating season. Females that matured during the period of poor food conditions showed an extraordinary delay in primiparity and exhibited conspicuous perineal swelling in the summer of 1977. Researchers studied the development of perineal swelling under standard conditions of constant provisioning from 1990 to 1995. First perineal swelling appeared at 5 years of age under standard conditions but appeared at 8 years of age under poor food conditions. The extraordinary delay in primiparity did not occur among females that were 6 years old when food conditions were improved in summer. We deduced that female Japanese macaques have a critical age of 5 to 6 years for sexual maturation. If the critical age is exceeded under poor food conditions, sexual maturation is hard to achieve even with improvements in food conditions. Seasonal changes in the incidence of perineal swelling were related to the period of high body weight. Rapid improvements in food conditions probably caused perineal swelling and activated sex hormones in female Koshima Japanese macaques.     

Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx)

We present 12 years of perineal swelling data for a semifree-ranging colony of mandrills (Mandrillus sphinx), and evaluate the influence of rank, parity, and seasonality on reproductive parameters. Female sexual swellings showed a seasonal pattern, with August the median month of ovulation. Overlapping periovulatory periods did not decrease the likelihood of conception. Females showed their first genital swelling at age 3.6 years (n = 28; range, 3.2-4.6 years), and higher-ranking females experienced their first swelling earlier than low-ranking females. Median postpartum amenorrhea (PPA) duration was 208 days (n = 92; range, 74-538 days). PPA was longer in primiparous females than in multiparous females, but PPA duration was unrelated to female rank. Median follicular phase duration was 24 days for the first cycle after parturition (n = 84; range, 12-40 days), shortening to 17 days in subsequent cycles (n = 55; range, 6-39 days). The follicular phase was longer in nulliparous females than in parous females, but was unrelated to female rank. Median cycle length (from one sexual swelling breakdown to the next) was 38 days (n = 57; range, 18-108 days). Eighty-seven percent of conceptions occurred within two cycles, and half of the nulliparous females conceived during their first swelling cycle. Lower-ranking females were more likely to require more cycles to conceive than higher-ranking females. The cycling phase was significantly longer in nulliparous females than in parous females, and was also significantly longer in lower-ranking females than in higher-ranking females. We discuss the influence of provisioning on female reproductive parameters, the influence of parity and rank on the different phases of the interbirth interval, and the evolution of long and variable follicular phases in mandrills.     

First postpartum ovulations and corpora lutea in ewes which lamb in the breeding season

Two experiments involving crossbred ewes which lambed during the breeding season were performed to determine whether: (a) the interval to first postpartum ovulation could be reduced by weaning or mastectomy; (b) there are differences in luteal structure and luteinizing hormone (LH) receptor concentration between first postpartum corpora lutea induced with GnRH and normal cycling corpora lutea and (c) pretreatment of postpartum ewes with progesterone would affect luteal LH receptor concentration and luteal phase serum progesterone concentration.In experiment I, the mean interval (±SEM) to the first postpartum ovulation was 22.3 ± 1.1 days and was not significantly altered by weaning or mastectomy. More than half of the ewes had small, short-lived peaks of serum progesterone associated with short-lived corpora lutea prior to the normal luteal phase rise of serum progesterone. In experiment II, 2 h after GnRH injection on day 18 postpartum, serum LH concentrations were higher in ewes which received progesterone treatment on days 13 and 14 than in control ewes. Progesterone treatment did not affect mean corpus luteum weight (157 mg) or concentration of LH receptors (0.95 fmol/mg) in first postpartum corpora lutea, but progesterone-treated ewes had significantly higher endogenous serum progesterone concentrations on days 21–24. GnRH-induced corpora lutea from postpartum ewes were lighter in weight, paler in color, had lower LH receptor concentrations and had a more regressed histological appearance than corpora lutea of a similar age from normal, cycling ewes.     

Female reproductive cycles and the sexual behavior of moor macaques (Macaca maurus) in their natural habitat,South Sulawesi,Indonesia

The female reproductive cycles and sexual behavior of moor macaques (Macaca maurus) were studied in their natural habitat. Female moor macaques showed repeated perineal swelling. The average cycle length was 36.2 days and the mean duration of swelling was 11.9 days. The estimated duration of gestation in two observed cases was 175 and 176 days, respectively. Females did not exhibit post-conception sexual swelling. Males appeared to ejaculate in multi-mounts. Serial mounting by the alpha male was concentrated on swelling females, while second- and third-ranking males sometimes mounted non-swelling females in series.     

Detecting ovulation in Macaca nemestrina by correlation of vaginal cytology, body temperature and perineal tumescence with laparoscopy

Vaginal cytology, basal body temperature, and perineal tumescence were correlated with laparoscopic observations during the menstrual cycles of five pigtail monkeys (Macaca nemestrina) of known fertility. Percentages of cells obtained in vaginal smears revealed systematic variation in the presence of cell types in relation to the menstrual cycle. Measuring the percentage of exfoliate vaginal epithelial cells containing pyknotic nuclei proved to be of little value for separating the menstrual cycle into its follicular and luteal phases, nor did body temperature provide an accurate index for the occurrence of ovulation. Perineal tumescence, however, measured from the first day of menses to onset of detumescence, was a reliable indicator of the lengths of the follicular and luteal phases as correlated with laparoscopic confirmation of ovulation. Maximal perineal tumescence usually occurred within 12 hours of ovulation, although on one occasion the two events were separated by 48 hours.     

The influence of male presence or absence on the reproductive cycle of celebes black ape females (Macaca nigra)

The effect of male presence on female menstrual cycles was studied in a group of 13 adult female and 3 adult male Celebes black apes (Macaca nigra) living in an outdoor enclosure. When males were absent, all cycling females had longer durations of maximal perineal swelling. Overall cycle length also appeared to be longer when males were absent, but there was no statistically significant increase. The data suggest that male absence results in a longer late follicular stage, perhaps indicating a delay in ovulation. Whereas these findings do imply that male presence may influence female macaque reproductive condition, it is acknowledged that this effect is much weaker than the demonstrated influence of female macaques on male reproductive state.     

Influence of Pregnancy Spacing on Outcome of Pregnancy

To assess the significance of the length of time between two pregnancies on the outcome of the second we used information collected by the British Perinatal Mortality Survey of 1958. From questionnaires on the 16,994 singleton births in the first week of March 1958 and the 7,117 singleton stillbirths and neonatal deaths in March, April, and May 1958 we abstracted information on the date and outcome of any preceding pregnancy. The interpregnancy interval was taken as the length of time between this preceding pregnancy and the last menstrual period before the index pregnancy. The most important factors influencing pregnancy spacing were outcome of the preceding delivery, social class, and maternal age. When these variables had been taken into account we found that the length of interpregnancy interval had little effect on stillbirth rates. High neonatal death rates, however, occurred when interpregnancy intervals were less than six months (P <0·005), though longer intervals had no significant effects.     

Birth of rhesus macaque (Macaca mulatta) infants after in vitro fertilization and gestation in female rhesus or pigtailed (Macaca nemestrina) macaques

A study was conducted to assess the possibility of using pigtailed macaques (Macaca nemestrina) as recipients for rhesus macaque (Macaca mulatta) embryos. A total of 250 oocytes were collected from 11 rhesus monkeys during 12 follicular aspirations. We performed 15 embryo transfers with two embryos each into rhesus recipients, which resulted in eight pregnancies, of which two were lost during the second trimester. Among the remaining six pregnant rhesus macaques, two were carrying twins, resulting in the birth of eight infants. Twelve transfers of rhesus embryos into pigtailed macaques resulted in one pregnancy and the birth of one infant. Fetal growth and development were monitored by monthly ultrasound examinations, during which biparietal measurements were taken and compared with those derived from 22 pregnant control monkeys. In vitro fertilization-derived singletons tended to develop faster than did twins and naturally conceived control singletons during the initial months of pregnancy and weighed more at birth than did twins. There were pronounced morphologic changes in the placenta of the rhesus that developed in the female pigtailed macaque. These included an irregular shape, elevated placenta-to-birth-weight ratio, and an abnormal length and diameter of the umbilical cord. Histologic analyses of the rhesus-pigtailed placenta showed evidence of maternal-placental floor infarction and thrombosis of the spiral artery with resulting infarction of the villi. These results demonstrate that pigtailed macaques can carry rhesus fetuses to term, but further studies are necessary to determine the cause of the decreased pregnancy rates and observed placental abnormalities.     

Reproduction and social rank in female stumptail Macaques (Macaca arctoides)

Reproductive physiology was studied in female stumptail macaques. Initially the monkeys were housed indoors (individually and in small groups) and later as one large (92 individuals) social group in an outdoor cage. Most data were collected during the 4-year outdoor period. Plasma progesterone determination in blood samples taken at weekly intervals allowed estimation of ovulation and conception dates. The age at first ovulation (X =3.73 years) was positively correlated with body weight at 3 years of age. The average age at first birth was 4.90 years. Gestation lengths averaged 176.6 days. Following a live birth ovulations returned after a mean interval of 11 months but following an abortion or still birth this interval was 1 month. Usually a number of ovulatory cycles (X =2.37) preceded a conception. Interbirth intervals (IBIs) in the outdoor cage (X =619.4 days) were significantly longer than IBIs during the indoor period (X =523.1), because indoors the infants were weaned at the age of 7 months, while outdoors weaning occurred more naturally. IBIs following abortions or still births (X =291.9 days) were significantly shorter than IBIs following live births. Age at first ovulation, age at first birth, IBIs, and infant production rates were not correlated with dominance rank. Ovarian cycle lengths (X =30.2 days, mode = 28 days) were comparable to previously reported data from laboratory-housed stumptails. No systematic seasonal fluctuations were found in the onset of sexual maturity, in ovarian cycle lengths, in copulation frequencies, and in distribution of births.     

Growth and development of the term and premature pig-tailed macaque (Macaca nemestrina): Cardiovascular and respiratory changes during the first 3 weeks of life

Growth and development of the infant pigtailed macaque (Macaca nemestrina) over the first 3 weeks of life have been characterized by the variables of body weight, blood pressure, heart rate, ventilation, blood gas tensions, and lung mechanics. The effects of prematurity on postnatal developmental trends were assessed at gestational ages of 135–145 days (0.80 of term) and 150–155 days (0.91 of term). There was no indication that cesarean section, restraint, or instrumentation had any significant influence on the measurements. Gestational age at delivery had no effect on the minute ventilation per kilogram body weight, the hematocrit, or the heart rate; however, body weight, tidal volume, respiratory frequency, arterial gas tensions, blood pressure, and lung compliance did vary with gestational age at delivery. Postnatal maturational changes in these variables were similar between term and premature animals. The data for infant macaques and newborn humans were compared. The newborn macaque appears to be an excellent model of human developmental trends (and/or disease state) over the first 3 weeks of life, though some potentially important differences have been found.     

Impact of lactation upon fertility in the New World primate capuchin monkey (Cebus apella)

In the present paper, we have studied the impact of lactation upon fertility in the capuchin monkey, Cebus apella, under laboratory conditions. Nursing females (ten females, 12 postpartum periods) presented lactational amenorrhea (first menses at 159.2 +/- 9.0 vs 42.6 +/- 5.8 days postpartum in five non-nursing females, seven postpartum periods). Plasma estradiol and progesterone concentrations during lactational amenorrhea were lower than those during the follicular phase of the menstrual cycle. Prolactin was higher than in non-nursing females at 31-60 days postpartum. Interbirth interval, studied in three non-nursing (four intervals) and six nursing females (eight intervals) lasted for 349.5 +/- 11.8 and 613.4 +/- 30.8 days, respectively. In non-nursing females, early recovery of the menstrual cycle was followed by a residual infertility (mating but no pregnancy) lasting 152.8 +/- 7.9 days. In nursing females, recovery of the menstrual cycle was followed by an extended residual infertility of 301.5 +/- 22.7 days. Thus, in the capuchin monkey, nursing prolongs the interbirth interval by inducing lactational amenorrhea and extending the residual infertility period.     

Hormonal synchronization of the menstrual cycles of pigtail macaques to facilitate biomedical research including modeling HIV susceptibility

Background Menstrual cycle synchronization of female pigtail macaques could prove an invaluable resource in studies of the reproductive tract, associated infections, and other potential research fields. We tested whether use of an oral progesterone and estradiol combination tablet could synchronize menstrual cycles following treatment discontinuation. Methods Daily desogestrel 0.075 mg and ethinyl estradiol 0.01 mg were administered orally to three pigtail macaques at visual onset of perineal sex swelling and were continued until all animals had received it for at least 45 days. The hormones were discontinued, and these three macaques and three controls were observed for menstruation and had blood progesterone and estrogen measured over an additional 2‐month period. Results All treatment animals showed spontaneous menstrual cycle synchronization for 2 months after menstrual cycling resumed. Conclusion Progesterone and estradiol combination therapy can be used in pigtail macaques to induce synchronized cycling that persists in the absence of on‐going hormone treatments.     

Nutrition, infant feeding and post-partum amenorrhoea in rural Bangladesh

The extent to which differences in the duration of postpartum amenorrhea among chronically malnourished women in rural Bangladesh are related to seasonal patterns of food supply, maternal nutrition, education, and patterns of infant feeding was investigated by application of multivariate hazards models with time-varying covariates. The data were derived from the Birth Interval Dynamics study in Matlab and covered close to 1800 births. Parity, education, season of birth, maternal weight, and infant supplementation all were found to affect the duration of postpartum amenorrhea among these women. Education of 5 or more years had a positive effect on the resumption of menses. Higher parity women, who were older, had longer periods of amenorrhea, as did women who gave birth in October-December. As a measure of nutritional status, the woman's weight at pregnancy termination showed a highly significant positive coefficient, indicating that improved maternal nutrition increased the likelihood of resuming menstruation. Food supplementation, which tends to decrease breastfeeding, also significantly increased the risk of resuming menstruation and had an effect independent of the other variables. When the data were analyzed by season, the most striking finding was the strong influence of education on children born during October-December (who are too young to be directly affected by the larger food supply at birth during the harvest season). The other seasons showed weaker effects of education and a stronger effect of supplementation, perhaps because these infants are older during the harvest season and thus can benefit from supplements.     

Physiology of maternal separation in a bonnet macaque infant

A bonnet monkey infant (M. radiata) was monitored both physiologically and behaviorally during a separation experiment in which both its mother and other conspecifiecs were removed from its social group leaving the bonnet infant with three adult pigtailed females. The separated infant exhibited the characteristic slouched posture of depression and physiological changes including decreases in the heart rate and body temperature, increases in cardiac arrhythmias, and alterations in sleep patterns, as has been previously described in separated pigtailed infants. Persistent decreases in heart rate and body temperature were noted following reunion with the mother, possibly reflecting a disturbance in the mother-infant relationship secondary to the mother's having come into estrus during the period of separation. This study indicates that the physiological correlates of maternal separation previously described in pigtailed infants are not species specific.     

Predictors of fecundability and conception waits among the Dogon of Mali

Surprisingly little is known about the mechanisms that underlie variation in female fertility in humans. Data on this topic are nonetheless vital to a number of pragmatic and theoretical enterprises, including population planning, infertility treatment and prevention, and evolutionary ecology. Here we study female fertility by focusing on one component of the interbirth interval: the waiting time to conception during menstrual cycling. Our study population is a Dogon village of 460 people in Mali, West Africa. This population is pronatalist and noncontracepting. In accordance with animist beliefs, the women spend five nights sleeping at a menstrual hut during menses. By censusing the women present at the menstrual huts in the study village on each of 736 consecutive nights, we were able to monitor women's conception waits prospectively. Hormonal profiles confirm the accuracy of the data on conception waits obtained from the menstrual hut census (Strassmann [1996], Behavioral Ecology 7:304–315). Using survival analysis, we identified significant predictors of the waiting time to conception: wife's age (years), husband's age (<35, 35–49, >49 years), marital duration (years), gravidity (number of prior pregnancies), and breast-feeding status. Additional variables were not significant, including duration of postpartum amenorrhea, sex of the last child, nutritional status, economic status, polygyny, and marital status (fiancée vs. married). We fit both continuous and discrete time survival models, but the former appeared to be a better choice for these data. Am J Phys Anthropol 105:167–184, 1998. © 1998 Wiley-Liss, Inc.     

Reproductive parameters and paracallosal skin color changes in captive female Guinea baboons,Papio papio

Reproductive data are presented for female Papio papio housed in the Zoological Park of Paris and are compared with previously published data from free‐ranging populations of other baboon species. The results indicate similar intermenstrual intervals and durations of sexual swelling. Sexual swelling and pregnancy are accelerated in captivity, while postpartum amenorrhea and interbirth interval are reduced. Interbirth intervals in P. Papio were short, approximately 13 months in the case of viable, surviving infants and approximately 11 months in the case of stillbirth or neonatal mortality. The shorter interval may represent the lower physiological limit, and the generally shorter interbirth interval reported here may be explained by lower stress and reduced maternal investment costs in the captive environment. Paracallosal skin color variations during the menstrual cycle were influenced by parity, but sexual swelling patterns were not. The paracallosal skin changes might be used by males as a cue to females' reproductive status. Am. J. Primatol. 47:67–74, 1999. © 1999 Wiley‐Liss, Inc.     

Relationships between pregnancy spacing,sex of infants,maternal age,and birth order,and neonatal and post‐neonatal mortality in Bangladesh

Abstract

The relationships between length of the interpregnancy interval, outcome of the pregnancy preceding the interval, sex of the infants, pregnancy order, maternal age, and maternal history of previous child deaths and neonatal and postneonatal mortality were explored in a rural Bangladeshi population using a multiple regression analysis. Specific interactions between the interpregnancy interval, outcome of the pregnancy preceding the interval, sex of the infants, and history of previous child deaths were examined. An inverse relationship was observed between postneonatal mortality and the length of the interpregnancy interval when the pregnancy preceding the interval was a surviving infant. No such trend was observed for neonatal mortality. Post‐neonatal mortality rates among children whose mothers had experienced two or more previous child deaths were essentially the same as that for infants whose mothers had experienced 0–1 child deaths when the interpregnancy intervals were more than 24 months. Although female infants have a lower neonatal mortality than male infants, the neonatal mortality rate for female infants conceived less than twelve months following a male infant birth was higher than for a male infant conceived less than twelve months following another male infant birth. Post‐neonatal mortality is consistently higher for female compared to male infants in all interval categories.