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.     

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.     

Sources of variation in interbirth intervals among captive bonnet macaques (Macaca radiata)

Female fitness is a function of variation in the length of females' reproductive careers, the viability of their offspring, and the frequency with which they give birth. Infant loss shortens interbirth intervals in most primate species, but we know considerably less about other factors that contribute to variation in the length of interbirth intervals within groups. In one large captive group of bonnet macaques, maternal parity, age, experience, family size, and recent reproductive history are all associated with variation in the length of intervals that follow the birth of surviving infants. Primiparous females have the longest interbirth intervals, while multiparous females who have produced surviving infants in the past and have raised their last infant successfully have the shortest interbirth intervals. Infant sex and maternal rank have no direct effect upon the length of interbirth intervals. One of the underlying causes of variation in the length of interbirth intervals after surviving births seems to be variation in the timing of conceptions among females. Females who conceive early in the mating season tend to have shorter interbirth intervals than other females. However, females who are multiparous, experienced, and have recently raised infants have late conceptions and short interbirth intervals.     

Weaning, body weight, and postpartum amenorrhea duration in pigtailed macaques (Macaca nemestrina)

Early permanent infant separation or weaning decreases the time interval between pregnancies and interbirth intervals for many female primates. At least part of the interpregnancy interval consists of postpartum amenorrhea, a period of non-menstruation lasting from the time of birth until the female begins to ovulate. This study investigated the effects of weaning age and dam's body weight on the duration of the interval between pregnancies, the duration of postpartum amenorrhea, and the number of cycles to conception in a year-round breeder. Female pigtailed macaques (Macaca nemestrina) have an observable perineal swelling that fluctuates throughout the menstrual cycle and provides a means of detecting ovulation. The perineal swelling records of socially housed pigtailed macaques were studied from July 1996 to September 1998. Postpartum amenorrhea data were obtained on 44 females who gave birth to normal, viable infants. As weaning age increased and dam's weight decreased, postpartum amenorrhea, and consequently the interval between pregnancies, increased in duration. The interpregnancy interval consisted almost entirely of the postpartum amenorrhea phase. Our finding that a higher dam's body weight decreased the length of postpartum amenorrhea duration lends support to the hypothesis that a minimum body weight is necessary for menstrual cycles to occur. Most females became pregnant on their first ovulation regardless of weaning age and whether or not they were carrying an infant. As the weaning age of the infant and the dam's weight increased, ovulation went from occurring after separation to occurring before separation.     

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.     

Nursing does affect the duration of the post-partum to ovulation interval in cotton-top tamarins (Saguinus oedipus)

Reports on callitrichid monkeys have not revealed a significant effect of nursing on interbirth intervals or on post-partum to ovulation intervals. We examined 25 post-partum intervals in cotton-top tamarin females to determine whether nursing infants would affect the length of the post-partum to ovulation interval. Urinary LH/CG and oestrone conjugates were measured in urine samples collected in the 6 weeks after birth. The post-partum to ovulation interval is the number of days between parturition and the rise of urinary LH and oestrone conjugates associated with ovulation. There was an 84% conception rate post partum. Neither mother's parity nor sex of the infants influenced the length of the post-partum to ovulation interval. The post-partum to ovulation interval for females nursing 2 infants was twice as long as for those not nursing or nursing 1 infant (P less than 0.05). The range of post-partum to ovulation interval lengths was more variable in nursing than in non-nursing females (P less than 0.01). Females spent less than 50% of observed time in contact and less than 20% of observed time nursing their infants. Neither the number of tamarins within the family nor the amount of time the mother was in contact with infants correlated with the length of the post-partum to ovulation interval. However, there was a positive correlation between the percentage time that mothers nursed 1 infant at a time and the length of the post-partum to ovulation interval (r = 0.75, P less than 0.02). The underlying mechanisms of suckling-induced delay of ovulation are present in the cotton-top tamarin as in other primate species. However, these nursing effects do not cause the substantial delay in fertility post partum that is associated with non-callitrichid primates.     

Long-term data on the reproduction and maintenance of a colony of common marmosets (Callithrix jacchus jacchus) 1972-1983

We have used our laboratory records to compare data on the reproduction and maintenance of common marmosets in different colonies and to provide additional information on the species in captivity. Data are presented for a period of 12 years. This was long enough to allow information on longevity, mortality, aggression and incest. In addition 543 infants were born from a total of 202 births. No seasonality was found and the highest proportion of births overall was that of triplets. A significantly greater proportion of males was born, but perinatal mortality reduced this to a proportion of 52.2% surviving males. The interbirth interval for all normal births ranged from 145 to 382 days, with a median of 158 days. There was no evidence that interbirth intervals increased with age. The proportion of non-breeding pairs was small (4 out of 28) and progesterone assays showed that these females were ovulating.     

Reproduction in wild female olive baboons

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

Determinants of fecundity and reproductive success in captive vervet monkeys

Between 1975 and 1983, adult female vervet monkeys (Cercopithecus aethiops sabaeus) over 3.5 years of age, living in two undisturbed social groups in a captive colony in Sepulveda, California, have averaged 1.0 births per female year with a mean interbirth interval of 10.7 months. Increased fecundity did not result in decreased survival rates of offspring in this population. Fecundity was influenced by the mother's age and dominance rank. The primary factor in the age-fecundity relationship was the age at first birth, which varied from three to five years. High-ranking females contributed the most to the high rate of fecundity, with significantly shorter interbirth intervals, more births per female year, and more surviving infants compared to low-ranking females.     

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

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

Estimating hominid life history: the critical interbirth interval

Unlike any great apes, humans have expanded into a wide variety of habitats during the course of evolution, beginning with the transition by australopithecines from forest to savanna habitation. Novel environments are likely to have imposed hominids a demographic challenge due to such factors as higher predation risk and scarcer food resources. In fact, recent studies have found a paucity of older relative to younger adults in hominid fossil remains, indicating considerably high adult mortality in australopithecines, early Homo, and Neanderthals. It is not clear to date why only human ancestors among all hominoid species could survive in these harsh environments. In this paper, we explore the possibility that hominids had shorter interbirth intervals to enhance fertility than the extant apes. To infer interbirth intervals in fossil hominids, we introduce the notion of the critical interbirth interval, or the threshold length of birth spacing above which a population is expected to go to extinction. We develop a new method to obtain the critical interbirth intervals of hominids based on the observed ratios of older adults to all adults in fossil samples. Our analysis suggests that the critical interbirth intervals of australopithecines, early Homo, and Neanderthals are significantly shorter than the observed interbirth intervals of extant great apes. We also discuss possible factors that may have caused the evolutionary divergence of hominid life history traits from those of great apes.     

Birth spacing in langur monkeys (Presbytis entellus)

This paper presents 10 years of reproductive data on birth interval length and 5 years of data on reproductive behavior postpartum from a captive colony of gray langur monkeys (Presbytis entellus)housed in Berkeley, California. Birth intervals of females following different pregnancy and nursing schedules are compared. Females whose infants survive to the age of 9 months have a median birth interval of 15.4 months. The experimental separation of mothers from infants for a period of 2 weeks, 6 to 9 months postpartum, had no significant effect on the median birth interval length. Females experiencing a pregnancy failure or the loss of a neonate had median birth intervals of 9.6 and 10.7 months, respectively. These intervals were significantly shorter than the birth intervals of females whose infants survived to 9 months, showing that the presence of a nursing infant delays the female’s time to next conception by approximately 5 to 6 months. Females experienced a median of three estrous periods (two estrous cycles) before conceiving postpartum, regardless of pregnancy outcome or length of infant survival, and females rarely conceived during their first estrous period postpartum. Weaning did not occur until after the mother’s next conception. These data indicate that, in populations of langurs characterized by average birth intervals of 15 to 16 months, the loss of an infant after the age of 5 to 6 months will not accelerate a female’s ability to conceive or shorten the birth interval length. The available data on birth spacing from populations of free-ranging langurs are reviewed. It could not be demonstrated that non-Himalayan populations are characterized by birth intervals which are as long as 20 to 24 months. Rather, it is suggested that female langurs inhabiting seasonally arid sites, such as Jodhpur, Abu, and Dharwar, may be capable of producing infants on the average of every 15 to 16 months. Flexibility in the timing of births and the lack of well-defined birth seasons at these sites may be explained by this species’ dietary and digestive adaptations. Additionally, data on birth spacing and the age of missing infants from the above field sites, where it has been suggested that infanticide following changes in male leadership occurs habitually, do not lend support to the sexual selection hypothesis of infanticide as proposed by S. Hrdy (1974, 1977).     

Are daughters more costly to produce for Japanese macaque mothers?: Sex of the offspring and subsequent interbirth intervals

Based on a sample of 237 live births recorded over a period of 30 years, a tendency for longer interbirth intervals following the birth of daughters than sons was recognized, in the provisioned Arashiyama troop of Japanese macaques. This may indicate that female infants were more costly to produce than male infants. This tendency seemed to be independent of a mother’s rank.     

Birth Intervals inM. sylvanus of Gibraltar

The length of the birth interval inMacaca sylvanus of Gibraltar was defined and one-year intervals were found to be normative. The effect of infant loss on the interbirth interval was assessed and found to have no influence. Variability in the birth interval in comparable species is noted.     

Interbirth interval variation in three sympatric species of neotropical monkey

Relatively few papers have focused on interbirth intervals in primates, even though the spacing between births is one of the primary determinants of female reproductive success in long-lived mammals. We present life history data from a ten-year field study of Costa Rican capuchins (Cebus capucinus), howlers (Alouatta palliata), and spidei monkeys (Ateles geoffroyi). Analyses of intraspecific variability found no significant differences attributable to individual variation in age, parity, weight, or maternal rank. Loss of an infant significantly shortened the interbirth interval in all three species. There was no correlation between annual rainfall and birth rates, but there was a significant clustering of births in the dry season. Survival analyses demonstrated a significant difference between the median interbirth intervals of the three species. Howlers have the shortest intervals (19.9 months), capuchins exhibit longer intervals (26.36 months), and spider monkeys have the longest intervals (34.72 months;. This comparative pattern does not correspond to relative body weights of the three species, but does correspond to relative brain weights. Comparisons to other primates with similar life history characteristics demonstrate that interbirth intervals are best examined at the level of their three component phases: gestation, lactation, and cycling to re-conception. © 1995 Wiley-Liss, Inc.     

Troop history,female reproductive strategies and timing of male change in Hanuman langurs,Presbytis entellus

Female reproductive data are presented from 9 years of longitudinal observations on two troops of Hanuman langurs (Presbytis entellus) living around Jodhpur, India. On the basis of 89 live births interbirth intervals were calculated to examine the effect of demographic factors on reproductive behaviour and troop composition. Sex of an infant seems to influence the length of intervals which are longer after the birth of female infants at an average of 1.7 months. It is suggested that this may be an outcome of differential maternal investment by allocating more time and energy towards female infants who run a higher mortality risk than male infants, at least up to an age of 27 months. Troopspecific interbirth intervals are influenced by social events. If the last infant is still alive when the next one is conceived, the intervals are significantly longer than after the premature loss of an infant (Bijolai troop: 15.6 vs. 12.1 months; Kailana-1 troop: 16.7 vs. 11.4 months). During undisturbed male tenureship intervals are shorter than after a male change (Bijolai troop: 14.3 vs. 16.0 months; Kailana-I troop: 15.6 vs. 17.5 months). Thus the frequency of male changes can influence the demography of a troop. Furthermore, the data suggest that take-overs are optimally timed by males. New males tend to take over a troop when most of the females are cycling.     

Infanticide and juvenilicide in Hanuman langurs (Presbytis entellus) around Jodhpur,India

Ten cases of infant killings and 2 cases of juvenile killings were observed in two troops of Hanuman langurs, (Presbytis entellus) around Jodhpur, India. Fatal attacks on infants and juveniles are classified into four categories. The process of infanticide was observed from start to end and is described in detail for 3 cases. The age of the victims ranged from 0.2 to 48 months. The interbirth interval among females whose infants were killed is significantly shorter compared to females whose infants survived. In ourt study, 7 cases support the reproductive advantage hypothesis, that infanticide is an adaptive behaviour to increase male reproductive success. The remaining 5 cases do not fit into the reproductive advantage hypothesis. In these cases, victims are over 8 months old, and as such their deaths could not shorten the interbirth interval. It appears that by killing older infants and juveniles the males obtain an advantage in resource competition for their offspring. An alternative is that new males chase or peripheralise the older infants and juveniles, which leads to 97% predominant uni-male troop structure in Jodhpur.     

Reproduction of the emperor tamarin (Saguinus imperator) in captivity,with comparisons to cotton-top and golden lion tamarins

Little information has been published on the reproductive biology and behavior of the emperor tamarin (Saguinus imperator). We analyzed twelve years of data on emperor tamarins at the Los Angeles Zoo and made comparisons with data on cotton-top tamarins (Saguinus o. oedipus) and golden lion tamarins (Leontopithecus rosalia) from the same collection. Secondary sex ratios did not differ significantly from 50:50. Births were not strictly seasonal for any species. The number of infants reared had a significant effect on interbirth interval for all species, with shorter intervals when only one or no infants were reared, but females did sometimes conceive early in lactation. In emperor tamarin families, all fathers and most older siblings carried new infants, usually beginning within a few days after a birth. Previous exposure to younger siblings did not appear to be critical to the development of competent parental behavior by zooborn emperor tamarin females.     

Relationship between plasma beta-carotene concentrations during the peripartum period and ovulation in the first follicular wave postpartum in dairy cows

Beta-carotene functions independently of vitamin A in the reproductive performance of dairy cows. The concentrations of beta-carotene in plasma decrease during the dry period, and reach a nadir in about the first week postpartum. This coincides with a negative energy balance, which affects the onset of the first ovulation in early postpartum cows. Thus, we hypothesised that plasma beta-carotene concentrations during the peripartum period may affect ovulation in the first follicular wave postpartum in dairy cows. The aim of the present study was to investigate changes in the profiles of plasma beta-carotene concentrations during the peripartum period in ovulatory and anovulatory cows during the first follicular wave postpartum. We used 22 multiparous Holstein cows, which were fed a total mixed ration consisting of grass, corn silage and concentrate, and collected blood samples for beta-carotene and progesterone analysis from week 3 prepartum to week 3 postpartum when the period of day 0-6 after parturition was regarded as the parturient week (week 0). The first ovulation was confirmed using the profile of plasma progesterone concentrations and colour Doppler ultrasound. Thirteen cows ovulated during the first postpartum follicular wave. Parity, the dry-off period, calving interval, mastitis episodes, and actual 305 days' milk yield during the previous lactation, and milk composition in the last month during the previous lactation in this study did not differ between ovulatory and anovulatory cows. Differences in the plasma beta-carotene profile were observed between ovulatory and anovulatory cows. Plasma beta-carotene concentrations at week 3 prepartum were greater in ovulatory cows (2.97+/-0.24 mg/L) than in anovulatory cows (1.53+/-0.14 mg/L; P<0.001), after that its concentrations in ovulatory cows decreased and reached the lowest level at week 1 postpartum, although its concentrations in anovulatory cows remained unchanged. No differences in plasma beta-carotene concentrations between the two groups were observed postpartum. The present study indicates for the first time that the lower beta-carotene concentrations in plasma during the prepartum period is associated with anovulation during the first follicular wave postpartum.     

Mother-infant relationships in Vervet Monkeys: Response to new adult males

The reaction of mothers to replacement of breeding adult males was studied in two captive groups of vervet monkeys. Mother-infant behavior for 15 infants born in the season following the introduction of new males was compared to mother-infant behavior for 35 infants born with adult males that had been resident in the group for more than a year. The mothers responded to the presence of new males by being more protective toward their infants in the first 3 months. Increased protectiveness disappeared in the second 3 months, and in the infant’s sixth month of life mothers with new males in the group became more rejecting than mothers with long-term resident males. The combination of increased protectiveness and increased rejection was unusual among the mothers with long-term resident males but was the most common mothering style used in the presence of new males. The rate of rejection was inversely correlated with the interbirth interval, and mothers with new males in the group conceived sooner and had significantly shorter inter-birth intervals compared to mothers with long-term resident males.