Reproductive efficiency in the common marmoset (Callithrix jacchus): A longitudinal study from ovulation to birth monitored by ultrasonography

Abstract: This study examines reproductive efficiency in the common marmoset monkey, Callithrix jacchus, using sequential ultrasound examinations to establish ovulation number, implantation rate, and incidence of prenatal loss. Ultrasound was carried out with a 10 or 7.5 mHz probe in nonsedated animals, daily during the late follicular phase, approximately twice a week until day 20 after ovulation, and at days 35, 56, and 85 of pregnancy to enable visualization of gestation sacs, heartbeats, and fetal heads, respectively. Ovulatory follicles could be seen 3–4 days before ovulation and by day –2, 98% of ovulating follicles were >2mm diameter, although almost 10% of follicles of this size disappeared without ovulating. Total number of ovulating follicles for 15 females was 45 (mean ovulation rate ? 3.0, range 2–4). In the 14 animals that conceived, 41 corpora lutea were identified (mean ovulation rate = 2.9) within 10 days of ovulation. All pregnancies went to term (no abortion occurred) resulting in the birth of 37 neonates (9 triplets, 5 twins) and an average litter size of 2.64. All four losses were confined to the embryonic period (< day 85), two occurring before day 35, one between days 35 and 56, and one between days 56 and 85. In demonstrating that 90% of ovulatory follicles gave rise to live offspring, the results of this study indicate an extremely high reproductive efficiency in the marmoset monkey (when maintained under favorable captive conditions) and a rate of prenatal loss much lower than that reported for other primate species.     

Patterns of prenatal survival in the common marmoset (Callithrix jacchus)

Abstract: Fifty common marmoset pregnancies were monitored using ultrasound. The objective was to ascertain if fetal mortality was related to litter size. Prior to analysis we determined abortion rate and litter size were not influenced by repeated ultrasound. Mortality was unrelated to litter size and occurred fairly late in gestation. All singletons born in this study began gestation as twins. It is hypothesized that marmosets may be able to adjust litter size late in pregnancy in response to proximate environmental factors.     

Ultrasonographic and hormonal monitoring of pregnancy in the saddle back tamarin,Saguinus fuscicollis

Ultrasonography was used in six saddle back tamarin females (Saguinus fuscicollis) to diagnose pregnancy, monitor the patterns of uterine growth and embryonic/foetal development and examine the incidence loss of single embryos/foetuses. Pregnancy was reliably diagnosed 17 days after conception, 10 days earlier than by plasma progesterone measurement. The patterns of uterine and embryonic/foetal growth paralleled those reported for the common marmoset, including a delay in embryonic development. The results support the hypothesis of retardation of organogenesis in most callitrichid species. Individual embryos could be reliably identified from day 50 of pregnancy; a loss of single embryos/foetuses after this stage did not occur. All pregnancies were carried to term, resulting in five times twins and one singleton. The smaller litter size compared to the common marmoset may be due to loss of single embryos at earlier stages of pregnancy or to a lower ovulation rate.     

Post-conception reproductive competition in cooperatively breeding common marmosets

Common marmosets are cooperatively breeding monkeys that exhibit high female reproductive skew. Subordinate females usually fail to breed as a consequence of ovulation suppression and inhibition of sexual behavior, and, even when they do breed, typically rear fewer infants than dominants. We evaluated possible mechanisms of post-conception reproductive competition by comparing hormonal profiles across pregnancy, pregnancy outcomes, infant survivorship, and behavior in laboratory-housed families containing one (N=9) or two (N=7) breeding females. Breeding females in plurally breeding groups did not exhibit well-defined dominance relationships and rarely engaged in escalated aggression with one another. No significant differences were found among singly breeding mothers, plurally breeding mothers, and plurally breeding daughters in urinary chorionic gonadotropin or estradiol sulfate concentrations during pregnancy, fetal biparietal diameter, frequency of spontaneous abortion, frequency of stillbirths, number of live-born infants per litter, or infant mortality rates. When females gave birth while another female in the family was pregnant, however, their infants were highly likely to be killed. The perpetrator was definitively identified in only one family, in which a pregnant female killed her daughter's infant. These results are consistent with observations of free-living common marmosets and suggest that breeding females do not regularly influence one another's pregnancy outcomes, but that they may commonly kill each other's infants, especially during their own pregnancy. Our findings further suggest that infanticide by breeding females may have selected for the evolution of reproductive restraint in subordinate female marmosets.     

A case report of spontaneous opening of congenitally fused labia in a female common marmoset (Callithrix jacchus) followed by pregnancy and birth of twins

A first case of spontaneous opening of congenitally fused labia (CFL phenotype) in a captive common marmoset followed by pregnancy and birth is presented here. The occurrence of this phenotype has been previously published in captive marmosets, but so far the etiology is unknown.     

Timing of parturition in the rat: an analysis of successive births

To determine whether consecutive parturitions within individual rats are likely to occur around the same time of the 24h day, female rats mated prior to ovulation and maintained on a LD 12:12 photoperiod, were observed over either two or three parturitions. A subgroup of females was placed on constant light during the second gestation in order to determine the role of photoperiod in the temporal synchronization of consecutive births. The major findings were 1. individual females tended to give birth around the same time of the day on consecutive births so long as the photoperiod remained constant; 2. the small percentage of births occurring during darkness, the less-prevalent time of the photoperiod for birthing, were anomalous births for individual females; and 3. litter weight was a significant factor in predicting time of birth for females, but this effect interacted with photoperiod. These data elucidate the importance of knowing previous birth time, litter weight, and photoperiod on predicting the time of parturition in the rat.     

Reproductive output, maternal age, and survivorship in captive common marmoset females (Callithrix jacchus)

Common marmosets (Callithrix jacchus) demonstrate significant variation in reproductive output on both a yearly and lifetime basis in comparison to other anthropoid primates. We explore the factors that may be most important in determining reproductive variation in captive common marmosets. Studies have found that maternal age, maternal condition, and dam survivorship are related to reproductive output; however, these reports are not in agreement and are far from conclusive. With the use of a large, multicolony, demographic database pooling data across five marmoset colonies, we examined litter information for 1,649 litters, and reproductive summaries for 400 dams to assess 1) how reproductive output variation (total production, total weaned production) is determined by litter size, interbirth interval (IBI), age at first birth, and dam survival age; 2) the relationship between maternal age and reproductive output variables; and 3) relationship between the reproductive output variables and survival. We used stepwise regression procedures to describe the amount of variation in lifetime reproductive output among dams, and found that mean litter size accounted for 18% of the variance in total production, survival age accounted for 10.6%, age at first birth accounted for 8.8%, and mean IBI accounted for 5%. For total (nonzero) weaned production, survival age accounted for 7.6% of variance, age at first birth accounted for 7.2%, mean IBI accounted for 2%, and mean litter size accounted for 1.6%. We identified significant effects (P<0.05) of maternal age on litter size and IBI length, but no effect of dam age on weaned litter size. Cox proportional hazards regression analyses revealed significant effects (P<0.01) of number of litters, age at first birth, and site on dam survivorship. Dams that produced more litters showed higher survivorship. Age at first birth showed a positive relationship with dam survivorship, i.e., dams that delayed first reproduction had higher survival. Our findings about reproductive variation in marmosets may have practical applications for the management of marmoset breeding colonies.     

Reproduction in captive common marmosets (Callithrix jacchus)

Though sexual maturation may begin at around one year of age, first successful reproduction of the common marmoset (Callithrix jacchus) is likely to be later, and it is generally recommended that animals not be mated before 1.5 years of age. The average gestation period is estimated to be 143 to 144 days. A crown-rump length measurement taken by use of ultrasonography during the linear, rapid, prenatal growth phase (between approx. days 60 and 95) can be compared against standard growth curves to estimate delivery date to within 3 to 4 days, on average. Marmosets produce more young per delivery than does any other anthropoid primate, and have more variation in litter size. Many long-established colonies report that triplets are the most common litter size, and there is documented association between higher maternal body weight and higher ovulation numbers. Higher litter sizes generally do not generate higher numbers of viable young. Marmosets are unusual among primates in having a postpartum ovulation that typically results in conception and successful delivery; reported median inter-birth intervals range from 154 to 162 days. However, pregnancy losses are quite common; one study of a large breeding colony indicated 50 percent loss between conception and term delivery. The average life span for breeding females is around six years; the range of reported average lifetime number of litters for a breeding pair is 3.45 to 4.0. Our purpose is to provide an overview of reproduction in the common marmoset, including basic reproductive life history, lactation and weaning, social housing requirements, and common problems encountered in the captive breeding of this species. A brief comparison between marmoset and tamarin reproduction also will be provided.     

Reproductive parameters of the common genet <Emphasis Type="Italic">Genetta genetta</Emphasis> (Linnaeus, 1758) in Southwest Europe

We used information from 148 litters belonging to 119 different wild and captive female common genets (Genetta genetta) in SW Europe over a period of almost 50 years to study certain reproductive parameters. Data were obtained from a combination of sources including carcasses, live captures, telemetry-based studies, captive genets, and reports in the literature. The circannual pattern of breeding was fairly similar in both wild and captive genets, with births occurring in all months except December, albeit with a large peak in spring and a secondary peak in autumn. The sex ratio at birth was near to 1:1, and mean litter size was 2.16 ± 0.76 cubs/litter with a range of 1–5 cubs. Litters of two cubs were the most frequent both in wild and captive settings. In captivity, we have observed the births of replacement litters and double litters; however, we did not find evidence of wild females that having two litters in the same year. We conclude that the possibility of breeding at any time of the year is facilitated by the continuous spermatogenesis of the males and by the ability of females to enter into estrus after losing a litter prematurely and to breed twice in the same year.     

Body Weight of Wild and Captive Common Marmosets (Callithrix jacchus)

Captive studies and occasional trappings of wild individuals indicate that callitrichids have small size and body weight and lack sexual dimorphism. We compared body weights of captive and wild Callithrix jacchus obtained by repeatedly weighing subjects from two populations in Brazil. We obtained captive data by routinely weighing 138 individuals from the Universidade Federal do Rio Grande do Norte colony and wild data via regular trapping of 243 individuals in 15 free-ranging groups from IBAMA's field site in Nísia Floresta. We assigned all subjects to one of four age classes—infant, juvenile, subadult, and adult—according to their birth dates or size, reproductive status, and dental development. There is no significant difference between males and females in any of the four age classes, but captive subjects were heavier than wild ones in all age classes but infant. Reproductive and nonreproductive adult females showed no statistical difference in weight. These results accord with previous reports of lack of body size sexual dimorphism in common marmosets and suggest that differences between wild and captive common marmosets are not constitutional, but are instead a consequence of diet and physical activity. The absence of weight difference between reproductive and nonreproductive females suggests that any possible advantage from high rank is outweighed by the costs of reproduction in common marmosets.     

Ecology and age,but not genetic ancestry,predict fetal loss in a wild baboon hybrid zone

Objectives

Pregnancy failure represents a major fitness cost for any mammal, particularly those with slow life histories such as primates. Here, we quantified the risk of fetal loss in wild hybrid baboons, including genetic, ecological, and demographic sources of variance. We were particularly interested in testing the hypothesis that hybridization increases fetal loss rates. Such an effect would help explain how baboons may maintain genetic and phenotypic integrity despite interspecific gene flow.

Materials and Methods

We analyzed outcomes for 1020 pregnancies observed over 46 years in a natural yellow baboon-anubis baboon hybrid zone. Fetal losses and live births were scored based on records of female reproductive state and the appearance of live neonates. We modeled the probability of fetal loss as a function of a female's genetic ancestry (the proportion of her genome estimated to be descended from anubis [vs. yellow] ancestors), age, number of previous fetal losses, dominance rank, group size, climate, and habitat quality using binomial mixed effects models.

Results

Female genetic ancestry did not predict fetal loss. Instead, the risk of fetal loss is elevated for very young and very old females. Fetal loss is most robustly predicted by ecological factors, including poor habitat quality prior to a home range shift and extreme heat during pregnancy.

Discussion

Our results suggest that gene flow between yellow and anubis baboons is not impeded by an increased risk of fetal loss for hybrid females. Instead, ecological conditions and female age are key determinants of this component of female reproductive success.     

Relations among birth condition, maternal condition, and postnatal growth in captive common marmoset monkeys (Callithrix jacchus)

The present study characterizes the relations among maternal condition, litter size, birth condition, and growth in body weight for a population of common marmosets. The subjects of the study were marmosets born into a single colony between 1994 and 2001. Three sets of analyses were conducted to answer the following questions: 1) Is there a relationship between litter size, maternal condition, and birth condition? In the study population, maternal body weight, maternal age, litter size, and birth condition were related in a complex fashion. Birth weight and prenatal long‐bone growth, as reflected in knee–heel length, were both related to maternal age, with older mothers supporting higher prenatal growth. Age and maternal condition appeared to interact as determinants of long‐bone growth, as the combination of older and larger mothers resulted in significantly longer knee–heel lengths in their offspring. 2) Is there a relationship between birth condition or maternal condition and subsequent growth or final adult size? The early growth rate in this population was similar to early growth rates reported for three different marmoset colonies, suggesting that early growth may be relatively inflexible in this species. However, within this population, the variation that did occur in early growth rate was related to birth weight and maternal weight. Later growth and adult weight were related to birth weight and litter size: small twin infants displayed slower later growth rates and were smaller as adults than twins that began life at a higher birth weight, while the birth weight of triplets was not related to adult size. In these marmosets, small infants that were the result of increased litter size differed from small infants whose small birth size resulted from other factors. This reinforces the proposal that the causes of low birth weight will be relevant to the development of the marmoset as a model of prenatal environmental effects. Am. J. Primatol. 62:83–94, 2004. © 2004 Wiley‐Liss, Inc.     

Interactions between infant growth and survival: Evidence for selection on age-specific body weight in captive common marmosets (Callithrix jacchus)

The objective of this study is to investigate factors influencing infant survival in captive common marmosets. We investigated the influence of age-specific weight, litter size, caging, and the presence of helpers on survival to 6 months of age in 189 Callithrix jacchus infants. Infant survival was analyzed using Cox Proportional Hazards regression, and fitness functions were plotted to explore the relationship between survival and growth. Results indicate that weights at birth and 120 days significantly affect future survival probability. Litter size significantly influences survival prior to 60 days of age with larger litters having poorer survival. Males and females did not have significantly different survival and the presence of helpers in the group did not influence survival probability. Patterns of survival with respect to age-specific weights suggest stabilizing selection on birth weight and directional selection on weight at 120 days of age. Am. J. Primatol. 42:269–280, 1997. © 1997 Wiley-Liss, Inc.     

Placental efficiency and intrauterine resource allocation strategies in the common marmoset pregnancy

Mothers and fetuses are expected to be in some degree of conflict over the allocation of maternal resources to fetal growth in the intrauterine environment. Variation in placental structure and function may be one way a fetus can communicate need and quality to its mother, potentially manipulating maternal investment in its favor. Whereas common marmosets typically produce twin litters, they regularly give birth to triplet litters in captivity. The addition of another fetus is a potential drain on maternal resource availability and thus a source of elevated conflict over resource allocation. Marmoset littermates share a single placental mass, so that differences in the ratio of fetal to placental weight across litter categories suggest the presence of differential intrauterine strategies of resource allocation. The fetal/placental weight ratio was calculated for 26 marmoset pregnancies, representing both twin and triplet litters, to test the hypothesis that triplet fetuses respond to intrauterine conflict by soliciting placental overgrowth as a means of accessing maternal resources. In fact, relative to fetal mass, the triplet marmoset placenta is significantly undergrown, with individual triplets associated with less placental mass than their twin counterparts, suggesting that the triplet placenta is relatively more efficient in its support of fetal growth. There still may be an important role for maternal-fetal conflict in the programming of placental structure and function. Placental adaptations that solicit potential increases of maternal investment may occur at the microscopic or metabolic level, and thus may not be reflected in the size of the placenta as a whole.     

Supplementation of dextrose to the diet during the weaning to estrus interval affects subsequent variation in within-litter piglet birth weight

Effects of supplementation of dextrose to the diet of sows during the weaning-to-estrus interval (WEI) on subsequent litter size and within-litter variation were investigated. After weaning, 223 sows (first to fifth parity) were fed 3.5 kg/d. Half of the sows additionally received 150 g of dextrose per day as topdressing on the feed. WEI and estrus duration were determined as well as subsequent pregnancy rate and litter size. Piglets were weighed individually at birth and at weaning (day 26.4; S.D.: 2.5). Supplementation of dextrose to the diet during the WEI did not affect WEI (106 h), pregnancy rate (88.2%), farrowing rate (84.2%), subsequent litter size (total born: 13.70), or birth weight (1599 g). The within-litter variation in birth weight was lower in sows on the dextrose treatment (CV: 17.5% versus 21.2% for the dextrose and control group, respectively, P=0.03). From this experiment, we concluded that addition of dextrose during the weaning to estrus interval did not increase litter size, but seems to affect the uniformity in birth weight of the litter.     

Relationships between fetal biometry, maternal factors and birth weight of purebred domestic cat kittens

The goal of this study was to evaluate the relation between kittens' birth weights and biometrical factors from the kittens and the mother during pregnancy. Knowing fetal birth weight could help in detecting abnormalities before parturition. A Caesarean-section or a postnatal management plan could be scheduled. Consequently, the neonatal mortality rate should be decreased. We used ultrasonographic measurements of femur length (FL) or fetal biparietal diameter (BPD), pregnancies, and maternal factors to obtain a model of prediction. For this purpose, linear mixed-effects models were used because of random effects (several fetuses for one queen and a few paired measurements) and fixed effects (litter size, pregnancy rank, weight, wither height, and age of the queen). This study was performed in 24 purebred queens with normal pregnancies and normal body conditions. Queens were scanned in the second half of pregnancy, using a micro-convex probe. They gave birth to 140 healthy kittens whose mean birth weight was 104 g (ranged 65 to 165 g). No correlation between the birth weight and the age of the queen, as a maternal factor alone, was observed. But the birth weight was found to be inversely proportional to the pregnancy rank and the litter size. Moreover, birth weight increased when the weight and wither height of queen increased. BPD and FL increased linearly during pregnancy so a model was used to estimate mean birth weight. Using this model, we found a correlation between mean birth weights and an association of parameters: maternal factors (wither height and age), and litter size.     

Insulin-stimulating diets during the weaning-to-estrus interval do not improve fetal and placental development and uniformity in high-prolific multiparous sows

Piglet birth weight and litter uniformity are important for piglet survival. Insulin-stimulating sow diets before mating may improve subsequent piglet birth weights and litter uniformity, but the physiological mechanisms involved are not clear. This study evaluated effects of different levels of insulin-stimulating feed components (dextrose plus starch; fed twice daily) during the weaning-to-estrus interval (WEI) on plasma insulin and IGF-1 concentrations, and on follicle development and subsequent luteal, fetal and placental development and uniformity at days 42 to 43 of pregnancy. During WEI, multiparous sows were isocalorically fed diets supplemented with 375 g/day dextrose plus 375 g/day corn starch (INS-H), with 172 g/day dextrose plus 172 g/day corn starch and 144 g/day animal fat (INS-L), or with 263 g/day animal fat (CON). Jugular vein catheters were inserted through the ear vein at 1.5 days before weaning to asses plasma insulin and IGF-1 concentrations. After estrus, all sows received a standard gestation diet until slaughter at days 42 to 43 of pregnancy. The dextrose plus starch-diets enhanced the postprandial insulin response in a dose-dependent manner (e.g. at day 2 insulin area under the curve was 4516 μU/444 min for CON, 8197 μU/444 min for INS-L and 10 894 μU/444 min for INS-H; s.e.m. = 694; P < 0.001), but did not affect plasma IGF-1 concentrations during the first 3 days of WEI. Follicle development and subsequent luteal, fetal and placental development and uniformity were not affected by the dietary treatments, nor related to plasma insulin and IGF-1 concentrations during WEI. Pre-weaning plasma insulin and IGF-1 concentrations were negatively related to sow body condition loss during lactation, but were not related to subsequent reproduction characteristics. This study shows that dietary dextrose plus starch are effective in stimulating insulin secretion (both postprandial peak and long-term concentration), but not IGF-1 secretion during the first 3 days after weaning in multiparous sows. The extreme insulin-stimulating diets during WEI did, however, not improve follicle development, or subsequent development and uniformity of fetuses and placentas in these high-prolific sows (27.0 ± 0.6 ovulations; 18.6 ± 0.6 vital fetuses).     

Relationships between fetal biometry,maternal factors and birth weight of purebred domestic cat kittens

The goal of this study was to evaluate the relation between kittens' birth weights and biometrical factors from the kittens and the mother during pregnancy. Knowing fetal birth weight could help in detecting abnormalities before parturition. A Caesarean-section or a postnatal management plan could be scheduled. Consequently, the neonatal mortality rate should be decreased. We used ultrasonographic measurements of femur length (FL) or fetal biparietal diameter (BPD), pregnancies, and maternal factors to obtain a model of prediction. For this purpose, linear mixed-effects models were used because of random effects (several fetuses for one queen and a few paired measurements) and fixed effects (litter size, pregnancy rank, weight, wither height, and age of the queen). This study was performed in 24 purebred queens with normal pregnancies and normal body conditions. Queens were scanned in the second half of pregnancy, using a micro-convex probe. They gave birth to 140 healthy kittens whose mean birth weight was 104 g (ranged 65 to 165 g). No correlation between the birth weight and the age of the queen, as a maternal factor alone, was observed. But the birth weight was found to be inversely proportional to the pregnancy rank and the litter size. Moreover, birth weight increased when the weight and wither height of queen increased. BPD and FL increased linearly during pregnancy so a model was used to estimate mean birth weight. Using this model, we found a correlation between mean birth weights and an association of parameters: maternal factors (wither height and age), and litter size.     

Genetic control of multiple births in low ovulating mammalian species

In mammals, litter size is a highly variable trait. Some species such as humans or cattle are monotocous, with one or sometimes two newborns per birth, whereas others, the polytocous species such as mice or pigs, are highly prolific and often produce a dozen newborns at each farrowing. In monotocous species, however, two or three newborns per birth may sometime be unwanted. In more polytocous species such as sheep or pigs, litter size is studied in order to increase livestock prolificacy. By contrast, twinning rates in humans or cattle may increase birth difficulties and health problems in the newborns. In this context, the aim of our review was to provide a clearer understanding of the genetic and physiological factors that control multiple births in low-ovulating mammalian species, with particular focus on three species: sheep, cattle, and humans, where knowledge of the ovulation rate in one may enlighten findings in the others. This article therefore reviews the phenotypic and genetic variability observed with respect to ovulation and twinning rates. It then presents the QTL and major genes that have been identified in each species. Finally, we draw a picture of the diversity of the physiological mechanisms underlying multiple ovulation. Although several major genes have been discovered in sheep, QTL detection methods in humans or cattle have suggested that the determinism of litter size is complex and probably involves several genes in order to explain variations in the number of ovulations.

     

Characteristics of reproductive biology and proximate factors regulating seasonal breeding in captive golden-headed lion tamarins (Leontopithecus chrysomelas)

Reproduction is highly demanding in terms of energy expenditure, and the costs and benefits associated with postponing or investing in a reproductive effort are crucial determinants of an individual's fitness. Understanding the reproductive potential of a species under varying ecological conditions offers important insights into the dynamics of its social system. This study provides the first detailed analysis of the reproductive potential of wild- and captive-born golden-headed lion tamarins (Leontopithecus chrysomelas) under captive conditions, based on studbook data compiled during 1984-2000. Litters produced by wild-born females breeding in captivity are similar in size to litters observed in the wild, but smaller than litters of captive-born females. The more stringent ecological conditions experienced by wild-born females during maturation may result in a lifelong effect on litter size. However, interbirth intervals are shorter for wild-born than captive-born females. The relatively smaller burden of infant care that results from having smaller litters may allow wild-born females to sustain the next pregnancy sooner. Reproduction in the Brazilian captive population is highly seasonal for both wild-born females and females born in captivity in Brazil. Changes in photoperiod over a year provide a proximate explanation for changes in the proportion of conceptions and births per month. Outside Brazil, breeding occurs year-round, and no clear birth peak is apparent. Information from field reports that could be used to relate this finding to ecological factors, such as resource availability, is unavailable.