Developmental plasticity of the microscopic placental architecture in relation to litter size variation in the common marmoset monkey (Callithrix jacchus).

Fetal demand, shaped by factors such as number of fetuses, may alter placental regulation of exchange, even when maternal nutrition restriction is not overt. The marmoset is an interesting model in which to examine this aspect of placental function due to unique placentation that leads to multiple fetuses sharing a unified placental mass. We demonstrated previously that the triplet marmoset placenta exhibits significantly higher efficiency than does the twin placenta. Here, we test the hypothesis that this increased efficiency is due to increases in changes in the microscopic morphology of the placenta. Stereology was employed to analyze the microscopic architecture of placentas from twin and triplet pregnancies. Compartments of interest were the trabeculae, intertrabecular space, fetal capillaries, and the surface area of the maternal-fetal interface. Placentas from the two litters did not differ significantly in overall volume or individual volumetric compartments, but triplet placentas exhibited significant expansion of the trabecular surface area in comparison to twins (p=0.039). Further, the two groups differed in the isomorphy coefficient, with triplet placentas having a significantly higher coefficient (p=0.001) and potentially a more complex microscopic topography. Differences in the maternal-fetal interface may be due to developmental constraints on gross placental growth that occur earlier in gestation, such that the only option for maintaining sufficient access to maternal resources or signaling pathways late in gestation is via an expansion of the interface. Despite the significant increase in overall surface area, individual triplet fetuses are associated with much less surface area than are individual twins, suggestive of alterations in metabolic efficiency, perhaps via differential amino acid transport regulation.

Neonatal behavioral scoring of common marmosets (Callithrix jacchus): relation to physical condition and survival.

A seven-task behavioral test was performed on 86 common marmoset (Callithrix jacchus) infants, 24-36 h following birth. This report describes the test outcome and its relation to physical condition and survival of the infants. The percentage of infants receiving a perfect score on a given task ranged from 30.6 (rooting) to 70.6% (grasping). Heavier infants were more likely to have perfect scores for crawling (F=4.20, P=0.044) and infants with a longer knee-heel length tended to be more likely to have a perfect grasping score (F=3.63, P=0.06). While the modal score was a perfect score for most individual tasks, the modal number of total perfect scores that a given infant received was 3-4 and only 4.7% of infants received perfect scores on all seven tasks. These results suggest that this group of behavioral tasks will produce a variable response within a population of neonates. While no individual behavioral score predicted survival during week 1, the number of perfect scores across all tasks was predictive of survival outcome; infants with a higher total number of perfect scores were more likely to survive (F=6.02, P=0.018). When all combinations of tests were compared, the best predictor of survival was outcome on four of the seven tests, all related to motor skills (F=7.46, P=0.009).

Photic and nonphotic circadian phase resetting in a diurnal primate, the common marmoset.

Despite the considerable literature on circadian entrainment, there is little information on this subject in diurnal mammals. Contributing to this lack of understanding is the problem of separating photic from nonphotic (behavioral) phase-resetting events in diurnal species. In the present study, photic phase resetting was obtained in diurnal common marmosets held under constant dim light (DimDim; <0.5 lx) by using a 20-s pulse of bright light to minimize time available for behavioral arousal. This stimulus elicited phase advances at circadian time (CT) 18-22 and phase delays at CT9-12. Daily presentation of these 20-s pulses produced entrainment with a phase angle of approximately 11 h (0 h = activity onset). Nonphotic phase resetting was obtained under DimDim with the use of a 1-h-induced activity pulse, consisting of intermittent cage agitation and water sprinkling, delivered in total darkness to minimize photic effects. This stimulus caused phase delays at CT20-24, and entrainment to a scheduled daily regimen of these pulses occurred with a phase angle of approximately 0 h. These results indicate that photic and nonphotic phase-response curves (PRCs) of marmosets are similar to those of nocturnal rodents and that nonphotic PRCs are keyed to the phase of the suprachiasmatic nucleus pacemaker, not to the phase of the activity-rest cycle.

Relations among measures of body composition, age, and sex in the common marmoset monkey (Callithrix jacchus).

Few studies of body composition have been done in New World primates. In the study reported here, four methods of assessing body composition (body weight, anthropometry, labeled-water dilution, and total body electroconductivity) were compared in 20 marmosets, aged 0.96 to 7.97 years. Males and females did not differ in any measure (P > 0.05). Body weight ranged from 272 to 466 g, and body fat estimates varied from 1.6 to 19.5%. Strong positive correlations were observed between total body water and total body electroconductivity (R2 = 0.77), body weight and fat-free mass (males R2 = 0.95; females R2 = 0.91), and body weight and fat mass (males R2 = 0.86; females R2 = 0.85; P < 0.01). Male and female slopes were equivalent (P > 0.05) for the regressions of fat and fat-free mass against body weight. Positive correlations also were observed between girth measures and fat-free mass (R2 = 0.48 to 0.78) and fat mass (R2 = 0.60 to 0.74; P < 0.01). A good second- order polynomial relationship was observed between age and fat-free mass for the combined sample (R2 = 0.64). Results indicated that: subjects were lean; there was no sexual dimorphism relative to measures; body weight provided a reliable estimate of fat and fat-free mass; and within-subject body weight changes reflected a similar relationship between body weight and fat-free mass as did that across subjects.

Effects of allocare-givers on fitness of infants and parents in callitrichid primates.

The effects of callitrichid primate helpers (allocare-givers other than an infant's father) on the survival, reproduction or behavior of infants and parents are reviewed, using both published studies and data from free-ranging golden lion tamarins (Leontopithecus rosalia). Three lines of evidence suggest that helpers may increase their own inclusive fitness: (1) The number of adult males acting as helpers in free-ranging groups is correlated with the number of surviving infants in 3 callitrichid species. However, the lack of a negative correlation with number of infants dying suggests that activities other than direct infant care (e.g. territory defense) may be more important, especially in newly formed groups. (2) In 2 species, captive groups with helpers carry infants for longer periods of time than do groups without helpers. Whether such differences would translate into meaningful survival differences in free-ranging groups is unclear. (3) Helpers reduce the energetic burden of parents by reducing the amount of time they spend transporting or provisioning infants in at least 4 species. Reproductive males are more likely than reproductive females to benefit from the presence of helpers, reducing their investment in infant care activities as the number of helpers in the group increases. In free-ranging golden lion tamarins, the reproductive tenure of males, but not females, increases with the number of helpers in the group, suggesting that a reduction in energetic investment may translate into increased survival. 'Decisions' made by helpers to participate in infant transport are weighed against competing needs for foraging, vigilance, territory defense and, in some cases, prospecting for breeding opportunities. Given this complexity, a sophisticated model may be required to answer the question of how helpers 'decide' to participate in infant care versus other activities.

Ingestion of calcium solutions by common marmosets (Callithrix jacchus).

Callithrix jacchus, the common marmoset, is a small New World primate that feeds on insects, fruit, and gum, and has a high reproductive rate for a primate. Insects are generally a poor source of dietary calcium, while gums may contain significant levels of calcium. Their high reproductive rate also suggests that reproductive female C. jacchus might be susceptible to calcium deficiency. Thus, we hypothesized that common marmosets might find solutions containing calcium to be palatable. We used choice experiments to examine this phenomenon in 14 male and 19 female common marmosets. Animals were presented with identical water bottles containing either deionized water or a calcium lactate solution (either 2% or 4% calcium lactate by weight) and intake was measured. Serum 25-OH-vitamin D was monitored in a subset of the animals in the experiment to examine the role of vitamin D in this behavior. Our results demonstrated that C. jacchus can distinguish between plain water and a calcium lactate solution, and that in general they prefer calcium solutions. Although animals with marginal vitamin D status did have strong preferences for calcium solutions, they did not ingest significantly more of the calcium solutions than animals that were vitamin D-replete. Nulliparous females and males did not differ in the amounts of calcium solutions ingested. Lactating females ingested the greatest volume of the calcium solutions.

Estimation of gestational ages in the common marmoset (Callithrix jacchus) from published prenatal growth curves.

This report compares estimated gestational ages from published cubic spline curves to gestational ages estimated retrospectively from delivery dates in 28 pregnancies from ten common marmosets (Callithrix jacchus). Both CRL- and BPD-based estimates of gestational age were closely correlated with delivery-based gestational age estimates. Of the three ultrasound machines used, the one with 16 shades of gray and a sequential linear array overestimated gestational age during early pregnancy, based on CRL measures. Measures from the other two machines (64 or 264 shades of gray; linear sector and annular array or electronic phase array) were similar and resulted in a correlation of the two estimates of gestational age of 0.94 and a mean difference between the two estimates of 0.16 days with 80% of CRL-based gestational age estimates being within +/- 5 days of the delivery-based estimate. The reliability of BPD-based estimates of gestational age was strongly related to pregnancy outcome. BPD-based estimates underestimated gestational age in poor outcome pregnancies (i.e., those in which infants died within 7 days of birth) but not in good outcome pregnancies. The combined CRL- and BPD-based estimates on poor outcome pregnancies suggest that there was less growth in BPD in late gestation for those pregnancies that resulted in nonviable offspring. For good outcome pregnancies, the correlation between BPD-based and delivery-based estimates of gestational age was 0.871 and the mean difference between the two estimates was -0.06 days with 83.3% of BPD-based estimates falling within +/- 5 days of delivery-based estimates.

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.

Number of ovulations in the marmoset monkey (Callithrix jacchus): relation to body weight, age and repeatability.

The relation between number of ovulations and body weight, age or maternal identity was examined in 69 ovarian cycles from 29 captive-born common marmoset monkeys (Callithrix jacchus). Specifically, we addressed the following questions: was there high repeatability of ovulation number? Most of the variation in ovulation number was within, rather than between subjects. Repeatability in number of ovulations was 0.081 (n = 20 females with 2-6 ovulatory cycles per female); was age related to number of ovulations? There was no relation between age and number of ovulations, either within or between subjects; and was weight related to number of ovulations? Weight was related to number of ovulations. When the relation between number of ovulations (1-2 versus 3-4) and weight was examined through a logistic regression, there was a significant relation. Also, of the 11 subjects which had a variable number of ovulations across cycles, 90.9% were heavier when ovulating 3-4 than when ovulating 2. These results are discussed as the basis for the proposal that callitrichid primates may have been selected for potential variation in reproductive output and that this variation may be related to energy availability.

Genetic and environmental impacts on litter size and early infant survival in three species of callitrichids.

Callitrichids are unusual among anthropoid primates in that they can deliver one to four offspring per litter in captivity. Factors underlying intraspecific variation in litter size are unclear. Data from the Oak Ridge Associated Universities (ORAU) Marmoset Research Center provided an opportunity to investigate determinants of variation in (1) average litter size at birth and (2) average litter size surviving to 2 weeks of age in Saguinus fuscicollis, S. oedipus, and Callithrix jacchus. The objectives were to (1) investigate the impact of parity, husbandry, origin (wild or captive), and subspecific hybridization on phenotypic variance in litter size and (2) to estimate the heritability of litter size at birth and at 14 days. Husbandry changes were the only significant covariate and increased litter size at birth in C. jacchus only. Heritability estimates for average litter size at birth were significant only in S. fuscicollis (h2 = 0.306). Heritability of average litter size at 2 weeks of age was not significantly greater than zero. Estimates of genetic variability were relatively high, however both traits had very high levels of residual variance. The results suggest that litter size is a malleable trait that may respond to environmental factors.

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

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.

Social implications of gummivory in marmosets.

Gummivory or exudate feeding is a major dietary specialization which has received relatively little attention in the literature. While plant exudates contribute to the diet of many primate species, we suggest that the callitrichid species Cebuella pygmaea and Callithrix jacchus are obligate exudate feeders under free-ranging conditions. Callithrix jacchus provides an excellent model for examining the effects of exudate feeding and foraging upon social behavior, since other callitrichid species of similar body size do not share this dietary specialization. We review the effects of exudate foraging on specific social behaviors observed both in field and laboratory populations of C. jacchus. By comparing this species to closely related species, exudate foraging is seen to (1) be retained under laboratory conditions, (2) increase the frequency of territorial marking behavior while decreasing the frequency of overt aggression in males, (3) decrease the duration of infant care, and (4) increase the number of nonadults in social groups but not affect group size. The evidence presented supports the hypothesis that the consequences of exudate foraging in C. jacchus are fundamental and socially complex.

Follicular development and ovulation in the marmoset monkey as determined by repeated laparoscopic examination.

This paper describes the course of follicular development in vivo in the marmoset monkey, the only anthropoid primate with a relatively high (2-4) and variable ovulation number. Results are presented in relation to predictions from a mathematical model of control of follicle selection and ovulation number. Repeated laparoscopic examinations during the follicular phase were conducted for 14 cycles. Ovulatory follicles were 1.0 mm (median) in diameter at Day 6 and could be distinguished from nonovulatory follicles by Day 8, at which point they were 2.0 mm in diameter. Ovulations were not synchronous; the most common observation 1-2 days after the estradiol peak was ovulation of one follicle but not the other. Examination of the course of follicular development within a cycle and the distribution of ovulation sites both supported predictions stemming from a mathematical model of follicle selection developed by Lacker et al. [Biol Reprod 1987; 37:570-580]. Specific findings were the following: 1) Variations in patterns of follicle growth within a cycle resembled those generated by the model; in 64% of cycles, the 2-3 ovulatory follicles grew at similar rates. However, in 36% of cycles, ovulatory follicles displayed disparate rates of growth. 2) An examination of the distribution of ovulation sites (right versus left) revealed no significant difference from a binomial distribution, suggesting the likelihood that interovarian (rather than intraovarian) factors control this distribution.

Features of female reproductive senescence in tamarins (Saguinus spp.), a New World primate.

Cyclical changes in concentration of plasma progesterone, urinary oestrone-conjugates and urinary luteinizing hormone (LH) were compared in young and older cotton-top tamarins (Saguinus oedipus) and saddle-backed tamarins (S. fuscicollis). A group of six young adult tamarin females (4-5 years of age) was sampled over eight periods of 6-8 weeks and six older (14-20 years of age) females were sampled over thirteen periods. There was hormonal evidence of ovulation in all of the sampling periods for young females; in five of thirteen periods, older females displayed no evidence of ovulation. Of the six older females, two were anovulatory in one sampling period, while one female displayed no evidence of ovulation in any of three sampling periods. Generally, females over 17 years of age either did not ovulate or displayed abnormally long periods of moderate concentrations of progesterone and oestrone conjugates. Basal concentrations of LH differed in individuals, but were not always higher in older females. In contrast to patterns of reproductive senescence in other primates, older, anovulatory tamarins displayed moderate concentrations of urinary oestrone conjugates (5-50 micrograms/mg creatinine) and plasma progesterone (8-19 ng/ml), both of which are hormones of probable luteal origin in these species. This result suggests continued production of steroids by the luteal cells of the prominent interstitial gland in reproductively senescent tamarins. This suggestion was reinforced by histological examination of the ovaries of four older, anovulatory females; few primary follicles were found. Three females had no normal antral follicles, but all females had large luteal masses. The presence of functional luteal cells in the older ovaries, which do not experience regular follicular development, may distinguish ovarian ageing in New World primates from that of Old World primates.

Reproductive factors affecting survivorship in captive Callitrichidae.

Efforts to breed Callitrichidae in captivity have resulted in high fertility accompanied by high infant mortality. This paper investigates the relationship between reproductive characteristics and survivorship in the Oak Ridge and Associated Universities (ORAU) callitrichid colony. Records of 2,834 individuals were analyzed using Cox Proportional Hazards regression to investigate factors affecting infant survivorship. Species and birth cohort were found to have a significant (P less than 0.05) effect on survivorship. Litter size also was an important factor in determining survivorship. Individuals born into singlet and twin litters had significantly (P less than 0.001) higher survivorship than triplets. Factors which affect survivorship perinatally (0-1 months of age), prior to breeding age and subsequent to the first month of life were then investigated. Litter size was a significant (P less than 0.05) factor in determining survivorship perinatally, with twins having significantly higher survivorship than both singlets and triplets. After the first month of life, litter size no longer showed a significant effect on survivorship. Records of 145 dams were analyzed using the same procedures to investigate reproductive characteristics associated with survivorship. Age at first litter showed a significant (P less than 0.01) positive relationship with dam survivorship. These results suggest various factors affect survivorship at specific temporal points during development, and also suggest selection for survivorship perinatally to be strongly associated with litter size, possibly through sibling competition and maternal effects.

Kin preference in marmosets and tamarins: Saguinus oedipus and Callithrix jacchus (Callitrichidae, primates).

Field studies on callitrichid primates have suggested that some species may exhibit a communal breeding system in which two or more males mate with a single female and cooperatively participate in infant rearing. However, high levels of aggression have been observed between males under both laboratory and field conditions. In avian models for communal breeding, cooperating males are often closely related. In a laboratory test of a hypothesis of the amelioration of aggression based on kinship, four mated pairs of both Saguinus oedipus and Callithrix jacchus were introduced to both novel male conspecifics and to their own male siblings, from whom they had been separated for a minimum of 4 months. Significant differences (P less than .01) were seen in the responses of the two species to male conspecifics generally: S. oedipus males responded to intruders with overt aggression significantly more frequently than did marmosets while C. jacchus males more frequently scent-marked than did tamarins. Evidence of preference for kin males was seen in the significantly decreased frequencies of these behaviors in the presence of kin males over those observed in the presence of novel males. It is argued that, under field conditions, cooperation between male callitrichids may be facilitated by kinship. Further, twin births, short gestation lengths, and interbirth intervals seen in callitrichid primates all contribute to the number of socially familiar kin with which an individual animal might cooperate.

Maintenance of cotton-top tamarins fed an experimental pelleted diet versus a highly diverse sweetened diet.

The future study of colon disease in captive callitrichid colonies may require manipulation of diets. The limited knowledge of the nutritional requirements for these species and the varied diets and supplementations fed to these animals in various colonies suggest the importance of testing the palatability and acceptability of diets for these primates. Individually housed cotton-top tamarins (Saguinus oedipus) were given either the regular Oak Ridge Associated Universities (ORAU) diet (monkey chow slurry, canned diet and supplements), a similar slurry using an experimental natural ingredient diet plus supplements, or the experimental diet without supplements. Neither dry food consumption, body weight, fecal output, nor the histological evaluation of the colons were affected by these diets. Daily intake of protein and calories were higher than previously reported estimates for the species. These results demonstrate that a natural ingredient non-sweetened pelleted diet is palatable for cotton-top tamarins for a period of 3.5 months, however, further testing over longer time periods is necessary. The nonnutritional (e.g. psychological) advantages of providing a highly diverse diet to primates housed in a relatively monotonous environment should be considered before adopting such a diet for an entire colony.

Histologic evidence for age-related differences in ovarian function in tamarins (Saguinus sp.; primates).

The ovaries of 15 tamarins (Saguinus sp.) between 2 and 16 yr of age were collected at necropsy and examined for evidence of age-related differences. As expected, there was a marked decline in the number of primary follicles with advancing age. Age and the number of primary follicles available had minimal effect on the number of follicles recruited into the preantral population; however, there were significant decreases in the number of large preantral and antral follicles with increasing age. The observed decline in follicular development with age was consistent with a reproductive decline with age observed in some tamarin females. Luteal-like masses were found in all ovaries examined and their size and appearance was unrelated to age.