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.     

Differential infant carrying in captive and wild common marmosets (Callithrix jacchus)

Callitrichids are communal breeders that lack sexual dimorphism, and only a few studies have examined behavioral gender differences among them. The purpose of this study was to investigate gender differences in infant carrying in 16 captive and seven wild common marmoset groups. Our results showed that female–female twin pairs were carried significantly more often by fathers than were male–male and male–female pairs both in the wild and in captivity. We suggest these differences may be related to different reproductive potentials of male and female Callithrix jacchus and possibly to future breeding competition among females.     

Feeding behavior of Geoffroy's marmoset (Callithrix geoffroyi) in an Atlantic forest fragment of South-eastern Brazil

We report on the diet and feeding behaviour of a group of Geoffroy's marmosets (Callithrix geoffroyi) in an Atlantic forest fragment in south-eastern Brazil, studied during the period February 1993 to Januaray 1994. Major food categories were gums (68.6%) fruits (15%), and small animal prey (invertebrates 14.6% and vertebrates 0.8%). Dietary changes were observed between the wet and dry seasons, although they were not statistically significant. Insects and gums were consumed throughout the year but fruits were more prevalent in the diet in the wet season. Plant species exploited for their gums includedInga stipularis, followed byAcacia paniculata, Paulinia carpopodia, andBauhinia angulosa. Chemical analysis of the gum of the four species most used all presented high values for carbohydrates and crude proteins. Fruits of an unidentified species of Myrtaceae (sp. 2) were consumed the most. Animal prey consisted mainly of insects, arachnids, snails, and in three cases, lizards and frogs, with orthopterans being the most prevalent insect prey. This study demonstrates thatC. geoffroyi efficiently exploits resources typically available in secondary and disturbed forest habitat. The main threat to the species is forest destruction, degradation, and fragmentation, but the management of small forest fragments may be an effective corservation strategy.     

A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity

Most New World monkey species have both dichromatic and trichromatic individuals present in the same population. The selective forces acting to maintain the variation are hotly debated and are relevant to the evolution of the ‘routine’ trichromatic colour vision found in catarrhine primates. While trichromats have a foraging advantage for red food compared with dichromats, visual tasks which dichromats perform better have received less attention. Here we examine the effects of light intensity on foraging success among marmosets. We find that dichromats outperform trichomats when foraging in shade, but not in sun. The simplest explanation is that dichromats pay more attention to achromatic cues than trichromats. However, dichromats did not show a preference for foraging in shade compared with trichromats. Our results reveal several interesting parallels with a recent study in capuchin monkeys (Cebus capucinus), and suggest that dichromat advantage for certain tasks contributes to maintenance of the colour vision polymorphism.     

The development of infant-caregiver relationships in captive common marmosets (Callithrix jacchus)

The growing independence of infant common marmosets from their caregivers is promoted primarily by their caregivers, who increasingly often prevent the infants from climbing onto them and decreasingly often pick the infants up. Infants achieve independence from their mothers, fathers, and older siblings at different rates and develop characteristically different relationships with them. Infants that are most rejected by caregivers spend the least time on them. When rejected by their parents, infants tend to spend their time with their twins, rather than seeking to climb onto other caregivers. Caregivers do not compensate for unduly large or small amounts of care given by other members of the group. It is argued that if we are to understand the development of caregiver-infant relationships in species with multiple caregivers, we must discover the rules by which infants assess the amount of care they perceive themselves to have received and caregivers assess the amount of care they perceive themselves to have offered. The implications of a simple model based on expected levels of caregiving and careseeking are explored, particularly with respect to competition and compensation.     

Maternal gestational androgens are associated with decreased juvenile play in white-faced marmosets (Callithrix geoffroyi)

Exposure to androgens during prenatal development shapes both physiological and behavioral developmental trajectories. Notably, in rhesus macaques, prenatal androgen exposure has been shown to increase rough-and-tumble play, a prominent behavioral feature in males during the juvenile period in primates. While macaques are an Old World, polygamous species with marked sexually dimorphic behavior, New World callitrichine primates (marmosets and tamarins) live in cooperative breeding groups and are considered to be socially monogamous and exhibit minimal sexual dimorphism in social play, which suggests that androgen may affect this species in different ways compared to macaques. In addition, we previously described considerable variation in maternal androgen production during gestation in marmosets. Here we tested the association between this variation and variation in offspring rough-and-tumble play patterns in both males and females. We measured testosterone and androstenedione levels in urine samples collected from pregnant marmoset mothers and then observed their offspring's play behavior as juveniles (5-10 months of age). In contrast to findings in rhesus macaques, hierarchical regression analyses showed that higher gestational testosterone levels, primarily in the second semester, were associated with decreased rough-and-tumble play in juveniles, and this relationship appears to be driven more so by males than females. We found no reliable associations between gestational androstenedione and juvenile play behavior. Our findings provide evidence to suggest that normative variation in levels of maternal androgen during gestation may influence developmental behavioral trajectories in marmosets in a way that contradicts previous findings in Old World primates.     

Home range of a Geoffroy's marmoset group, Callithrix geoffroyi (Primates, Callitrichidae) in South-eastern Brazil

The home range of one group of the Geoffroy's marmoset (Callithrix geoffroyi) was studied in a fragment of the Atlantic Forest in south-eastern Brazil, between February 1993 and January 1994. The total home range was 23.3 ha and the area used in the dry season was significantly larger than that of the wet season. The smallest distance travelled by group was 480 m/day in May and the longest was 1,980 m/day in March, but with no significant differences between seasons. The total home range used for this species agrees with the ecological grouping of the genus Callithrix proposed by Rylands & Faria (1993) and may be associated with the habitat structure, the limit of the fragment and the inexistence of neighbouring groups.     

Sex differences in food acquisition and aggression in captive common marmosets (Callithrix jacchus)

Competition for food within the social group has been postulated as an important factor affecting primate social organization. This study examined how factors such as sex, aggression, dispersion of food, and amount of difficulty involved in obtaining food affect the distribution of food in common marmoset (Callithrix jacchus) social groups. Mated pairs of adultC. jacchus were presented with food that was either dispersed or concentrated, and either difficult or easy, to obtain. The number of food pieces obtained, aggressive displays, incidents of physical aggression, and amount of time spent searching for food were recorded for each animal. Neither dispersion nor difficulty in obtaining food had significant effects on the distribution of food or any of the other behaviors examined. The primary factors affecting food distribution were aggression and amount of time spent searching. Females obtained more food than males in all situations because they were more aggressive and apparently more motivated to search for food than were males.     

Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour

It has been suggested that the major advantage of trichromatic over dichromatic colour vision in primates is enhanced detection of red/yellow food items such as fruit against the dappled foliage of the forest. This hypothesis was tested by comparing the foraging ability of dichromatic and trichromatic Geoffroy's marmosets (Callithrix geoffroyi) for orange- and green-coloured cereal balls (Kix) in a naturalized captive setting. Trichromatic marmosets found a significantly greater number of orange, but not green, Kix than dichromatic marmosets when the food items were scattered on the floor of the cage (at a potential detection distance of up to 6 m from the animals). Under these conditions, trichromats but not dichromats found significantly more orange than green Kix, an effect that was also evident when separately examining the data from the end of the trials, when the least conspicuous Kix were left. In contrast, no significant differences among trichromats and dichromats were seen when the Kix were placed in trays among green wood shavings (detection distance < 0.5 m). These results support an advantage for trichromats in detecting orange-coloured food items against foliage, and also suggest that this advantage may be less important at shorter distances. If such a foraging advantage for trichromats is present in the wild it might be sufficient to maintain the colour vision polymorphism seen in the majority of New World monkeys.     

Infant survival and number of helpers in captive groups of common marmosets (Callithrix jacchus)

In a colony of captive marmoset monkeys (Callithrix jacchus), the survival rate of infants up to the age of 90 days after birth was analyzed with special reference to the number of members in the group. The number of group members (newborns excluded) varied between two (parents only) and 18 (parents plus non-reproductive helpers); the number of adult group members varied between two and 15. Five hundred ninety-two live-born, parent-reared infants of 263 litters from 56 breeding females were included in the analysis. The greatest reproductive success was observed in groups of ten to 11 members or four to five adults, including the parents. However, the survival rate was fairly constant over group size at approximately 80% of an expected maximum value and no significant correlation was observed between the total number of group members and infant survival rate, or between the number of adult members and infant survival. While helpers may be necessary to increase the survival rate of infants in wild groups, help of non-reproductive animals is not required in captivity, where energetic demands are comparatively low and ecological constraints absent. Under laboratory conditions the parents' skill in infant handling and the mother's physical condition, i.e., the ability to provide enough milk for the infants, is likely to be the most important factor for infant survival. © 1993 Wiley-Liss, Inc.     

A quantitative description of copulatory and associated behaviors of captive marmosets (Callithrix jacchus)

Measurements of male and female copulatory behavior in pairs of common marmosets were made during 30-min mating tests (n = 170). For the male,both frequencies and latencies of mounting, pelvic thrusting, and ejaculatory behaviors were analyzed. For the female, frequencies of proceptive displays (tongue-flicking) and of sexual receptivity were measured. The sexual and associated behavior of the marmoset is compared to that of other primates and the suitability of this species for laboratory studies of neurohumoral mechanisms and sexual behavior is assessed.     

Social relationships and individual contribution to cooperative behaviour in captive common marmosets (Callithrix jacchus)

The social relationships between the members of a family consisting of eight captive common marmosets (Callithrix jacchus) are here examined, as well as the participation of individual family members in infant carrying and defensive behaviour against non-related intruders (adolescent males). Within the social relationships, a clear division of the family into three subgroups (parents, adult offspring, non-adult offspring) could be determined, whereby the adult offspring, especially with respect to the parents, occupy a peripheral position. In the types of cooperative behaviour examined here, substantial participation in infant carrying could be observed in only four family members (parents, adult son, one subadult daughter), and in defence against intruders in only two family members (adult son, one subadult daughter). Participation in infant carrying remained stable throughout the study period. Conversely, individual changes in participation in defence against intruders could be determined, dependent upon the presence of infants carried. The advantages and disadvantages of social substructuring observed are discussed here, in particular the peripheral position of adult offspring, possible connections in individually varied participation in cooperative behaviour, and possible regulative mechanisms. In view of past studies on cooperative behaviour among marmosets, it is here presumed that pronounced individual differences result from a division of labour within the family with respect to various aspects of cooperative behaviour.     

A field study of Geoffroy's tamarin (Saguinus geoffroyi) in Panama

A 3-month field study was conducted in Panama to determine presence and relative abundance of Saguinus geoffroyi, the Geoffroy's tamarin, and status of its habitat (see Acknowledgments for taxonomic note). This primate has a wide geographical distribution in eastern Panama; however, local distribution is highly variable. Tropical forest habitat is rapidly being converted for agriculture and timber. Areas where human access was strictly limited showed tamarin densities significantly greater than in less protected areas. Disturbance has a distinct impact on population densities. There may also be a relationship between tamarin abundance and specific types of vegetation. Future actions regarding the conservation of S. geoffroyi and its habitat are recommended.     

Effects of familiarity on the behaviour towards intruders in captive common marmosets (Callithrix jacchus)

A study on the behaviour of a group of common marmosets (Callithrix jacchus) towards unrelated intruding conspecifics (juvenile male twins) was performed. The group members' proximity to the intruders during two consecutive study periods was analyzed. During the first period in which the experimental conditions as well as the intruders were unfamiliar, all but one group member were equally likely to stay near the intruders and usually more than three individuals were present simultaneously. During the second period the group members showed different scores of proximity towards the intruders. One individual, an adult male, was in close proximity nearly the whole time. Additionally, the number of individuals simultaneously staying near the intruders was clearly reduced. It is argued that (1) the change in behaviour of the group members was affected by the increasing familiarity and (2) intruder experiments with unfamiliar conspecifics are only of partial value for clarification of the process of immigration.     

Stress reactivity in young marmosets (Callithrix geoffroyi): ontogeny, stability, and lack of concordance among co-twins

Variation in response styles in the hypothalamic-pituitary-adrenal (HPA) axis are known to be predictors of short- and long-term health outcomes. The nature of HPA responses to stressors changes with developmental stage, and some components of the stress response exhibit long-term individual consistency (i.e., are trait-like) while others are transient or variable (i.e., state-like). Here we evaluated the response of marmoset monkeys (Callithrix geoffroyi) to a standardized social stressor (social separation and exposure to a novel environment) at three different stages of development: juvenile, subadult, and young adult. We monitored levels of urinary cortisol (CORT), and derived multiple measures of HPA activity: Baseline CORT, CORT reactivity, CORT Area Under the Curve (AUC), and CORT regulation. Juvenile marmosets exhibited the most dramatic stress response, had higher AUCs, and tended to show poorer regulation. While baseline CORT and CORT regulation were not consistent within an individual across age, CORT reactivity and measures of AUC were highly correlated across time; i.e., individuals with high stress reactivity and AUC as juveniles also had high measures as subadults and adults, and vice-versa. Marmoset co-twins did not exhibit similar patterns of stress reactivity. These data suggest that regardless of the source of variation in stress response styles in marmosets, individually-distinctive patterns are established by six months of age, and persist for at least a year throughout different phases of marmoset life history.     

Hematology of common marmosets (Callithrix jacchus)

The hematology of the common marmoset (Callithrix jacchus) was investigated to provide reference values for the normal animal. Red blood cell counts, white blood cell counts, hemoglobins, mean cell volumes and differential white blood cell mean values were determined for Texas A&M colony-born animals and those obtained from the wild. The analyses were completed on 31 animals, three times each, for a total of 93 analyses, which included 16 colony-born and 15 wild-born marmosets. The hematological mean values found for marmosets were similar to those mean values reported for humans. The ranges for the hematology values were much narrower in the colony-born marmosets, and the average white blood cell count was significantly lower in these animals. This indicated that it is possible to produce and maintain a more uniform animal in the colony environment and, consequently, these animals are more suitable than wild-born animals for use as models for human research.     

Cross-fostering between two species of marmosets (Callithrix jacchus) and Callithrix penicillata)

Cross-fostering technique can be defined as adoption of infants by adults of other species. This phenomenon is poorly investigated because very young animals have few opportunities to interact peacefully with non-conspecific adults, either in captivity or in natural conditions. This study describes the induction of cross-fostering in captivity between white tufted-ear (Callithrix jacchus) and black tufted-ear marmosets (Callithrix penicillata). We conclude that this technique can be very useful for preserving the life of rejected by parents or orphan infants, mainly in the case of species with low reproduction rate in captivity or those threatened by extinction, as well for investigating the environmental effects on the typical behavior of species (courtship, food preference, vocalization patterns, e.g.).