Leslie J. Digby

Infant care, infanticide, and female reproductive strategies in polygynous groups of common marmosets (Callithrix jacchus)

Reproduction in marmoset and tamarin groups is typically restricted to a single dominant female, but it is unclear why subordinate females tolerate delayed reproduction. The presence of two breeding females in free-ranging groups of common marmosets (Callithrix jacchus) presented a unique opportunity to examine differences in the reproductive strategies of dominant and subordinate females. Three groups were monitored for 12–18 months at a forest reserve in northeastern Brazil. Data on infant care were collected during two consecutive all-day follows every 10 days until the infants were 2 months old. Carrying patterns for infants born to dominant females were similar to those observed in groups containing a single breeding female. All group members over 5 months of age participated in infant care, and dominant females allowed some group members to carry their infants from the 1 st day of life. In contrast, subordinate females were protective of their offspring and were their sole caretakers for at least a week following birth. One infant born to a subordinate was killed in an attack involving the dominant female. Overall, dominant females gave birth to more infants and had higher infant survival than did subordinate breeding females. subordinate females were successful in rearing young only when the timing of births was such that they did not overlap with the dependency period of infants born to the dominant female. These patterns suggest that subordinate females may face resource competition, especially over access to helpers. In times of severe competition, subordinate females that delay reproduction may be avoiding a wasted reproductive effort.

Social organization in a wild population of Callithrix jacchus

Data are presented on group dynamics in a wild population of the common marmoset, Callithrix jacchus, in northeastern Brazil. Three marked and habituated groups were observed, and composition noted, for at least 5 days a month over 12-18 consecutive months. Group sizes ranged from 5 to 15 individuals, and changes in group composition were the result of births, immigrations, and disappearances. No immigrations into the main study groups were observed throughout the study period. None of the three known emigrants was known to join an established or incipient group for up to 10 weeks after their departure. One group contained only breeding individuals and their offspring. Observations of recruitment and loss in the other two groups suggest that they, too, were extended family groups. The group dynamics described in studies of other populations of Callithrix suggest that extended family groups, or at least groups consisting of breeding individuals and their close relatives, may be characteristic of those populations.

Genetic Analysis of Group Composition and Breeding System in a Wild Common Marmoset (Callithrix jacchus) Population

We established pedigree relations in three wild common marmoset social groups for which observational data were available, together with genotypes of some individuals from neighboring groups. Relatedness of 40 individuals were based on 11 microsatellite loci amplified from nDNA obtained noninvasively from plucked hair. The wild marmosets were only half as variable as a captive population characterized previously: 2–6 alleles/locus; HO = 0.41 and HE = 0.35. Parentage exclusion probabilities were 61.8% for an offspring and one alleged parent and 90.7% for an offspring with one confirmed and one alleged parent. Each group (n = 5–14 individuals) had two breeding females and ≥2 adult males. Within each group the infants and reproductively inactive adults were closely related to at least the breeding females; the latter were related to each other as closely as mother/infant pairs or sisters. Relatedness of adult males was lower, indicating recent intergroup dispersal. Genetic data confirm Callithrix jacchus live in relatively stable extended family groups of closely related individuals. Matings occurred preferentially among the least related adults and most infants were fathered by the dominant male. The genetic data are consistent with polygynmonandry as are the field observations. Callithrix have variable mating systems, ranging from monogamy to polyandry to polygyny within social groups plus extragroup copulations; our data provide no evidence for polyandry and are inconclusive with respect to extragroup paternity. Nevertheless, noninvasive multilocus genotyping methods will resolve these questions when longer-term studies of entire populations are undertaken.

Multiple breeding females in free-ranging groups ofCallithrix jacchus

We present observations on the breeding patterns in a free-ranging population of common marmosets, Callithrix jacchusWe found evidence of the simultaneous presence of two reproductively active females in all three monitored groups. We recorded at least one full reproductive cycle (conception-birth) for two females in each group, but other adult females did not breed. An overview of data from other callitrichid field studies indicates that the observed pattern may be an additional characteristic of the flexibility of the social organization of common marmosets. Comparisons with data from other sites where callithrixhas been studied indicate that the presence of a second breeding female in a group may be related to high population density, though the underlying mechanisms remain unclear.

Social organization in a wild population ofCallithrix jacchus: II. Intragroup social behavior

The social behavior of the common marmoset has been well studied in captivity, but little is known about the social dynamics of this species in its natural habitat. Social relationships were studied in three polygynous groups of common marmosets,Callithrix jacchus, in northeastern Brazil. Breeding adults appeared to be the center of social life and were the most frequent grooming partners or nearest neighbors for most adult group members. The observations of unidirectional agonistic interactions suggest that breeding adults were also dominant over all other group members, but that neither sex was dominant over the other. The dynamics of within-group social relationships are likely to be important determinants in the reproductive strategies employed by marmoset females.

Wild Callithrix groups: Stable extended families?

Data from field studies of three Callithrix species, C. flaviceps, C. intermedia, and C. jacchus, are considered in an attempt to characterize group dynamics in this genus. The three groups considered in detail contrast significantly in many behavioral (mating system, ranging behavior, activity patterns) and ecological (zoogeography, habitat, diet) variables. Despite this, all three groups are highly similar in a number of characteristics, including relatively large size, high reproductive output, and low rates of migration. The evidence suggests that Callithrix groups may frequently encompass three generations and are characterized by a high degree of both stability and relatedness between group members.

Sexual Behavior and Extragroup Copulations in a Wild Population of Common Marmosets (Callithrix jacchus)

Sexual behavior and mating patterns are described for 3 free-ranging groups of common marmosets living in a coastal forest in northeastern Brazil. Each group contained 2 breeding females. Within groups, sexual behavior was generally restricted to breeding females and a single behaviorally dominant male. Of 101 mounts and copulations, 24 involved pairings of individuals from 2 different groups. Extragroup sexual behavior was performed by both breeding and nonbreeding group members, and 65% of all adults mounted or copulated with an extragroup individual at least once. Sexual behavior occurred throughout the female reproductive cycle but was significantly more frequent during an 11-day ‘conception period’. Thus, while female marmosets show no physical signs of estrus, both males and females likely do have some information about the timing of ovulation. Mating patterns in this population included both polygyny and monogamy and varied between groups and over time.

Female dominance in blue-eyed black lemurs(Eulemur macaco flavifrons).

Female dominance is unusual among mammals and has been described in detail for only a handful of species. Here we present data on the frequency and outcome of dominance interactions in seven semi-free ranging and captive groups of blue-eyed black lemurs (Eulemur macaco flavifrons) housed at the Duke University Primate Center. We collected over 260 hours of focal data during which all occurrences of dominant-subordinate interactions were recorded. We collected data outside the typical breeding and birthing seasons for this species, thus eliminating possible confounding factors and increased aggression associated with these periods. We found that females were dominant over males in all seven groups, with females winning 99% of all dominance interactions.E. m. flavifrons used aggressive dominance (e.g. chase, cuff, bite) in 81% of all interactions, with the remainder of interactions being decided using social dominance (e.g. deference in the form of supplants or cowers). Older females were dominant over younger females in two out of three multi-female groups (in each case, younger females were daughters), and younger males (sons of the dominant female) received less aggression from females than did older males (n = 2 groups). Caging and group size appear to play a minimal role in the expression of female dominance. While confirmation must await further observations on free-ranging groups ofE. m. flavifrons, our data strongly suggest that this subspecies can be characterized as female dominant.

Balancing Cooperation and Competition in Callitrichid Primates: Examining the Relative Risk of Infanticide Across Species

At least eight cases of infanticide by females other than the mother have been observed in wild groups of common marmosets (Callithrix jacchus), with several more cases described for captive groups. Infanticide by females other than the mother has not, however, been documented for wild groups of other callitrichid species. Why might such overt aggression toward infants be more likely in one species than in others? In the common marmoset, a variety of social, reproductive and ecological characteristics – including short inter-birth intervals (and the resulting potential for overlap of pregnancies and births), habitat saturation, small home ranges, and low cost of infant care (including decreased travel costs and short dependency periods compared to other callitrichids) – may contribute to an increased likelihood of two breeding females being present in a group, which in turn may give rise to the potential for competition between breeding females and, ultimately, to infanticide. These conditions are less common in wild groups of most other callitrichid species. All callitrichids balance the need for cooperative care of young with the reproductive competition that results from limited reproductive opportunities; however, ecological and social conditions appear to tip the balance toward infanticide more frequently in common marmosets than in other callitrichid species.

Activity and Ranging Patterns in Common Marmosets (Callithrix jacchus)

The geographic range of the marmosets and tamarins (tribe Callitrichini; sensu Rosenberger et al. 1990) spans from Panama to northern Bolivia and throughout much of Colombia, Peru, Ecuador, and Brazil (Rylands et al., 1993; Hershkovitz, 1977). In these areas they exist in a variety of habitats including the primary rain forests of the Amazon basin, the Atlantic forests of southeastern Brazil, and the xeric thorn scrub (caatinga) and savannah forests (cerrado) of northeastern Brazil (Rylands, 1993; Rylands & de Faria, 1993). In these and other habitats, field studies have documented considerable variability in the social organization and ecology of callitrichin species. It has been hypothesized that some aspects of callitrichin social organization, in particular mating and infant care patterns, are related to the high cost of rearing infants in these species (see below). Few studies have attempted to quantify these costs under natural conditions (Goldizen, 1987; see also Tardif, 1997), and it remains unclear whether variation in ecological factors may result in species differences in the costs of infant care.