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.     

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.     

Carrying behaviour in captive and wild marmosets (Callithrix jacchus): A comparison between two colonies and a field site

Data on callitrichids infant carrying is highly variable, and there is some disagreement over the relative involvement of different group members. Considering that variation may result from different social and environmental conditions it is important to compare data from different environments. The purpose of this study was to compare infant carrying in 11Callithrix jacchus groups living in two colonies, in the UK and Brazil, or in a field site in the northeastern Brazil. No differences were found in the amount of time that infants were carried, in the three environmental conditions, during weeks 1 to 4, 7, and 10. Fathers and mothers carried infants for equivalent amounts of time in the three conditions, but helpers from natural groups carried infants more than their captive counterparts. In general, adult helpers carried infants more than subadults and juveniles. The results suggest that carrying is a stable feature inCallithrix jacchus groups, but there is a trend suggestive of an extended carrying period in natural groups. Mothers behaviour were remarkably stable, but fathers behaviour, although comparable, was more conspicuous in captivity than in the field, what may be attributed to paternity certainty. Finally, the greater participation of field helpers in carrying is considered as deriving mostly to age of helpers than to group size.     

Food selection of semifree common marmosets (Callithrix jacchus): Indications for optimal foraging

In this investigation a group of common marmosets (Callithrix jacchus) consisting of two parents and their six progeny of various ages were allowed free access to an open-air enclosure, which was equipped with a heated hut, roofed veranda, external cage, and a runway system made of roofing slats and a few small trees. Feeding places, sitting boards and sleeping boxes were distributed throughout the whole area. This investigation covered a total of 254 hours of observation. The hut and its immediate vicinity can be considered as being the core area of the home-range, as the maximum frequencies of both feeding and location occurred there. Through the experimental variation in the type of foods provided at specific feeding places, it was obvious that the closeness of the feeding place to the hut was more important to the marmosets than the type of food placed there. The marmosets apparently reduced the energy output when searching for food by minimizing the distance to the food patches.     

The fertility of daughters in common marmoset (Callithrix jacchus jacchus) family groups

Observations previously made in the field of inter-group mating raised questions concerning the fertility of daughters in family groups and about possible competition between mothers and daughters. To test whether daughters in captive family groups could become pregnant, daughters from four groups were placed with a strange male for a period of 30 min, twice a week for eight weeks. No changes were observed in the mother/daughter interactions during the time in which the daughters were allowed contact with the strange male. Two of the daughters showed signs of ovulation and the male only copulated with these animals. One daughter became pregnant, but it was aggression with her siblings rather than her mother which necessitated removing her from her family group.     

Visual scanning by common marmosets (Callithrix jacchus): Functional aspects and the specialrrole of adult males

The rates of visual scanning and vocalizations were studied in a group of captive marmosets (Callinthrix jacchus) after the presentation of five different stimuli (artificial flower, playback of long calls, female/male conspecific, stuffed wild cat) in order to assess the function of visual scanning. Only the presentation of a stuffed cat induced a significant response. The adult males in particular increased their scanning rate and all adult individuals decreased their rate of vocalizations. The results indicate that visual scanning in marmosets is an appropriate measure of vigilance which seems to serve the function of predator detection and avoidance. The strong response of adult males suggests that they play a special role in predator detection.     

Hand preference study in marmosets (Callithrix jacchus) using food reaching tests

Hand preference has been investigated in New World primates but the data obtained thus far are controversial. In this study we investigated hand preference in common marmosets,Callithrix jacchus, during the execution of a reaching for food task. We used 46 adult common marmoset males (n=27) and females (n=19) from the Universidade of Rio Grande do Norte colony, both wild and captive-born. To test the hand preference we used a device measuring 10 cm², with a central hole 1 cm in diameter, to force the animal to use only one hand to reach for food on a food dish located underneath. Each animal was tested 5 times and had to make a maximum of 20 successful attempts per session. A total of 100 successful attempts per animal and 4,600 successful attempts for all animals were recorded during the experiment. Latency and duration of the sessions were measured and we found preference for the use of one of the hands in common marmoset individuals, i.e. 45 of total of 46 animals used significantly more the right or the left hand when performing the task. However no bias at the population level was found. Females born in captivity presented an increase in the duration of latency for the first successful attempt and in the total duration of the test sessions. These findings might be indicating differences associated with a natural tendency for females to be more selective and to spend more time exploring alimentary sources. Additionally, captive-born females may have a constrain in developing cognitive abilities regarding foraging since they have food available during most part of the time.     

Exploratory behavior and learning in laboratory marmosets (Callithrix jacchus jacchus): Comparisons between experimental-cage and home-cage activity

In this paper I examine exploratory behavior and learning in two groups of common marmosets (Callithrix jacchus jacchus), both living under laboratory conditions. The main aim of my studies was to compare behavior occurring in an experimental testing situation with home-cage behavior, and to assess conditions under which exploration is enhanced. One group of marmosets was tested individually in an experimental room away from a larger animal holding room, and a second group was observed in their own home cages, surrounded by other marmosets. Marmosets in both groups were given the opportunity to learn simple tasks, such as pressing a lever for food or jumping on to a wire grid to open a door and see a neighbouring marmoset, and were provided with sets of novel or familiar objects to encourage play and exploration. In the isolated experimental cage, marmosets which learnt a lever-pressing task showed higher general activity levels than controls; in the home cages the mere addition of novel objects resulted in enhancements in exploratory behavior (measured in terms of contacts with the objects). Although the activities associated with learning tended to decline over time, the novel objects remained a constant interest throughout the experiment. The results have implications for maintaining marmosets in captivity, especially in situations when they are housed separately.     

Reproductive patterns and birth seasonality in a South-American breeding colony of common marmosets,Callithrix jacchus

We analyzed data on captive-born and wild-caught females housed under natural conditions in a colony located in northeastern Brazil. No differences in reproductive performance were found between captive-born and wild-caught females. Twins were the most frequent litter size, followed by triplets and singletons. No parity effect was observed, with similar infant survival for nulliparous and multiparous females. No significant departures in sex ratio were detected for births and mortality of the male and female infants. The age of the females at the time of pairing showed a negative correlation with pairing-parturition length, but did not affect infant survival. The prolongation in pairing-parturition interval (PPI) and interbirth interval (IBI) was related to birth seasonality. The births were clustered in the second half of the dry season and the beginning of the wet season (November–March), and the time of pairing and the time of infant birth influenced the PPI and IBI, respectively. The use of outdoor cages, which allowed the animals to be aware of the seasonal variations in photo-period and rainfall seems to be sufficient to time the reproductive activity, even when the animals are maintained on a constant food supply.     

Hormonal changes related to paternal and alloparental care in common marmosets (Callithrix jacchus)

The physiological mechanisms of parental and alloparental care in cooperatively breeding nonhuman primate species such as the common marmoset (Callithrix jacchus) are poorly known. In this study, we examined prolactin and cortisol plasma levels of fathers and older offspring of both sexes, with and without previous experience in infant carrying, around parturition and during infant carrying. Blood samples were collected from fathers and older offspring and prolactin and cortisol were measured by RIA and EIA, respectively. Prolactin levels of both caretakers were not influenced by infant's birth, previous experience or proximity to parturition. However, prolactin levels increased in both caretakers while in physical contact with infants and also with the number of infants being carried in older offspring. These findings suggest that increased prolactin seems to be mainly due to physical effort rather than a physiological trigger of paternal and alloparental care in common marmosets. Cortisol levels were higher for experienced fathers shortly before parturition which could act to reinforce affiliative bonds between breeding males and females at this time or in the ability of males to detect the proximity of the parturition or both.     

Effects of positive interaction with caretakers on the behaviour of socially housed common marmosets (Callithrix jacchus)

Every aspect of the life of the captive non-human primates should be carefully attended to, as updated refinement concept recommends. Interaction with humans as environmental enrichment for these animals is believed to be of value, but it has been subject to little quantitative evaluation. This study investigates the effects of positive interaction with humans on the behaviour of a captive colony of common marmosets (Callithrix jacchus). The study was composed of two phases: baseline condition, where the interaction with humans was represented by routine care and management; and a second phase (‘Human Interaction Effects’), in which a familiar caretaker spent additional 20 min per day with each family, interacting actively and positively with the monkeys. In order to assess potential durable effects of such interaction, data were collected only when caretaker was absent. Between the two phases, a period of interaction 4 weeks long per family took place with the caretaker. The sampling method used was a 10 s scan sampling, with daily sessions 30 min long. Following the period of additional interaction with caretaker, the marmosets showed an increased level of grooming and playful activities, generally considered signs of increased level of welfare; however, they also showed lower levels of self-scratching and locomotion. A trend towards reduced contact vocalizations was also observed. These results suggest that simple, unstructured positive interactions between humans and marmoset monkeys may be part of a program aimed at maximising the level of welfare of captive non-human primates.     

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.     

Interactions between parents and infants,and infants-father separation in the common marmoset (Callithrix jacchus)

The New World monkey,Callithrix jacchus, diversely from most Old World primates, shares infant care among all family members. This paper intends to describe a pattern of infant care in the common marmoset, and to verify if the infant-father separation induces a depression reaction, such as found in other separation studies. In Experiment 1, 11 families (mother, father, and twin newborn infants) ofCallithrix jacchus were observed from 1st to 36th days of infants' life. It was noted that infants were carried most of the time in the beginning of life, and that from the 4th day on this care came mostly from the father. In Experiment 2, nine families were divided in three separation groups (15, 30, and 45 days of infants' life). Each group had a control and two experimental families. Removal of the father was done for three days, beginning at the indicated infants' ages. Results showed that upon removal of the father, the mother assumes the infants' care, and no depression reaction appeared.     

The Pair-Bond Formation and Its Role in the Stimulation of Reproductive Function in Female Common Marmosets (Callithrix jacchus)

The sociosexual relationship between male and female common marmosets (Callithrix jacchus) is characterized by pair-bond formation, which includes sexual and social interactions such as contact, huddling and allogrooming. The formation of heterosexual pairs in captivity sometimes is unsuccessful in terms of reproduction. We investigated the existence of a correlation between characteristics of sociosexual interaction of marmoset pairs and its role in stimulating reproductive function in females. We studied pair-bond formation during the first 10 weeks of pairing in eight unrelated heterosexual pairs of common marmosets (Callithrix jacchus) without prior sexual experience. In three of them, pregnancy occurred during the study period (group SR), and we compared the profile of their sociosexual interactions with that of the five other couples in which pregnancy was not registered (group NS) during that period. The results show differences between the two groups, related mainly to affiliative responses between male and female, with significantly higher levels of allogrooming and simultaneous piloerection in the SR group. Although we did not find significant differences in the frequency of mounting behavior between groups, their reproductive success was different, suggesting that some behavioral patterns related to cooperative interactions between the male and female could be expressing the pair-bond. These behaviors may be influencing the females' physiology and consequently successful reproduction in the species.     

Intercellular communication between cultured granulosa cells of the marmoset (Callithrix jacchus)

Summary The influence of follicle-stimulating hormone, forskolin, insulin-like growth factor type I, epidermal growth factor, and 12-tetradecanoyl-phorbol-13-acetate on marmoset granulosa cell communication via gap junctions was investigated by morphological means and microinjection of carboxyfluorescein. Gap junctions between neighbouring granulosa cells were present in all groups. The number, but not length, of gap junctions between marmoset granulosa cells increased when the cells had been treated with follicle-stimulating hormone, insulin-like growth factor type I, and follicle-stimulating hormone plus insulin-like growth factor type I. No effect on gap junctions was seen, after exposure of the cells to the other three substances. Carboxyfluorescein and counting of the surrounding labelled cells showed that supplementation with follicle-stimulating hormone, forskolin, insulin-like growth factor type I and epidermal growth factor from the beginning of cultivation led to an increase in stained cells after 48 h. When treatment was started in 48 h cultures the substances reached their maximal activity within 30 min (forskolin and epidermal growth factor) or 3 h (follicle-stimulating hormone and insulin-like growth factor type I). Spreading of the fluorescen dye was inhibited when the medium was supplemented with 12-tetradecanoyl-phorbol-13-acetate. This effect was maximal after 30 min. Additive effects regarding the coupling of the cells were seen by combining of epidermal growth factor with follicle-stimulating hormone, but not with insulin-like growth factor type I or forskolin plus follicle-stimulating hormone.     

Responses to natural and synthetic phee calls by common marmosets (Callithrix jacchus)

Captive adult common marmosets (Callithrix jacchus) produce whistlelike “phee” calls in two contexts: in the home cage, where phee calls may function as part of territorial marking behavior, and when separated from social companions, where phee calls may function to reunite conspecifics. Natural and synthesized calls representing the acoustic structure of male and female calls in each context were presented to adult marmosets in a playback paradigm. Marmosets demonstrated discriminative abilities according to the context of the call and the caller's sex. Vocal and behavioral responses indicated increased vigilance and territorial behavior, following playbacks of naturally produced calls as well as synthetic calls. All animals scanned more frequently following produced calls as well as synthetic calls. All animals scanned more frequently following natural home cage as well as isolation calls, but only increased contact behavior (trills) in response to home cage calls. The responses were dimorphic according to the sex of the caller, where adult males scanned more following male calls, and adult females were more aggressive following male and female calls. The differential behavioral responses to playbacks of marmoset phee calls suggest a biological relevance to subtle differences found in the acoustic parameters of the phee call. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, in the public domain in the United States of America.

     

Social context affects phee call production by nonreproductive common marmosets (Callithrix jacchus)

Common marmosets produce two variants of their long call (phee call) in different situations. Intergroup calls are produced in territorial situations, and intragroup separation calls are produced by marmosets isolated from group members. Marmoset groups frequently include postpubertal, nonreproductive members; their roles in the spontaneous production of territorial vocalizations is unclear. This study analyzed the production of home cage phee calls by nonreproductive, postpubertal marmosets while they were housed in their natal groups and after pairing with an opposite-sex conspecific. Additionally, the production of the separation phee call variant was assessed in both social conditions. The results indicated that the marmosets rarely produced home cage, or territorial, phee calls while they were natally housed. In contrast, both males and females produced the territorial phee call at a much higher rate as early as 4 days after pairing. Age-matched females remaining in their natal groups throughout the study produced home cage phee calls infrequently. Most marmosets produced separation phee calls at a high rate after separation from either their natal group or a partner, suggesting that the makeup of a social group has little effect on an animal's motivation to reunite with conspecifics. These results suggest that the social environment has an important influence on the production of territorial phee calls. Am. J. Primatol. 43:135–146, 1997. © 1997 Wiley-Liss, Inc.     

Time course of vocal modulation during isolation in common marmosets (Callithrix jacchus)

Common marmosets vocalize phee calls as isolation calls, which seem to facilitate their reunion with family groups. To identify multiple acoustic properties with different time courses, we examined acoustic modulations of phees during different social contexts of isolation. Subject marmosets were totally isolated in one condition, were visually isolated and could exchange vocalizations in another condition, and were visually isolated and subsequently totally isolated in a third condition. We recorded 6,035 phees of 10 male–female marmoset pairs and conducted acoustic analysis. The marmosets frequently vocalized phees that were temporally elongated and louder during isolation, with varying time courses of these changes in acoustic parameters. The vocal rates and sound levels of the phees increased as soon as the marmosets saw their pair mates being taken away, and then gradually calmed down. The phee duration was longer in conditions during which there were no vocal responses from their pair mates. Louder vocalizations are conspicuous and seem to be effective for long‐distance transmission, whereas shorter call duration during vocal exchanges might avoid possible vocal overlap between mates. Am. J. Primatol. 72:681–688, 2010. © 2010 Wiley‐Liss, Inc.     

Characteristics of the circadian activity rhythm in common marmosets (Callithrix j. jacchus)

The circadian activity rhythm of the common marmoset, Callithrix j. jacchus was investigated by long-term recording of the locomotor activity of 15 individuals (5 males, 10 females) from 1.5 to 8 years old, both under constant illumination and under LD 12:12. The mean period of the spontaneous circadian rhythm was 23.2 ± 0.3 h. Neither sex-specific differences nor a systematic influence of light intensity on the spontaneous period were observed, but the period was dependent on the duration of the trial and on the age of the individual. Due to the short spontaneous period, in LD 12:12 there was a distinct advance of the activity phase with respect to the light time and a masking of the true onset of activity by the inhibitory direct effect of low light intensity during the dark time. After an 8 h delay shift of the LD 12:12, re-entrainment of the circadian activity rhythm required an average of 6.8 ± 0.7 days; the average re-entrainment time after an 8 h phase advance of the LD cycle was 8.6 ± 1.3 day. This directional effect is ascribed to characteristics of the phase-response curve. No ultradian components were observed, either in the LD-entrained or the free-running circadian activity rhythm.     

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.