Playful interactions in family groups of the common marmoset (Callithrix jacchus jacchus)

Play behaviour in six family groups of common marmosets (Callithrix jacchus jacchus) is described. Playful behaviour patterns comprised a distinct repertoire of behaviour and the patterns formed ordered sequences. The differences in the play of adults and offspring are described and analysed. Adult play was infrequent and most took the form of adult-offspring interactions; it contained fewer bouts of chasing and was less active, and adults elicited fewer bouts. No differences attributable to sex could be determined in the play of offspring and the only pattern that decreased with age was bouncing gait. Possible partner preferences were analysed, and it was found that marmoset twins showed an overall preference for playing with the twin. The vocalizations heard during bouts of play were recorded and analysed and their relationship to non-playful vocalization discussed; during bouts of play younger animals were found to vocalize to older animals. Marmoset play wrestling differed in form from aggressive wrestling, and patterns occurred during aggressive interactions which were not observed in play. The play of marmosets is discussed with regard to the socioecology of the species and compared to the play of other mammalian species.     

Pair-bond formation and breeding success in the common marmosetCallithrix jacchus jacchus

The breeding records from 22Callithrix jacchus jacchus females aged 13–23 months were examined. It was evident that females aged more than 18 months when first paired bred sooner, as did females paired with sexually experienced males. A detailed behavioral investigation of nine newly formed pairs was carried out for 10 weeks. Males showed more following, sniffing, tail-raised presents, and affectional behavior than their mates, while females showed more soliciting. Only females gave the submissive vocalization (ngÄ). This shows that there is a degree of sexual dimorphism in the behavior of this monogamous monkey. Four of the nine pairs failed to conceive within 12 weeks of pairing;the females of these pairs behaved more submissively than successful breeders, showing more ngÄ and less bristling and sexual behavior. In all cases the four females were housed in close proximity to dominant relatives and this was considered to be a significant factor.     

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.     

Scent marking and associated behaviour in captive Common marmosets (Callithrix jacchus jacchus) with a description of the histology of scent glands

The histological structure of the scent marking glands of Callithrix jacchus jacchus is described. Frequencies of scent marking were variable and bore no relation to reproductive states. Scent marking was temporally associated with sensory and piloerection behaviours. Possible functions of scent marking in C. J. jacchus are discussed.     

Species differences in response to conspecific intruders inCallithrix jacchus andSaguinus oedipus

In this study, the first performed on two species of callitrichid primates under identical conditions, the responses elicited in newly mated individuals by conspecific intruders were compared in four pairs of Callithrix jacchusand four pairs of Saguinus oedipus.Intruders were systematically varied in terms of sex and the social context in which they were met. Clear sexual dimorphism was observed in the behavior of Saguinus oedipus,but the behavior of males and females was less dimorphic in Callithrix jacchus.Males and females of both species showed an increase in agonistic and display behavior in the presence of same-sex intruders, but the mode of behavior varied both with sex and species. Social facilitation, as indicated by increased frequencies of agonistic and display responses in the presence of a mate, was observed only in males of both species. Neither C. jacchusnor S. oedipusdisplayed clear evidence of a monogamous mating system like that of Callicebusor of a polygynous mating system like that of Saimiri.Observed differences in the responses to conspecifics between these two species in the laboratory may be explained by facultative differences in mating systems resulting from differences in ranging and foraging behavior under freeranging conditions.     

Changes in the size,composition, and reproductive condition of wild marmoset groups (Callithrix jacchus jacchus) in north east Brazil

Five groups ofCallithrix jacchus jacchus were studied in the field in north east Brazil. Group size and composition were similar to that described for other callitrichids, but changes in group membership occurred much more frequently than previously reported. There was a 50% turnover in group membership in a six month period, and adult males changed groups particularly often. Most groups contained only one reproductively active female, but there was evidence that one group contained two females that were reproductively active simultaneously. Some groups had several adult females, and the role of reproductive female switched from one individual to another with time. Individual marmosets are faced with an unusually wide range of alternative life history strategies involving different combinations of location and reproductive condition. We argue that marmoset social organization is best studied at the level of the whole population within an area, rather than at the level of the individual group.     

Reconciliation following aggression in patas monkeys,Erythrocebus patas

Following intra-group aggression, obvious conciliatory displays are absent from the behavioural repertoire of patas monkeys, Erythrocebus patas, while many other Old World primate species show special reconciliation gestures. When 10-min focal-animal samples that began after spontaneous aggression were compared with matched-control samples, captive adult female patas followed up on aggressive interactions, interacting sooner and more often with former opponents during post-conflict observations than during matched-control observations. Almost one-third of post-conflict observations included affiliative behaviour between former opponents, which is termed reconciliation. Matrilineally related opponents were more likely to reconcile with one another than were unrelated animals. No effect of the dominance hierarchy on tendency to reconcile was found. Thus, patas monkeys showed general patterns in post-conflict behaviour that were similar to those seen in other primates previously investigated.     

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.     

Birth and perinatal behaviour in family groups of the common marmoset (Callithrix jacchus jacchus), compared to other primates

Birth and perinatal behaviour in five family groups of the common marmoset are described. Information is given on 16 births, seven of which are described in detail.The birth process was divided into five stages; data are presented on the durations of the stages and the behaviours exhibited by the female in each stage.Infant marmosets cling unaided to the pelage of the female from birth, and the behaviour of neonates and the reactions of the female to infants are discussed.The interactions of other group members to the mother and neonates were analysed. The adult male's first interactions with the neonates appeared to occur much earlier (less than one hour after birth) than in other non-human primate species.Perinatal behaviour in marmosets is compared to that recorded in other non-human primate species and discussed in relation to the social organisation of C. j. jacchus.     

Field observations on group size and composition of the common marmoset (Callithrix jacchus jacchus), at Tapacura,Brazil

A five and a half month field study on the common marmosetCallithrix jacchus jacchus, was carried out during the dry season at Tapacura near Recife, Brazil. Twelve groups were counted and group sizes ranged between 3 and 13 animals. The age/sex class composition of three groups was determined by observation of one group and by trapping two others. Five groups were counted over a period of five months and one group over four months, during which two confirmed cases of immigration into groups were observed. The evidence for birth seasonality is considered. Data are presented to support the hypothesis that there is only one breeding female per group, although a group containing two mature females was observed. The observations are compared with those obtained for other Callitrichid species.     

Spatio-temporal dynamics of rabies and habitat suitability of the common marmoset Callithrix jacchus in Brazil

Rabies transmitted by wildlife is now the main source of human rabies in the Americas. The common marmoset, Callithrix jacchus, is considered a reservoir of rabies causing sporadic and unpredictable human deaths in Brazil, but the extent of the spillover risk to humans remains unknown. In this study, we described the spatiotemporal dynamics of rabies affecting C. jacchus reported to Brazil’s Ministry of Health passive surveillance system between 2008 and 2020, and combined ecological niche modelling with C. jacchus occurrence data to predict its suitable habitat. Our results show that 67 outbreaks (91 cases) of rabies affecting C. jacchus were reported by 41 municipalities between January 2008 and October 2020, with a mean of 5 outbreaks/year [range: 1–14]. The maximum number of outbreaks and municipalities reporting cases occurred in 2018, coinciding with higher surveillance of primate deaths due to Yellow Fever. A mean of 3 [1–9] new municipalities reported outbreaks yearly, suggesting potential spatial expansions of the C. jacchus variant in northeastern Brazil and emerging rabies spillover from vampire bat Desmodus rotundus to C. jacchus in the north and south. Outbreaks were concentrated in the states of Ceará (72%) and Pernambuco (16%) up to 2012, but are now reported in Piauí since 2013, in Bahia since 2017 (D. rotundus’ antigenic variant, AgV3) and in Rio de Janeiro since 2019 (AgV3). Besides confirming suitable habitat for this primate in the northeast and the east coast of Brazil, our Maximum Entropy model also predicted suitable habitat on the north and the west states of the country but predicted low habitat suitability among inland municipalities of the Caatinga biome reporting rabies. Our findings revealed new areas reporting rabies infecting C. jacchus, highlighting the need to implement strategies limiting spillover to humans and to better understand the drivers of C. jacchus rabies dynamics.     

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.     

Characterization of the expressed immunoglobulin IGHV repertoire in the New World marmoset Callithrix jacchus

The common marmoset (Callithrix jacchus jacchus) is a member of the Callithrichinae, a family of outbred New World primates with limited MHC polymorphisms and a propensity to develop spontaneous or experimentally induced autoimmunity. C. jacchus marmosets are susceptible to experimental allergic encephalomyelitis (EAE), and spontaneously develop autoimmune colitis and thyroiditis. Such disease models approximate the complexity of human autoimmune disorders, and allow an investigation of the respective roles of T-cell and antibody responses to self-antigens in outbred species. A key issue for further definition of the pathogenic antibody responses in human autoimmunity is to understand the diversity of the immunoglobulin repertoire in primate models. Here, we characterized the expressed immunoglobulin IGHV repertoire of the C. jacchus marmoset. Six IGHV subgroups were identified which show a high degree of sequence similarity to their human IGHV counterparts (IGHV1, IGHV3, IGHV4, IGHV5, IGHV6, and IGHV7). As in the expressed human IGHV repertoire, the framework regions are more conserved when compared to the complementarity-determining regions (CDRs), with the greatest degree of variability located in CDR3. Predicted structural features are highly conserved between C. jacchus and human IGHV. This information now provides a framework for studies of the antigen-specific repertoire of pathogenic antibodies in EAE and other immune-mediated diseases.     

“Environmental stress” and reproductive success in the common marmoset (Callithrix jacchus jacchus)

The present report documents the breeding success of a new colony of common marmosets (Callithrix jacchus jacchus) and demonstrates a correlation between environmental stress and reproductive success. Environmental conditions ranged chronologically over 40 months, through four periods: I) the initial period, when the colony was formed; II) a phase of relative environmental stability; III) a stage of “environmental stress” (when the colony was disrupted by nearby construction); and IV) a return to a stable environment. Examination of reproductive status during each period indicated that the colony exhibited severe reproductive suppression during the time of the environmental disruption. Parity and the number of live births decreased and the number of spontaneous abortions increased during this period. Reproductive success remained low during period IV. More triplets than twins were born during the period of relative environmental stability.     

Chromosome studies of Saguinus midas niger (Callithricidae,Primates) from Tucurui,Para, Brazil: Comparison with the karyotype of Callithrix jacchus

The karotype of Saguinus midas niger was studied by G-, C-, and nuclear organizer region (NOR)-banding techniques. Variations in C-banding patterns were observed in some chromosomes. The banding patterns obtained were compared with those previously described for Callithrix jacchus. The two species differ by a reciprocal translocation involving pairs 9 and 16; by a paracentric inversion in chromosomes 1, 13, 14, 18, and 22; and by a pericentric inversion in at least four subtelocentric pairs (chromosomes 19, 20, 21, and 22), dislocating the nucleolar organizer region from the small short arm in C. jacchus to the proximal segment of the long arm in S. m. niger (or vice versa). The amount of constitutive heterochromatin is greater in S. m. niger than in C. jacchus, especially in chromosomes 4, 7, and 14. The Y chromosome is smaller in C. jacchus than in S. m. niger.     

Cooperative nest‐defence behaviour and territory quality in a resident and socially monogamous passerine

Nest defence is a fundamental aspect of parental care in secondary cavity‐nesting birds, and predation or competition for nesting sites can involve different defensive behaviours. Because habitat quality determines breeding success, we were interested in whether breeding pairs of the Eurasian nuthatch, Sitta europaea, established in more favourable environment also manifest higher probability of cooperative behaviour during their nest‐site defence. To explore this relationship, we quantified behavioural displays of both parents and analysed activity budget ethogram data from simulated territorial intrusions performed in the chick‐feeding phase with one conspecific and two different heterospecific stimuli (dummies of nuthatch, starling and woodpecker). We found that paired individuals shared their roles during nest‐site defence to a considerable extent. Males had a significantly higher number of attacks on intruders than females, and females performed more threat displays and controls of the brood than males. Multinomial analysis of the cooperative behaviour suggested that pairs in a high‐quality territory had higher probability of reciprocal substitution of different roles towards a balance between attacks, threat displays and nest controls. Contrary to this, pairs in a low‐quality territory had less likely pairwise combinations of simultaneous behavioural states that are associated with effective nest‐site defence. The difference in response probability according to territory quality was, however, highly variable in view of the stimulus that was used in simulated territorial intrusion. Because individual roles and the complex behavioural repertoire of pairs altered in response to territory quality and potential nest‐site competitor or brood predator, our results suggest that the cooperative nest‐defence behaviour could be linked to the breeding success of this year‐round territorial species living in a heterogeneous forest habitat.     

Chromosome comparison among five species of platyrrhini (Alouatta caraya,Aotus azarae,Callithrix jacchus,Cebus apella,andSaimiri sciureus)

Karyotypes of 82 individuals from five Platyrrhini species (Alouatta caraya, Aotus azarae, Callithrix jacchus, Cebus apella, andSaimiri sciureus) were studied and compared using a G-banding technique. Cytogenetic analysis showed full chromosome or full arm homologies among these geographically neighbouring species. A small number of chromosomal rearrangements (inversions, deletions, and translocations) could be detected among these taxa. These five species are closely related in chromosomal evolution. An interesting correspondance was found betweenCebus apella chromosomes and those of the other four species.Alouatta caraya andCebus apella are the closest species.Callithrix jacchus andAotus azarae would have the most separated karyotypes.     

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.     

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.     

Temporal and structural features of infant calls in relation to caregiving behaviour in common marmosets,Callithrix j. jacchus

The role of infants in the communal rearing system of marmosets and tamarins has received little attention although their demands may not be complied by inadequate helpers. As acoustic signalling plays an important role in their social communication, it is expected to be an effective way for infants to signal their demand for care. As a first approach, this study focussed on the use and quality of ‘tsik’ calls given by infants of common marmosets (Callithrix j. jacchus) in the context of caregiving. The acoustic and non-acoustic behaviour of a group of common marmosets were recorded during the first two weeks of the life of two infants (twins). Vocalizations were classified, and the structure of the infants' ‘tsik’ calls was quantified by measuring specific signal parameters. Infants gave ‘tsik’ calls in close temporal relation to caregiving behaviour. Specific parameters covaried with the subsequent behaviour of potential caretakers. Values of call duration, start frequency, peak frequency, and range were lower when infants' calls were followed by no reaction or an approach of group members, whereas these parameters showed higher values when followed by a transfer of infants. Our results suggest that the actual demand of infants is encoded in the variations of ‘tsik’ calls.