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.     

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.     

Urine collection in the common marmoset (Callithrix jacchus) and its applicability to endocrinological studies

We investigated a new method of urine collection in the common marmoset. We entered the cage as soon as the light cycle started in the breeding room and collected urine from the animal directly without any restraint. We were able to take separate samples from completely different individuals housed together for behavioral studies in the same cage. Urine and blood samples were taken from individuals from late pregnancy through postpartum nursing period. Cortisol and prolactin concentrations measured in urine were compared to those measured in blood to evaluate this collection method. LH/CG level in the urine samples was also measured. Urine data in females indicated a tendency toward high cortisol values during late pregnancy, a sharp drop before parturition, and increase after delivery. In females cortisol levels measured in blood closely resembled concentrations measured in urine. Urine cortisol in males clearly indicated an increase postpartum, but the increase was not indicated in plasma. Plasma and urine prolactin concentrations in females made a similar increase during lactation. Male's plasma prolactin clearly indicated an increase directly proportional to strong behavioral contact with the infant. We also confirmed hormonal changes during pregnancy, and postpartum ovulation and subsequent pregnancies, from urine LH/CG data. We found this method extremely useful because of the high correlation between cortisol, prolactin and LH/CG data from blood and urine. Additionally, we collected urine samples with little stress to the animal from fear, irritation, pain, etc.     

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.     

Behavioral and hormonal response of common marmosets, <Emphasis Type="Italic">Callithrix jacchus</Emphasis>, to two environmental conditions

Captive animals of several species change their behavioral pattern and hormonal profile in response to physical (for example, cage size and temperature) and social (for example, group size and social isolation) modification of their environment. To evaluate the effect of environmental change in captivity, the affiliative (contact/proximity and allogrooming) and individual (approach, leaving, scent mark, locomotion, and autogrooming) behavior of five family groups of common marmosets, Callithrix jacchus, were recorded on weekdays (non-quiet) and at the weekend (quiet) for two months. In addition, fecal samples were collected for four of these groups to measure their cortisol levels under both conditions. The behavioral pattern and hormonal profile of breeding pairs and their offspring were modified by different management routines used in the experimental conditions. We found that the animals spent more time in affiliative interactions at the weekend, whereas on weekdays, they showed more individual behaviors. Moreover, cortisol levels of breeding pairs and their offspring were higher on weekdays, suggesting that common marmosets living in captivity react to environmental modification by changing their behavioral and hormonal pattern.     

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.     

Suppression of prolactin does not reduce infant care by parentally experienced male common marmosets (Callithrix jacchus)

High levels of prolactin have been found to correlate with the expression of paternal care in a variety of taxa. However, in mammals, there is little experimental evidence that prolactin is causally involved in the stimulation or maintenance of paternal care. Here, we suppressed prolactin production in paternally experienced common marmoset fathers in their family groups during the first 2 weeks after their infants were born. Circulating prolactin levels were suppressed using cabergoline (Dostinex: Pfizer), a long acting dopamine (D2) agonist with minimal behavioural side-effects. A within-subject design was used to compare behavioural and hormonal data on 5 paternally experienced fathers during two consecutive births. Cabergoline reduced prolactin to negligible levels in all fathers without effecting testosterone, DHT and cortisol and without adverse side-effects. However, lowering prolactin had no significant effect on the expression of majority of the behaviour patterns associated with paternal care. These included infant carrying, infant grooming and the frequency with which fathers retrieved and rejected infants. The only infant-related behaviour to be affected was the frequency with which fathers touched, licked and investigated infants. We noted a marginally significant increase in this behaviour during cabergoline treatment. Despite the lack of effect on paternal care, cabergoline did exert an effect on the affiliative/sexual behaviour of fathers as there was a significant increase in the grooming behaviour fathers directed at and received from their mates during drug treatment. This study showed that experienced male marmosets can express paternal behaviour in the absence of the high prolactin levels normally seen after infants are born.     

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.     

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.     

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.     

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.     

Alloparental Responsiveness to Newborns by Nonreproductive,Adult Male,Common Marmosets (Callithrix jacchus)

Parental care in mammals is influenced by sensory stimuli from infants, and by changes in the hormone levels of caretakers. To determine the responsiveness to infant cues in nonreproductive adult male common marmosets (Callithrix jacchus) with and without previous experience in caretaking, we exposed 12 males to newborn marmosets and assessed their cortisol plasma levels and behavioral response. Newborn marmosets housed in transparent enclosures were placed inside the cages of the adult male subjects. Males were exposed four times to two different experimental conditions: (a) newborn enclosures remained closed during the observation period and (b) newborn enclosures were opened during the observation period to allow direct social interaction by the adult males. Blood samples from adult males were collected after each behavioral observation trial to measure the levels of cortisol. The behavioral responses of adult males exposed to the closed and open newborn enclosures showed a significant difference only with respect to the frequency of displacements, where males moved among the quadrants of their own cages with greater frequency when the newborn enclosure was sealed. Experienced males approached newborn enclosures more frequently, spent more time in close proximity, and carried and recovered newborns more quickly than inexperienced males. The successive exposure to newborns increased the responsiveness in inexperienced males. The highest levels of plasma cortisol in adult males were recorded following periods of exposure to the sealed newborn enclosures. This suggests that successive exposure to newborns and previous alloparental caregiving experience while living in family groups influences the responsiveness of male marmosets to the sensory cues of newborns. Am. J. Primatol. 75:145‐152, 2013. © 2012 Wiley Periodicals, Inc.     

Prolactin levels of fathers and helpers related to alloparental care in common marmosets, Callithrix jacchus

Previous studies have suggested that prolactin may play a role in regulating allocare behaviour in cotton-top tamarins, Saguinus oedipus. In this study, we investigate the prolactin profile of 3 groups of captive common marmosets, Callithrix jacchus. Carrying behaviour in this species was observed after parturition. Prolactin assays of blood samples of both fathers and helpers (sub-adult non-fathers) in 3 family groups were taken for 8 weeks before and after birth of the infants. The after-birth condition was divided into 2 groups: carrying and non-carrying animals. The results suggest a relationship between prolactin levels and allocare behaviour, with carrying behaviour being associated with increased prolactin in both fathers and helpers. This suggests that extra prolactin is produced in response to physical contact, and may be associated with carrying behaviour. Also, prolactin production may be related to learning parental skills in Neotropical primates.     

The behavioral context of visual displays in common marmosets (Callithrix jacchus)

Communication is important in social species, and may occur with the use of visual, olfactory or auditory signals. However, visual communication may be hampered in species that are arboreal have elaborate facial coloring and live in small groups. The common marmoset fits these criteria and may have limited visual communication. Nonetheless, some (contradictive) propositions concerning visual displays in the common marmoset have been made, yet quantitative data are lacking. The aim of this study was to assign a behavioral context to different visual displays using pre–post‐event‐analyses. Focal observations were conducted on 16 captive adult and sub‐adult marmosets in three different family groups. Based on behavioral elements with an unambiguous meaning, four different behavioral contexts were distinguished: aggression, fear, affiliation, and play behavior. Visual displays concerned behavior that included facial expressions, body postures, and pilo‐erection of the fur. Visual displays related to aggression, fear, and play/affiliation were consistent with the literature. We propose that the visual display “pilo‐erection tip of tail” is related to fear. Individuals receiving these fear signals showed a higher rate of affiliative behavior. This study indicates that several visual displays may provide cues or signals of particular social contexts. Since the three displays of fear elicited an affiliative response, they may communicate a request of anxiety reduction or signal an external referent. Concluding, common marmosets, despite being arboreal and living in small groups, use several visual displays to communicate with conspecifics and their facial coloration may not hamper, but actually promote the visibility of visual displays. Am. J. Primatol. 75:1084–1095, 2013. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.     

Behavioral discrimination between circumgenital odor from peri-ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus)

Social peer groups of callitrichid monkeys [marmosets and tamarins] exhibit intrasexual dominance hierarchies in captivity. This laboratory study employed two-choice behavioral discrimination bioassys to test the hypothesis that scent from female common marmosets contains chemical cues that permit discrimination between dominant females in the peri-ovulatory versus luteal phase of the ovarian cycle and females holding dominant versus subordinate status. When scent from only dominant females was presented, marmosets directed significantly greater amounts of investigatory behavior toward peri-ovulatory scent versus scent collected during the luteal phase of the ovarian cycle. Animals of both sexes demonstrated significant discriminatory behavior between scent deposited by dominant versus subordinate females, but only when the dominant female was in the peri-ovulatory phase of the ovarian cycle. Test animals directed equal amounts of investigative behavior toward scent from luteal-phase dominant females and subordinate females. Female test subjects deposited significantly more scent marks over presented scents than did male subjects, particularly when the scent had been donated by a peri-ovulatory female. Chemical odors specific to the peri-ovulatory and luteal phases of the ovarian cycle may play a role in mediating behavioral interactions among marmosets. Am. J. Primatol. 46:265–284, 1998. © 1998 Wiley-Liss, Inc.