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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Sperm head morphometry in ejaculates of adult marmosets (Callithrix jacchus): A model for studying sperm subpopulations and among-donor variations

In humans and other mammals, sperm morphology has been considered one of the most important predictive parameters of fertility. The objective was to determine the presence and distribution of sperm head morphometric subpopulations in a nonhuman primate model (Callithrix jacchus), using an objective computer analysis system and principal component analysis (PCA) methods to establish the relationship between the subpopulation distribution observed and among-donor variation. The PCA method revealed a stable number of principal components in all donors studied, that represented more than 85% of the cumulative variance in all cases. After cluster analysis, a variable number (from three to seven) sperm morphometric subpopulations were identified with defined sperm dimensions and shapes. There were differences in the distribution of the sperm morphometric subpopulations (P < 0.001) in all ejaculates among the four donors analyzed. In conclusion, in this study, computerized sperm analysis methods combined with PCA cluster analyses were useful to identify, classify, and characterize various head sperm morphometric subpopulations in nonhuman primates, yielding considerable biological information. In addition, because all individuals were kept in the same conditions, differences in the distribution of these subpopulations were not attributed to external or management factors. Finally, the substantial information derived from subpopulation analyses provided new and relevant biological knowledge which may have a practical use for future studies in human and nonhuman primate ejaculates, including identifying individuals more suitable for assisted reproductive technologies.     

Serum levels of prolactin during the ovarian cycle,pregnancy, and lactation in the common marmoset (Callithrix jacchus)

A homologous double-antibody radioimmunoassay developed for humans was used to measure serum prolactin, progesterone, and estradiol in common marmosets. In the ovarian cycle of common marmosets, serum progesterone began to increase after an estradiol surge, attained a peak level, and then declined before the ensuing pre-ovulatory rise in estradiol. During the luteal phase, the change in serum concentrations of estradiol was synchronized with that of progesterone. During the ovarian cycle there was no consistent change in serum prolactin concentrations. During the last 75 days of pregnancy the prolactin level was higher than during the ovarian cycle and the first 70 days of pregnancy. Moreover, during lactation, mothers with suckling twin infants had a higher prolactin level than during the final stage of pregnancy.     

Neonatal behavioral scoring of common marmosets (Callithrix jacchus): relation to physical condition and survival

A seven-task behavioral test was performed on 86 common marmoset (Callithrix jacchus) infants, 24-36 h following birth. This report describes the test outcome and its relation to physical condition and survival of the infants. The percentage of infants receiving a perfect score on a given task ranged from 30.6 (rooting) to 70.6% (grasping). Heavier infants were more likely to have perfect scores for crawling (F=4.20, P=0.044) and infants with a longer knee-heel length tended to be more likely to have a perfect grasping score (F=3.63, P=0.06). While the modal score was a perfect score for most individual tasks, the modal number of total perfect scores that a given infant received was 3-4 and only 4.7% of infants received perfect scores on all seven tasks. These results suggest that this group of behavioral tasks will produce a variable response within a population of neonates. While no individual behavioral score predicted survival during week 1, the number of perfect scores across all tasks was predictive of survival outcome; infants with a higher total number of perfect scores were more likely to survive (F=6.02, P=0.018). When all combinations of tests were compared, the best predictor of survival was outcome on four of the seven tests, all related to motor skills (F=7.46, P=0.009).     

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.     

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.     

Behavioral and cardiophysiological responses of common marmosets (Callithrix jacchus) to social and environmental changes

Under captive conditions common marmosets (Callithrix jacchus) show socially monogamous propensities. Male and female form a social bond as characterized by signs of behavioral arousal during separation of the pairmates, high levels of affiliative interactions between pairmates and agonistic responses towards strange conspecifics. In the present study behavioral and cardiophysiological responses of mated individuals of common marmosets were recorded while the animals were in an unfamiliar environment (1) alone, (2) with the pairmate, or (3) with an opposite-sexed stranger. Pairmates of 6 established pairs were tested in 3 replicates yielding a total of 36 trials per experiment. A trial was divided into three 10-min segments (baseline; unfamiliar environment; reunion). Behavioral responses were videotaped with a remote controlled camera system installed within the cage. Systolic (SBP) and diastolic blood pressure (DBP), and heart rate (HR) as well as locomotor activity (ACT) were recorded telemtrically through peritoneally implanted transmitters. The individuals’ responses measured while in an unfamiliar environment was only reduced by the pairmate, but not by an opposite-sexed stranger. No affiliative behaviors occurred between strange conspecifics, whereas aggressive and sexual behaviors were observed. During reunion with the pairmate individuals recovered physiologically. The present study shows that an individualized pair bond exists between pairmates of common marmosets. Further, it becomes evident that establishing a social bond with the pairmate is important for maintaining physiological homeostasis.