Groups Of Common Marmosets Research Articles

"Monkeying around" together facilitates problem solving.

Sehner et al. (PNAS Nexus, 2022, 1-14) report that groups of common marmosets solve problems more frequently and faster than individuals working alone. This result is partially explained by greater persistence at the task in the group context and may have important implications for the evolution of cognition and culture.

Problem-solving in groups of common marmosets (Callithrix jacchus): more than the sum of its parts.

Human hypercooperativity and the emergence of division of labor enables us to solve problems not only effectively within a group but also collectively. Collective problem-solving occurs when groups perform better than the additive performance of separate individuals. Currently, it is unknown whether this is unique to humans. To investigate the evolutionary origin of collective problem-solving and potential precursors, we propose a continuum of group effects on problem-solving, from simple to complex ones, eventually culminating in collective problem-solving. We tested captive common marmosets with a series of problem-solving tasks, either alone or in a group. To test whether the performance of a group was more than the sum of its parts, we compared real groups to virtual groups (pooled scores of animals tested alone). Marmosets in real groups were both more likely to solve problems than marmosets within the virtual groups and to do so faster. Although individuals within real groups approached the problem faster, a reduction in neophobia was not sufficient to explain the greater success. Success within real groups arose because animals showed higher perseverance, especially after a fellow group member had found the solution in complex tasks. These results are consistent with the idea that group problem-solving evolved alongside a continuum, with performance improving beyond baseline as societies move from social tolerance to opportunities for diffusion of information to active exchange of information. We suggest that increasing interdependence and the adoption of cooperative breeding pushed our ancestors up this scale.

Foraging networks and social tolerance in a cooperatively breeding primate (Callithrix jacchus).

Within-group competition over food resources can be a major cost of social living. In the wild, foragers are confronted with social (e.g. hierarchical rank) and ecological (e.g. food availability and distribution) challenges that affect their foraging decisions and feeding success. Exhibiting prosocial behaviours, such as tolerance at feeding sites, can benefit group members by developing affiliative social relationships, enhancing access to resources and maximizing fitness. We examined social tolerance at feeding sites in Callithrix jacchus, a cooperatively breeding primate species. We investigated the set of social (rank, age and sex) and ecological (food availability) factors that influence the structure and dynamics of within-group foraging association networks. We designed and conducted an experimental field study of four wild groups of common marmosets in which we controlled food distribution (concentrated or scattered) and productivity (high, medium or low food rewards). Then, we used social network analyses to assess the number and strength of foraging associations among group members, their effects on individual food consumption, and whether recent experiences with conspecifics during foraging affected subsequent associations. Overall, common marmoset foraging association networks were cohesive, as group members jointly occupied feeding sites. The number and strength of associations varied depending on the ecological context. Associations were stronger during conditions in which food was concentrated at a single site. Individuals obtained greater access to food resources when sharing a feeding site with conspecifics, but once a food item was obtained, the forager moved to a nearby tree and consumed it away from others. Additionally, the strength of previous foraging associations and subsequent levels of social tolerance at feeding sites were positively related, a relationship compatible with the ability of memorizing associations over time and recalling the information in future decision-making. In sum, marmosets adjusted their partner choices and the strength of foraging associations in response to food availability. They exhibited increased social tolerance at feeding sites during conditions in which opportunities for contest competition were expected to be greatest. These cooperative breeding primates appear to mutually benefit by maintaining cohesive and strong affiliative relationships, and by increasing opportunities for coordinated behaviour and offspring survival.

Balancing contest competition, scramble competition, and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus).

Models of primate sociality focus on the costs and benefits of group living and how factors such as rank, feeding competition, alliance formation, and cooperative behavior shape within-group social relationships. We conducted a series of controlled field experiments designed to investigate how resource distribution (one or three of four reward platforms) and amount of food on a reward platform affected foraging strategies and individual feeding success in four groups of wild common marmosets (Callithrix jacchus) living in the Caatinga of northeastern Brazil. At our field site, common marmoset groups are characterized by a single breeding female who can produce twin litters twice per year, strong social cohesion, and cooperative infant care provided principally by several adult male helpers. We found that except for the dominant breeding female, rank (based on aggression) was not a strong predictor of feeding success. Although the breeding female in each group occupied the highest rank position and obtained the greatest daily feeding success, all other group members, including adults and juveniles experienced relatively equal feeding success across most experimental conditions. This was accomplished using a balance of behavioral strategies related to contest competition, scramble competition (associated with a finder's advantage), and social tolerance (sharing the same feeding platform). Based on these results, the social structure of common marmosets is best described as "single female dominance," with the breeding female maximizing food intake needed to offset the energetic costs associated with reproductive twinning and the ability to produce two litters per year. Cooperative infant caregiving, in which the number of helpers is positively correlated with offspring survivorship, requires a set of behavioral strategies that serve to reduce contest competition and promote prosocial behaviors at feeding sites.

Detection of insect prey by wild common marmosets: The effect of color vision.

Most species of New World primates have an unusual color vision pattern that can affect an individual's ability to detect food. Whereas males can only be dichromatic, females can be either dichromatic or trichromatic. Trichromats are expected to have an advantage in detecting conspicuous food whereas dichromats should be better at locating cryptic resources. Here we aimed to understand how color vision phenotype influences insect foraging by five groups of common marmosets living in a semiarid environment. We recorded insect predation events, noting morphotype and color of the captured insect, and the substrate from which it was captured. Color modeling suggested that, for all values of chromatic contrast resulting from comparing the measured insect-substrate pairs, trichromats outperformed dichromats. Females showed an overall higher insect capture rate than males. Females also showed a higher capture rate of conspicuous insects but there was no sex difference for the capture of cryptic insects. When we compared only dichromatic individuals there was no difference between sexes. These findings suggest that differences found in capture rate related not only to sex but also to visual polymorphism and that the latter is a crucial factor determining insect capture rate in common marmosets. Nevertheless, these results should be interpreted with caution because of the small number (three) of dichromat females and the unknown phenotype of the remaining females. Our results support the balancing selection hypothesis, suggesting that the advantage of one phenotype over the other may depend on environmental circumstances. This hypothesis has recently been considered as the most plausible for the maintenance of visual polymorphism in New World primates.

Long-term-stability of relationship structure in family groups of common marmosets, and its link to proactive prosociality

Cooperatively breeding, group-living common marmosets show differentiated relationships, where more strongly bonded dyads within a group engage more in affiliative interactions than less strongly bonded ones. Intriguingly, recent results suggest that strong bonds do not only occur between breeding partners but between individuals from any sex or status, and that strong-bond partners exhibit correlated oxytocin fluctuations (dyadic oxytocin synchrony, OTS) over a period of six weeks. To date, it is unclear whether such relationships are stable over time and whether they are also reflected in higher partner-specific proactive prosociality. To assess the long-term stability of the relationship structure of common marmoset family groups, we investigated whether hormonal and behavioral markers of group structure (dyadic OTS, dyadic affiliation, and individual group integration) in common marmoset families remained stable over a period of six months. We collected baseline urinary OT and social behavior of 36 dyads from three family groups in a non-reproductive period (period A), and again six months later, around the birth of new infants (period B). Patterns of dyadic OTS, dyadic affiliation, and individual group integration were consistent between the two study periods. Oxytocin data from a fourth group (10 dyads), collected in two non-reproductive periods separated by a period of more than five years, could replicate this finding. Furthermore, OTS was also correlated with proactive prosociality that was assessed experimentally for 38 dyads during an earlier study. These results suggest that differentiated relationships are stable over time, even between group members other than the breeding pair, and that more strongly bonded partners also show higher levels of proactive prosociality. Future studies are necessary to identify whether these relationships have an adaptive function, perhaps with regard to positive consequences on cooperativeness.

Behavioral and hormonal response of common marmosets, Callithrix jacchus, 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.

Zonisamide Increases Dopamine Turnover in the Striatum of Mice and Common Marmosets Treated With MPTP

The effect of zonisamide, an antiepileptic agent with anti-parkinsonian effects, was studied on dopamine neurons of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated C57 mice and common marmosets. Groups of mice (n = 8 - 9) were treated with: MPTP (15 mg/kg every 2 h x4); MPTP plus zonisamide (40 mg/kg administered 1 h before each MPTP dose); MPTP plus selegiline (2 mg/kg administered 1 h before the first MPTP dose); zonisamide (40 mg/kg x4); and saline controls. Groups of common marmosets (n = 4 - 6) were treated with: MPTP (2.5 mg/kg every 24 h x3); MPTP plus zonisamide (40 mg/kg administered 1 h before each MPTP dose); MPTP plus selegiline (2 mg/kg administered 1 h before the first MPTP dose); and saline controls. Brain dopamine and its metabolites were determined by HPLC. Dopamine content decreased in the striatum of MPTP-treated mice and monkeys. Co-administration of selegiline inhibited the effect of MPTP and dopamine contents were similar to those of the controls. Co-administration of zonisamide did not inhibit the effect of MPTP on dopamine content, but increased striatal dopamine turnover of animals treated with MPTP plus zonisamide more than in those treated with MPTP alone. MPTP treatment caused a compensatory increase of dopamine turnover in the striatum by remaining neurons. Zonisamide may help dopaminergic neurons by increasing striatal dopamine turnover following MPTP treatment.

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.

Different ovarian responses to potential mates underlie species-specific breeding strategies in common marmoset and Goeldi's monkey

Callitrichids are cooperative breeders, characterized by obligate twinning, extensive paternal care, and monopolization of reproduction by the dominant female. This is the case in the common marmoset, and in common marmoset groups of more than one adult female, subordinate females are typically acyclic consistent with infertility. However, one callitrichid, Goeldi's monkey, gives birth to singletons and exhibits low paternal care. Given these reproductive traits of Goeldi's monkey, we hypothesized that there would not be suppression of ovarian activity. To test this hypothesis, we applied non-invasive endocrine methods in a step-wise experiment with laboratory groups of both species. In each species, six pairs of sisters were studied alone, in visual contact with an unrelated male and in a polygynous trio with the male, and urine samples were collected for determination of oestrogen titres reflecting ovarian activity. Common marmoset sister pairs exhibited a marked difference in social status: during the study 5 of 6 dominant females conceived but only 1 of 6 subordinate females; the remaining 5 subordinates were acyclic at the end of the study, and instances of ovulation typically resulted in aggression. Goeldi's monkey sister pairs showed no status differences: in all pairs, however, both sisters exhibited a temporary cessation of ovarian cyclicity on trio formation, followed by ovulation and conception. We conclude that these marked differences in ovarian responses reflect the differences in inter-female competition for paternal caregiving resources. In common marmosets with high inter-female competition, suppression of ovulation functions to reduce aggression received by subordinate females; in Goeldi's monkey with low competition, temporary cessation of ovulation could facilitate female choice.

Infanticide and cannibalism in a free‐ranging plurally breeding group of common marmosets (Callithrix Jacchus)

Our study presents a detailed description of infanticide and cannibalism in a free-ranging plurally breeding group of Callithrix jacchus. The 1-month-old infant was the daughter of the dominant female, and was attacked by the group's second breeding female. Two months later, the latter gave birth to twins and appeared to have become the dominant female. These findings confirm and extend previous reports of infanticide by pregnant female marmosets, and indicate that infants of dominant breeding female, as well as those of subordinate females, are vulnerable to infanticide in plurally breeding groups. With respect to the cannibalism, this act seemed to be mainly a response to the prompt availability of food, represented by the killed infant.

Fragmentation causes rarity in common marmosets in the Atlantic forest of northeastern Brazil

The purpose of this study was to investigate the population status of the common marmosets, Callithrix jacchus, in one of their main habitats, the northeastern Atlantic forest of Brazil, where only 2% of its original area remains as small and isolated forest fragments, to determine long-term viable populations. The study was carried out in 15 forest fragments, measuring from 3,478.3 ha (the largest) to 6 ha, which were invariably subjected to high human impact. Line transect surveys were carried out between January 2002 and December 2004, along transects measuring from 350 to 4,000 m, between 0500 h and 0900 h. Common marmosets were registered in 73% (n = 11) of the forest fragments, were not recorded in the largest one, the Coimbra Forest, and group sizes varied from 1 to 4 individuals. A negative significant relationship was detected between the size of the fragment and the number of sightings of common marmosets. It is shown that the number of groups of common marmosets dwelling in this highly impacted landscape is nowadays lower than necessary for long-term survival. Additionally, smaller fragments having more groups suggests that they live in total association with humans, which assure their subsistence through the supply of introduced and exotic foods.

Contested dominance modifies the anovulatory consequences of social subordination in female marmosets

Dominance status among female marmosets is reflected in agonistic behavior and ovarian function. Socially dominant females receive submissive behavior from subordinates, while exhibiting normal ovulatory function. Subordinate females, however, receive agonistic behavior from dominants, while exhibiting reduced or absent ovulatory function. Such disparity in female fertility is not absolute, and groups with two breeding females have been described. The data reported here were obtained from 8 female-female pairs of captive female marmosets, each housed with a single unrelated male. Pairs were classified into two groups: "uncontested" dominance (UD) and "contested" dominance (CD), with 4 pairs each. Dominant females in UD pairs showed significantly higher frequencies (4.1) of agonism (piloerection, attack and chasing) than their subordinates (0.36), and agonistic behaviors were overall more frequently displayed by CD than by UD pairs. Subordinates in CD pairs exhibited more agonistic behavior (2.9) than subordinates in UD pairs (0.36), which displayed significantly more submissive (6.97) behaviors than their dominants (0.35). The data suggest that there is more than one kind of dominance relationship between female common marmosets. Assessment of progesterone levels showed that while subordinates in UD pairs appeared to be anovulatory, the degree of ovulatory disruption in subordinates of CD pairs was more varied and less complete. We suggest that such variation in female-female social dominance relationships and the associated variation in the degree and reliability of fertility suppression may explain variations of the reproductive condition of free-living groups of common marmosets.

Sleeping sites of common marmosets (Callithrix jacchus) in defaunated urban forest fragments: a strategy to maximize food intake

AbstractThe purpose of this study was to investigate if there was any species‐specific type and structure of sleeping sites of common marmosetsCallithrix jacchusand their key determinant. The study was conducted in an urban fragment of the Atlantic forest of north‐eastern Brazil, where a group of common marmosets was followed for 488 h. For this purpose we usedad libobservations, performed twice a week, when the animals were entering and leaving the sleeping sites, identified potential predators of the common marmosets through interviews with local people, and identified the trees that provided them with fruit and/or exudate during the study. Five sleeping sites were identified, all invariably in the border of the native forest and the orchard. No predators of common marmosets were seen by local people or recorded during this study, and the sleeping trees were located invariably in the place where there was the highest concentration of feeding trees, regardless of its structure. There was no species‐specific type and structure of sleeping places of common marmosets. The key variable defining the choice of a sleeping place was the availability and location of immediate sources of food.

Adult-infant food transfer in common marmosets: an experimental study

Infant marmosets and tamarins obtain solid food items from adults during and after the time of weaning. In addition to providing nutrients, food transfers may provide infants with the opportunity to learn about diet. The aim of this study was to investigate patterns of begging and food transfer in captive groups of common marmosets during tests with 1) palatable novel food, 2) unpalatable novel food, and 3) familiar food. Infants may gain an opportunity to learn about diet breadth by preferentially begging for novel rather than familiar items, while adults may facilitate infant learning by differing in their willingness to transfer food depending upon the food's novelty or palatability. In this study, infants exhibited more interest and begging with novel food items than with familiar ones. However, food transfers were not more likely to occur with novel foods than with familiar ones, and in fact adults were more likely to refuse infant begging attempts with novel foods. The palatability of the food also did not influence the rates of refusal and transfer: adults transferred palatable and unpalatable novel foods with similar frequencies. These results suggest that infant marmosets gain an opportunity to learn about diet breadth by begging for novel foods, but adults do not preferentially transfer novel or palatable food items.

Fecal androgen levels in common marmoset (Callithrix jacchus) males living in captive family groups

In captive common marmoset groups, the reproductive inhibition observed in subordinate female seems to be a result of olfactory, visual and behavioral cues from the dominant female. However, few studies have examined the relationship among adult males living in the same social group. These studies have shown that reproductive failure among peer males seems to be based on hormonal and behavioral mechanisms. New insights on sexual strategies in primates have been shown using fecal steroids, but so far no information is available for common marmoset males. In the present study, we evaluated the influence of light-dark cycle, age and reproductive condition on the profile of fecal androgens in males living in the same family group. Feces were collected from six fathers and six sons for androgen determination during the light phase of the 24-h cycle for eight days randomly distributed over a 4-week period. Androgen levels were determined by enzyme immunoassay technique. Adult sons showed higher androgen levels (166.97 +/- 22.95 ng/g) than fathers (80.69 +/- 44.38 ng/g) and juveniles (49.06 +/- 23.15 ng/g; P < 0.05). No diurnal variation (P > 0.05) in fecal androgen profile was observed in adults or juveniles. No indication of androgen-mediated social competition between fathers and adult sons was demonstrable. These results provide basic information on fecal androgen profile useful to investigate the socioendocrinology of free-ranging common marmoset males and verify that, in contrast to daughters, the reproductive suppression of sons is not based on physiological inhibition of their gonads.

Grooming as a reward? Social function of grooming between females in cooperatively breeding marmosets

Classical models of grooming predict that subordinate primates will direct grooming towards dominants to receive coalitionary support from them. In contrast, recent reviews suggest that grooming asymmetries can change with social system and ecological conditions and should reflect asymmetries in services provided by different members of the dyad. We studied grooming patterns between females in six wild groups of common marmosets, Callithrix jacchus, to investigate the relation between social structure and grooming between females in a cooperatively breeding species. We observed grooming frequently and consistently in all study groups. Breeding females groomed nonbreeding females more than vice versa, and grooming between breeding and nonbreeding females was not related to agonistic behaviour. Our results provide some support to the hypothesis that grooming asymmetries are related to differences in services provided by different group members. We suggest that, in cooperatively breeding systems, breeding females may use grooming as an incentive for helper females to stay in the group.

Grooming Circadian Rhythmicity, Progesterone Levels and Partner Preference of the Reproductive Pair of a Captive Common Marmoset (Callithrix jacchus) Family Group during Pregnancy and after Parturition

One family group of common marmosets (Callithrix jacchus) maintained in captivity under natural environmental conditions (Natal, Brazil, 05°46'S, 35°12'W) was observed by focal sampling at two non-consecutive days per week during two non-consecutive pregnancies (pregnancy 1: the last 8 fortnights before parturition; pregnancy 2: the last 5 ones) and after parturition (4 fortnights for both). The hourly percentiles of the duration of self-grooming and allogrooming interactions of the reproductive pair were submitted to Cosinor analysis for the 24-h period (p ≤ 0.05). The reproductive female's progesterone was monitored by fecal collection twice a week between 7:00 h to 9:00 h. Levels of progesterone were determined by ELISA method. During pregnancy 1, all interactions of the reproductive pair showed a 24-h statistically significant period. However, after parturition this periodicity is not present in some behaviors of the reproductive male. This animal presents the 24-h periodicity only toward to the reproductive female, the subadult son and to the newborns. Hormonal levels of the reproductive female showed isolated increases above 100 ng/g at the second and third fortnight after parturition, but did not characterize ovulation. Between pregnancy 1 and 2, the family was increased by the birth of four animals. During pregnancy 2, a statistically significant 24-h period was find only in self-grooming of the reproductive male and female, and in the interactions between the reproductive pair. Also, in the interactions of the reproductive male with only one of the juvenile son. After parturition the reproductive female ovulated at the second fortnight and became pregnant again. At this time, those interactions still have a 24-h period, except in grooming directed to the juvenile son by the reproductive male. As in the first post-partum, grooming directed to the newborns showed statistically significant 24-h period. These results suggest that the reproductive pair performs 24-h rhythmic grooming interactions only with some animals, supposed to be the preferential grooming partners. Furthermore, the temporal grooming expression in common marmosets may be affected by the reproductive condition (progesterone levels) of the reproductive female, by the care of newborn after parturition and the group size.

Behavioral and Hormonal Analysis of Social Relationships Between Oldest Females in a Wild Monogamous Group of Common Marmosets (Callithrix jacchus)

Social organization in common marmosets (Callithrix jacchus) appears to be based on a hierarchy of dominance, in which dominant females limit the reproductive functioning of subordinates. Reduced fertility was documented for captive but not for wild females. We investigated social dynamics and hormonal profiles of females living in a wild group. We collected behavioral and hormonal data during 7 mo from the reproductive and two nonreproductive adult females (probably daughters), and their interactions with the reproductive male. The subjects lived in a monogamous group at Nisia Floresta field station in northeastern Brazil. We collected behavioral data as all day follows, once a week and fecal material twice a week. We analyzed fecal samples for cortisol and progesterone using enzyme immuno assay (EIA) techniques. During the first three months we monitored the reproductive female (GRE) and the oldest nonreproductive female, (GIO). After the disappearence of GIO, we monitored the next oldest subordinate adult female, (GRA). GRE had just given birth at the beginning of the study, and she gave birth 6 mo later. During the last 2 weeks of GRE's gestation, GRA showed elevated progesterone levels, indicating ovarian cycling. Cortisol levels from GRE and GRA reached very high levels then. During GRA's cycling period, her interactions with the reproductive male (GT) were lower than when she was not cycling. We saw sexual interactions only between GT and GRE. The results provide evidence that ovarian function in mature subordinate females might be affected by the reproductive condition of the dominant female.

Scent-marking behavior in wild groups of common marmosets ( Callithrix jacchus )

Scent-marking in mammals has been frequently related to within-group social and reproductive dominance and to defense of territory and resources. We studied the scent-marking behavior of five wild groups of common marmosets, Callithrix jacchus, during 5 months of the fruiting season in northeastern Brazil. Circumgenital marking was the most common type of marking. Marks were distributed throughout the home range and were deposited mainly during travel and intergroup encounters. Although marks were commonly deposited at gum trees, there was no evidence that the animals used scent marks to label fruiting trees or sleeping sites. Contrary to expectations, reproductively dominant females did not mark more than reproductively subordinate females. Moreover, during intergroup encounters, reproductively subordinate females displayed higher frequencies of scent-marking than the reproductively dominant females of their group. Our results suggest that scent-marking is not strictly tied to reproductive dominance or territorial (or resource) defense in common marmosets. Because marks provide information about individual identity and reproductive condition, scent marks could serve different functions when used by different individuals. The high frequency of marking by reproductively subordinate females during intergroup encounters suggests that scent-marking might be used to signal to individuals of neighboring groups. Our data highlight the importance of social and ecological variables in scent-marking behavior.