Wild Common Marmosets Research Articles

Choosing the best way: how wild common marmosets travel to efficiently exploit resources

While foraging, animals have to find potential food sites, remember these sites, and plan the best navigation route. To deal with problems associated with foraging for multiple and patchy resources, primates may employ heuristic strategies to improve foraging success. Until now, no study has attempted to investigate experimentally the use of such strategies by a primate in a context involving foraging in large-scale space. Thus, we carried out an experimental field study that aimed to test if wild common marmosets (Callithrix jacchus) employ heuristic strategies to efficiently navigate through multiple feeding sites distributed in a large-scale space. In our experiment, we arranged four feeding platforms in a trapezoid configuration with up to 60 possible routes and observe marmosets’ decisions under two experimental conditions. In experimental condition I, all platforms contained the same amount of food; in experimental condition II, the platforms had different amounts of food. According to the number and arrangement of the platforms, we tested two heuristic strategies: the Nearest Neighbor Rule and the Gravity Rule. Our results revealed that wild common marmosets prefer to use routes consistent with a heuristic strategy more than expected by chance, regardless of food distribution. The findings also demonstrate that common marmosets seem to integrate different factors such as distance and quantity of food across multiple sites distributed over a large-scale space, employing a combination of heuristic strategies to select the most efficient routes available. In summary, our findings confirm our expectations and provide important insights into the spatial cognition of these small neotropical primates.

Navigating in a challenging semiarid environment: the use of a route-based mental map by a small-bodied neotropical primate.

To increase efficiency in the search for resources, many animals rely on their spatial abilities. Specifically, primates have been reported to use mostly topological and rarely Euclidean maps when navigating in large-scale space. Here, we aimed to investigate if the navigation of wild common marmosets inhabiting a semiarid environment is consistent with a topological representation and how environmental factors affect navigation. We collected 497h of direct behavioral and GPS information on a group of marmosets using a 2-min instantaneous focal animal sampling technique.We found that our study group reused not only long-route segments (mean of 1007m) but entire daily routes, a pattern that is not commonly seen in primates. The most frequently reused route segments were the ones closer to feeding sites, distant to resting sites, and in areas sparse in tree vegetation. We also identified a total of 56 clustered direction change points indicating that the group modified their direction of travel. These changes in direction were influenced by their close proximity to resting and feeding sites. Despite our small sample size, the obtained results are important and consistent with the contention that common marmosets navigate using a topological map that seems to benefit these animals in response to the exploitation of clustered exudate trees. Based on our findings, we hypothesize that the Caatinga landscape imposes physical restrictions in our group's navigation such as gaps in vegetation, small trees and xerophytic plants. This study, based on preliminary evidence, raises the question of whether navigation patterns are an intrinsic characteristic of a species or are ecologically dependent and change according to the environment.

Callitrichid responses to dead and dying infants: the effects of paternal bonding and cause of death.

Many primates show responses to dead infants, yet testing explanations for these behaviors has been difficult. Callitrichids present a unique opportunity to delineate between hypotheses, since unlike most species, male caretakers form closer social bonds with infants than mothers. Callitrichids are also known to commit infanticide, leaving obvious wounds that may enable them to more readily recognize death. We present: (1) a case study of a wild common marmoset (Callithrix jacchus) group responding to an infant's natural death, and (2) a review of published infant deaths across callitrichids (N = 16), testing for trends in the sex of reacting individuals and cause of death. In our case study, several group members frequently interacted with the dead infant, attempting to carry it. However, the strongest response was from a male that remained with the corpse for ~ 3h, despite his group leaving the area. Across callitrichid species, corpse interactions were significantly sex-biased: 100% (N = 6) of accidental deaths involved corpse interaction by males (p = 0.007), compared to 60% (N = 3 of 5) by females (p = 0.095). Cause of death also played a significant role, with individuals attempting to carry dead infants in 100% (N = 6) of accidental deaths, but only 11.1% (N = 1 of 9) of infanticides (p = 0.001). Although the available literature is small and potentially subject to publication biases, these data support the idea that visually obvious wounds may influence callitrichids' perception of dead conspecifics. Additionally, male-biased patterns of corpse interaction in callitrichids indicate that social bonds likely shape reactions to the dead, in addition to kinship. While published data on primate thanatology are limited, this study demonstrates quantitative approaches that can provide empirical insights into primates' responses to dead conspecifics.

Wild common marmosets (Callithrix jacchus) employ spatial cognitive abilities to improve their food search and consumption: an experimental approach in small-scale space.

The ability of an animal to integrate and retain spatial information of resources often depends on the spatial memory and the speed at which this memory crystallizes. These become especially important once foragers reach their target area. However, very little is known about how wild common marmosets encode spatial information when feeding rewards are near to each other in a small-scale space. With this in mind, we performed field experiments to test foraging decisions related to a small-scale space setting. Specifically, we tested the (i) short- and (ii) long-term spatial memory, as well as (iii) the ability to remember the spatial location of resources after a single visit (one-trial spatial learning). The study was conducted with four groups of wild common marmosets (Callithrix jacchus) living in a semiarid Caatinga environment. We observed that individuals were able to retain spatial information of food sources on both a short- and long-term basis and to learn the spatial location of these resources after a single visit. We suggest that such abilities during foraging can improve the search for scattered resources with fluctuations of food availability. Presumably, this would be particularly advantageous in Caatinga, with its vegetation exhibiting asynchronous phenological patterns. Altogether, our results demonstrate that common marmosets employ all three studied spatial cognitive abilities to improve their food search and consumption.

Trait variation and trait stability in common marmosets (Callithrix jacchus) inhabiting ecologically distinct habitats in northeastern Brazil.

Understanding the set of factors that promote and constrain a species' ability to exploit ecologically distinct habitats is central for addressing questions of intraspecific variability in behavior and morphology. In this study, we compared newly collected data with published data on body measurements, group size and composition, daily path length, home range, and reproductive output in wild common marmosets naturally inhabiting two contrasting environments in northeastern Brazil: the Atlantic Forest (AF), which is characterized by high biodiversity and reduced seasonality in food availability and the Caatinga (CAT), which is characterized by a severe hot and dry season lasting from 5 to 11 months, drought-resistant plant species, and reduced primary productivity. Despite marked differences in ecological conditions, CAT marmosets and AF marmosets differed minimally in daily path length, home range, reproductive output, and infant survivorship. CAT marmosets were found to live in smaller groups containing fewer adult females than AF marmosets, and also were characterized by a greater surface area to body mass ratio, a trait that may represent an adaptation to the hot and dry conditions of the Caatinga. We propose that in conjunction with body mass reduction, minor adjustments in behavior, the exploitation of cacti as a source of water and nutrients, and access to exudates as a dependable year-round food resource, common marmosets successfully used the same adaptive pattern to maintain high reproductive output and infant survivorship in exploiting these two ecologically distinct environments.

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.

Video demonstrations seed alternative problem-solving techniques in wild common marmosets.

Studies of social learning and tradition formation under field conditions have recently gained momentum, but suffer from the limited control of socio-ecological factors thought to be responsible for transmission patterns. The use of artificial visual stimuli is a potentially powerful tool to overcome some of these problems. Here, in a field experiment, we used video images of unfamiliar conspecifics performing virtual demonstrations of foraging techniques. We tested 12 family groups of wild common marmosets. Six groups received video demonstrations (footage of conspecifics either pulling a drawer open or pushing a lid upwards, in an 'artificial fruit'); the other six groups served as controls (exposed to a static image of a conspecific next to the fruit). Subjects in video groups were more manipulative and successful in opening the fruit than controls; they were also more likely to use the technique they had witnessed and thus could serve as live models for other family members. To our knowledge, this is the first study that used video demonstrations in the wild and demonstrated the potent force of social learning, even from unfamiliar conspecifics, under field conditions.

Memory, transmission and persistence of alternative foraging techniques in wild common marmosets

Experimental studies on traditions in animals have focused almost entirely on the initial transmission phase in captive populations. We conducted an open diffusion field experiment with 13 groups of wild common marmosets, Callithrix jacchus. Seven groups contained individuals that were already familiar with the task (‘push or pull’ box) and thus served as potential models for naïve individuals. Additionally, in four groups one individual was trained for one of the two possible techniques and in two control groups no skilled individuals were present. First, we investigated whether experienced individuals would remember how to solve the task even after 2 years without exposure and whether they would still prefer their learned technique. Second, we tested whether naïve individuals would learn socially from their skilled family members and, more importantly, whether they would use the same technique. Third, we conducted several test blocks to see whether the individual and/or group behaviour would persist over time. Our results show that wild common marmosets were able to memorize, learn socially and maintain preferences of foraging techniques. This field experiment thus reveals a promising approach to studying social learning in the wild and provides the basis for long-term studies on tradition formation.

Hunting strategies in wild common marmosets are prey and age dependent

We investigated the hunting strategies of wild common marmosets (Callithrix jacchus) to determine whether the strategies differed among animals of different age classes and/or prey type. The study was conducted in a fragment of Atlantic Rain Forest, situated 40 km from Recife (PE/Brazil). Twenty-seven individuals from four social groups were observed. Captured prey items were divided into three categories. The hunting strategies of the common marmosets were ranked into four categories. The acquisition of larger prey (items more than 2.0 cm) involved the appropriate body movements and postures that concealed the approaching marmosets, whereas the acquisition of smaller prey (items under 2.0 cm) involved less concealing behaviors. Furthermore, adults and juveniles (age ≥ 5 months) were more capable of capturing larger prey than were younger (1-2 months) or older infants (3-4 months). Although older infants were successful in capturing certain prey, they often failed when they attempted to capture larger prey that jumped and/or used flight to escape. The results suggest that both the experience of the monkeys and escape behavior of the prey affect predation efficiency in wild common marmosets.

Digestion in the common marmoset (Callithrix jacchus), a gummivore–frugivore

Wild common marmosets (Callithrix jacchus) feed on fruits, insects, and gums, all of which provide different digestive challenges. Much of the ingested mass of fruits consists of seeds. In general, seeds represent indigestible bulk to marmosets and could inhibit feeding if they are not eliminated rapidly. In contrast, gums are beta-linked polysaccharides that require microbial fermentation. Their digestion would benefit from an extended residence time within the gut. Earlier research found that mean retention time (MRT) for a liquid digestive marker (cobalt EDTA) was significantly longer than MRT for a particulate marker (chromium-mordanted fiber), suggesting that common marmosets preferentially retain liquid digesta. We conducted two four-day-long digestion trials on 13 individually housed adult common marmosets fed a single-item, purified diet in order to examine the relations among MRT of cobalt EDTA and chromium-mordanted fiber, food dry matter intake (DMI), and apparent digestibility of dry matter (ADDM). We compared the MRT values with the data from the previous study mentioned above and a study using polystyrene beads. There were no significant correlations among MRT, ADDM, or DMI, although increases in DMI between trials were associated with decreases in MRT. ADDM was consistent within individuals between trials; but the mean values ranged from 75.0 to 83.4% among individuals. We found no difference in MRT between the liquid (17.5 + or - 1.6 hr) and particulate (17.9 + or - 1.4 hr) markers. Although these values were not significantly different than found previously, the MRT for chromium-mordanted fiber tended to be longer. This probably reflects the relatively small size of the chromium-mordanted fiber particles used in this study. An inverse relationship between particle size and MRT was evident; the mean MRT of polysterene beads, the largest marker, was only 8.3 + or - 1.5 hr. Marmosets appear to retain liquids and small particles within the gut longer than large particles.

Vocalisations of wild common marmosets are influenced by diurnal and ontogenetic factors

The vocalisations of wild common marmosets, Callithrix jacchus, were recorded to investigate whether call rate by individuals is affected by time of day, age, sex or dominance rank within a group. We also investigated how vocalisation pitch was affected by age, focussing on a single common call, the trill call. Adults vocalised more than juveniles or infants during the majority of daylight hours. Only the call rate of juveniles varied significantly over the day. No differences were found between either sex or dominance rank with respect to rate of vocalisations. The trill calls emitted by young wild common marmosets were of a higher pitch than those emitted by adults. We conclude that the auditory communication of wild common marmosets is related to the age of the animals, both in terms of call rate and the physical characteristics of their vocalisations.

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.

Structure and Usage of the Vocal Repertoire of Callithrix jacchus

We recorded the vocal repertoire and behavior of individuals from 3 groups of wild common marmosets (Callithrix jacchus) via focal sampling and ad libitum sampling in a fragment of Atlantic Rain Forest in Pernambuco, northeast Brazil. Our aims were: 1) to provide a detailed quantitative description of the vocalizations and vocal repertoire of common marmosets in the wild, and to compare the repertoire with that described from conspecific captives; 2) to investigate if differences exist in vocal repertoire between wild individuals of different ages; and 3) to explore the behavioral contexts associated with specific vocalizations in free-living Callithrix jacchus. This is the first study describing common marmoset calls in the wild and it shows that their vocal repertoire comprises 13 different calls. Though wild and captive calls were similar, differences occurred in the form of the alarm calls given for different potential predators, the tse call, and very brief whistle. In addition, the tsee call did not occur in wild individuals and wild infants did not utter the twitter call. The age of the subjects influenced the call types present in the vocal repertoire, e.g., the loud cry was specific to infants, whereas only adults gave alarm calls. The behavior of both the caller and the potential receivers seemed to affect the frequency of wild common marmoset calls. One could predict intricate vocalization-based communications for the system based on their relatively complex social organization and densely leafed arboreal habitat. Our study confirms the prediction.

Predation by the tayra on the common marmoset and the pale-throated three-toed sloth

Predation on arboreal mammals is rarely observed in the wild. Here we describe the first confirmed observations of predation on a juvenile wild common marmoset (Callithrix jacchus) and on a neonate wild pale-throated three-toed sloth (Bradypus tridactylus) by the mustelid carnivore Eira barbara, the tayra. We discuss predation on both of the prey species and review the nature of predation by the tayra.

The composition of milk from free‐living common marmosets (Callithrix jacchus) in Brazil

Common marmosets, one of the smallest anthropoid primates, have a relatively high reproductive rate, capable of producing twins or triplets twice per year. Growth and development of infants is relatively rapid, and lactation is relatively short at less than 3 months. Although mean values for the proximate composition (dry matter, protein, fat and sugar) of captive common marmoset milks fall within anthropoid norms, composition is highly variable among individual samples, with concentrations of milk fat ranging from below 1 to over 10%. To examine the extent to which this variation might be a consequence of captive conditions, we collected milk samples from wild common marmosets freely living on a farm in the state of Rio de Janeiro, Brazil. The proximate composition of the milk samples was assayed using identical techniques as used for the captive marmoset milks. The composition of the milk of wild common marmosets was also variable, but tended to be lower in dry matter, fat, protein and gross energy, and higher in sugar than milks from captive animals. Interestingly, the percentage of estimated gross energy from the protein fraction of the milks was relatively constant in both wild and captive marmosets and did not differ between wild and captive animals: 1 kcal of common marmoset milk contains on average (+/-SEM) 0.035+/-.001 g of protein regardless of the gross energy content of the milk or whether the milk was from a wild or captive animal. In contrast, in 1 kcal of low-energy milks, the amount of sugar was significantly higher and the amount of fat significantly lower than in 1 kcal of high-energy milks. Thus, common marmoset milk exhibits axes of variability (especially fat concentration) as well as a significant stability in the relative amount of protein.

Social influences on the development of foraging behavior in free‐living common marmosets (Callithrix jacchus)

In this study we investigated the extent and pattern of social influences (i.e., the use of a conspecific as a model) on the foraging behavior of immature, wild common marmosets (Callithrix jacchus) as a function of the age of individuals. We compared the foraging activities and interactions with subadult and adult group members (older than 15 months) of young infants (1-2 months old), older infants (3-4 months old), and juveniles (5-10 months old). In addition to measuring the intensities of model-independent foraging (MIF) and merely paying attention to the model's foraging activities, we examined the frequencies of three types of model-dependent foraging (MDF): "follow the model", "manipulate the same object", and "forage together". We found that older infants were the most attentive and most socially-influenced foragers among the three age categories in absolute terms, but were not more attentive than young infants given their low foraging activity. Juveniles, in contrast, tended to have reduced overall foraging intensity compared to infants, but showed relatively more MDF in cases in which they observed subadult or adult models. Female models appeared to be more attractive than male models. These findings suggest that infants are generally more attentive to the foraging behavior of subadults and adults than juveniles, with the latter being more influenced when they had observed a model before. These subtle age-dependent effects of social foraging not only extend the assumption that young primates seek information from adults, they also suggest a complex interplay among physical and cognitive maturation, independence, and social dynamics.

Can wild common marmosets (Callithrix jacchus) solve the parallel strings task?

Patterned string tasks are a test of perceptual capacity and the understanding of means-end connections. Primates can solve complex forms of this task in laboratories. However, this may not indicate the level of such cognition that is commonly employed in the wild, where decision-making time is often short and distractions such as predator avoidance and competition between conspecifics are often prevalent. The current study tests whether wild common marmosets (Callithrix jacchus) can successfully complete the simplest form of the patterned string task, parallel strings, while in their natural environment. Although 12 out of 13 marmosets could successfully complete the task, in previous laboratory-based studies on primates, the errors at this task by all primate species tested were consistently lower than in the present study. This is probably explained by the added difficulties imposed by the natural setting of the task in the present study, exemplified by a significant increase in observed vigilance behaviour by subject animals prior to attempts at the task that were unsuccessful. The undertaking of such tasks by common marmosets in situ probably provides a more reasonable representation of the levels of cognitive capacity expressed by this species in the wild than do laboratory-based studies of the task.

Behavioral strategies and hormonal profiles of dominant and subordinate common marmoset (Callithrix jacchus) females in wild monogamous groups

New insights into the mating systems of common marmosets suggest that they are mainly monogamous, although polygyny and polyandry occasionally occur. Long-term monitoring of wild common marmosets has shown that some reports of polygynous groups (i.e., groups that contain more than one reproducing female) in fact indicate an unbalanced reproductive output associated with extragroup copulation. In this study we describe the behavioral and hormonal profiles of common marmoset (Callithrix jacchus) females living in three wild monogamous groups (Q, PBf, and T), varying from five to 11 individuals, at Nísia Floresta field station, RN, Brazil. The mating system of the groups was previously characterized in terms of affiliative, sexual, and mate-guarding behaviors. Behavioral data were collected once a week, and fecal samples were collected at least twice a week for 10-16 months, depending on the group. A preferential allogrooming relationship was recorded between dominant males and females. Under field conditions the reproductive inhibition of subordinate females appears to be more behavioral than hormonal, since subordinate females of the three groups ovulated and two conceived during the study. In these cases, the subordinate and dominant females reproduced 1 month apart, and infanticide (one case confirmed and one suspected) appeared to be part of the reproductive strategy of dominant females. Following the infanticide, ovarian inhibition (group T) or emigration and return to the natal group (group PBf) were observed. In the third group (Q) the subordinate female showed hormonal profiles compatible with pregnancy, but no infants were seen. These findings reflect the different alternatives that wild subordinate common marmoset females use to reproduce.

Infanticide and Cannibalism in Wild Common Marmosets

Infanticide has been observed in many different species [1], including common marmosets [2-4], due to sexual selection, reproductive strategies or resource competition [3, 5, 6], which may ultimately lead to exploitation (cannibalism) [1, 7]. Wild callithrichids have a very flexible mating system, including monogamy, polygynandry, polyandry and polygyny [4, 8, 9], with Monteiro da Cruz [10] finding all these patterns within the same population. This results from the high degree of deforestation of their habitat [4], but non-monogamous groups cannot ensure successful rearing of infants, since helpers are crucial and should be present in high numbers [11]. In this study, we show for the first time that cannibalism can follow infanticide, and we hypothesise that it is a result of both competition for scarce resources and the need for animal protein, exacerbated by forest degradation.