Object permanence in common marmosets (Callithrix jacchus)

A series of 9 search tasks corresponding to the Piagetian Stages 3-6 of object permanence were administered to 11 common marmosets (Callithrix jacchus). Success rates varied strongly among tasks and marmosets, but the performances of most subjects were above chance level on the majority of tasks of visible and invisible displacements. Although up to 24 trials were administered in the tests, subjects did not improve their performance across trials. Errors were due to preferences for specific locations or boxes, simple search strategies, and attentional deficits. The performances of at least 2 subjects that achieved very high scores up to the successive invisible displacement task suggest that this species is able to represent the existence and the movements of unperceived objects.     

Geometrical gaze following in common marmosets (Callithrix jacchus)

A series of experiments investigating the degree of gaze understanding in common marmosets (Callithrix jacchus) is reported. Results show that marmosets follow the gaze of a human experimenter readily and also use the gaze to locate food in a modified version of the object choice task if influences of chance probabilities and prepotent response tendencies are controlled for. In addition, this new version of the task allows the assessment of the accuracy of gaze following. Marmosets precisely extrapolate gaze direction, past distracting objects and from considerable distances, thereby meeting the criteria of so-called geometrical gaze following. The presence of this ability in common marmosets suggests that higher forms of gaze following might be more widely distributed among nonhuman primates than previously thought.     

Performance on patterned string problems by common marmosets (Callithrix jacchus)

This experiment examined the performance of common marmosets (Callithrix jacchus) on a series of patterned string problems to assess the marmosets’ understanding of means–ends relationships. One marmoset, Jet, was exposed to a series of problems that were ordered in terms of perceived difficulty during two testings that were separated by 1 year. In the second testing, Jet received problems that had been used during the first testing along with three new problems. Each of the new problems was designed to be an exemplar of the type of problem that Jet had experienced difficulty with in the first testing. A second marmoset, Peaches, was tested on the same set of problems given to Jet in the second testing. Results indicated that the marmosets’ performance on these problems fell into three categories. In one category, some problems were solved without evidence of trial-and-error learning. In a second category, there were problems in which the marmosets responded at chance levels initially but evidenced improvement as a function of extended testing. In a third category, some problems appeared to be virtually unsolvable even with extended testing. Taken together, these results indicate that the marmosets were able to learn the means–ends connection between pulling a string and obtaining food. This learning was best characterized as a trial-and-error process for some problem forms, while for others there appeared to be rapid learning that did not require extensive practice. The instances of rapid learning may be the result of the application of a simple spatial proximity rule in which the marmosets chose the string that was closest to an imaginary line drawn between the marmoset and the reinforcer.     

Facial expressions in common marmosets (Callithrix jacchus) and their use by conspecifics

Facial expressions have been studied mainly in chimpanzees and have been shown to be important social signals. In platyrrhine and strepsirrhine primates, it has been doubted that facial expressions are differentiated enough, or the species socially capable enough, for facial expressions to be part of their communication system. However, in a series of experiments presenting olfactory, auditory and visual stimuli, we found that common marmosets (Callithrix jacchus) displayed an unexpected variety of facial expressions. Especially, olfactory and auditory stimuli elicited obvious facial displays (such as disgust), some of which are reported here for the first time. We asked whether specific facial responses to food and predator-related stimuli might act as social signals to conspecifics. We recorded two contrasting facial expressions (fear and pleasure) as separate sets of video clips and then presented these to cage mates of those marmosets shown in the images, while tempting the subject with food. Results show that the expression of a fearful face on screen significantly reduced time spent near the food bowl compared to the duration when a face showing pleasure was screened. This responsiveness to a cage mate’s facial expressions suggests that the evolution of facial signals may have occurred much earlier in primate evolution than had been thought.     

Activity of common marmosets (Callithrix jacchus) in limited spaces: hand movement characteristics

The increasing popularity of marmoset monkeys (Callithrix jacchus) in anatomical, behavioral, and electrophysiological studies has called for a detailed analysis of their natural behavior within limited spaces. In the present study, the authors analyzed hand movements during horizontal and vertical progressions in a cylinder. The trajectory of each hand covered the entire cylinder floor during horizontal progressions and the entire cylinder wall during vertical progressions. Different marmosets have different patterns of hand movement. The average maximum angle of hand movements for all marmosets during horizontal and vertical progressions oscillates, although the average over time is constant and similar for both hands, whereas head movements during horizontal progressions become smaller with successive progressions. Another observed difference between rats and monkeys was in the size of head and hand movements at the beginning of each experimental session. During the 1st horizontal progression, all marmosets moved their heads to a greater extent than their hands. This sequential head and hand movement is referred as bistable behavior. The bistable pattern of motor behavior, which was also observed in successive progressions, may be derived from an inherent fear of predators or exploratory interest of a novel environment.     

Perception of biological motion in common marmosets (Callithrix jacchus): by females only

The ability to perceive biological motion (BM) has been demonstrated in a number of species including humans but the few studies of non-human primates have been relatively inconclusive. We investigated whether common marmosets (Callithrix jacchus) are able to perceive biological motion, using a novel method to test non-human primates. Marmosets (7 male and 7 female) were trained to remove a cover from a container and look inside it, revealing a computer screen. Then they were presented with images on this computer screen consisting of a novel BM pattern (a walking hen) and 4 manipulations of that pattern (a static frame of this pattern and inverted, scrambled, and rotating versions of the pattern). The behavioural responses of the marmosets were recorded and used to assess discrimination between stimuli. BM was attended to by females but not males, as shown by active inspection behaviour, mainly movement of the head towards the stimulus. Females paid significantly less attention to all of the other stimuli. This indicates the females’ ability to attend to biological motion. Females showed slightly more attention to the inverted BM than to the static, scrambled, and rotating patterns. The males were less attentive to all of the stimuli than were the females and, unlike the females, responded to all stimuli in a similar manner. This sex difference could be due to an inability of males to recognise BM altogether or to a lesser amount of curiosity. Considered together with the findings of previous studies on chicks and humans, the results of the present study support the notion of a common mechanism across species for the detection of BM.     

Social mobbing calls in common marmosets (Callithrix jacchus): effects of experience and associated cortisol levels

We compared the mobbing response to model snakes of two groups of captive-born common marmosets (Callithrix jacchus) differing in genetic relatedness, age and past experience. Mobbing vocalisations (tsik calls), other mobbing behaviour and attention to the stimulus were recorded for 2 min. intervals pre-exposure, during exposure to various stimuli and post-exposure. Marmosets in one group were vocally reactive to all stimuli, although more so to one particular stimulus resembling rearing snakes and modified images of it, whereas the marmosets in a younger and genetically unrelated group attended to the stimuli but made very few mobbing calls. The parent stock of the first group had suffered stress in early life and had developed a phobic response to a specific stimulus, which they had transmitted to their offspring. A third group, matching the older group in age range but genetically unrelated, was also found to be unresponsive to the stimulus that elicited the strongest response in the first group. Cortisol levels in samples of hair were assayed and a significant negative correlation was found between the number of tsik calls made during presentation of the stimuli and the cortisol level, showing that mobbing behaviour/behavioural reactivity is associated with low levels of physiological stress.     

Development of hand preferences in marmosets (Callithrix jacchus) and effects of aging

The authors investigated the development of unimanual hand use and hand preferences during feeding in 15 marmosets (Callithrix jacchus), ages birth to 51-70 months. Bimanual hand use was common at 1-2 months, but by 5-8 months unimanual holding had developed and so had significant hand preferences. Half of the marmosets preferred to pick up and take food to the mouth with the left hand, and half preferred the right hand. Individuals maintained the same hand preference at all ages examined. Significant relationships were also found between the postures adopted during feeding and the direction of hand preferences displayed by juvenile marmosets. There was a positive correlation between increased suspension and increased left-hand preference, and a negative correlation between increased feeding in a tripedal posture and increased left-hand preference. These results are discussed in terms of motor development and hemispheric specialization.     

Visuospatial reaching preferences of common marmosets (Callithrix jacchus): an assessment of individual biases across a variety of tasks

Using multiple measures of hand preference, the authors investigated lateralization at an individual level in 21 common marmosets. Despite showing group biases for sensory and communication functions, these same marmosets did not show a group bias in direction of lateralized hand use. Hand preferences were recorded on four novel reaching tasks requiring different levels of visual guidance and postural control. As found for simple food holding (with the same subjects), they displayed strong individual hand preferences but no group bias indicative of handedness. The strength of hand preference was influenced by task demands: stronger preferences were expressed when subjects adopted a suspended posture, and when "successful" versus "unsuccessful" foraging strategies were compared. Comparisons between visuospatial reaching and simple food holding preferences also revealed that half of the subjects displayed a division of function between the hands/hemispheres; subjects displayed opposing preferences in simple and visuospatial reaching, which would be beneficial for the performance of coordinated bimanual tasks. Given the apparent absence of a selective advantage for handedness, the authors suggest that hand preferences may reflect hemispheric dominance of other cognitive domains (i.e., temperament).     

Watching others in a positive state does not induce optimism bias in common marmosets (Callithrix jacchus), but leads to behaviour indicative of competition

Animal Cognition - Emotional contagion is suggested to facilitate group life by enhancing synchronized responses to the environment. Cooperative breeders are an example of a social system that...     

Even simple forms of social learning rely on intention attribution in marmoset monkeys (Callithrix jacchus)

Intention attribution guides the cognitively most demanding forms of social learning, such as imitation, thereby scaffolding cumulative cultural evolution. However, it is not thought to be necessary for more basic forms of social learning. Here we present evidence that in marmoset monkeys (Callithrix jacchus) even most basic forms of social learning such as enhancement depend on intention attribution. Marmosets perceived the behavior of a conspecific and a conspecific-like robot, but not that of a moving black box, as goal directed. Their subsequent choice behavior was shaped by social facilitation and stimulus enhancement, that is, by very simple forms of social learning, but only when exposed to the conspecific and robot, which they previously had perceived as intentional agents. We discuss the implications of this finding for contemporary debates about social learning, including emulation learning and ghost control studies, the necessity of goal-directed copying for cumulative cultural evolution, and the limits of current classification systems of social learning for the evolution of social and asocial learning.     

Modulation of physical understanding by common marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>)

The understanding of physical causality in common marmosets was tested using support problems in which a pair of sheets was presented to determine whether subjects would choose the sheet that had a food item on it (i.e., the sheet was supporting the food item). In two experiments, the conditions were manipulated in terms of the length of the sheet, the distance between the sheet and the food item, the presence of a gap separating the two sheets, and the size of the food item. In Experiment 1, the marmosets had difficulty rejecting an irretrievable food item when it was located closer to them than a retrievable item. Although their performance was strongly affected by the size of the irretrievable food item, they quickly learned to reject that alternative. In contrast, no improvement was found when one sheet was divided into two pieces such that the food item could not be retrieved when its near side was pulled. A similar response tendency was observed in Experiment 2, in which the effects of the large food item were examined in three different conditions. Thus, common marmosets were influenced by the perceptual features of the food in solving the support problems, as are other non-human primates. In addition, they consistently failed to appreciate the presence of a gap and, therefore, failed to reject the distracter alternative. However, all animals rapidly learned that the size of the food item was an irrelevant variable, and some showed an elementary conceptual understanding of support. These findings suggest that marmosets’ physical understanding may improve with experience.     

Representation of serial order in pigeons (Columba livia)

In Experiment 1, 2 groups of pigeons were trained to respond to either a 4-item (A→B→C→D) or 5-item (A→B→C→D→E) list. After learning their respective list, half of the subjects were trained on a positive pair with reinforcement provided when pairs were responded to in the order true to that of the original sequence (4-item: B→C; 5-item: B→D). The remaining subjects were trained on a negative pair with reinforcement provided for responding to the pairs in the order opposite to that learned in the original sequence (4-item: C→B; 5-item: D→B). Subjects in the positive pair condition learned their respective pair faster than did subjects in the negative pair condition. In Experiment 2, after reaching criterion on a 4-item list, subjects received 16 BC probe trials spread across 4 sessions of training. Subjects performed significantly above chance on the probe trials. The performance of our subjects in Experiments 1 and 2 demonstrates that, similar to monkeys, pigeons form a representation of the lists that they learn.     

Representation of serial order in monkeys (Cebus apella)

Cebus monkeys were trained on a five-item serial learning task, symbolized as ABCDE; the initial stages of training were on the shorter subseries AB, ABC, and ABCD. To assess the monkeys' knowledge of the sequential position of each item, pair-wise tests were given to 2 subjects after acquisition of the ABCD series and to 4 subjects after reaching criterion on the ABCDE series. In both tests, the monkeys performed at high levels on the interior pairs, which were BC for the ABCD series, and BC, BD, and CD for the ABCDE series. These results, as well as the orderly relations observed in the pair-wise tests between first-item response latency and first-item position and between second-item response latency and number of missing items, indicated that the monkeys had developed a well-organized internal representation of the four- and five-item series. Although pigeons are also capable of learning four-item and five-item series, they apparently do not develop a comparable representational structure. The disparity between the monkeys' and pigeons' representational competence for serial order is predictable from the difference in their capacities for associative transitivity.     

A test for order relevance in a three-element serial learning task

Rats were trained in a straight runway on a simple three-element series of differing reward quantities. The first trial of the series ended with a two-pellet reward, and the second and third trials ended with a 12-pellet reward and a nonreward, respectively (2-12-0). All animals developed accurate anticipation of the terminal nonreward in the 2-12-0 series before it was rearranged for two test days during which the elements appeared in the order 12-2-0. The rats' anticipation of the terminal nonreward did not transfer to the reordered series, a result taken to mean that anticipation had been based upon interitem associations among memorial representations of the differing reward quantities. A second transfer test to 0-0-0, given after anticipation was reestablished to the 2-12-0 series, gave evidence that the ordinal position of the series elements was also a source of anticipation; the animals continued to run relatively slowly on the third trial in extinction. In neither transfer test was there evidence that the rats employed the strategy of enumerating rewarded trials, because counting is an order-irrelevant process.     

Testing for social learning and imitation in common marmosets, <Emphasis Type="Italic">Callithrix jacchus</Emphasis>, using an artificial fruit

We tested for social learning and imitation in common marmosets using an artificial foraging task and trained conspecific demonstrators. We trained a demonstrator marmoset to open an artificial fruit, providing a full demonstration of the task to be learned. Another marmoset provided a partial demonstration, controlling for stimulus enhancement effects, by eating food from the outside of the apparatus. We thus compared three observer groups, each consisting of four animals: those that received the full demonstration, those that received the partial demonstration, and a control group that saw no demonstration prior to testing. Although none of the observer marmosets succeeded in opening the artificial fruit during the test periods, there were clear effects of demonstration type. Those that saw the full demonstration manipulated the apparatus more overall, whereas those from the control group manipulated it the least of the three groups. Those from the full-demonstration group also contacted the particular parts of the artificial fruit that they had seen touched (localised stimulus enhancement) to a greater extent than the other two groups. There was also an interaction between the number of hand and mouth touches made to the artificial fruit for the full- and partial-demonstration groups. Whether or not these data represent evidence for imitation is discussed. We also propose that the clear differences between the groups suggest that social learning mechanisms provide real benefits to these animals in terms of developing novel food-processing skills analogous to the one presented here.