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.     

Characteristics of serial order learning in common marmosets (Callithrix jacchus)

We investigated the characteristics of serial order learning in common marmosets (Callithrix jacchus). Five marmosets were trained in a sequential responding task in which they were required to touch four graphic patterns in a given order (A→B→C→D) to obtain a reward. All five marmosets learned the task with over 65% accuracy. Shuffling the positions of B, C, and D immediately after the marmoset had correctly identified and selected the first stimulus (A) either decreased accuracy or lengthened response latency for the second stimulus (B). These results suggest that the marmosets planned the response to the second stimulus before they touched the first stimulus. In addition, when we presented a pair of stimuli (AB, AC, AD, BC, BD, and CD pairs), the marmosets responded to the stimuli in the pair in the appropriate order, according to the learned order (A→B→C→D). The analyses of first and second response latencies clearly demonstrated both the first-item and missing-item effects in task performance. Our data provide direct evidence that marmosets can learn the relative order of the four stimuli in a sequential responding task. (PsycINFO Database Record (c) 2012 APA, all rights reserved).     

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...     

Object permanence in lemurs

Object permanence, the ability to mentally represent objects that have disappeared from view, should be advantageous to animals in their interaction with the natural world. The objective of this study was to examine whether lemurs possess object permanence. Thirteen adult subjects representing four species of diurnal lemur (Eulemur fulvus rufus, Eulemur mongoz, Lemur catta and Hapalemur griseus) were presented with seven standard Piagetian visible and invisible object displacement tests, plus one single visible test where the subject had to wait predetermined times before allowed to search, and two invisible tests where each hiding place was made visually unique. In all visible tests lemurs were able to find an object that had been in clear view before being hidden. However, when lemurs were not allowed to search for up to 25-s, performance declined with increasing time-delay. Subjects did not outperform chance on any invisible displacements regardless of whether hiding places were visually uniform or unique, therefore the upper limit of object permanence observed was Stage 5b. Lemur species in this study eat stationary foods and are not subject to stalking predators, thus Stage 5 object permanence is probably sufficient to solve most problems encountered in the wild.     

Object permanence in five-month-old infants

A new method was devised to test object permanence in young infants. Five- month-old infants were habituated to a screen that moved back and forth through a 180-degree arc, in the manner of a drawbridge. After infants reached habituation, a box was centered behind the screen. Infants were shown two test events: a possible event and an impossible event. In the possible event, the screen stopped when it reached the occluded box; in the impossible event, the screen moved through the space occupied by the box. The results indicated that infants looked reliably longer at the impossible than at the possible event. This finding suggested that infants (1) understood that the box continued to exist, in its same location, after it was occluded by the screen, and (2) expected the screen to stop against the occluded box and were surprised, or puzzled, when it failed to do so. A control experiment in which the box was placed next to the screen provided support for this interpretation of the results. Together, the results of these experiments indicate that, contrary to Piaget's (1954) claims, infants as young as 5 months of age understand that objects continue to exist when occluded. The results also indicate that 5-month-old infants realize that solid objects do not move through the space occupied by other solid objects.     

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.     

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.     

Object permanence in dogs: Invisible displacement in a rotation task

Dogs were tested for object permanence using an invisible displacement in which an object was hidden in one of two containers at either end of a beam and the beam was rotated. Consistent with earlier research, when the beam was rotated 180°, the dogs failed to find the object. However, when the beam was rotated only 90°, they were successful. Furthermore, when the dogs were led either 90° or 180° around the apparatus, they were also successful. In a control condition, when the dogs could not see the direction of the 90° rotation, they failed to find the object. The results suggest that the 180° rotation may produce an interfering context that can be reduced by rotating the apparatus only 90° or by changing the dogs’ perspective. Once the conflict is eliminated, dogs show evidence of object permanence that includes invisibly displaced objects.     

Object permanence in cats (Felis catus): an ecological approach to the study of invisible displacements.

A single invisible displacement object permanence task was administered to 19 cats (Felis catus). In this task, cats watched a target object from behind a transparent panel. However, cats had to walk around an opaque panel to reach the object. While cats were behind the opaque panel, the object was hidden behind one of two screens. As cats did not perceive the disappearance of the object behind the target screen, the object was invisibly hidden. Results showed that cats solved this task with great flexibility, which markedly contrasts with what has been observed in previous research. The discussion emphasizes the difference between the typical Piagetian task in which the information necessary to succeed must be dealt with in retrospective way, whereas in our task cats had to anticipate a new position of the object. The ecological relevance of this new task is also discussed.     

Object permanence in orangutans (Pongo pygmaeus), chimpanzees (Pan troglodytes), and children (Homo sapiens).

Juvenile and adult orangutans (n = 5; Pongo pygmaeus), chimpanzees (n = 7; Pan troglodytes), and 19- and 26-month-old children (n = 24; Homo sapiens) received visible and invisible displacements. Three containers were presented forming a straight line, and a small box was used to displace a reward under them. Subjects received 3 types of displacement: single (the box visited 1 container), double adjacent (the box visited 2 contiguous containers), and double nonadjacent (the box visited 2 noncontiguous containers). All species performed at comparable levels, solving all problems except the invisible nonadjacent displacements. Visible displacements were easier than invisible, and single were easier than double displacements. In a 2nd experiment, subjects saw the baiting of either 2 adjacent or 2 nonadjacent containers with no displacements. All species selected the empty container more often when the baited containers were nonadjacent than when they were adjacent. It is hypothesized that a response bias and inhibition problem were responsible for the poor performance in nonadjacent displacements.     

Recognition of a 3D snake model and its 2D photographic image by captive black tufted-ear marmosets (Callithrix penicillata)

Two-dimensional (2D) displays of real three-dimensional (3D) objects are frequently used experimental tools in animal studies. Whether marmoset monkeys, with their highly diverse and complex anti-predation strategies, readily recognized 2D representations of potential threats has yet to be determined, as seen in other primates. Thus, the behavioral responses of adult captive black tufted-ear marmosets (Callithrix penicillata) toward an unfamiliar motionless snake-model and its photograph were assessed. Pictorially naïve subjects were randomly divided into two groups (n = 12/each) and submitted to two trials. Group 1 was initially exposed to the 3D object and after 1 week to its photograph. Group 2 was first presented the picture and only tested with the real object 1 week later. All 15-min trials were divided into three consecutive 5-min intervals: pre-exposure, exposure and post-exposure. In the presence of the 3D snake object, regardless of its presentation order, the frequency of direct gazes, head-cocks, tsik-tsik alarm/mobbing calls and genital displays increased significantly. The photograph induced a similar response, although only when the object had been previously presented, as significantly higher levels of these behaviors were seen in Group 1 than Group 2. Proximity to the stimulus, aerial scan, terrestrial glance, displacement activities and locomotion were not consistently influenced by the stimuli’s presence and/or order of presentation. Therefore, marmosets recognized and responded appropriately to biologically and emotionally relevant 3D and 2D stimuli. Since the aversive/fearful reactions toward the photograph were only seen after the snake object had been presented, the former seems to be essentially a learned response.     

Development of object permanence in food-storing magpies (Pica pica)

The development of object permanence was investigated in black-billed magpies (Pica pica), a food-storing passerine bird. The authors tested the hypothesis that food-storing development should be correlated with object-permanence development and that specific stages of object permanence should be achieved before magpies become independent. As predicted, Piagetian Stages 4 and 5 were reached before independence was achieved, and the ability to represent a fully hidden object (Piagetian Stage 4) emerged by the age when magpies begin to retrieve food. Contrary to psittacine birds and humans, but as in dogs and cats, no "A-not-B error" occurred. Although magpies also mastered 5 of 6 invisible displacement tasks, evidence of Piagetian Stage 6 competence was ambiguous.