Capuchin monkeys (Cebus apella) respond to video images of themselves

Many studies have used mirror-image stimulation in attempts to find self-recognition in monkeys. However, very few studies have presented monkeys with video images of themselves; the present study is the first to do so with capuchin monkeys. Six tufted capuchin monkeys were individually exposed to live face-on and side-on video images of themselves (experimental Phase 1). Both video screens initially elicited considerable interest. Two adult males looked preferentially at their face-on image, whereas two adult females looked preferentially at their side-on image; the latter elicited lateral movements and head-cocking. Only males showed communicative facial expressions, which were directed towards the face-on screen. In Phase 2 monkeys discriminated between real-time, face-on images and identical images delayed by 1 s, with the adult females especially preferring real-time images. In this phase both screens elicited facial expressions, shown by all monkeys. In Phase 3 there was no evidence of discrimination between previously recorded video images of self and similar images of a familiar conspecific. Although they showed no signs of explicit self-recognition, the monkeys’ behaviour strongly suggests recognition of the correspondence between kinaesthetic information and external visual effects. In species such as humans and great apes, this type of self-awareness feeds into a system that gives rise to explicit self-recognition.     

Concept learning by monkeys with video picture images and a touch screen.

Two rhesus monkeys were trained in a same/different task to discriminate digitized computer-stored picture stimuli. The pictures were digitized from 35-mm slides and presented in pairs on a computer monitor. The monkeys were required to touch the pictures and then make a choice response to indicate whether the pictures were identical or nonidentical. The response areas and stimuli were located to the sides of the picture stimuli. Responses were defined and monitored by an infrared matrix touch screen. After learning the same/different task, both monkeys showed performance accuracy with novel picture stimuli similar to that with training picture stimuli. This accurate novel-picture transfer indicates that a same/different concept had been learned, a concept similar to the one they had previously demonstrated in a different apparatus with rear-projected slide stimuli and a response lever.     

Experimental evidence for route integration and strategic planning in wild capuchin monkeys

Both in captivity and the wild, primates are found to travel mostly to the nearest available resource, but they may skip over the closest resource and travel to more distant resources, which are often found to be more productive. This study examines the tradeoff between distance and reward in the foraging choices of one group of wild capuchin monkeys (Cebus apella nigritus) using feeding platforms in large-scale foraging experiments conducted over four years. Three feeding sites were arrayed in an oblique triangle, such that once the monkey group had chosen one site to feed, they had a choice between two remaining sites, a close one with less food and the other up to 2.3 times as far away but with more food. Sites were provisioned once per day. The capuchins generally chose the closer feeding site, even when the more distant site offered up to 12 times as much food. The distances to, rewards of, or various profitability measures applied to each alternative site individually did not explain the group’s choices in ways consistent with foraging theory or principles of operant psychology. The group’s site choices were predicted only by comparing efficiency measures of entire foraging pathways: (1) direct travel to the more rewarding distant site, versus (2) the longer ‘detour’ through the closer site on the way to the more distant one. The group chose the detour more often when the reward was larger and the added detour distance shorter. They appeared to be more sensitive to the absolute increase in detour distance than to the relative increase compared to the straight route. The qualitative and quantitative results agree with a simple rule: do not use the detour unless the energy gain from extra food outweighs the energy cost of extra travel. These results suggest that members of this group integrate information on spatial location, reward, and perhaps potential food competition in their choice of multi-site foraging routes, with important implications for social foraging. This contribution is part of the special issue “ A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007b).     

On loss aversion in capuchin monkeys

Chen, Lakshminarayanan, and Santos (2006) claim to show in three choice experiments that monkeys react rationally to price and wealth shocks, but, when faced with gambles, display hallmark, human-like biases that include loss aversion. We present three experiments with monkeys and humans consistent with a reinterpretation of their data that attributes their results not to loss aversion, but to differences between choice alternatives in delay of reinforcement.     

Metamemory in tufted capuchin monkeys (Cebus apella)

Whereas evidence for metacognition by nonhuman primates has been obtained in great apes and old world monkeys, it is weaker in new world monkeys. For instance, capuchin monkeys may fail to recognize their own knowledge of the location of invisible bait. In the present study, we tested whether tufted capuchin monkeys would flexibly change their behavior in a delayed matching-to-sample (DMTS) test depending upon the strength of their memory trace of the sample. In Experiment 1, two monkeys were tested on a modified 9-alternative DMTS task with various delays on a computerized display. In some trials, the monkeys could choose whether to go for a memory test or for a simple key touch as an escape from the test. In other trials, they were forced to go for the memory test. Both monkeys escaped from the memory test more often when their matching accuracy on forced tests was lower. In one of the monkeys, the matching accuracies on chosen memory tests decreased more slowly as a function of delay length, and were higher after long delays than those on forced memory tests. This suggests that at least one capuchin monkey was able to recognize the strength of his own memory trace. Experiment 2 employed occasional no-sample tests, in which the monkeys faced the task choice without presentation of any sample for the trial. The monkey who was successful in Experiment 1 declined the memory test more often in no-sample trials than regular trials, further indicating metamemory in this individual. In Experiment 3, this successful monkey received a task, in which he was sometimes able to choose between shape MTS or texture MTS tasks. However, his matching accuracies did not differ between chosen tasks and forced tasks. Thus, the metamemory possessed by this new world monkey species may be more like a flag, showing strength of memory trace, than an elaborate representation showing details of the memory trace.     

Acquisition and maintenance of delayed matching-to-sample in tufted capuchin monkeys

Delayed matching-to-sample (DMTS) is a commonly used procedure to investigate short-term memory. For the study of functions of forgetting, the delay between the disappearance of the sample stimulus and appearance of choices is manipulated. The intertrial interval (ITI) is also varied to assess interference effects. Performance decrements have been observed as delay increases and, in some cases, performance recovery occurs when ITIs are increased. Other studies indicate that the higher the ITI/delay ratio, the greater the accuracy in DMTS. In this study, 2 experiments investigated DMTS performances of 3 tufted capuchin monkeys as function of delay and ITI. In Experiment 1, alternation of gradual increases of delay and ITI was effective in producing ≥90% accuracy at delays as long as 90 s. Individual monkeys differed in the highest value of delay at which this criterion was met. In Experiment 2, the monkeys were exposed to 5-s DMTS with different ITIs to assess the effects of various ITI/delay ratios on accuracy. Highest accuracy tended to occur at the higher ITI/delay ratios.     

Observational learning of tool use in children: Investigating cultural spread through diffusion chains and learning mechanisms through ghost displays

In the first of two experiments, we demonstrate the spread of a novel form of tool use across 20 “cultural generations” of child-to-child transmission. An experimentally seeded technique spread with 100% fidelity along twice as many “generations” as has been investigated in recent exploratory “diffusion” experiments of this type. This contrasted with only a single child discovering the technique spontaneously in a comparable group tested individually without any model. This study accordingly documents children’s social learning of tool use on a new, population-level scale that characterizes real-world cultural phenomena. In a second experiment, underlying social learning processes were investigated with a focus on the contrast between imitation (defined as copying actions) and emulation (defined as learning from the results of actions only). In two different “ghost” conditions, children were presented with the task used in the first experiment but now operated without sight of an agent performing the task, thereby presenting only the information used in emulation. Children in ghost conditions were less successful than those who had watched a model in action and showed variable matching to what they had seen. These findings suggest the importance of observational learning of complex tool use through imitation rather than only through emulation. Results of the two experiments are compared with those of similar experiments conducted previously with chimpanzees and are discussed in relation to the wider perspective of human culture and the influence of task complexity on social learning.     

Capuchin monkeys (Cebus apella) succeed in a test of quantity conservation

Nonhuman animals demonstrate a number of impressive quantitative skills such as counting sets of items, comparing sets on the basis of the number of items or amount of material, and even responding to simple arithmetic manipulations. In this experiment, capuchin monkeys were presented with a computerized task designed to assess conservation of discrete quantity. Monkeys first were trained to select from two horizontal arrays of stimuli the one with the larger number of items. On some trials, after a correct selection there was no feedback but instead an additional manipulation of one of those arrays. In some cases, this manipulation involved moving items closer together or farther apart to change the physical arrangement of the array but not the quantity of items in the array. In other cases, additional items were added to the initially smaller array so that it became quantitatively larger. Monkeys then made a second selection from the two arrays of items. Previous research had shown that rhesus monkeys (Macaca mulatta) succeeded with this task. However, there was no condition in that study in which items were added to the smaller array without increasing its quantity to a point where it became the new larger array. This new condition was added in the present experiment. Capuchin monkeys were sensitive to all of these manipulations, changing their selections when the manipulations changed which array contained the larger number of items but not when the manipulations changed the physical arrangement of items or increased the quantity in one array without also reversing which of the two arrays had more items. Therefore, capuchin monkeys responded on the basis of the quantity of items, and they were not distracted by non-quantitative manipulations of the arrays. The data indicate that capuchins are sensitive to simply arithmetic manipulations that involve addition of items to arrays and also that they can conserve quantity.     

Influence of two types of information trials on the formation of a discrimination-reversal learning set in Japanese monkeys

Abstract: Three groups of male adult Japanese monkeys were trained in 30 discrimination-reversal learning-set (LS) problems using the Wisconsin General Test Apparatus. A control group ( N = 3) was trained in the standard procedure: acquisition of up to 12 consecutive correct responses, reversal to the same criterion, and then shift to a new problem. To the other two groups, three information trials signaling the stimulus value in reversal were given after they reached the criterion in acquisition. Subjects in the positive-stimulus information (PSI) group ( N = 4) were exposed only to the reversal positive stimulus, and a response to it was rewarded. Subjects in the negative-stimulus information (NSI) group ( N = 4) were exposed only to the reversal negative stimulus, and any response to it was not rewarded. Information trials reduced reversal errors and NSI trials were more effective than PSI trials in error reduction ( p < .05). Information trials also aided in acquisition: the NSI and PSI groups learned the acquisition phase of the problems with significantly fewer errors than control group ( p < .01) in the last stage of training. The implications of these results are discussed in relation to strategy learning and attention learning in LS formation.     

Note on aversion learning to the shape of food by monkeys

Vervet and grivet monkeys were repeatedly tested eating bar- and circle-shaped cookies. One subject was always injected with lithium immediately after eating cookies with the circle shape and learned to avoid the circular cookies while continuing to eat the bar-shaped cookies. Another subject received similar treatment except that lithium injections were always delayed 30 minutes after access to the circle-shaped cookies. She also acquired a discriminative aversion. Aversion learning was not observed with 60-minute delayed toxicosis or with lithium injections administered unpaired with access to the cookies. The two types of cookies differed only in shape, and conditioning and test sessions were conducted in total darkness to preclude the use of visual cues. Therefore, the avoidance observed in subjects conditioned with immediate and 30-minute delayed toxicosis represents a conditioned aversion to the shape of the cookies as revealed by tactile cues. These findings illustrate that monkeys can learn to select food on the basis of tactile stimuli when such stimuli are conditioned with delayed aversive stimulation.     

Relational and absolute stimulus learning by monkeys in a memory task.

Three experiments showed stimulus control by either the absolute properties of probe stimuli, relational properties of the probe-list relationship, or both in a serial probe recognition memory task in which a four-item memory list was followed by a single probe (test) item. In Experiment 1, 3 rhesus monkeys received 39 to 75 repetitions of the same 24-trial stimulus sequence. Special tests showed stimulus control by the absolute properties of the probe stimuli. Retention of previous relational control was demonstrated by the good transfer (83%) to novel list and probe stimuli at the beginning of Experiment 2. During Experiment 2, control by absolute properties of the probe stimuli gradually reoccurred. Only a small measure of control by list stimuli could be detected or promoted. In Experiment 3, 4 monkeys were shown to have largely lost their ability to perform on the basis of the list-probe relationship, and were performing primarily on the basis of the absolute properties of the probe stimuli. Over the next 15 weeks, these monkeys were transferred to new stimuli at the beginning of each week. Control by the relational aspects of the task gradually returned. As transfer performance increased, control by the absolute properties of the probe stimuli was eliminated. The results are discussed in terms of stimulus control and performance strategies used by the monkeys.     

Copying without rewards: socially influenced foraging decisions among brown capuchin monkeys

An individual’s foraging activity can be influenced by the choices made by nearby conspecifics. The interest shown in the location and characteristics of a feeding patch may depend on the feeding success of a conspecific there, a process that needs to be distinguished from choices guided by rewards to the observer itself. We investigated how rewards for both self and others influence the foraging choices of captive capuchin monkeys (Cebus apella). Thirteen adult capuchins observed familiar female conspecific models explore one of three opaque boxes under three conditions. In the first, there were no rewards available to either monkey; in the second, rewards were available to the model only; and in the third, both monkeys could retrieve a reward. Under all conditions, subjects more often explored the same box as the model than was expected by chance. Thus, without ever receiving a reward themselves or without seeing another receive rewards, subjects’ searches were directed at the box explored by another monkey. The tendency to match the model’s choice increased if the subject was rewarded. We compared these results to control conditions in which the model was either absent, or present but not allowed to demonstrate. Subjects’ located the reward less often in control conditions, than in the experimental conditions. We conclude that extrinsic rewards, while helpful, are not required for partners to influence the foraging choices of capuchins, and that the unrewarded copying of foraging choices demonstrated here may provide the basis for additional social influences on learning. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007)     

Experimental field study of hand preference in wild black-horned (<Emphasis Type="Italic">Cebus nigritus</Emphasis>) and white-faced (<Emphasis Type="Italic">Cebus capucinus</Emphasis>) capuchins: evidence for individual and species differences

In this experimental field investigation, we compare the degree to which wild capuchins in Brazil (Cebus nigritus) and Costa Rica (Cebus capucinus) exhibit individual- and population-level handedness during three visually-guided tasks. These tasks required reaching to remove a large leaf covering a hidden food reward, seizing the food reward, and manipulating a tool (pulling a wooden dowel) in order to obtain access to an embedded food reward. Studies in some populations of captive capuchins indicate evidence for both individual hand preferences and population-level handedness. In this study, six of eight wild C. capucinus and six of seven wild C. nigritus exhibited a significant hand preference during individual tasks, but no individual exhibited a consistent preference across all three tasks. Task-specialization, or the tendency for most individuals in the same group or population to use the same hand to accomplish a particular task, also was evaluated. Cebus nigritus showed a significant bias toward the use of the right hand in removing the leaf. Although the number of individual capuchins in both species that manipulated the dowels was limited (N = 7), each individual that manipulated the dowels in eight or more instances had a positive handedness index, suggesting a greater use of the right hand to accomplish this task. Overall, our results provide preliminary support for individual- and population-level handedness in wild capuchin monkeys.     

Rhesus monkeys lack a consistent peak-end effect

In humans, the order of receiving sequential rewards can significantly influence the overall subjective utility of an outcome. For example, people subjectively rate receiving a large reward by itself significantly higher than receiving the same large reward followed by a smaller one (Do, Rupert, & Wolford, 2008). This result is called the peak-end effect. A comparative analysis of order effects can help determine the generality of such effects across primates, and we therefore examined the influence of reward-quality order on decision making in three rhesus macaque monkeys (Macaca mulatta). When given the choice between a high–low reward sequence and a low–high sequence, all three monkeys preferred receiving the high-value reward first. Follow-up experiments showed that for two of the three monkeys their choices depended specifically on reward-quality order and could not be accounted for by delay discounting. These results provide evidence for the influence of outcome order on decision making in rhesus monkeys. Unlike humans, who usually discount choices when a low-value reward comes last, rhesus monkeys show no such peak-end effect.     

Effective use of the blank comparison procedure in simple discrimination by infant capuchin monkeys: A methodological note

In studies of simple and conditional discrimination, procedures are needed to measure those aspects of stimuli that control behavior. The blank comparison procedure is one such procedure. It was designed explicitly for assessing S+ and S- functions when discriminative stimuli are presented simultaneously. In this procedure, a neutral stimulus serves sometimes as S+ and sometimes as S-. Its discriminative function is defined in relation to other stimuli in the display. The present study aimed to prepare 2 infant female capuchin monkeys for the effective use of the blank comparison procedure in a simple discrimination task. First, simple discrimination training was applied up to a stable accuracy criterion of ≥90%. This training was followed by the replacement of S+ and then of S- stimuli with new stimuli. Ultimately, trials with the blank comparison were introduced. Following this sequence, both monkeys immediately displayed highly accurate blank-comparison performances without the need for stimulus control shaping or other preparatory discrimination training. Thus, this procedure sequence may be an efficient, effective method for establishing blank-comparison baselines for experimental analyses of S+/S- discriminative functions and perhaps for other applications in teaching simple and conditional discrimination performances to this species and others.     

Observational learning from tool using models by human-reared and mother-reared capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Studies of wild capuchins suggest an important role for social learning, but experiments with captive subjects have generally not supported this. Here we report social learning in two quite different populations of capuchin monkeys (Cebus apella). In experiment 1, human-raised monkeys observed a familiar human model open a foraging box using a tool in one of two alternative ways: levering versus poking. In experiment 2, mother-raised monkeys viewed similar techniques demonstrated by monkey models. A control group in each population saw no model. In both experiments, independent coders detected which technique experimental subjects had seen, thus confirming social learning. Further analyses examined fidelity of copying at three levels of resolution. The human-raised monkeys exhibited fidelity at the highest level, the specific tool use technique witnessed. The lever technique was seen only in monkeys exposed to a levering model, by contrast with controls and those witnessing poke. Mother-reared monkeys instead typically ignored the tool and exhibited fidelity at a lower level, tending only to re-create whichever result the model had achieved by either levering or poking. Nevertheless this level of social learning was associated with significantly greater levels of success in monkeys witnessing a model than in controls, an effect absent in the human-reared population. Results in both populations are consistent with a process of canalization of the repertoire in the direction of the approach witnessed, producing a narrower, socially shaped behavioural profile than among controls who saw no model. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Object retrieval through observational learning in 8- to 18-month-old infants

Observational learning was studied in 8-, 10-, 12-, 15- and 18-month-old infants. Using object-retrieval tasks of relatively comparable difficulty for each age group, we showed that between 10 and 12 months there is a change in the capacity to learn a new skill by observation.     

Contexts of a person's prior intentions facilitate observational learning in 2.5-year-old children

We examined whether contexts suggesting an actor's prior intentions facilitate observational learning in 2.5-year-olds. In Experiment 1, children observed an experimenter handle one box before proceeding to open a second box. In two prior intention conditions, children either watched the experimenter extract a toy from the first box or saw that the box had already been opened. In two no prior intention conditions, children watched the demonstration with only the second box or paired with irrelevant actions upon the first box. Children successfully opened the second box more often in the two prior intention conditions than in the two no prior intention conditions. Experiment 2 investigated stimulus generalization as another explanation for these results. A functionally different trap-tube task served as the pre-demonstration apparatus. Before watching the experimenter open the box, children either saw her extract a toy from the tube with a stick or observed the toy accidentally fall from the opening. In both cases, children opened the box at similar high rates. We discuss children's use of others’ prior intentions or observable outcomes in observational learning.     

Humour production may enhance observational learning of a new tool-use action in 18-month-old infants

Many studies have shown that making children laugh enhances certain cognitive capacities such as attention, motivation, perception and/or memory, which in turn enhance learning. However, no study thus far has investigated whether laughing has an effect on learning earlier in infancy. The goal of this study was to see whether using humour with young infants in a demonstration of a complex tool-use task can enhance their learning. Fifty-three 18-month-old infants participated in this study and were included either in a humorous or a control demonstration group. In both groups infants observed an adult using a tool to retrieve an out-of-reach toy. What differed between groups was that in the humorous demonstration group, instead of playing with the toy, the adult threw it on the floor immediately after retrieval. The results show that infants who laughed at the demonstration in the humorous demonstration group reproduced significantly more frequent target actions than infants who did not laugh and those in the control group. This effect is discussed with regard to individual differences in terms of temperament and social capacities as well as positive emotion and dopamine release.