Rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) succeed on a computerized test designed to assess conservation of discrete quantity

Conservation of quantity occurs through recognition that changes in the physical arrangement of a set of items do not change the quantity of items in that set. Rhesus monkeys (Macaca mulatta) were presented with a computerized quantity judgment task. Monkeys were rewarded for selecting the greater quantity of items in one of two horizontal arrays of items on the screen. On some trials, after a correct selection, no reward was given but one of the arrays was manipulated. In some cases, this manipulation involved moving items closer together or farther apart to change the physical arrangement of the array without changing 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 another selection from the two rows of items. Monkeys were sensitive to these manipulations, changing their selections when the number of items in the rows changed but not when the arrangement only was changed. Therefore, monkeys responded on the basis of the quantity of items, and they were not distracted by non-quantitative manipulations of the sets.Electronic Supplementary Material Supplementary material is available for this article at     

Monkeys (Macaca mulatta and Cebus apella) track, enumerate, and compare multiple sets of moving items

Despite many demonstrations of numerical competence in nonhuman animals, little is known about how well animals enumerate moving stimuli. In this series of experiments, rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella) performed computerized tasks in which they had to enumerate sets of stimuli. In Experiment 1, rhesus monkeys compared two sets of moving stimuli. Experiment 2 required comparisons of a moving set and a static set. Experiment 3 included human participants and capuchin monkeys to assess all 3 species' performance and to determine whether responding was to the numerical properties of the stimulus sets rather than to some other stimulus property such as cumulative area. Experiment 4 required both monkey species to enumerate subsets of each moving array. In all experiments, monkeys performed above chance levels, and their responses were controlled by the number of items in the arrays as opposed to nonnumerical stimulus dimensions. Rhesus monkeys performed comparably to adult humans when directly compared although capuchin performance was lower.     

Delaying gratification for food and tokens in capuchin monkeys (Cebus apella) and chimpanzees (Pan troglodytes): when quantity is salient, symbolic stimuli do not improve performance

Capuchin monkeys have been tested for the capacity to delay gratification for accumulating rewards in recent studies and have exhibited variable results. Meanwhile, chimpanzees have consistently excelled at this task. However, neither species have ever been tested at accumulating symbolic tokens instead of food items, even though previous reports indicate that tokens sometimes facilitate performance in other self-control tasks. Thus, in the present study, we tested capuchin monkeys and chimpanzees for their capacity to delay gratification in a delay maintenance task, in which an experimenter presented items, one at a time, to within reach of an animal for as long as the animal refrained from taking them. In Experiment 1, we assessed how long capuchin monkeys could accumulate items in the delay maintenance task when items were food rewards or tokens exchangeable for food rewards. Monkeys accumulated more food rewards than they did tokens. In Experiment 2, we tested capuchin monkeys and chimpanzees in a similar accumulation test. Whereas capuchins again accumulated more food than tokens, all chimpanzees but one showed no difference in performance in the two conditions. These findings provide additional evidence that chimpanzees exhibit greater self-control capacity in this task than do capuchin monkeys and indicate that symbolic stimuli fail to facilitate delay maintenance when they do not abstract away from the quantitative dimension of the task. This is consistent with previous findings on the effects of symbols on self-control and illuminates what makes accumulation a particularly challenging task.     

Quantity judgments of sequentially presented food items by capuchin monkeys (Cebus apella)

Recent assessments have shown that capuchin monkeys, like chimpanzees and other Old World primate species, are sensitive to quantitative differences between sets of visible stimuli. In the present study, we examined capuchins’ performance in a more sophisticated quantity judgment task that required the ability to form representations of food quantities while viewing the quantities only one piece at a time. In three experiments, we presented monkeys with the choice between two sets of discrete homogeneous food items and allowed the monkeys to consume the set of their choice. In Experiments 1 and 2, monkeys compared an entirely visible food set to a second set, presented item-by-item into an opaque container. All monkeys exhibited high accuracy in choosing the larger set, even when the entirely visible set was presented last, preventing the use of one-to-one item correspondence to compare quantities. In Experiment 3, monkeys compared two sets that were each presented item-by-item into opaque containers, but at different rates to control for temporal cues. Some monkeys performed well in this experiment, though others exhibited near-chance performance, suggesting that this species’ ability to form representations of food quantities may be limited compared to previously tested species such as chimpanzees. Overall, these findings support the analog magnitude model of quantity representation as an explanation for capuchin monkeys’ quantification of sequentially presented food items.

How do tufted capuchin monkeys (Cebus apella) understand causality involved in tool use?

Four tufted capuchin monkeys (Cebus apella) were trained to choose from 2 hook-like tools, 1 of which successfully led to collecting food, whereas the other did not because of inappropriate spatial arrangement of the tool and the food. In Experiment 1, all of the monkeys successfully learned the basic task. The monkeys performed successfully with tools of novel colors and shapes in Experiments 2-5. These results demonstrate that the monkeys used the spatial arrangement of the tool and the food as a cue. However, they failed when there were obstacles (Experiment 6) or traps (Experiment 7) on the path along which the monkeys dragged tools. These results may suggest that capuchin monkeys understand the spatial relationship between 2 items, namely, food and the tool, but do not understand the spatial relationship among 3 items, namely, food, tool, and the environmental condition. The possible role of stimulus generalization is also considered.     

Auditory--visual cross-modal perception of communicative stimuli in tufted capuchin monkeys (Cebus apella)

Research on cross-modal performance in nonhuman primates is limited to a small number of sensory modalities and testing methods. To broaden the scope of this research, the authors tested capuchin monkeys (Cebus apella) for a seldom-studied cross-modal capacity in nonhuman primates, auditory-visual recognition. Monkeys were simultaneously played 2 video recordings of a face producing different vocalizations and a sound recording of 1 of the vocalizations. Stimulus sets varied from naturally occurring conspecific vocalizations to experimentally controlled human speech stimuli. The authors found that monkeys preferred to view face recordings that matched presented vocal stimuli. Their preference did not differ significantly across stimulus species or other stimulus features. However, the reliability of the latter set of results may have been limited by sample size. From these results, the authors concluded that capuchin monkeys exhibit auditory-visual cross-modal perception of conspecific vocalizations.     

Self-control and tool use in tufted capuchin monkeys (Cebus apella)

Self-control is defined as forgoing immediate gratification to obtain a greater reward. Tool use may relate to self-control because both behaviors may require foresight and deliberate control over one's actions. The authors assessed 20 capuchin monkeys (Cebus apella) for the ability to delay gratification in a tool task. Subjects were given rod-shaped food items that could either be consumed immediately or be carried to an apparatus and used to extract a more preferred food. The authors found that some monkeys were able to exhibit self-control. Monkeys with relatively more tool use experience demonstrated the greatest levels of self-control. These results indicate that capuchins are capable of delaying gratification when a higher quality reinforcer is present and that tool experience can influence levels of self-control in this task.     

Weber's Law influences numerical representations in rhesus macaques (Macaca mulatta)

We present the results of two experiments that probe the ability of rhesus macaques to match visual arrays based on number. Three monkeys were first trained on a delayed match-to-sample paradigm (DMTS) to match stimuli on the basis of number and ignore continuous dimensions such as element size, cumulative surface area, and density. Monkeys were then tested in a numerical bisection experiment that required them to indicate whether a sample numerosity was closer to a small or large anchor value. Results indicated that, for two sets of anchor values with the same ratio, the probability of choosing the larger anchor value systematically increased with the sample number and the psychometric functions superimposed. A second experiment employed a numerical DMTS task in which the choice values contained an exact numerical match to the sample and a distracter that varied in number. Both accuracy and reaction time were modulated by the ratio between the correct numerical match and the distracter, as predicted by Weber's Law.     

Identity concept learning in matching-to-sample tasks by tufted capuchin monkeys (Cebus apella)

The abstract concept of equivalence is considered one of the bases of higher-order cognition, and it has been the subject of considerable research in comparative cognition. This study examined the conditions under which tufted capuchin monkeys (Cebus apella) are able to acquire an identity concept. Six capuchin monkeys were trained to solve a visual matching-to-sample (MTS) task on the basis of perceptual identity. The acquisition of the identity rule was inferred from the subject’s ability to solve transfer tests with novel stimuli. We evaluated the ability of the capuchin monkeys to match the shape of novel stimuli after training with both several small stimulus sets (Experiment 1) and a large stimulus set (Experiment 2). Moreover, we examined the ability of capuchins to transfer the concept to novel visual dimensions, such as colour and size and to transfer to novel spatial arrangements of the stimuli (Experiment 2). We demonstrated that the ability of capuchins to match novel stimuli was improved by increasing the number of stimuli used during training (Experiments 1 and 2) and that after a widely applicable identity concept based on the stimulus shape was acquired, the capuchins were able to match stimuli according to an identity rule based on both the colour and size of the stimuli and when the spatial arrangement of the stimuli was varied (Experiment 2). This study is the first to demonstrate that the size of the training set affects the acquisition of an abstract identity concept in an MTS task in non-human primates.     

Capuchin monkeys (Cebus apella) let lesser rewards pass them by to get better rewards

Self-control is defined as foregoing an immediate reward to gain a larger delayed reward. Methods used to test self-control comparatively include inter-temporal choice tasks, delay of gratification tasks, and accumulation tasks. To date, capuchin monkeys have shown different levels of self-control across tasks. This study introduced a new task that could be used comparatively to measure self-control in an intuitive context that involved responses that required no explicit training. Capuchin monkeys (Cebus apella) were given a choice between two food items that were presented on a mechanized, revolving tray that moved those foods sequentially toward the monkeys. A monkey could grab the first item or wait for the second, but was only allowed one item. Most monkeys in the study waited for a more highly preferred food item or a larger amount of the same food item when those came later, and they inhibited the prepotent response to grab food by not reaching out to take less-preferred foods or smaller amounts of food that passed directly in front of them first. These data confirm that the mechanisms necessary for self-control are present in capuchin monkeys and indicate that the methodology can be useful for broader comparative assessments of self-control.     

Generalization hypothesis of abstract-concept learning: learning strategies and related issues in Macaca mulatta, Cebus apella, and Columba livia

The generalization hypothesis of abstract-concept learning was tested with a meta-analysis of rhesus monkeys (Macaca mulatta), capuchin monkeys (Cebus apella), and pigeons (Columba livia) learning a same/different (S/D) task with expanding training sets. The generalization hypothesis states that as the number of training items increases, generalization from the training pairs will increase and could explain the subjects' accurate novel-stimulus transfer. By contrast, concept learning is learning the relationship between each pair of items; with more training items subjects learn more exemplars of the rule and transfer better. Having to learn the stimulus pairs (the generalization hypothesis) would require more training as the set size increases, whereas learning the concept might require less training because subjects would be learning an abstract rule. The results strongly support concept or rule learning despite severely relaxing the generalization-hypothesis parameters. Thus, generalization was not a factor in the transfer from these experiments, adding to the evidence that these subjects were learning the S/D abstract concept.     

Improving arithmetic performance with number sense training: An investigation of underlying mechanism

A nonverbal primitive number sense allows approximate estimation and mental manipulations on numerical quantities without the use of numerical symbols. In a recent randomized controlled intervention study in adults, we demonstrated that repeated training on a non-symbolic approximate arithmetic task resulted in improved exact symbolic arithmetic performance, suggesting a causal relationship between the primitive number sense and arithmetic competence. Here, we investigate the potential mechanisms underlying this causal relationship. We constructed multiple training conditions designed to isolate distinct cognitive components of the approximate arithmetic task. We then assessed the effectiveness of these training conditions in improving exact symbolic arithmetic in adults. We found that training on approximate arithmetic, but not on numerical comparison, numerical matching, or visuo-spatial short-term memory, improves symbolic arithmetic performance. In addition, a second experiment revealed that our approximate arithmetic task does not require verbal encoding of number, ruling out an alternative explanation that participants use exact symbolic strategies during approximate arithmetic training. Based on these results, we propose that nonverbal numerical quantity manipulation is one key factor that drives the link between the primitive number sense and symbolic arithmetic competence. Future work should investigate whether training young children on approximate arithmetic tasks even before they solidify their symbolic number understanding is fruitful for improving readiness for math education.     

Token mediated tool exchange between tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Three experiments were conducted to test whether a pair of tufted capuchin monkeys (Cebus apella) could generalize their ability to exchange tokens and tool objects with a human experimenter to similar exchanges with a conspecific partner. Monkeys were tested in side-by-side enclosures, one enclosure containing a tool-use apparatus and one or more token(s), and the other enclosure containing one or more tool object(s). The monkeys willingly transferred tokens and tools to a conspecific with little practice. Following a small amount of training, we also found that the monkeys would select situation-appropriate tokens to exchange for specific tools, but did not select appropriate tool objects in response to another monkey’s token transfers. Implications regarding role reversal are discussed.     

Cooperative problem solving by tufted capuchin monkeys (Cebus apella): spontaneous division of labor, communication, and reciprocal altruism

Using an experimentally induced cooperation task, the authors investigated whether tufted capuchin monkeys (Cebus apella) share the following 3 characteristics of cooperation with humans: division of labor, communication, and reciprocal altruism. In Experiment 1, the authors trained individual monkeys to perform the necessary sequence of actions for rewards and tested them in pairs to assess whether they could solve the task by spontaneously dividing the sequence of actions. All pairs solved this task. In Experiment 2, monkeys worked in the cooperation task and a task requiring no partner help. They looked at the partner significantly longer in the former task than in the latter, but communicative intent could not be determined. In Experiment 3, only 1 of 2 participants obtained a reward on each trial. Monkeys maintained cooperation when their roles were reversed on alternate trials. Their cooperative performances demonstrated division of labor; results suggest task-related communication and reciprocal altruism.     

Nonverbal estimation during numerosity judgements by adult humans

On an automated task, humans selected the larger of two sets of items, each created through the one-by-one addition of items. Participants repeated the alphabet out loud during trials so that they could not count the items. This manipulation disrupted counting without producing major effects on other cognitive capacities such as memory or attention, and performance of this experimental group was poorer than that of participants who counted the items. In Experiment 2, the size of individual items was varied, and performance remained stable when the larger numerical set contained a smaller total amount than the smaller numerical set (i.e., participants used numerical rather than nonnumerical quantity cues in making judgements). In Experiment 3, reports of the number of items in a single set showed scalar variability as accuracy decreased, and variability in responses increased with increases in true set size. These data indicate a mechanism for the approximate representation of numerosity in adult humans that might be shared with nonhuman animals.     

Nonverbal estimation during numerosity judgements by adult humans

On an automated task, humans selected the larger of two sets of items, each created through the one-by-one addition of items. Participants repeated the alphabet out loud during trials so that they could not count the items. This manipulation disrupted counting without producing major effects on other cognitive capacities such as memory or attention, and performance of this experimental group was poorer than that of participants who counted the items. In Experiment 2, the size of individual items was varied, and performance remained stable when the larger numerical set contained a smaller total amount than the smaller numerical set (i.e., participants used numerical rather than nonnumerical quantity cues in making judgements). In Experiment 3, reports of the number of items in a single set showed scalar variability as accuracy decreased, and variability in responses increased with increases in true set size. These data indicate a mechanism for the approximate representation of numerosity in adult humans that might be shared with nonhuman animals.     

Quantity estimation and comparison in western lowland gorillas (Gorilla gorilla gorilla)

We investigated the quantity judgment abilities of two adult male western lowland gorillas (Gorilla gorilla gorilla) by presenting discrimination tasks on a touch-screen computer. Both gorillas chose the larger quantity of two arrays of dot stimuli. On some trials, the relative number of dots was congruent with the relative total area of the two arrays. On other trials, number of dots was incongruent with area. The gorillas were first tested with static dots, then with dots that moved within the arrays, and finally on a task where they were required to discriminate numerically larger subsets within arrays of moving dots. Both gorillas achieved above-chance performance on both congruent and incongruent trials with all tasks, indicating that they were able to use number as a cue even though ratio of number and area significantly controlled responding, suggesting that number was not the only relevant dimension that the gorillas used. The pattern of performance was similar to that found previously with monkeys and chimpanzees but had not previously been demonstrated in gorillas within a computerized test format, and with these kinds of visual stimuli.     

An assessment of memory awareness in tufted capuchin monkeys (Cebus apella)

Humans, apes, and rhesus monkeys demonstrate memory awareness by collecting information when ignorant and acting immediately when informed. In this study, five capuchin monkeys searched for food after either watching the experimenter bait one of four opaque tubes (seen trials), or not watching (unseen trials). Monkeys with memory awareness should look into the tubes before making a selection only on unseen trials because on seen trials they already know the location of the food. In Experiment 1, one of the five capuchins looked significantly more often on unseen trials. In Experiment 2, we ensured that the monkeys attended to the baiting by interleaving training and test sessions. Three of the five monkeys looked more often on unseen trials. Because monkeys looked more often than not on both trial types, potentially creating a ceiling effect, we increased the effort required to look in Experiment 3, and predicted a larger difference in the probability of looking between seen and unseen trials. None of the five monkeys looked more often on unseen trials. These findings provide equivocal evidence for memory awareness in capuchin monkeys using tests that have yielded clear evidence in humans, apes, and rhesus monkeys.     

Quantity representation in children and rhesus monkeys: linear versus logarithmic scales

The performances of 4- and 5-year-olds and rhesus monkeys were compared using a computerized task for quantity assessment. Participants first learned two quantity anchor values and then responded to intermediate values by classifying them as similar to either the large anchor or the small anchor. Of primary interest was an assessment of where the point of subjective equality (PSE) occurred for each species across four different sets of anchors to determine whether the PSE occurred at the arithmetic mean or the geometric mean. Both species produced PSEs that were closer to the geometric mean for three of four anchor sets. This indicates that monkeys and children access either a logarithmic scale for quantity representation or a linear scale that is subject to scalar variability, both of which are consistent with Weber's law and representation of quantity that takes the form of analog magnitudes.     

Attention allocation modulates the processing of hierarchical visual patterns: a comparative analysis of capuchin monkeys (Cebus apella) and humans

Humans show a global advantage when processing hierarchical visual patterns, and they detect the global level of stimulus structure more accurately and faster than the local level in several stimulus contexts. By contrast, capuchins (Cebus apella) and other monkey species show a strong local advantage. A key factor which, if manipulated, could cause an inversion of this effect in monkeys is still to be found. In this study, we examined whether it was possible to induce attention allocation to global and local levels of perceptual analysis in capuchin monkeys and if by doing so, their local dominance could be reversed. We manipulated attentional bias using a matching-to-sample (MTS) task where the proportion of trials requiring global and local processing varied between conditions. The monkeys were compared with humans tested with the same paradigm. Monkeys showed a local advantage in the local bias condition but a global advantage in the global bias condition. The role of attention in processing was confined to the local trials in a first phase of testing but extended to both local and global trials in the course of task practice. Humans exhibited an overall global dominance and an effect of attentional bias on the speed of processing of the global and local level of the stimuli. These results indicate a role for attention in the processing of hierarchical stimuli in monkeys and are discussed in relation to the extent to which they can explain the differences between capuchin monkeys and humans observed in this and other studies.