I know you are not looking at me: capuchin monkeys’ (<Emphasis Type="Italic">Cebus apella</Emphasis>) sensitivity to human attentional states

The present study asked whether capuchin monkeys recognize human attentional states. The monkeys requested food from the experimenter by extending an arm (pointing) toward the baited one of two transparent cups. On regular trials the experimenter gave the food immediately to the monkeys upon pointing but on randomly inserted test trials she ignored the pointing for 5 s during which she displayed different attentional states. The monkeys looked at the experimenter's face longer when she looked at the monkeys than when she looked at the ceiling in Experiment 1, and longer when she oriented her head midway between the two cups with eyes open than when she did so with eyes closed in Experiment 2. However, the monkeys showed no differential pointing in these conditions. These results suggest that capuchins are sensitive to eye direction but this sensitivity does not lead to differential pointing trained in laboratory experiments. Furthermore, to our knowledge, this is the first firm behavioral evidence that non-human primates attend to the subtle states of eyes in a food requesting task.     

Monkeys fail to reciprocate in an exchange task

Exchanges form the basis of human economies. Animals too can engage in reciprocal interactions but they do not barter goods like humans, which raises the question of the abilities necessary for trading to occur. Previous studies have shown that non-human primates can exchange food with human partners. Here, we tested the ability of brown capuchin monkeys and Tonkean macaques to reciprocate in a task requiring two conspecifics to exchange tokens in order to obtain rewards from an experimenter. We recorded 56 transfers between subjects in capuchin monkeys and 10 in Tonkean macaques. All transfers were passive in both species. Capuchins preferentially picked up tokens valuable for them in the partner’s compartment. They tended to manipulate the partner-valued tokens more often than the no-value ones, leading to more opportunities for these tokens to end up within reach of the partner. Despite optimal conditions where values of goods were defined and known by partners, however, none of the pairs tested engaged in short-term reciprocal interactions. These results indicate that calculated reciprocity was difficult if not impossible in the animals tested.     

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.     

Capuchin monkeys (Cebus apella) are sensitive to others’ reward: an experimental analysis of food-choice for conspecifics

The issue whether non-human primates have other-regarding preference and/or inequity aversion has been under debate. We investigated whether tufted capuchin monkeys are sensitive to others’ reward in various experimental food sharing settings. Two monkeys faced each other. The operator monkey chose one of two food containers placed between the participants, each containing a food item for him/herself and another for the recipient. The recipient passively received either high- or low-value food depending on the operator’s choice, whereas the operator obtained the same food regardless of his/her choice. The recipients were either the highest- or lowest-ranking member of the group, and the operators were middle-ranking. In Experiment 1, the operators chose the high-value food for the subordinate recipient more frequently than when there was no recipient, whereas they were indifferent in their choice for the dominant. This differentiated behavior could have been because the dominant recipient frequently ate the low-value food. In Experiment 2, we increased the difference in the value of the two food items so that both recipients would reject the low-value food. The results were the same as in Experiment 1. In Experiment 3, we placed an opaque screen in front of the recipient to examine effects of visual contact between the participants. The operators’ food choice generally shifted toward providing the low-value food for the recipient. These results suggest that capuchins are clearly sensitive to others’ reward and that they show other-regarding preference or a form of inequity aversion depending upon the recipients and the presence of visual contact.     

Olive baboons communicate intentionally by pointing

A pointing gesture creates a referential triangle that incorporates distant objects into the relationship between the signaller and the gesture’s recipient. Pointing was long assumed to be specific to our species. However, recent reports have shown that pointing emerges spontaneously in captive chimpanzees and can be learned by monkeys. Studies have demonstrated that both human children and great apes use manual gestures (e.g. pointing), and visual and vocal signals, to communicate intentionally about out-of-reach objects. Our study looked at how monkeys understand and use their learned pointing behaviour, asking whether it is a conditioned, reinforcement-dependent response or whether monkeys understand it to be a mechanism for manipulating the attention of a partner (e.g. a human). We tested nine baboons that had been trained to exhibit pointing, using operant conditioning. More specifically, we investigated their ability to communicate intentionally about the location of an unreachable food reward in three contexts that differed according to the human partner’s attentional state. In each context, we quantified the frequency of communicative behaviour (auditory and visual signals), including gestures and gaze alternations between the distal food and the human partner. We found that the baboons were able to modulate their manual and visual communicative signals as a function of the experimenter’s attentional state. These findings indicate that monkeys can intentionally produce pointing gestures and understand that a human recipient must be looking at the pointing gesture for them to perform their attention-directing actions. The referential and intentional nature of baboons’ communicative signalling is discussed.     

The origins of belief representation: Monkeys fail to automatically represent others’ beliefs

Young infants’ successful performance on false belief tasks has led several researchers to argue that there may be a core knowledge system for representing the beliefs of other agents, emerging early in human development and constraining automatic belief processing into adulthood. One way to investigate this purported core belief representation system is to examine whether non-human primates share such a system. Although non-human primates have historically performed poorly on false belief tasks that require executive function capacities, little work has explored how primates perform on more automatic measures of belief processing. To get at this issue, we modified Kovács et al. (2010)’s test of automatic belief representation to examine whether one non-human primate species—the rhesus macaque (Macaca mulatta)—is automatically influenced by another agent’s beliefs when tracking an object’s location. Monkeys saw an event in which a human agent watched an apple move back and forth between two boxes and an outcome in which one box was revealed to be empty. By occluding segments of the apple’s movement from either the monkey or the agent, we manipulated both the monkeys’ belief (true or false) and agent’s belief (true or false) about the final location of the apple. We found that monkeys looked longer at events that violated their own beliefs than at events that were consistent with their beliefs. In contrast to human infants, however, monkeys’ expectations were not influenced by another agent’s beliefs, suggesting that belief representation may be an aspect of core knowledge unique to humans.     

Do chimpanzees know what others can and cannot do? Reasoning about ‘capability’

Much recent comparative work has been devoted to exploring what nonhuman primates understand about physical causality. However, few laboratory experiments have attempted to test what nonhumans understand about what physical acts others are capable of performing. We tested seven chimpanzees’ ability to predict which of two human experimenters could deliver a tray containing a food reward. In the ‘floor’ condition, legs were required to push the tray toward the subject. In the ‘lap’ condition, arms were required to hand the tray to the subject. In Exp. 1, chimpanzees begged (by gesturing) to either an experimenter whose legs were not visible (LNV) or whose arms were not visible (ANV). Rather than flexibly altering their preferences between conditions, the chimpanzees preferred the ANV experimenter regardless of the task. In subsequent experiments, we manipulated various factors that might have controlled the chimpanzees’ preferences, such as (a) distance between experimenter and subject (Experiment 2), (b) amount of occlusion of experimenters’ body (Experiments 2 and 3), (c) contact with the food tray (Experiments 3 and 4) and (d) positioning of barriers that either impeded the movement of the limbs or not (Experiment 5). The chimpanzees’ performance was best explained by attention to cues such as perceived proximity, contact, and maximal occlusion of body that although highly predictive in certain tasks, were irrelevant in others. When the discriminative role of such cues was eliminated, performance fell to chance levels, indicating that chimpanzees do not spontaneously (or after considerable training) use limb visibility as a cue to predict the ability of a human to perform particular physical tasks. Thus, the current findings suggest a possible failure of causal reasoning in the context of reasoning about the use of the limbs to perform physical acts.     

Wild robins (Petroica longipes) respond to human gaze

Gaze following and awareness of attentional cues are hallmarks of human and non-human social intelligence. Here, we show that the North Island robin (Petroica longipes), a food-hoarding songbird endemic to New Zealand, responds to human eyes. Robins were presented with six different conditions, in which two human experimenters altered the orientation or visibility of their body, head or eyes in relation to mealworm prey. One experimenter had visual access to the prey, and the second experimenter did not. Robins were then given the opportunity to ‘steal’ one of two mealworms presented by each experimenter. Robins responded by preferentially choosing the mealworm in front of the experimenter who could not see, in all conditions but one. Robins failed to discriminate between experimenters who were facing the mealworm and those who had their head turned 90° to the side. This may suggest that robins do not make decisions using the same eye visibility cues that primates and corvids evince, whether for ecological, experiential or evolutionary reasons.     

Multimodal communication by captive chimpanzees (Pan troglodytes)

Many studies have shown that apes and monkeys are adept at cross-modal matching tasks requiring the subject to identify objects in one modality when information regarding those objects has been presented in a different modality. However, much less is known about non-human primates’ production of multimodal signaling in communicative contexts. Here, we present evidence from a study of 110 chimpanzees demonstrating that they select the modality of communication in accordance with variations in the attentional focus of a human interactant, which is consistent with previous research. In each trial, we presented desirable food to one of two chimpanzees, turning mid-way through the trial from facing one chimpanzee to facing the other chimpanzee, and documented their communicative displays, as the experimenter turned towards or away from the subjects. These chimpanzees varied their signals within a context-appropriate modality, displaying a range of different visual signals when a human experimenter was facing them and a range of different auditory or tactile (attention-getting) signals when the human was facing away from them; this finding extends previous research on multimodal signaling in this species. Thus, in the impoverished circumstances characteristic of captivity, complex signaling tactics are nevertheless exhibited by chimpanzees, suggesting continuity in intersubjective psychological processes in humans and apes.     

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.     

Transport of tools to food sites in tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Tool use and transport represent cognitively important aspects of early hominid evolution, and nonhuman primates are often used as models to examine the cognitive, ecological, morphological and social correlates of these behaviors in order to gain insights into the behavior of our early human ancestors. In 2001, Jalles-Filho et al. found that free-ranging capuchin monkeys failed to transport tools (stones) to food sites (nuts), but transported the foods to the tool sites. This result cast doubt on the usefulness of Cebus to model early human tool-using behavior. In this study, we examined the performance of six captive tufted capuchin monkeys (Cebus apella) in a tool transport task. Subjects were provided with the opportunity to transport two different tools to fixed food reward sites when the food reward was visible from the tool site and when the food reward was not visible from the tool site. We found that the subjects quickly and readily transported probing tools to an apparatus baited with syrup, but rarely transported stones to a nut-cracking apparatus. We suggest that the performance of the capuchins here reflects an efficient foraging strategy, in terms of energy return, among wild Cebus monkeys.     

Conserved evolutionary history for quick detection of threatening faces

Humans quickly recognize threats such as snakes and threatening faces, suggesting that human ancestors evolved specialized visual systems to detect biologically relevant threat stimuli. Although non-human primates also detect snakes quickly, it is unclear whether primates share the efficient visual systems to process the threatening faces of their conspecifics. Primates may not necessarily process conspecific threats by facial expressions, because threats from conspecifics in natural situations are often accompanied by other cues such as threatening actions (or attacks) and vocal calls. Here, we show a similar threat superiority effect in both humans and macaque Japanese monkeys. In visual search tasks, monkeys and humans both responded to pictures of a threatening face of an unfamiliar adult male monkey among neutral faces faster than to pictures of a neutral face among threatening faces. However, the monkeys’ response times to detect deviant pictures of a non-face stimulus were not slower when it was shown among threat faces than when it was shown among neutral faces. These results provide the first evidence that monkeys have an attentional bias toward the threatening faces of conspecifics and suggest that threatening faces are evolutionarily relevant fear stimuli. The subcortical visual systems in primates likely process not only snakes, but also more general biological threat-relevant stimuli, including threatening conspecific faces.     

读心的比较研究：非人灵长类与人类在心理理论上的异同点及其解释

利用非人灵长类开展比较研究是探索心理理论本质、起源和进化动因的重要途经。大量实证研究显示非人灵长类可以表现出一些基础心理理论成分, 包括联合注意、意图理解和一级观点采择, 这表明心理理论在灵长类动物的进化谱系中具有进化连续性。然而, 非人灵长类无法像人类一样达成二级观点采择和错误信念理解, 潜心智化假说、替代表征假说、最小限度心理理论假说和意识关系假说试图对此差异进行解释。尽管视角与具体内容不同, 但这些假说都强调, 非人灵长类无法对其他个体关于外部世界的心理信念形成表征, 信念表征是非人灵长类与人类读心能力的重要分界点。未来研究需要重点澄清共享意图、语言机制以及社会生态环境因素与心理理论产生的相互影响作用。     

Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task

The ability of 3 capuchin monkeys (Cebus apella) to use experimenter-given cues to solve an object-choice task was assessed. The monkeys learned to use explicit gestural and postural cues and then progressed to using eye-gaze-only cues to solve the task, that is, to choose the baited 1 of 2 objects and thus obtain a food reward. Increasing cue-stimulus distance and introducing movement of the eyes impeded the establishment of effective eye-gaze reading. One monkey showed positive but imperfect transfer of use of eye gaze when a novel experimenter presented the cue. When head and eye orientation cues were presented simultaneously and in conflict, the monkeys showed greater responsiveness to head orientation cues. The results show that capuchin monkeys can learn to use eye gaze as a discriminative cue, but there was no-evidence for any underlying awareness of eye gaze as a cue to direction of attention.     

Monkeys represent others' knowledge but not their beliefs

The capacity to reason about the false beliefs of others is classically considered the benchmark for a fully fledged understanding of the mental lives of others. Although much is known about the developmental origins of our understanding of others' beliefs, we still know much less about the evolutionary origins of this capacity. Here, we examine whether non-human primates - specifically, rhesus macaques (Macaca mulatta) - share this developmental achievement. We presented macaques with a looking-time measure of false belief understanding, one that had recently been developed for use with 15-month-old human infants. Like human infants, monkeys look longer when a human experimenter fails to search in the correct location when she has accurate knowledge. In contrast to infants, however, monkeys appear to make no prediction about how a human experimenter will act when she has a false belief. Across three studies, macaques' pattern of results is consistent with the view that monkeys can represent the knowledge and ignorance of others, but not their beliefs. The capacity to represent beliefs may therefore be a unique hallmark of human cognition.     

Cognitive consequences of cooperative breeding in primates?

Several hypotheses propose that cooperative breeding leads to increased cognitive performance, in both nonhuman and human primates, but systematic evidence for such a relationship is missing. A causal link might exist because motivational and cognitive processes necessary for the execution and coordination of helping behaviors could also favor cognitive performance in contexts not directly related to caregiving. In callitrichids, which among primates rely most strongly on cooperative breeding, these motivational and cognitive processes include attentional biases toward monitoring others, the ability to coordinate actions spatially and temporally, increased social tolerance, increased responsiveness to others’ signals, and spontaneous prosociality. These processes are likely to enhance performance particularly in socio-cognitive contexts. Therefore, cooperatively breeding primates are expected to outperform their independently breeding sister taxa in socio-cognitive tasks. We evaluate this prediction by reviewing the literature and comparing cognitive performance in callitrichids with that of their sister taxa, i.e. squirrel monkeys, which are independent breeders, and capuchin monkeys, which show an intermediate breeding system. Consistent with our prediction, this review reveals that callitrichids systematically and significantly outperform their sister taxa in the socio-cognitive, but not in the non-social domain. This comparison is complemented with more qualitative evaluations of prosociality and cognitive performance in non-primate cooperative breeders, which suggest that among mammals, cooperative breeding generally produces conditions conducive to socio-cognitive performance. In the hominid lineage, however, the adoption of extensive allomaternal care presumably resulted in more pervasive cognitive consequences, because the motivational consequences of cooperative breeding was added to an ape-level cognitive system already capable of understanding simple mental states, which enabled the emergence of shared intentionality.     

Now you see me,now you don't: evidence that chimpanzees understand the role of the eyes in attention

Chimpanzees appear to understand something about the attentional states of others; in the present experiment, we investigated whether they understand that the attentional state of a human is based on eye gaze. In all, 116 adult chimpanzees were offered food by an experimenter who engaged in one of the four experimental manipulations: eyes closed, eyes open, hand over eyes, and hand over mouth. The communicative behavior of the chimpanzees was observed. More visible behaviors were produced when the experimenter's eyes were visible than when the experimenter's eyes were not visible. More vocalizations were produced when the experimenter's eyes were closed than when they were open, but there were no differences in other attention getting behaviors. There was no effect of age or rearing history. The results suggest that chimpanzees use the presence of the eyes as a cue that their visual gestures will be effective.     

How tree shrews (Tupaia belangeri) perform in a searching task: evidence for strategy use

This study investigated how male tree shrews (Tupaia belangen) performed in a searching task while in their home cages and assessed whether different food distributions affected their performance. The animals were faced with a holeboard containing 9 food sources arranged in a 3 x 3 matrix or in 3 clusters, each containing 3 sources. Animals tended to start and end the trials from preferred locations, thereafter solving the task by strategically organizing the reward collection according to a minimum-distance principle. In the cluster configuration, they visited the sources hierarchically. Food distribution did not affect the performance. Comparison with data from mice and capuchin monkeys revealed that tree shrews and capuchins solved the task in a similar strategic way, whereas mice did not. These findings attract particular attention because of the phylogenetic position of tree shrews, which are regarded as closely related to primates.     

‘Unwilling’ versus ‘unable’: capuchin monkeys’ (Cebus apella) understanding of human intentional action

A sensitivity to the intentions behind human action is a crucial developmental achievement in infants. Is this intention reading ability a unique and relatively recent product of human evolution and culture, or does this capacity instead have roots in our non‐human primate ancestors? Recent work by Call and colleagues (2004) lends credence to the latter hypothesis, providing evidence that chimpanzees are also sensitive to human intentions. Specifically, chimpanzees remained in a testing area longer and exhibited fewer frustration behaviors when an experimenter behaved as if he intended to give food but was unable to do so, than when the experimenter behaved as if he had no intention of giving food. The present research builds on and extends this paradigm, providing some of the first evidence of intention reading in a more distant primate relative, the capuchin monkey (Cebus apella). Like chimpanzees, capuchin monkeys distinguish between different goal‐directed acts, vacating an enclosure sooner when an experimenter acts unwilling to give food than when she acts unable to give food. Additionally, we found that this pattern is specific to animate action, and does not obtain when the same actions are performed by inanimate rods instead of human hands (for a similar logic, see Woodward, 1998 ). Taken together with the previous evidence, the present research suggests that our own intention reading is not a wholly unique aspect of the human species, but rather is shared broadly across the primate order.     

I acknowledge your help: capuchin monkeys’ sensitivity to others’ labor

Our society is sustained by wide-ranging cooperation. If individuals are sensitive to others’ gains and losses as well as the amount of labor, they can ensure future beneficial cooperative interaction. However, it is still an open question whether nonhuman primates are sensitive to others’ labor. We asked this question in tufted capuchin monkeys in an experimental food-sharing situation by comparing conditions with labor by two participants equalized (Equal labor condition) or unequalized (Unequal labor condition). The operator monkey pulled the drawer of one of the two food containers placed between two monkeys, each containing a food for him/herself and another for the recipient monkey. The recipient received either high- or low-value food depending on the operator’s choice, whereas the operator obtained the same food regardless of his/her choice. In Unequal labor condition, the operator first had to pull the handle of the board to which the containers were glued and then pull the drawer of one of the containers, while the recipient received food with no labor. In Equal labor condition, the recipient had to pull the handle of the board so that the operator could operate a container. Results showed that operators chose the high-value food container for recipients more often than when the recipient was absent only in Equal labor condition. This suggests that capuchin monkeys are sensitive to others’ labor and actively give food to a partner who has helped them to complete a task.