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Tufted Capuchin Monkeys (Cebus Apella) Show Understanding of Human Attentional States When Requesting Food Held by a Human

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Tufted Capuchin Monkeys (Cebus Apella) Show Understanding of Human Attentional States When Requesting Food Held by a Human Anim Cogn (2010) 13:87–92 DOI 10.1007/s10071-009-0248-6 ORIGINAL PAPER Tufted capuchin monkeys (Cebus apella) show understanding of human attentional states when requesting food held by a human Yuko Hattori · Hika Kuroshima · Kazuo Fujita Received: 16 January 2009 / Revised: 28 May 2009 / Accepted: 28 May 2009 / Published online: 11 June 2009 © Springer-Verlag 2009 Abstract Researchers have investigated to what extent others’ attentional states, although this ability appears lim- non-human primates understand others’ attentional states, ited compared to what is seen in humans. as this ability is considered an important prerequisite for theory of mind. However, previous studies using food Keywords Social cognition · Non-human primates · requesting tasks have failed to show that non-human prima- Attention · Eye gaze tes attribute perception to others as a function of their atten- tional states. One possible reason is that food requesting tasks may require subjects not only to take into account an Introduction experimenter’s attentional state but also to direct it toward the food. The present study tested tufted capuchin mon- Understanding others’ visual perception is an important keys’ (Cebus apella) understanding of others’ attentional prerequisite for development of theory of mind in human states in a food requesting task. In the Wrst situation, mon- children. Flavell et al. (1981) distinguished two stages of keys were required only to attract an experimenter’s atten- understanding others’ visual perception. In the Wrst stage, tion. In the second situation, the monkeys were required to referred to as Level 1 visual perspective-taking, children both attract the experimenter’s attention and direct it are able to determine what others can or cannot see based toward food on a table. The results revealed that capuchin upon the presence or absence of visual obstructions in their monkeys showed evidence of understanding the experi- line of sight. Later, in Level 2 visual perspective-taking, menter’s attentional variations only in the former condition. children are able to mentally recreate the visual representa- This suggests that previous tasks, requiring referential ges- tions possessed by other individuals and to determine how tures, lacking in most non-human primates, failed to reveal an object appears to individuals viewing the object from a sensitivity to human attentional states because the subjects diVerent position. However, there is controversy about the might not have understood the requesting situation. In con- extent to which nonhuman primates share humans’ ability clusion, capuchin monkeys can understand variations in to relate mental states, such as what others can and cannot see, to seeing. In Wfteen experiments, Povinelli and Eddy (1996) tested Present Address: whether juvenile chimpanzees understood the necessary Y. Hattori (&) conditions underlying others’ visual perception, in terms of Primate Research Institute, Kyoto University, bodily and facial orientation and states of the eyes. They Kanrin 41-2, Inuyama, Aichi 484-8506, Japan trained each ape to extend their hand through one of the two e-mail: [email protected] holes on a Plexiglas wall to request food from one of two Y. Hattori experimenters who each held food. In test trials, a human Japan Society for the Promotion of Science, Tsukuba, Japan experimenter stood behind each hole, with food available on the table between them. One experimenter could see the H. Kuroshima · K. Fujita Department of Psychology, Graduate School of Letters, ape but the other could not, due to facing the other way, Kyoto University, Kyoto, Japan occluding the face with a bucket, closing the eyes, etc. 123 88 Anim Cogn (2010) 13:87–92 When the subjects had to choose which of the two humans direct it to the target of interest (Gomez 2005). The latter to beg food from, they showed no diVerential responses may require the use of “referential gestures”, that is direct- except in the most basic condition in which one experi- ing others’ attention to a location of an object, which are menter faced the ape and the other had her back turned. The relatively rare in non-human primates (see Call and investigators concluded that these young chimpanzees did Tomasello 1994; Leavens et al. 2005; Liebal et al. 2007 for not seem to understand precisely how visual perception examples in captive apes). Although monkeys can learn to works, especially the role of the eyes. make an action when an experimenter looks at them, the Other studies, using object-choice procedures have situation is unnatural and apparently diYcult to recognize largely also failed to demonstrate nonhuman primates’ use as a requesting situation. Recently, however, chimpanzees of eyes as an eVective cue. Typically, subjects are presented were reported to attract others’ attention using vocal and with two opaque containers, only one of which contains manual gestures Xexibly, matched to variations in the food. An experimenter then gives a social cue such as look- experimenter’s attentional states (i.e. open or closed eyes) ing, orienting his/her head, pointing, and so on toward the (Hostetter et al. 2007). This suggests that non-human pri- container with food inside. Typically when non-human pri- mates may be in fact sensitive to variable attentional states, mates are tested with this paradigm, results are poorer for but the unnaturalness of many requesting tasks might limit use of eye-gaze cues than other cues (chimpanzees, Call the expression of their sensitivity. If so, then previous et al. 1998, 2000; rhesus monkeys, Anderson et al. 1996; “cooperative paradigms” have probably underestimated the capuchin monkeys, Anderson et al. 1995; Vick and extent of the ability to read attentional states. Anderson 2000). In this study, we hypothesized that a new “cooperative For successful performance in the tasks above, the sub- paradigm,” in which the subjects request food held directly ject has to respond to attentional states of a “cooperative” in an experimenter’s hand (Hand situation), would be more trainer, who will reward the subject with food if the likely to reveal monkeys’ true understanding of attentional response is correct. This is an unusual situation in the sub- states. In this situation, monkeys only have to attract the jects’ daily life. On the other hand, Vick and Anderson experimenter’s attention in order to request food. We com- (2003), Flombaum and Santos (2005) and Hare et al. (2000, pared performances in this situation with those on trials 2001, 2003) used a “competitive paradigm”, in which the using a more conventional paradigm in which the subjects subject must use a human’s or conspeciWc’s attentional have to ask the experimenter to hand over food on a table states to outcompete the opponent in a contest for food; this (Table situation). We predicted that in the new paradigm is probably a more familiar kind of situation for monkeys. (Hand situation), monkeys would produce their request Actually, Vick and Anderson (2003) reported that three action diVerentially according to the attentional state of the olive baboons successfully learned to exploit a human experimenter, whereas in the conventional paradigm (Table experimenter’s head orientation as a cue to obtain a food situation), they would not. We also predicted that they item. Flombaum and Santos (2005) also demonstrated that would respond diVerentially to variations in the experi- rhesus monkeys selectively stole grapes from an experi- menter’s attentional states in the new paradigm. SpeciW- menter who was not able to see the grape more often than cally, the monkeys would respond less to an experimenter from an experimenter who was even based on the experi- with eyes closed than to an experimenter looking at either menter’s eye gaze. Additionally, with competitive para- food or the monkeys. This is because Hattori et al. (2007) digm, Hare et al. (2000, 2001, 2003) found that subordinate found that capuchin monkeys are sensitive to eye gaze in chimpanzees but not capuchin monkeys took a dominant conventional food request paradigm. In Hattori et al. the individual’s perspective into account and went preferen- monkeys requested food using a trained pointing-like tially for food that only they and not the dominant could behavior, and frequency of pointing and looking duration to see. Thus results obtained from “competitive” paradigms an experimenter’s face were measured. Although the fre- suggest that not only apes but also Old World monkeys quency of pointing did not change, looking duration diVered may have sensitivity to social cues such as head orientation Xexibly depending upon the experimenter’s state of gaze. and eye gaze, and represent perception in others to some We tested a New World species, tufted capuchin mon- extent. keys. The new cooperative paradigm seems ecologically Why do “cooperative paradigms” generally fail to reveal valid for this species because begging and sharing food are non-human primates’ understanding others’ attentional common even among unrelated individuals (de Waal 1997, states? As well as the unnaturalness of receiving coopera- 2000) and they may respond to conspeciWcs’ direct gaze tive food-related signals, some cooperative tasks with aYnitive facial expressions leading to active contact (e.g., Povinelli and Eddy 1996; Kaminski et al. 2004) (Weigel 1979). In the conventional cooperative paradigm, required two things of the subject as a requesting situation; the requesting task required subjects to direct the experi- namely, capture the attention of the addressee, and then menter’s attention to food, which requires referential 123 Anim Cogn (2010) 13:87–92 89 gestures and is clearly not adapted for capuchin monkeys or for other non-human primates. Tufted capuchin monkeys are evolutionarily more dis- tant from humans than are chimpanzees, but they show a variety of social abilities including coalition formation, group hunting and triadic awareness both in the Weld and in captivity, as well as advanced physical cognitive abilities (e.g., Perry et al.
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