Anim Cogn (2006) 9: 110–117DOI 10.1007/s10071-005-0007-2

ORIGINAL ARTICLE

Annika Paukner · James R. Anderson · Kazuo Fujita

Redundant food searches by capuchin monkeys (Cebus apella):a failure of metacognition?

Received: 15 March 2005 / Revised: 3 July 2005 / Accepted: 5 July 2005 / Published online: 24 September 2005C© Springer-Verlag 2005

Abstract This study investigated capuchin monkeys’ un-derstanding of their own visual search behavior as a meansto gather information. Five monkeys were presented withthree tubes that could be visually searched to determinethe location of a bait. The bait’s visibility was experimen-tally manipulated, and the monkeys’ spontaneous visualsearches before tube selection were analyzed. In Exper-iment 1, three monkeys selected the baited tube signifi-cantly above chance; however, the monkeys also searchedtransparent tubes. In Experiment 2, a bent tube in whichfood was never visible was introduced. When the bent tubewas baited, the monkeys failed to deduce the bait locationand responded randomly. They also continued to look intothe bent tube despite not gaining any pertinent informationfrom it. The capuchin monkeys’ behavior contrasts with theefficient employment of visual search behavior reported inhumans, apes and macaques. This difference is consistentwith species-related variations in metacognitive abilities,although other explanations are also possible.

Keywords Metacognition . Metacognitive awareness .Capuchin monkey . Visual search behavior

When humans are aware that they are missing importantinformation for correctly completing a task, or when theyare unsure about what to do, they often react predictably.For example, if they realize that a piece of information isnot sufficiently known to pass an exam, students may de-cide to study further (Nelson and Narens 1990). Seekinginformation or declining a response in a situation of uncer-tainty are indicative of metacognitive awareness, which is

A. Paukner (�) · J. R. AndersonDepartment of Psychology, University of Stirling,Stirling, FK9 4LA, UKe-mail: ap14@stir.ac.ukTel.: +44-1786-467640Fax: +44-1786-467641

K. FujitaDepartment of Psychology, Faculty/Graduate School of Letters,Kyoto University,Yoshida-honmachi, Sakyo, Kyoto 606-8501, Japan

defined as knowing about one’s own cognitive states (Smithet al. 1995). Metacognitive awareness has been investigatedin several non-human species, including dolphins, pigeonsand a few species of primates (e.g. Smith et al. 1995; Inmanand Shettleworth 1999; Hampton 2001; for a review, seeSmith et al. 2003). For example, Hampton (2001) found thatrhesus macaques (Macaca mulatta) may decline a memorytrial that they are unlikely to complete correctly and optfor a new, easier trial instead. This behavior suggests thatrhesus macaques are capable of accurately monitoring theirown memory contents (Hampton 2001).

Griffin (2003) argued that all animals face uncertainty, forexample, when deciding whether a movement in the veg-etation is a predator or simply wind, or whether an objecton the ground is edible or not. Decisions regarding theseuncertainties can be crucially important for survival of ananimal. Therefore, a system for accurately monitoring un-certainties and controlling the animal’s behavior in terms ofeither seeking more information or deciding on the point ofcertainty sufficient for making an adaptive response wouldappear advantageous. It is therefore conceivable that natu-ral selection has led to metacognitive awareness evolvingin many species.

Regarding primates, chimpanzees (Pan troglodytes)and orangutans (Pongo pygmaeus) will efficiently seekadditional information. Call and Carpenter (2001) showedhollow tubes to these apes, one containing a food reward,and the apes were allowed to look into the tubes beforeselecting one. They received the reward only if theyselected the baited tube. Call and Carpenter (2001) foundthat both species were more likely to search for the rewardwhen they had not witnessed the baiting procedure and thusdid not know where the bait was. In addition, searchingthe tubes led to more correct tube selections. Apes behavesimilarly to 2.5-year-old children in this respect; the latteralso engage in visual searches when they do not know thecorrect location of a desirable objects (Call and Carpenter2001). Recently, Hampton et al. (2004) adapted the tubeparadigm to test rhesus macaques. Like humans and apes,the macaques searched more when they had not witnessedthe baiting, and selection accuracy increased when they

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searched. These findings suggest that metacognitiveawareness might have evolved in the common ancestors ofapes and the Old World monkeys, and could be widespreadamongst primates (Hampton et al. 2004).

In the present study, we used the tube paradigm to in-vestigate whether tufted capuchin monkeys (Cebus apella)efficiently seek additional information in a situation ofuncertainty. We chose capuchin monkeys as subjects be-cause they have been ascribed advanced cognitive abilitiessuch as visible displacements (Dumas and Brunet 1994)and seriation (McGonigle et al. 2003), but their metacog-nitive abilities have not yet been assessed. Furthermore,if similar metacognitive abilities to rhesus macaques andchimpanzees are found in this New World species, thenmetacognitive awareness may have evolved in the commonancestors of the Old World and New World monkeys. If ca-puchin monkeys possess similar metacognitive awareness,they should behave similarly to apes and rhesus macaques.In particular, we would expect that visual searches are re-stricted to trials in which they do not know the location of areward, and that visual searches result in increased selectionaccuracy. In Experiment 1, this hypothesis was tested bygiving capuchin monkeys a tube-based visual search task.The location of a food reward was either directly apparent,or could be discovered through searching. The monkeys’search patterns were analyzed with regard to the frequency,location and success of searches. In Experiment 2, we fur-ther tested the monkeys’ awareness of their own searchbehavior by presenting them with a bent tube, in which thebait could never be seen. We reasoned that if the monkeyswere monitoring the outcome of their own search behav-iors, they might realize that the bent tube never providedany useful information regarding the location of the bait, sothat if the other (straight) tubes were empty, the bait couldonly be within the bent tube. Therefore, they might selectthe bent tube without searching it first.

Experiment 1

Methods

Subjects and housing

The study was carried out at the Faculty of Letters, KyotoUniversity, in 2003. Subjects were one adult male (Heiji,9–year-old), three adult female (Kiki, 7–year-old; Theta,7-year-old; Zilla, 9-year-old) and one juvenile male(Zinnia, 2-year-old) tufted capuchin monkeys (Cebusapella), all captive born and raised by their biologicalmothers. Heiji, Zilla and Zinnia were housed together witha young adult male; Kiki and Theta were housed as a pair.Three monkeys (Heiji, Zilla and Theta) had previouslyparticipated in object discrimination tasks, and had beentrained to use a pointing/reaching gesture to indicate theirselections. Zilla was pregnant throughout the experimentalperiod and gave birth 4 weeks after completion of theexperiment. The monkeys were not deprived of food, butreceived part of their daily food rations during testing.

Apparatus

All monkeys were tested individually in a familiar testingcage made of transparent acrylic board (46 cm × 46 cm×52 cm). At the front of the cage was an opening (23.5 cm×3.5 cm), ca. 5 cm above the floor. This allowed themonkeys to reach out toward the three plastic tubes(40 cm× 5 cm diameter) that were fastened on a platformand held in position by wooden rails spaced 8 cm apart andperpendicular to the test cage. During testing, the tubeswere raised ca. 3 cm at the end furthest from the monkey,so that it was only possible to look through one tube at atime from any location within the cage. The platform wassituated on a small table (59.5 cm × 45.5 cm × 30 cm) thatwas in level with the floor of the cage. A white cardboardscreen was placed between the apparatus and the test cagewhen required to occlude the baiting process.

Preliminary training

Monkeys were given three to eight preliminary trainingsessions to familiarize them with the testing procedure andto establish a reaching response toward the tubes. Duringtraining, the openings of the tubes facing the monkey wereeach blocked with a small piece of white cardboard, so thatthe monkey would not learn to look into the tubes. Theexperimenter sat behind the apparatus facing the monkeywith the screen occluding both the experimenter and ap-paratus. In order to minimize unintentional cueing of thecorrect response, the experimenter remained passive andvisually focused on the opening of the test cage throughoutthe experiment.

Each trial started with the screen being removed, andthen a small piece of apple or sweet potato (the bait) beingvisibly put on top of one of the three opaque tubes. If themonkey reached toward the baited tube, it received the baitand the trial was ended by replacing the screen. If the mon-key reached toward a nonbaited tube, no reward was givenand the screen was replaced immediately. Reaching wassimply defined as an extension of the arm toward a tube asif the monkey was trying to touch the tube. Occasionally,the monkeys would tap the table in front of a tube, whichwas also considered an acceptable selection response. Inthe second training phase, several false baiting gestureswere added so that all tubes were touched once in randomorder but only one tube was baited. For the final train-ing phase, the experimenter placed the bait on top of onetube before removing the screen, with the platform situated35 cm in front of the test cage. After removing the screen,the platform was pushed ca. 5 cm toward but was still outof reach of the monkey. The first reach after the platformcame to a halt was taken as the response. Training sessionswere administered once a day and lasted ca. 20 min permonkey.

Once the monkeys were responding reliably, a more for-mal evaluation was conducted to make sure they understoodthe task. Each test session consisted of 24 trials. In 16 trials,the baiting was visible, i.e., the screen was removed before

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baiting so that the monkeys could see the baiting gesture.The remaining eight trials were unseen, i.e. the bait wasplaced on top of one tube before the screen was removedso that the monkeys did not see the baiting gesture. Eachmonkey was judged to have reached the criterion when itresponded correctly to a total of at least 20 trials per session(over 80% correct). Kiki and Zilla required three prelimi-nary training sessions to reach the criterion. Heiji and Thetarequired four and Zinnia required eight sessions.

Before the actual experiment, the experimenter removedthe cardboard that blocked visual access to the inside ofthe tubes and showed the tubes to the monkeys. All mon-keys showed interest in the tubes, and looked through themseveral times.

Preliminary experiment

In a pilot study, we adopted a procedure identical to thoseused by Call and Carpenter (2001) and Hampton et al.(2004). We placed the bait inside a tube so that it was notdirectly visible. We then presented the monkeys with twodifferent types of trials: seen trials, in which the monkeyssaw which tube the experimenter baited, and unseen trials,in which the monkeys did not observe the baiting. How-ever, we encountered problems with this procedure. In seentrials, the monkeys would immediately visually follow thefood reward during baiting and look into the baited tube,but even when the experimenter had deposited the rewardand, with a clearly empty hand, touched the top of other(empty) tubes, the monkeys would look into whichever tubewas being touched. It is not clear why the experimenter’shand gestures may have been too salient to the capuchinmonkeys, resulting in failure to visually disengage fromthem. Looking into a tube was therefore influenced by theexperimenter’s baiting gesture and not an unequivocal in-dication of metacognitive abilities, and became a confoundto the experimental paradigm.

To provide the monkeys with explicit information aboutthe bait location without using a baiting gesture, we alwaysbaited a tube while the screen was between the monkey andapparatus. However, we employed two different types oftubes. One type (as used during training and the preliminaryexperiment) was green-opaque and required the monkey tocrouch down to visually check the contents of the tube.The second type of tube was transparent which meant thatthe monkey could see directly if it was baited. This setupallowed the monkeys to know the location of the bait whena transparent tube was baited, and to be uncertain of the baitlocation when an opaque tube was baited. We consider thissetup to be functionally equivalent to the paradigm usingseen and unseen baiting gestures in Call and Carpenter(2001) and Hampton et al. (2004).

Experimental procedure

At the start of each trial, the experimenter sat behindthe apparatus, facing the monkey with the screen in

place occluding the experimenter and apparatus. Theexperimenter touched all three tubes in random order toeliminate any sound or movement cues. The bait wasplaced inside one of the tubes, at the end farthest from themonkey. The screen was then removed and the platformwas pushed toward the monkey after a 5 s delay. The firstreach after the platform came to a halt was taken as theresponse. If the monkey reached toward the baited tube,the experimenter retrieved the bait, gave it to the monkeyand replaced the screen. If the monkey reached towardan unbaited tube, the screen was replaced immediately. Ifno response occurred after 60 s, the screen was replaced,the bait was retrieved from the tube and the next trialstarted. Trials were separated by a 5 s inter-trial interval. Avideo camera placed behind the experimenter recorded allsessions.

Each monkey received a total of 72 trials in three ses-sions of 24 trials each, which were conducted once a dayfor three consecutive days. This relatively small numberof trials was intended to prevent an improvement in per-formance based on learned associations between searchbehaviors and food rewards. Each monkey received 54 tri-als in which two opaque tubes and one transparent tubewere used, with the location of the transparent tube and thebait counterbalanced across trials. When the transparenttube was baited, the monkeys could directly see the bait,so that (if aware of this knowledge) no searching was re-quired before choosing correctly. On the other hand, whenone of the opaque tubes was baited, the monkey couldimmediately see that the transparent tube was empty, and(if aware of this knowledge) could restrict its searches tothe opaque tubes. On the remaining 18 trials, one opaqueand two transparent tubes were used, with bait and tubelocations again counterbalanced. If a transparent tube wasbaited in these trials, the monkey again could see the baitimmediately, so no searches were necessary. If the opaquetube was baited, the monkey could see that the other twotubes were empty. Therefore, the monkey might deducethe location of the bait, and choose correctly without anyneed for searching. The order of trial types was random-ized with the only restriction that the bait was not hid-den at the same location for more than two consecutivetrials.

Data analysis

All sessions were videotaped for later analysis. Baiting ges-tures were not included in the footage, which allowed blindscoring of the monkeys’ behaviors. The number of looks,the tubes looked into and the order in which the tubes werelooked into were recorded from the moment the screen wasremoved until selection occurred. Forty percent of trialswere coded a second time to assess intra-observer relia-bility; consistency between codings was high (Pearson’scorrelations: r=+0.92, p<0.001 for searches; r=+0.96,p<0.001 for selection). Due to the small number of sub-jects, results were analyzed separately for each individualusing nonparametric tests.

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Results

Selection behavior

All monkeys selected a tube on all trials, but only threemonkeys (Zilla, Heiji and Kiki) chose the correct tubesignificantly above chance throughout the experiment(chance=33%, binomial tests: all p<0.001). The remain-ing two monkeys showed strong location biases: Zinniapreferentially selected the middle tube (61 selections outof 72) whilst Theta avoided the middle tube (7 selectionsout of 72). However, although Theta’s overall choices ap-peared random (29 correct out of 72), she chose the correcttransparent tubes significantly above chance (15 correct outof 27, binomial test: p=0.011). Since only three monkeyscompleted the overall task successfully, only these mon-keys’ data are considered in detail.

The visibility of the bait did not influence the outcome ofa trial. All the three monkeys were equally successful whenthe bait was placed inside a transparent tube (100, 88.9 and100% correct, respectively for Zilla, Heiji and Kiki) andwhen it was placed inside an opaque tube (95.6, 95.6 and97.8% correct, respectively).

Search behavior

Zilla, Heiji and Kiki searched on the first trial, and contin-ued to search at least one tube during all subsequent trials.Typically, the monkeys searched until they saw the baitand then either made a selection (47.2, 50 and 65.3% oftrials), or they continued to search but returned to searchin the baited tube with their last look before making aselection (12.5, 18.1 and 16.7% of trials, respectively)(Fig. 1).

Figure 2 shows the average number of looks per tubeper trial according to bait location and tubes searched. Themonkeys did not make fewer searches when the bait wasdirectly visible compared to trials when it was not directlyvisible (Mann–Whitney tests for each individual: Heiji:z=1.578; Kiki: z=−0.56; Zilla: z=−1.127, all p>0.05).When comparing the number of looks into the transpar-ent tubes and the opaque tubes during each trial (takinginto account the unequal number of tubes), no monkeylooked less into the former (68, 61 and 66 looks in to-tal) than into the latter (80, 70 and 69 looks in total, re-spectively; Wilcoxon Signed Rank tests: Heiji: z=−1.547,Kiki: z=−1.652, Zilla: z=0.520, all p>0.05). Selection ac-curacy was not associated with the increased number oflooks (correct selections: mean number of looks = 3.0,2.7 and 2.8 for Heiji, Kiki and Zilla, respectively; incor-rect selections: mean number of looks = 3.0, 2.0 and 3.6,respectively; Mann–Whitney tests: z=−0.077, z=−0.808and z=−1.842, respectively, all p>0.05). In trials with twoempty transparent tubes and a baited opaque tube, monkeysnever selected the opaque tube without searching in at leastone tube first.

Fig. 1 Setup of experiment during baiting. E: experimenter, M:monkey

Fig. 2 Experiment 1–average number of looks per tube per trialaccording to baiting conditions. TR-VI: looks into transparent tubeswith bait in transparent tube; OP-VI: looks into opaque tubes with baitin transparent tube; TR-IN: looks into transparent tube with bait inopaque tube; OP-IN: looks into opaque tubes with bait in opaque tube

Discussion

Although all five monkeys were successful during training,only three monkeys selected the correct tube significantlyabove chance during the experiment. Seeing the baitdirectly did not reduce the number of searches, and whenthe bait location was unknown, more searching did notlead to greater success. These results contrast with thoseof apes (Call and Carpenter 2001) and rhesus macaques(Hampton et al. 2004). In both these studies, subjectssearched less when they had direct information about thebait location, and in trials without such information, theywere more successful when they searched.

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The lack of association between searching and correct se-lections by the three capuchin monkeys could be attributedto the selection of the correct tube at ceiling levels, i.e.there were too few incorrect trials to analyze. The twomonkeys that failed to reliably select the correct tube alsodid not search reliably, again making it impossible to matchsearching behavior to successful outcomes.

Another behavioral difference between the apes and rhe-sus macaques on one hand and capuchin monkeys on theother emerged when direct information about the bait lo-cation was available. In trials in which an opaque tube wasbaited, we expected the monkeys to search in the opaquetubes. In trials in which a transparent tube was baited, westill expected the monkeys to search opaque tubes, per-haps to check if a second bait was available in one ofthe tubes. Both these search strategies are consistent withmetacognitive awareness, i.e. the monkeys might be awareof what information they have and what information theyare lacking at the beginning of a trial. However, it is notclear why the monkeys would search transparent tubes ifthey can directly see the contents of these tubes, and there-fore should already be aware of the relevant information.In contrast, both apes and rhesus macaques searched lessin seen trials when direct information about the bait loca-tion was available. A simple explanation for the capuchinmonkeys’ unnecessary searches could be that they failedto notice the bait inside the transparent tubes. However,one monkey reliably selected the correct tube only if itwas transparent, which makes this explanation unlikely.Searching in transparent tubes suggests that the capuchinmonkeys failed to effectively monitor the outcome of theirown visual search behavior, which implies a limitation ofmetacognitive awareness.

One important aspect of the experimental setup used fortesting capuchin monkeys, however, may have significantlyimpacted on the results of the present experiment. Whereasrhesus macaques and chimpanzees both encountered visi-ble baiting gestures, the capuchins received the additionalinformation of the bait’s location through the use of trans-parent tubes. In order to successfully complete the task,capuchin monkeys therefore needed to understand the con-cept of transparency, a requirement not posed by the visiblebaiting gesture. Even human infants encounter difficultieswith understanding transparency and object relations thatinvolve placement of objects into other objects. For ex-ample, infants who pass visible displacement tasks maynonetheless fail invisible displacement tasks that are con-ducted using transparent cups that clearly show the ob-ject to the infant (Bower 1982). One possible explanation,therefore, is that the capuchin monkeys failed to appre-ciate that the bait inside the tube was the same bait thatwas visible when looking through the tube. Even to thesingle monkey who in the absence of search behaviorschose the correct transparent tube, the bait may have beenno more than a discriminative marker without an under-standing that it was actually the same bait. Therefore, theexcessive search behavior of the capuchins may be causedby a failure to understand the nature of the transparenttubes.

Excessive search behavior on every trial led to an absenceof what Call and Carpenter (2001) termed ‘super-efficient’searches, that is, selecting a tube by inference based on in-direct knowledge gained about the bait location rather thanseeing the bait (either directly or through searching). Apartfrom the metacognitive skills (monitoring current knowl-edge states), this behavior seems to require other advancedcognitive abilities such as making logical deductions basedon inferential steps (if the bait is not in the first or sec-ond tube, it can only be in the third tube). ‘Super-efficient’searches also require an understanding of the limitationsof visual search behavior (for example, that a bait mightbe in a tube even though visual access into this tube isprevented). Call and Carpenter (2001) found that both 2.5-year-old children and chimpanzees engaged in these ‘super-efficient’ searches, although they did so only infrequentlyand preferred to locate the bait by searching instead. InExperiment 2, we devised a new procedure to test whethercapuchin monkeys can infer the bait location, and to fur-ther investigate their awareness of the consequences of theirown visual search behavior.

Experiment 2

In Experiment 2, one opaque tube with the end bent at 90◦was introduced. When this tube was baited, the bait couldnot been seen by looking into the tube. Hence unlike thestraight opaque tubes in Experiment 1, this bent tube of-fered no information about the bait location. In addition, themonkeys could easily identify this tube before searching.This setup therefore provided the opportunity to investi-gate how much capuchin monkeys understood about thepurpose and limitations of their own search behavior. Ourfirst question was whether the capuchin monkeys wouldinfer the bait location within the bent tube and select it ifthey could not see the bait in any other tubes. The secondquestion was whether they could do so without searchingthe bent tube first, thereby showing that they were aware ofthe limitations of their own visual search behavior.

Methods

The same five monkeys from the previous experiment weretested, and the same basic procedure was used. The appa-ratus consisted of one 90◦ horizontally bent opaque tube(42 cm × 5 cm) and two straight opaque tubes. The loca-tions of the bent tube and the bait were randomized acrosstrials, with the only restriction that the bait was not in thesame location for more than two consecutive trials. Mon-keys received one test session of 32 trials. On 12 of thosetrials, the bait was hidden in the bent tube. Prior to thestart of the experiment, the experimenter held up the benttube in front of the monkeys; all monkeys inspected thetube and looked into it several times. Data were collectedand analyzed as in Experiment 1. Forty percent of trialswere coded for a second time; intra-observer reliabilitybetween codings was high (Pearson’s correlation:

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r=+0.94, p<0.001 for searches; r=+0.98, p<0.001 forselection).

Results

Selection behavior

Kiki, Zinnia and Theta selected a tube on all trials. When thebait was located inside the bent tube, Heiji and Zilla failedto select a tube on four and six trials respectively despitesearching in all the tubes repeatedly. Looking at only thosetrials on which a selection was made, Zilla, Heiji and Kikiselected the correct tube significantly above chance (33%),only when a straight tube was baited (straight tube baited:Heiji: 20/20, Kiki: 13/20 and Zilla: 18/20 correct, binomialtests: all p<0.005; bent tube baited—Heiji: 3/8, Kiki: 4/12and Zilla: 2/6 correct, binomial tests: all p>0.05;). Thetaand Zinnia continued to show strong location biases againstand for the middle tube (0 and 29 selections out of 32,respectively). The following analyses are again restricted tothe three successful monkeys, assessed individually usingnonparametric tests.

Search behavior

Zilla, Heiji and Kiki looked into at least one tube onall trials. Figure 3 shows how the monkeys made signif-icantly more number of looks on trials when the bait wasin the bent tube compared to trials where the bait wasin a straight tube, regardless of whether the trial endedwith a correct or incorrect response (Mann–Whitney tests:Heiji: z=−3.569, p<0.001; Kiki: z=−1.988, p=0.047;Zilla: z=−3.269, p<0.001). Comparing the number oflooks into the straight tubes and the bent tube on eachtrial, the monkeys looked equally frequently into the benttube and the straight tubes (adjusted for unequal numberof tubes; Wilcoxon Signed Ranks tests: Heiji: z=−1.039,

Fig. 3 Experiment 2–average number of looks per tube per trialaccording to baiting conditions. ST-VI: looks into straight tubes, baitin straight tube; BE-VI: looks into bent tube, bait in straight tube;ST-IN: looks into straight tubes, bait in bent tube; BE-IN: looks intobent tube, bait in bent tube

Kiki: z=−0.744, Zilla: z=−1.034, all p>0.05). Finally, nosuccessful ‘super-efficient’ searches occurred, although atotal of 36 was possible for all the three monkeys combined.

Discussion

The same three monkeys completed Experiment 2 abovechance, but only when the bait was placed inside a straighttube and therefore could be located through visual search-ing. Furthermore, when the bait was inside the bent tube,the monkeys looked into the tubes more frequently, andtwo monkeys failed to select a tube on a total of 10 trials.It appears that the monkeys failed to understand the visualaffordances of the bent tube. Instead, they treated the benttube much as if it was a straight tube, i.e. when no baitwas visible, they continued searching and failed to inferthe bait’s location within the bent tube.

The monkeys did not avoid searching the bent tube, whichmay suggest that they failed to understand that lines ofsight must be straight. In humans, this ability appears todevelop around 5 years of age. Flavell et al. (1991) showedyoung children tubes with different degrees of curvature,and asked them to predict whether they would be able to seeobjects placed at the other end of the tubes when lookingthrough them. Over 70% of 3-year-old children and 53%of the 5-year-olds believed they would be able to see theobjects through a 90◦ bent tube, failing to appreciate thatlines of sight must be straight. The children were thenallowed to test their predictions and to look through oneof the tubes. After this feedback, the same tubes as in pre-feedback were shown to the children, who again were askedwhether they would be able to see an object placed at theother end of the tubes. This time, 80% of the 5-year-oldsgave the correct answer, while 68% of the 3-year-olds stillfailed to answer correctly.

Capuchin monkeys might similarly fail to realize thatthey cannot see around corners. However, since the baitingwas done invisibly, they did not know that the bait wasonly placed behind and not in front of the bend and there-fore always hidden from view. Possibly with more trials,the monkeys would have mastered this aspect of the ex-perimental procedure. We conducted only a small numberof trials to test the monkeys’ spontaneous understandingof their visual search behavior and to exclude improvedperformance through simple associations; however futurestudies could usefully run more trials with bent tubes toassess eventual adaptation of the monkeys’ understandingof their own search behavior.

General discussion

In two experiments, three out of five capuchin monkeyssuccessfully searched for a food reward that was placedinside one of the three tubes. In Experiment 1, thesemonkeys continued searching when they already knew(or should have known) that the bait was visible insidetransparent tubes. Searching did not increase their success,

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and no instances of inferring the bait location in an opaquetube occurred. In Experiment 2, when the bait was placedwithin a bent tube so that it could not be seen, the monkeysfailed to infer the correct location and selected tubesrandomly. The monkeys also persistently searched in thebent tube, failing to show any understanding that theycould not obtain any information about the bait locationfrom it.

This redundant search behavior by the capuchins con-trasts with what could be expected in the presence ofmetacognitive awareness, which would allow the monkeysto search only when necessary, i.e. when they do not al-ready have the relevant information. Instead, it appears thatseeing the bait inside a tube eventually triggered the se-lection of that tube. This interpretation is supported by thefact that in Experiment 1, the majority of trials consistedof the monkeys looking into the baited tube immediatelybefore making a selection, and the absence of any ‘super-efficient’ searches. Furthermore in Experiment 2, when thebait could not be seen, two otherwise successful monkeysfailed to select a tube on a total of 10 occasions. Executionof the selection response, after seeing the bait, is consistentwith response competition. In this context, response com-petition pits searching against selecting a tube (Hamptonet al. 2004); if the tendency to reach for a tube is weak,seeing the bait will strengthen the response.

If the response competition hypothesis is correct, a possi-ble explanation for the difference in searching behavior be-tween our capuchin monkeys and Hampton et al.’s (2004)rhesus macaques might lie in the two species’ thresholdfor the reaching response. Rhesus macaques might have alower reaching threshold than capuchin monkeys, the lat-ter requiring more searching before a selection is made.The present experimental setup might also have kept theswitchover point from searching to selection high, as mul-tiple looks into tubes were not penalized and it took littleeffort to check the tubes. In addition, capuchin monkeys areknown for their almost excessive curiosity and exploratorydrive (Fragaszy et al. 2005), which may have further in-creased this species’ likelihood of searching before makinga selection. Future studies might increase the relative costof searching by spacing the tubes further apart, or adjust-ing the height of tubes to make them more difficult to lookinto (Hampton et al. 2004). However, as Hampton et al.(2004) pointed out, the relative strength of search or choiceresponses could also be influenced by metacognitive abil-ities, in that awareness of an absence of knowledge aboutthe bait location could strengthen the search response. Thisinterpretation would suggest that capuchin monkeys have alower appreciation of the consequences of searching tubeson their knowledge states. However, given our small sam-ple size and lack of varied age and sex classes, the presentresults should be regarded as preliminary and in need ofreplication.

It is worth noting that a comparable failure to fully com-prehend the consequences of actions has been described forcapuchin monkeys’ tool use. Visalberghi and Limongelli(1996) reported that a capuchin monkey that used straw todip for honey through holes in the side of a box persisted in

trying to dip through the sides when the holes were movedto the top of the box. Fujita et al. (2003) found that capuchinmonkeys are sensitive to the spatial arrangements of foodand tools, but fail to take into account other environmen-tal circumstances. Fragaszy et al. (2004) argued that eventhough capuchin monkeys are proficient tool users, theyfail to understand the underlying causal relations betweentools and objects, and do not anticipate outcomes of theirmanipulations. Capuchins may therefore generally fail toconsider possible alternative future outcomes.

It is also conceivable that the capuchin monkeys’ exces-sive searching reflected an inability to inhibit previouslylearned behavioral sequences. Capuchin monkeys, but notchimpanzees, find it difficult to inhibit cursor movementsdirectly toward the goal in mazes presented on a computerscreen (Fragaszy et al. 2003). In spite of the limited numberof trials, it remains possible that our capuchin monkeys ac-quired an association between searching and food reward,in which case the tube paradigm would become no morethan a visual discrimination task. Difficulties with inhibit-ing learned behavioral sequences might have caused thetwo unsuccessful monkeys in the current study to developstrong location biases, and the three successful monkeys tounnecessarily search in the tubes.

One potentially fruitful approach would be to assess du-ration of visual search behavior in relation to decision pro-cesses. Using a simple discrimination task with stump-tailed macaques, Schrier (1983) found that the maximumfrequency of visual scanning coincided with the highestpercentage of correct selections, while the duration of fixa-tions remained stable. Schrier suggested that scanning pat-terns reflect stages of information processing, and dura-tion of fixations the later decision-making processes. If thisis correct and capuchin monkeys possess metacognitiveabilities, then we might expect to find the longest looksassociated with looking into the baited tube, reflecting adecision-making process, whereas looks into empty tubesmight be comparatively short, perhaps especially just be-fore making a selection. Unfortunately, the video record-ings of the present experiments did not give enough detailto investigate these issues, but future studies might utilizethis paradigm.

Metacognitive theories suppose an intimate link betweenunderstanding one’s own mental states and understandingothers’ mental states. For example, ‘simulation’ theoristshold that an individual first comes to understand its ownmental states through introspection. This insight is thenused to extrapolate from own mental states to those ofothers, through simulating their mental activity (Gordon1986; Goldman 1993; Povinelli and Vonk 2003). If thepresent results indicate limitations of capuchin monkeys’understanding of their own mental state of ‘knowing’, wemight expect related constraints on their understanding ofothers’ knowledge states and resulting behaviors. However,the data on this issue are equivocal. Capuchin monkeys canlearn to discriminate between a person ‘knowing’ and a per-son ‘guessing’ the location of a food reward, but it requiresmuch training and is not readily generalizable (Kuroshimaet al. 2002; 2003).

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In conclusion, compared to rhesus macaques and apes,capuchin monkeys show redundant searches on the tubetask, which might reflect limited metacognitive abilities,but other explanations are possible. Should additional evi-dence eventually weigh in favor of weak or absent metacog-nitive abilities in capuchin monkeys, then this might in-dicate an important phylogenetic difference between theOld World and New World monkeys, namely, the com-mon ancestors of the Old World monkeys and apes evolvedmetacognitive abilities after the split with the New Worldmonkeys.

Acknowledgements This work was supported by the JapaneseMinistry of Education, Culture, Science, Sports, and Technology(MEXT) through Grant in Aid for Scientific Research No. 13410026to K. Fujita, and the 21st Century Center of Excellence Program(D-10) to Kyoto University. The experiments in this paper compliedwith the Guide for the care and use of laboratory primates, PrimateResearch Institute, Kyoto University, and the current Japanese lawson animal experimentation.

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