learning and generalization of tool use by tufted capuchin monkeys (cebus apella) in tasks involving...

Learning and Generalization of Tool Use by Tufted Capuchin Monkeys(Cebus apella) in Tasks Involving Three Factors:

Reward, Tool, and Hindrance

Kazuo Fujita, Yoshiaki Sato, and Hika KuroshimaKyoto University

We tested 4 captive tufted capuchin monkeys (Cebus apella) for their understanding of physical causalityin variations of a 2-choice tool use task, 1 alternative of which allowed the monkeys easier access to food.Our monkeys, who had been adept at this task involving 2 items, that is, tool and food, quickly learned3-term problems involving food, tool, and 1 type of hindrance (an obstacle or a trap, which could preventsuccess). All of the monkeys generalized their performance to new problems with the other type ofhindrance and those with another familiar tool. These results suggest flexibility of their abilities toprocess complex physical information comprising 3 items in the environment, that is food–tool–hindrance spatial relationships. Such flexibility also implies that capuchin monkeys may possessrudimentary understanding of causal relationships involved in tool use.

Keywords: causal understanding, physical intelligence, tool use, tufted capuchin monkeys (Cebus apella)

Tool behavior by nonhuman animals has been widely analyzedboth in captivity and in the field. Tool use involves two aspects:the technique to maneuver the tool and the causal cognition atvarious levels to understand why the tool use leads to an otherwiseunattainable goal. Abundant research has shown techniques andrepertoires of animals’ tool behavior (see Anderson, 2006; Beck,1980, for comprehensive reviews across the animal kingdom;Emery & Clayton, 2004; Kacelnik, Chappell, Kenward, & Weir,2006, for reviews on corvids; Tomasello & Call, 1997, for a reviewon primates). Among primates, most work has focused on chim-panzees (e.g., Boesch & Boesch-Achermann, 2000; Goodall, 1986;Matsuzawa, 2001; McGrew, 1992, 1994; Ohashi, 2006; Visal-berghi & Fragaszy, 2002; Whiten et al., 1999, 2001; Yamakoshi,2001, 2004) and capuchin monkeys (e.g., Fragaszy, Visalberghi, &Fedigan, 2004; Ottoni & Mannu, 2001; Visalberghi, 1990). Manyexperimental studies of tool behavior have been conducted onprimates (chimpanzees: Kohler, 1921; capuchin monkeys: Kluver,1933; rhesus macaques: Nellmann & Trendelenburg, 1926; Shep-

herd, 1910), but how these species recognize causality involved inthis complex behavior remains controversial (Fragaszy, Visal-berghi, & Fedigan, 2004; Hauser & Santos, 2007; Povinelli, 2000;Tomasello & Call, 1997; Visalberghi & Fragaszy, 2006; Visal-berghi & Limongelli, 1996; Visalberghi & Tomasello, 1998).

Visalberghi and her coworkers (Limongelli, Boysen, & Visal-berghi, 1995; Visalberghi, Fragaszy, & Savage-Rumbaugh, 1995;Visalberghi & Limongelli, 1994, 1996; Visalberghi & Trinca,1989) investigated the causal comprehension in tool use tasks bytufted capuchin monkeys (Cebus apella), the most skillful toolusers among nonape primates, comparing them with great apes.They tested capuchins under several variations of the tube task inwhich the monkeys had to insert a stick into the tube to push thereward out. In a variation, the tube had a trap in the middle. Thus,the monkeys had to choose the side to insert the stick into so as tokeep the reward from dropping into the trap, that is, so that the trapwould not be on the passage of the reward pushed by the stick.Most monkeys failed in this “trap tube” task; only one capuchinsucceeded. Besides, even when the tube was placed upside down(inverted trap tube) so that there was no functional trap, the solesolver kept inserting the stick across the trap as if she had avoidedthe ineffective trap. Visalberghi and colleagues concluded that thismonkey did not understand the function of the trap, but used onlythe distance from the reward to the end of the tube as an associa-tive cue (Visalberghi & Limongelli, 1994). In contrast, two suc-cessful chimpanzees of five tested in the trap tube tasks showedmore flexible performances than capuchin monkeys, suggestingthat they understood the causal relationship between action andoutcome to some degree (Limongelli et al., 1995). However,success may not be shown in all situations; Povinelli (2000)showed that chimpanzees failed in the inverted trap condition ascapuchins in Visalberghi and Limongelli (1994). On the otherhand, in more recent tests, two orangutans and one chimpanzee of10 apes (orangutans, gorillas, chimpanzees, and bonobos) suc-

This article was published Online First August 16, 2010.Kazuo Fujita and Hika Kuroshima, Graduate School of Letters, Kyoto

University; and Yoshiaki Sato, Faculty of Letters, Kyoto University.Financial support was provided by the Japanese Society for the Promo-

tion of Science (JSPS) Grants-in-Aid for Scientific Research 13410026,17300085, and 20220004 to Kazuo Fujita, by a JSPS Research Fellowshipfor Young Scientists to Hika Kuroshima, by the Japan Ministry of Educa-tion, Culture, Sport, Science, and Technology (MEXT) 21st Century COEProgram D-10 to Kyoto University, and by the MEXT global COE Pro-gram D-07 to Kyoto University. We thank Primate Research Institute,Kyoto University, for providing monkeys through its Cooperative ResearchProgram. We are also grateful to James R. Anderson for editing a versionof the article.

Correspondence concerning this article should be addressed to KazuoFujita, Graduate School of Letters, Kyoto University, Yoshida-honmachi,Sakyo, Kyoto 606-8501, Japan. E-mail: [email protected]

Journal of Experimental Psychology: © 2010 American Psychological AssociationAnimal Behavior Processes2011, Vol. 37, No. 1, 10–19

0097-7403/10/$12.00 DOI: 10.1037/a0020274

10

ceeded in the modified trap tube task quickly in which the subjectswere allowed to choose among two actions, namely pushing out orraking in, for themselves, although the apes still failed in theoriginal trap tube task in which pushing out was the only way toobtain the reward (Mulcahy & Call, 2006). In another type of tubetask where subjects were required to modify tools to fit them forthe opening of the tube, chimpanzees, bonobos, and an orangutanshowed better performances than capuchins, although the apes andthe capuchins solved the problems as well (Visalberghi et al.,1995).

There is an argument that the inverted trap condition may not bea critical control to assess how the subjects understand the causal-ity involved in the task because there is no extra cost caused by the“error” (Seed, Tebbich, Emery, & Clayton, 2006). Indeed, humansalso showed such unnecessary bias (Silva, Page, & Silva, 2005).Thus, we should consider the possibility that the primates under-stood the function of the trap but still stuck to the strategy they hadlearned in the preceding training.

In a previous study, Fujita, Kuroshima, and Asai (2003) testedtufted capuchin monkeys for their causal understanding in anothertool use situation. We used the two-choice method devised byHauser and his coworkers with tamarins (Hauser, 1997; Santos,Rosati, Sproul, Spaulding, & Hauser, 2005), in which the twoalternatives were prearranged by the experimenter. Each alterna-tive included one piece of food and one tool, but only one alter-native led to easy access to the reward. All of the capuchins easilysolved the problems and generalized their performances to novelarrangements and tools. However, successful performances did notgeneralize to problems that included a hindrance located on thepath of the tools and the rewards. Therefore, capuchins appear tohave good understanding of how spatial relationships incorporat-ing two terms, tool and reward, cause success but poor understand-ing of incorporating three terms, tool, reward, and environment.The failure on the three-term task could explain why capuchinsfailed in the trap tube task.

However, capuchin monkeys may have deeper understanding ofcausality. Like chimpanzees’ nut cracking (Sugiyama & Koman,1979) and long-tailed macaques’ shell cracking (Malaivijitnond,Lekprayoon, Tandavanittj, Panha, Cheewatham, & Hamada,2007), capuchins crack open nuts with a stone, not only in captive(Anderson, 1990; Pouydebat, Gorce, Bels, & Coppens, 2006) andsemiwild situations (Ottoni, Dogo de Resende, & Izar, 2005;Ottoni & Mannu, 2001, 2003) but also in the wild (Fragaszy, Izar,Visalberghi, Ottoni, & Gomes de Oliveira, 2004; Moura & Lee,2004; Waga, Dacier, Pinha, & Tavares, 2006; see also Izawa &Mizuno, 1977). Capuchins also extract food with probing sticks incaptivity (Westergaard, Lundquist, Haynie, Kuhn, & Suomi, 1998;Westergaard, Lundquist, Kuhn, & Suomi, 1997) and in free-ranging situations (Lavallee, 1997), similar to wild chimpanzeesgathering termites or ants (Goodall, 1986; Nishida, 1973). Capu-chins may even transport tools (Cleveland, Rocca, Wendt, &Westergaard, 2004; Visalberghi, Spagnoletti, et al., 2009; see alsoJalles-Filho, da Cunha, & Salm, 2001). In fact, capuchins showvarious similarities to apes in tool use tasks. For instance, capu-chins, as well as chimpanzees, bonobos, and orangutans, modifiedsome of the tools potentially usable in the tube task (Visalberghi etal., 1995; Visalberghi & Trinca, 1989). Capuchins not only se-lected a stick of the appropriate thickness, but they also made thicksticks thinner so as to dip for honey with them through a small hole

(Anderson & Henneman, 1994). In the Hauser-type two-choicetasks, capuchins, unlike tamarins, converted the orientation of thetool (Cummins-Sebree & Fragaszy, 2005b). Cummins-Sebree andFragaszy (2005a) also reported that some capuchins mastered thecorrect manipulation of a hoe-like tool on the substrate withbarriers or holes to retrieve food. Capuchins are capable of usingmultiple tools in sequence; they can crack open walnuts with astone and then extract the meat with a stick (Westergaard &Suomi, 1993). Furthermore, they show different grips (power gripsor precision grips) when manipulating tools for different purposes(Westergaard & Suomi, 1997).

In this study, we conducted additional analyses of capuchins’causal cognition in the Hauser-type two-choice tasks, focusing onthe capuchins’ learning and generalization of the task involvingspatial relationships of the three elements of the tool use, namely,a reward (goal), tool (means), and environment. The third elementis often important in daily situations. In the present context, it wasphysical hindrance, which could prevent successfully obtainingfood. Although quite a few studies have analyzed the effects ofenvironmental objects such as a projection on the platform (capu-chins: Cummins-Sebree & Fragaszy, 2005a; Fujita et al., 2003)and a pitfall (chimpanzees: Limongelli et al., 1995; Povinelli,2000; Visalberghi & Limongelli, 1996; capuchins: Cummins-Sebree & Fragaszy, 2005a; Fujita et al., 2003; Visalberghi &Limongelli, 1994, 1996; vervet and tamarin monkeys: Santos,Pearson, Spaepen, Tsao, & Hauser, 2006), we stress here that thetwo-choice tasks have several advantages for analyzing causalunderstanding. First, the three-term spatial relationships among afood (target), tool (means), and hindrance (an obstacle or trap) inthe two-choice experiments simulate the essential parts of the traptube problem (a food, stick, and trap tube) in a simpler and moreobvious fashion (Povinelli, 2000). Second, the Hauser-type tasksfacilitate the experimental control of spatial relationships amongobjects on the substrate, so that we can set conditions to conductstricter analyses of the monkeys’ cognitive ability to handle thethree factors at a time. Third, these tasks require no pushing-outbehavior, which may interfere with learning how to avoid the trapin the trap tube tasks (Mulcahy & Call, 2006). Fourth, these tasksare more suitable for cross-species comparisons of tool use abilitythan other approaches such as the trap tube task because thetwo-choice tasks require participants simply to pull one of the toolspresented, with no particular dexterity required.

The failure of capuchins in the three-term tasks in Fujita et al.(2003) may have been due to a lack of ability. However, in fact, themonkeys received only 24 unique test trials for each of the twotypes of hindrances, trap and obstacle, which may not have beensufficient to move beyond an understanding of two-term spatialrelationships. To test the two possibilities, we first intensivelytrained capuchins that had learned the basic two-term problems onthe same 24 three-term problems; then we examined how themonkeys generalized their three-term performances to various newproblems, including ones presenting new tools and hindrances.

Before training the monkeys on three-term problems, we testedwhether our capuchins remembered how to succeed in two-termproblems involving only food and tool after a long period with norelevant testing. Then we trained the same monkeys on three-termproblems involving a reward, tool, and hindrance (Experiment 1).After reaching criterion, the monkeys were tested with arrange-ments that they never experienced in the training (Experiment 2).

11TOOL USE BY CAPTIVE CAPUCHINS

Next, they were given problems involving the kind of hindrancenot presented previously (trap problems for monkeys who wentthrough the obstacle problems in the training, and vice versa;Experiment 3). In the final test, we replaced the tool with a familiarnew tool used in the previous two-term problems (Experiment 4).

General Method

Subjects

The same four tufted capuchin monkeys (Cebus apella) from theprevious study (Fujita et al., 2003) participated: Heiji, 10-year-oldmale; Zilla, 10-year-old female; Kiki, 9-year-old female; and Pig-mon, 6-year-old male (ages at the start of the present study). Themonkeys, born and reared in a group cage at the Primate ResearchInstitute, Kyoto University, were provided by the institute by wayof its Cooperative Research Program. They lived in a group ofseven individuals at the Graduate School of Letters, Kyoto Uni-versity. The housing consisted of 10 interconnected cages, eachsized approximately 60 cm wide � 70 cm long � 80 cm high,which complied with the Guide for the Care and Use of Labora-tory Primates ( Primate Research Institute, Kyoto University,2006). The monkeys were not deprived of food or water. Rewardswere given as a part of their daily ration, the remainder of whichwas given after all scheduled experiments were completed. Theywere tested individually in the test room. The experiments wereconducted with the approval of the Animal Experiment Committeeof the Graduate School of Letters, Kyoto University. The monkeyshad various laboratory experiences, including experiments on tool use(Fujita et al., 2003), operant discriminations (Anderson, Kuwahata,Kuroshima, Leighty, & Fujita, 2005; Fujita & Giersch, 2005), socialintelligence (Anderson, Kuroshima, Hattori, & Fujita, 2005; Ander-son, Kuroshima, Kuwahata, & Fujita, 2004; Fujita, Kuroshima, &Masuda, 2002; Hattori, Kuroshima, & Fujita, 2005; Kuroshima,Fujita, Adachi, Iwata, & Fuyuki, 2003; Kuroshima, Fujita, Fuyuki,& Masuda, 2002), and mirror-image stimulation (Paukner, Ander-son, & Fujita, 2004) before this study.

Apparatus

The experimental box was made of transparent acrylic board,measuring 46 cm wide � 46 cm long � 52 cm high. One wall ofthe box had a door that could be slid upward to make an opening25 cm wide � 3 cm high at the bottom through which the monkeysreached their arms toward tools to collect a reward. See Fujita etal. (2003) for a photographic view of the apparatus.

A white bubbled vinyl chloride tray was used as a substrate fortool use, measuring 44 cm wide � 58 cm long. Three rails on thetray, one in the center and one about 10 cm from either edge,formed two channels and guided the manipulated tools in theappropriate direction. A black opaque panel made of vinyl chlo-ride, measuring 47 cm wide � 60 cm long, was used to block themonkey’s view when the experimenter prepared food, tool, andhindrance on the substrate for a trial.

Two kinds of tool made of baked black nontoxic clay (Fimo),also used in the previous study (hook and scoop in Fujita et al.,2003), were used. The tools were designed to collect an appropri-ately placed food reward by simply pulling them. The hook was astraight stick with a curved top like an inverted J (see Figure 1 in

Fujita et al., 2003, for an image). The scoop had three rectangularcorners at the top (see Figure 3 in Fujita et al., 2003, for an image).It had two horizontal bars that could catch a food reward; thus, itsfunction is a little more complicated than the hook. Two identicaltools of each kind were used. Their approximate width, length,diameter, and weight were as follows: hook, 6.5 cm, 22 cm, 10mm, and 27 g, respectively; scoop, 8 cm, 23 cm, 10 mm, and 29 g,respectively.

An obstacle and a trap were used as hindrances, the thirdelement (environment) mentioned in the introduction. Obstacleswere rectangular plastic erasers wrapped in yellow-green vinyltape, 2 cm wide � 4 cm long � 1 cm high, that were stuck withdouble-face tape to the substrate tray. Traps were visible pitfalls, 4cm wide � 3 cm long, on the substrate tray. All of the traps werelocated within 19 to 41 cm of the edge of the substrate trayadjacent to the experimental box.

Problems

Each problem provided two alternatives for the monkeys on theright and the left sides of the substrate, each of which had acombination of a food reward (a 5-mm cube of sweet potato), atool, and a hindrance (obstacle or trap). The grips of the tools werelocated within reach of the monkeys about 16 cm distant from thesliding door of the experimental box. In one of the two alterna-tives, simply pulling the tool allowed the monkey easy access tothe reward. In the other, however, the food was arranged so that itwould not get hooked by the pulled tool, the obstacle would blockthe path of the pulled tool, or the food would fall into the trap.Although skillful or random maneuvering of the tool in the latteralternative could occasionally lead to obtaining a reward, onlypulling the former was defined as a correct choice. In fact, obtain-ing the reward from the wrong alternative was rare.

We designed several sets of problems; a set contained 12 pairsof spatial arrangements of food, tool, and hindrance, each pre-sented once in a random order in each session. The arrangementswere all different except that those in Problems 1� through 6� ineach set were right–left switches of Problems 1 through 6. See theMethod section and figures of each experiment for the sets used ineach test.

Procedure

The door of the box was closed before each trial. The experi-menter (E) placed the opaque panel against the box to interrupt themonkey’s view. E then arranged two combinations of food, tool,and hindrance on the substrate tray. The panel was then removedand, after about 6 s, E opened the sliding door by 3 cm to allow themonkey to choose a tool. E closed the door as soon as the monkeypulled the appropriately arranged tool and obtained the reward(defined as correct trials) or pulled the inappropriately arrangedtool, which did not yield the reward (defined as incorrect trials).Intertrial intervals were about 30 s. Each session consisted of 12trials throughout the present series of experiments, as in Fujita etal. (2003). One session was run each day. All sessions werevideotaped. E recorded the monkeys’ first pull of the tool as theirchoice. Although the monkeys’ responses were obvious, an assis-tant coded the monkeys’ choice in randomly chosen three sessions

12 FUJITA, SATO, AND KUROSHIMA

of the recovery phase described below. The interobserver matchingof the recorded choice was 100%.

The subjects were tested for their long-term retention of thepreviously trained performances on the 12 two-term problemsinvolving food and hook tool used in Experiment 1 of Fujita et al.(2003) after 2 years 5 months with no relevant experience. Weplanned to repeat sessions until the monkeys reached the originalcriterion (Fujita et al., 2003) of 10 or more correct trials of 12 intwo consecutive sessions. In fact, all four monkeys immediatelyperformed almost perfectly and required only two sessions, theminimum number, to reach the criterion. Heiji showed 12 and 11correct choices of 12 in the first and the second sessions, respec-tively; Zilla showed 10 and 10; Kiki showed 11 and 12; Pigmonshowed 12 and 12. Thus, it is evident that tufted capuchin monkeysseem to possess robust and impressive long-term memory for thistype of cognitive skill. They went to Experiment 1 immediatelyafter this recovery phase.

Experiment 1: Three-Term Training

This experiment aimed to train the monkeys on three-termproblems involving food, a tool, and a hindrance. In Fujita et al.(2003), no monkey was successful in generalization to these prob-lems after being trained only on two-term problems. We hypoth-esized two possible accounts for this result. One is that the failurewas caused by cognitive limits of tufted capuchin monkeys, that is,because the species cannot understand the three-term spatial rela-tionship. The other is simple preseveration with the previouslyextensively trained strategy with the two-term spatial relationshiprequired in the original problems. If the former is true, tuftedcapuchin monkeys would simply have difficulty learning three-term problems, or, if the monkeys manage to solve the problems,they would show poor generalization to variously modified novelproblems. Alternatively, if the latter is true, the monkeys wouldlearn three-term problems without much difficulty and, oncelearned, they would show good generalization to novel problems.

Procedure

The hook was used as a tool as in the recovery phase. Theproblems were the four sets shown in Figures 1a–1d, two of whichwere for the obstacle condition and the other two were for the trapcondition. All sets were those used in Fujita et al. (2003).

The four sets were each assigned to each individual: ObstacleSet B (see Figure 1b) to Heiji, Trap Set B (see Figure 1d) to Zilla,Obstacle Set A (see Figure 1a) to Kiki, and Trap Set A (see Figure1c) to Pigmon. Training continued until the monkeys reached thesame criterion as in the recovery phase, 10 or more correct of 12trials in two consecutive sessions.

Because Zilla did not reach this criterion after 25 sessions, shewas switched to Obstacle Set B (see Figure 1b), and the experi-ment continued.

Results and Discussion

Heiji, Kiki, and Pigmon reached criterion in about 10 sessions(10, 8, 11 sessions, respectively), as did Zilla when she was givenObstacle Set B (11 sessions).

In Fujita et al. (2003), selection of correct options in three-termproblems was not above chance level in 24 unique test trials. Inthis experiment, however, the same monkeys easily learned toselect an appropriate alternative in the three-term task. This sug-gests that training on two-term problems did not lead to insightinto three-term relationships involved in these types of tool tasks.

This training on the three-term task was in fact faster than theirfirst training on the two-term task, which took 15–19 sessions.This finding implies that this species is indeed able to process suchhigher order, more complicated, causal relationships. However, itwas necessary to test whether this learning would generalize tonovel situations before concluding that a simple learning set can-not account for success with the three-term task. The followingexperiments addressed this question using variously modifiednovel problems.

Experiment 2: Generalization to New Arrangements ofthe Same Type of Hindrance

Although the capuchin monkeys learned to perform well onthree-term problems, they could have learned each single problemwithout understanding a general rule leading to success. Thisexperiment was designed to test whether the monkeys wouldgeneralize their three-term performances to untrained problems.

1 2 3 4 5 6

1st session

2nd session

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obst obst obst trap

(a) obstacle set A

(b) obstacle set B

(c) trap set A

(d) trap set B

(e)

Figure 1. (a)–(d) Arrangement of food, hook, and hindrance (obstacle ortrap) in Experiment 1: the obstacle condition Set A (a) and Set B (b) andthe trap condition Set A (c) and Set B (d). These arrangements are the sameas those in Fujita et al. (2003). (e) The number of correct choices of 12 byeach monkey in each session of the generalization test in Experiment 2.Heiji, Zilla, and Kiki were tested in new arrangements of the obstacle taskand Pigmon was tested in those of the trap task.


The monkeys were tested with the other set of the same type ofhindrance used in Experiment 1.

Procedure

The same tool (hook) was used as in Experiment 1, and themonkeys were presented with the problem sets not used duringtraining in the first experiment: Obstacle Set A (see Figure 1a) forHeiji and Zilla, Obstacle Set B (see Figure 1b) for Kiki, and TrapSet B (see Figure 1d) for Pigmon. We conducted two sessions of12 trials as a generalization test.


All of the monkeys showed good generalization to untrainedproblems. Figure 1e shows each monkey’s number of correctchoices. Two of the monkeys (Heiji, p � .039, and Kiki, p � .001,binomial tests) attained statistical significance in the first session,and the others (Zilla, p � .039, and Pigmon, p � .006) reached itin the second session. If we combine the two sessions, all monkeysperformed at above chance ( p � .001 for Heiji, p � .023 for Zilla,p � .001 for Kiki, and p � .002 for Pigmon).

The results suggest that the monkeys had not simply learned toperform on each arrangement in Experiment 2. That is, they arelikely to have learned some more general rule about how to solvethe problems presented in training that was applicable to novelsituations where the spatial relationship among food, tool, andhindrance was altered.

Experiment 3: Generalization to a New Type ofHindrance

In this experiment, we further examined what the monkeys hadlearned in the preceding experiments; specifically, the possibilityof hindrance-specific learning was examined. The monkeys werepresented the same type of hindrance throughout Experiments 1and 2 (obstacle for Heiji, Zilla, and Kiki, and trap for Pigmon), butin this experiment, obstacle sets and trap sets were switched (trapfor Heiji, Zilla, and Kiki, and obstacle for Pigmon).

Procedure

Confirmation phase. Zilla and Pigmon received a single ad-ditional session of the same three-term problems used in Experi-ment 2 to reach the same criterion, 10 or more correct choices intwo consecutive sessions. This additional session was unnecessaryfor Heiji and Kiki, who immediately reached this criterion duringthe two test sessions in Experiment 2.

The hook was used in this confirmation phase and the followingtest phase. Before the test phase, we presented one obstacle set orone trap set to confirm the performance shown so far by eachmonkey. The obstacle set was the 12 problems extracted from thetwo sets, which were assigned odd numbers in Figures 1a and 1b;the trap set was the 12 extracted problems, assigned odd numbersin Figures 1c and 1d. Heiji, Zilla, and Kiki received the obstacle setbecause they were given the obstacle condition in Experiments 1and 2, and Pigmon received the trap set. In this phase, we relaxedcriterion to 18 or more correct choices in 24 trials during twoconsecutive sessions, which was statistically significant. The mon-keys proceeded to the test phase after reaching this criterion.

Test phase. The type of hindrance was switched to Trap SetsA and B (see Figures 1c and 1d) for Heiji, Zilla, and Kiki, who hadbeen tested on the obstacle condition, and to Obstacle Sets A andB (see Figures 1a and 1b) for Pigmon, who had been tested on thetrap condition.

We conducted two test sessions in a row for each of the two sets,comprising 48 test trials. Two sessions per set were run succes-sively. The order of sets was counterbalanced across monkeys, asis shown in Figure 2.


Confirmation phase. All of the monkeys immediatelyreached criterion. Heiji, Zilla, Kiki, and Pigmon chose correctly in22, 20, 21, and 22 trials, respectively, of 24 trials.

Test phase. Figure 2 shows each monkey’s number of correctchoices in each session of the test phase. Three of the monkeys(Heiji, Kiki, and Pigmon) showed good scores in the test, althoughthey may not have attained statistical significance in the very firstsession. However, there appears to have been no improvement inthe second session. If we combine the two sessions for each test,most of the monkeys’ scores were above chance (first test: p �.064, p � .152, p � .002, p � .007; second test: p � .001, p �.152, p � .007, p � .023, for Heiji, Zilla, Kiki, and Pigmon,respectively). Finally, if all of the test sessions were combined, allperformances were above chance (binomial tests: p � .029 forZilla, p � .001 for Heiji, Kiki, and Pigmon).

As the monkeys committed more errors than in the previousexperiment, we looked into each configuration of problems. Threemonkeys tested in trap sets performed poorly in two types ofproblems: 3 and 3� in Trap Set A (6 correct/12 trials for the datafor three monkeys summed) and 4 and 4� in Trap Set B (5/12).However, they performed much better in similar problems: 6 and6� in Trap Set B (10/12) and 5 and 5� in Trap Set A (8/12). Thus,it is difficult to determine whether these poorly performed prob-lems were due to certain arrangements or to a random error.

We also compared two seemingly easy problems in which onlyone option had a hindrance (1, 1�, 2, and 2� in each set) and fourmore difficult problems having a hindrance in each option (all

trap obst

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obst-B

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** * * * *

++

+: p<0.10 (/24 trs.)

p<0.05(/12 trs.)

Heiji Zilla Kiki Pigmon1 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4

Figure 2. The number of correct choices of 12 by each monkey in eachsession of the generalization test in Experiment 3. Heiji, Zilla, and Kikiwere tested for their generalization to the trap task and Pigmon was testedfor his generalization to the obstacle task.


others). Three monkeys tested in trap sets were correct in 15(93.8%), 13 (81.3%), and 14 (87.5%) trials of 16 trials for theone-hindrance problems and in 23 (71.9%), 19 (59.4%), and 25(78.1%) trials of 32 for the two-hindrance problems for Heiji,Zilla, and Kiki, respectively. The last monkey (Pigmon) tested inobstacle sets was correct in 13 (81.3%) of 16 for one-hindranceproblems and 22 (68.8%) of 32 trials for two-hindrance problems.Although the monkeys’ accuracies were in general better forone-hindrance problems than two-hindrance problems, none of thecomparisons for each subject between one- and two-hindranceproblems reached statistical significance in Fisher’s exact tests( ps � .079, .116, .358, and .288 for Heiji, Zilla, Kiki, and Pigmon,respectively). Thus, the monkeys’ performances were comparableregardless of the number of hindrances in each problem.

One should note that the two kinds of hindrance, obstacle andtrap, are different in how to hinder the monkeys from collecting thereward. An obstacle blocks the tool; a trap captures the reward intoitself. In other words, the same arrangements of food, tool, andhindrance sometimes lead to different results. In particular, thevertical location of food and hindrance is critical only for traps(e.g., Problems 3 and 3� in Trap Set A), whereas the horizontallocation of food and hindrance inside the tool never matters (i.e.,always makes an incorrect option) for obstacles (e.g., Problems 2and 2� for Obstacle Set A).

To check whether and how the monkeys recognized the functionof the two types of hindrance, we compared performances betweenthe problems in which a different hindrance changes or obscuresthe correct option as noted above (i.e., trial Types 3 and 3� of theTrap Set A and 6 and 6� of the Trap Set B [see Figure 1c and d])and those in which it does not (all others). Because the number oftrials was only eight for each monkey, the data were summedacross monkeys. The monkeys in total answered correctly in 16(66.7%) of 24 trials for the former and 130 (77.4%) of 168 for thelatter. These two proportions were comparable ( p � .184, Fisher’sexact test). This shows that it is unlikely for the monkeys toconfuse the two types of hindrance. It should be noted, however,that the evidence was not the strongest because 16 of 24 in thesemost critical test trials was a little short of statistical significance( p � .076, one-tailed), probably due to the small N.

The fact that monkeys generalized their performances duringtraining on one type of hindrance to the other suggests that theyregistered the necessity of taking a third environmental elementinto account in order to collect the food inside the tool and, at leastto some degree, the different functions of different types of hin-drances. However, it is still possible for the monkeys to havelearned some unidentified simple rules. Experiment 4 examinedsuch possibilities using a different tool.

Experiment 4: Generalization to a New Tool

Experiment 4 further investigated the generality of what themonkeys learned in the preceding experiments. In this experiment,a new but familiar tool, the scoop, replaced the hook (see Figures3a–3d). The monkeys had experienced this tool in the two-termcontext with success (Fujita et al., 2003), but had never experi-enced it in the three-term context.

Procedure

Confirmation phase. To confirm the monkeys’ performanceson the hindrance tasks, we trained the monkeys on all of the four setsshown in Figures 1a–1d until they scored 32 or more correct choiceson 48 trials, a statistically significant score at the 5% level, within foursessions in which all of the four sets were presented once.

We then examined the monkeys’ performances on the two-termproblems using the scoop. We used the two sets from Experiment4 in Fujita et al. (2003). Each of the two sets was tested once.Because Trial Types 1 and 1� of Set B (see Fujita et al., 2003) hadno incorrect option, performance on those trials was omitted fromthe scores, leaving a maximum of 20 correct choices.

Test phase. The three-term arrangements with the scoopshown in Figures 3a–3d were presented. The two sets of theobstacle and trap conditions were each tested twice in sequence.Between the tests with different sets, we conducted at least onesession using the 12 arrangements extracted from those in theconfirmation phase of Experiment 3 using the hook.

Here, we summarize the testing procedure: first, confirmation on allof the hindrance task sets with the hook until reaching the criterion;second, two sessions of two-term problems with the scoop; third, atleast one session on the extracted hindrance (obstacle or trap) set;fourth, two sessions of one of the hindrance (obstacle or trap) setshown in Figure 9 in Fujita et al. (2003). The third and the fourthphases were repeated four times, once for each hindrance set. Theorder of testing for each monkey was as shown in Figure 3e.

1 2 3 4 5 6

*: p<0.05 (/48 trs.)

**

p<0.05(/12 trs.)

No.

of C

orre

ct C

hoic

e

******

obst-B

obst-A

trap-B

trap-A

Subjects & Test Sessions

1234567812345678 12345678 12345678Heiji Zilla Kiki Pigmon

(a) obstacle set A

(b) obstacle set B

(c) trap set A

(d) trap set B

(e)

Figure 3. (a)–(d) Arrangement of food and tool in the generalization testof Experiment 4: the obstacle condition Set A (a) and Set B (b), and the trapcondition Set A (c) and Set B (d). (e) The number of correct choices of 12by each monkey in each session of the generalization test in Experiment 4.



Confirmation phase. All monkeys immediately completedthe confirmation phase of the three-term problems with the hook infour sessions.

The performance in the two-term problems with the scoopwas also good for all monkeys; it was above chance for allmonkeys: Heiji (19 correct of 20, binomial test: p � .001) andPigmon (20 of 20, p � .001), and for Zilla and Kiki (16 of 20,p � .012 for each). The results suggest that the monkeysmaintained good performances on two-term problems with thescoop.

Test phase. Figure 3e shows each monkey’s number of cor-rect choices in each test session. The monkeys showed goodgeneralization to new problems, although not all monkeys reachedstatistical significance in the very first session of each test. Themaximum number was 48 for each condition (obstacle or trap).The performance in each condition for each monkey was abovechance (binomial tests: p � .006 for Zilla in the trap condition, p �.002 for Kiki in the trap condition, and p � .001 elsewhere). Toestimate whether the ratio of correct choices varied across condi-tions (obstacle or trap), we applied Fisher’s exact tests to the dataand failed to find a significant difference for any monkey ( p �.261 for Heiji, p � .137 for Zilla, p � .208 for Kiki, and p � .317for Pigmon).

We again looked into each configuration of problems as inExperiment 3. For obstacle sets, monkeys in total were worstfor 2 and 2� in Set A and 6 and 6� in Set B: 10 correct of 16trials. For trap sets, monkeys were worst for 5 and 5� in Set Aand for 4 and 4� in Set B: 9 correct of 16 for the former and 10of 16 for the latter. For three of these problems, the distancebetween the reward and the functional hindrance was greaterthan for most of the other problems. Thus, the monkeys mighthave had difficulty in avoiding options with such configura-tions.

We again compared two types of seemingly easy problems inwhich only one option had a hindrance (1, 1�, 2, and 2� in eachset) and the remaining four types of more difficult problemshaving a hindrance in each option (all others). For obstacle sets,the monkeys were correct in 14 (87.5%), 11 (68.8%), 14 (87.5%), and15 (93.8%) trials of 16 for the one-hindrance problems and in 29(90.6%), 30 (93.8%), 27 (84.4%), and 30 (93.8%) of 32 for thetwo-hindrance problems for Heiji, Zilla, Kiki, and Pigmon, respec-tively. Fisher’s exact tests revealed that Zilla’s data were signifi-cantly different between the two types ( p � .033), but her accu-racy was in fact higher for supposedly more difficult two-hindrance problems. No other monkeys’ data reached significance( ps � .546, .571, and .713 for Heiji, Kiki, and Pigmon, respec-tively). For trap sets, the monkeys were correct in 14 (87.5%), 12(75.0%), 14 (87.5%), and 14 (87.5%) trials of 16 for the one-hindrance problems and 24 (75.0%), 22 (68.8%), 22 (68.8%), and27 (84.4%) trials of 32 for the two-hindrance problems for Heiji,Zilla, Kiki, and Pigmon, respectively. None of these differencesreached statistical significance: ps � .272, .462, .144, and .571 forHeiji, Zilla, Kiki, and Pigmon, respectively. Thus, the monkeys’performances were mostly comparable regardless of the number ofhindrances in each problem.

The results suggest that the monkeys solved the three-term tasksin Experiments 1 to 3 in a way not specific to the task with the

hook. In other words, the monkeys had learned a rather generalrule that allowed them to perform correctly on three-term problemsinvolving food, tool, and hindrance, irrespective of the shape of thetool.

General Discussion

In the recovery phase, despite a break of almost 2.5 years, allfour tufted capuchin monkeys maintained their good performanceon the basic tool task. This result shows impressively persistentlong-term memory in this species of New World monkeys.

In Experiment 1, all monkeys learned to choose the correctalternative in three-term problems incorporating food, tool, andhindrance. In subsequent experiments, the monkeys showed pos-itive transfer to novel types of spatial arrangements of the threeterms (Experiment 2), to different types of hindrance (Experiment3), and to a new familiar tool (Experiment 4). These results clearlydemonstrate that failure by the same capuchins to generalize theirperformance on two-term tasks to three-term tasks in the previousstudy (Fujita et al., 2003) was not due to a cognitive limitation butto a task requirement in the original training. It may be noted thatone monkey, Zilla, failed to learn the trap task at first, but after-ward she showed a positive transfer to the trap task after learningthe obstacle task. Thus, the ability to process three elements at atime may be universal in this species.

Our results suggest that the capuchin monkeys learned a generalrule of how to select a correct option in this complex tool use taskinvolving three items, namely food, tool, and hindrance. Thisperformance shows an excellent capacity to handle physical chal-lenges in this New World monkey species. The transfer of themonkeys’ performances to untrained types of hindrance in Exper-iment 3 warrants special attention in this regard; the good perfor-mance in their initial training on three-term problems was notlimited to the hindrance the monkeys tackled. Thus, the rule thatthe monkeys abstracted seems to have been general enough to besuccessfully applied to different types of hindrance, which may bespelled out as (a) no part of the tool is on the other side of theobstacle, so that it would not block the tool; and (b) the food isneither in alignment with the trap or on the other side of it, so thatthe food would not come over the trap.

Although our series of experiments may not completely reject apossibility of a simple stimulus generalization, our demonstrationis consistent with the idea that tufted capuchin monkeys have arudimentary understanding of the causality in tool use involvingthe three terms, food, tool, and environment. These findings areconsistent with the nut-cracking behavior reported by Fragaszy,Izar, et al. (2004) and Moura and Lee (2004), which also involvesthree-term spatial relationships among a nut, a hammer, and a hardsubstrate. Capuchins are in fact even selective in using hammers ofvarious weights (Visalberghi, Addessi, et al., 2009), although suchexcellent performances still could be a result of individual trial-and-error experience.

It is more difficult to reconcile the present findings with thefailure by the same species in the trap tube task (Visalberghi &Limongelli, 1994), which also incorporates the three terms, food,stick, and trap, in a manner more similar to our task. Here, wepropose a few possible reasons why monkeys failed in the traptube task. One is that the trap tube apparatus may have lookedmore complicated than our two-choice situations to the monkeys


because the tube was supported by poles and the food was locatedinside the transparent tube, which made the view of the foodindirect. Another possibility is that the monkeys had to push thefood away and out the other side, which may have required greaterself-control. It should be noted that apes performed better whenthey raked in the reward in the tube than when they pushed it out(Mulcahy & Call, 2006). Finally, in the two-choice task, themonkeys were able to compare the probability of success betweentwo visible options, whereas in the trap tube task they could not.These factors might have concealed the capuchins’ fine sensitivityto spatial relationships.

An interesting future study may ask whether capuchin monkeysare able to create arrangements that allow smooth collection offood by the use of tools. The two-choice task used in this series ofexperiment asked their recognition of successful and unsuccessfularrangements. In situations that require creating arrangements, wemay be able to know their understanding of causality in muchmore detail. Important issues may be whether they displace theobstacles, whether they put a cap on the trap, or whether they placea tool of a suitable shape and size in a good orientation at a goodlocation.

Another question may be whether capuchin monkeys predict themovement of the tool and the reward. Recent studies suggest thathumans, when they recognize the goal of the moving object, movetheir eye gaze to the goal in advance to its actual motion (Eshuis,Coventry, & Vulchanova, 2009). It is expected that the monkeys’gaze may anticipate the current motion of the tool and the rewardif they predict the result. This finding would provide strongerevidence for understanding causality.

The two-choice method like the one conducted in this study hasvarious advantages for analyzing nonhuman animals’ understand-ing of causality. One is that this method enables systematic ma-nipulation of variables potentially contributing this aspect of cog-nition. Our research exemplified this merit. In our case, variousexperimental modifications in numbers, types, and arrangementsof tool and hindrance revealed excellent physical cognition bycapuchin monkeys. Seed et al. (2006) pointed out that transfertasks would form an important paradigm for investigating thenature of animal physical cognition, as opposed to tests for all-or-none possession of intelligence such as causal understanding. Thetwo-choice task can be such a method.

The second advantage is that this method enables direct com-parison of a wide range of animals because all they must do is topull one of the tools. This is an operation that even birds and fishcan manage using their mouth. The behavior involved—pulling—is also naturalistic and this factor may make the task eveneasier to handle for many species. We should test not only primatesbut also birds such as corvids, which show excellent tool-using andtool-making skills sometimes almost comparable to those of apes(Chappell & Kacelnik, 2002, 2004; Kenward, Weir, Rutz, &Kacelnik, 2005; Weir, Chappell, & Kacelnik, 2002; see alsoEmery & Clayton, 2004; Kacelnik et al., 2006). Such a compara-tive analysis should shed light on how this important cognitiveability might have evolved.

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Received January 6, 2010Revision received May 12, 2010

Accepted May 12, 2010 �

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