Journal of Experimental Psychology: © 2010 American Psychological Association

Animal Behavior Processes 0097-7403/10/$12.00 DOI: 10.1037/a0020274

2011, Vol. 37, No. 1, 10 –19

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 Kuroshima

Kyoto University

We tested 4 captive tufted capuchin monkeys (Cebus apella) for their understanding of physical causality
in 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 learned
3-term problems involving food, tool, and 1 type of hindrance (an obstacle or a trap, which could prevent
success). All of the monkeys generalized their performance to new problems with the other type of
hindrance and those with another familiar tool. These results suggest flexibility of their abilities to
process complex physical information comprising 3 items in the environment, that is food–tool–
hindrance spatial relationships. Such flexibility also implies that capuchin monkeys may possess
rudimentary 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 analyzed
both in captivity and in the field. Tool use involves two aspects:
the technique to maneuver the tool and the causal cognition at
various levels to understand why the tool use leads to an otherwise
unattainable goal. Abundant research has shown techniques and
repertoires 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 review
on 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). Many
experimental studies of tool behavior have been conducted on
primates (chimpanzees: Köhler, 1921; capuchin monkeys: Klüver,
1933; rhesus macaques: Nellmann & Trendelenburg, 1926; Shep-
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 Fellowship
for Young Scientists to Hika Kuroshima, by the Japan Ministry of Educa-
tion, Culture, Sport, Science, and Technology (MEXT) 21st Century COE
Program 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 Research
Program. We are also grateful to James R. Anderson for editing a version
of the article.
Correspondence concerning this article should be addressed to Kazuo
Fujita, Graduate School of Letters, Kyoto University, Yoshida-honmachi,
Sakyo, Kyoto 606-8501, Japan. E-mail: kfujita@bun.kyoto-u.ac.jp
herd, 1910), but how these species recognize causality involved in
this 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 by
tufted capuchin monkeys (Cebus apella), the most skillful tool
users among nonape primates, comparing them with great apes.
They tested capuchins under several variations of the tube task in
which the monkeys had to insert a stick into the tube to push the
reward 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 to
keep the reward from dropping into the trap, that is, so that the trap
would not be on the passage of the reward pushed by the stick.
Most monkeys failed in this “trap tube” task; only one capuchin
succeeded. Besides, even when the tube was placed upside down
(inverted trap tube) so that there was no functional trap, the sole
solver kept inserting the stick across the trap as if she had avoided
the ineffective trap. Visalberghi and colleagues concluded that this
monkey did not understand the function of the trap, but used only
the 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 showed
more flexible performances than capuchin monkeys, suggesting
that they understood the causal relationship between action and
outcome 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 as
capuchins in Visalberghi and Limongelli (1994). On the other
hand, in more recent tests, two orangutans and one chimpanzee of
10 apes (orangutans, gorillas, chimpanzees, and bonobos) suc-

10
 TOOL USE BY CAPTIVE CAPUCHINS
ceeded in the modified trap tube task quickly in which the subjects
were allowed to choose among two actions, namely pushing out or
raking in, for themselves, although the apes still failed in the
original trap tube task in which pushing out was the only way to
obtain the reward (Mulcahy & Call, 2006). In another type of tube
task where subjects were required to modify tools to fit them for
the opening of the tube, chimpanzees, bonobos, and an orangutan
showed better performances than capuchins, although the apes and
the capuchins solved the problems as well (Visalberghi et al.,
1995).
There is an argument that the inverted trap condition may not be
a 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, humans
also 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 had
learned in the preceding training.
In a previous study, Fujita, Kuroshima, and Asai (2003) tested
tufted capuchin monkeys for their causal understanding in another
tool use situation. We used the two-choice method devised by
Hauser and his coworkers with tamarins (Hauser, 1997; Santos,
Rosati, Sproul, Spaulding, & Hauser, 2005), in which the two
alternatives 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 easily
solved the problems and generalized their performances to novel
arrangements and tools. However, successful performances did not
generalize to problems that included a hindrance located on the
path of the tools and the rewards. Therefore, capuchins appear to
have 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 capuchins
failed in the trap tube task.
However, capuchin monkeys may have deeper understanding of
causality. 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) and
semiwild 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 in
captivity (Westergaard, Lundquist, Haynie, Kuhn, & Suomi, 1998;
Westergaard, Lundquist, Kuhn, & Suomi, 1997) and in free-
ranging situations (Lavallee, 1997), similar to wild chimpanzees
gathering termites or ants (Goodall, 1986; Nishida, 1973). Capu-
chins may even transport tools (Cleveland, Rocca, Wendt, &
Westergaard, 2004; Visalberghi, Spagnoletti, et al., 2009; see also
Jalles-Filho, da Cunha, & Salm, 2001). In fact, capuchins show
various similarities to apes in tool use tasks. For instance, capu-
chins, as well as chimpanzees, bonobos, and orangutans, modified
some of the tools potentially usable in the tube task (Visalberghi et
al., 1995; Visalberghi & Trinca, 1989). Capuchins not only se-
lected a stick of the appropriate thickness, but they also made thick
sticks thinner so as to dip for honey with them through a small hole
11
(Anderson & Henneman, 1994). In the Hauser-type two-choice
tasks, capuchins, unlike tamarins, converted the orientation of the
tool (Cummins-Sebree & Fragaszy, 2005b). Cummins-Sebree and
Fragaszy (2005a) also reported that some capuchins mastered the
correct manipulation of a hoe-like tool on the substrate with
barriers or holes to retrieve food. Capuchins are capable of using
multiple tools in sequence; they can crack open walnuts with a
stone and then extract the meat with a stick (Westergaard &
Suomi, 1993). Furthermore, they show different grips (power grips
or 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 on
the capuchins’ learning and generalization of the task involving
spatial relationships of the three elements of the tool use, namely,
a reward (goal), tool (means), and environment. The third element
is often important in daily situations. In the present context, it was
physical hindrance, which could prevent successfully obtaining
food. Although quite a few studies have analyzed the effects of
environmental 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 the
two-choice tasks have several advantages for analyzing causal
understanding. First, the three-term spatial relationships among a
food (target), tool (means), and hindrance (an obstacle or trap) in
the two-choice experiments simulate the essential parts of the trap
tube problem (a food, stick, and trap tube) in a simpler and more
obvious fashion (Povinelli, 2000). Second, the Hauser-type tasks
facilitate the experimental control of spatial relationships among
objects on the substrate, so that we can set conditions to conduct
stricter analyses of the monkeys’ cognitive ability to handle the
three factors at a time. Third, these tasks require no pushing-out
behavior, which may interfere with learning how to avoid the trap
in the trap tube tasks (Mulcahy & Call, 2006). Fourth, these tasks
are more suitable for cross-species comparisons of tool use ability
than other approaches such as the trap tube task because the
two-choice tasks require participants simply to pull one of the tools
presented, 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, the
monkeys received only 24 unique test trials for each of the two
types of hindrances, trap and obstacle, which may not have been
sufficient to move beyond an understanding of two-term spatial
relationships. To test the two possibilities, we first intensively
trained capuchins that had learned the basic two-term problems on
the same 24 three-term problems; then we examined how the
monkeys generalized their three-term performances to various new
problems, including ones presenting new tools and hindrances.
Before training the monkeys on three-term problems, we tested
whether our capuchins remembered how to succeed in two-term
problems involving only food and tool after a long period with no
relevant testing. Then we trained the same monkeys on three-term
problems 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).
12 FUJITA, SATO, AND KUROSHIMA
Next, they were given problems involving the kind of hindrance
not presented previously (trap problems for monkeys who went
through the obstacle problems in the training, and vice versa;
Experiment 3). In the final test, we replaced the tool with a familiar
new tool used in the previous two-term problems (Experiment 4).
General Method
Subjects
The same four tufted capuchin monkeys (Cebus apella) from the
previous study (Fujita et al., 2003) participated: Heiji, 10-year-old
male; 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). The
monkeys, born and reared in a group cage at the Primate Research
Institute, Kyoto University, were provided by the institute by way
of its Cooperative Research Program. They lived in a group of
seven individuals at the Graduate School of Letters, Kyoto Uni-
versity. The housing consisted of 10 interconnected cages, each
sized 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. Rewards
were given as a part of their daily ration, the remainder of which
was given after all scheduled experiments were completed. They
were tested individually in the test room. The experiments were
conducted with the approval of the Animal Experiment Committee
of the Graduate School of Letters, Kyoto University. The monkeys
had various laboratory experiences, including experiments on tool use
(Fujita et al., 2003), operant discriminations (Anderson, Kuwahata,
Kuroshima, Leighty, & Fujita, 2005; Fujita & Giersch, 2005), social
intelligence (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 of
the box had a door that could be slid upward to make an opening
25 cm wide ⫻ 3 cm high at the bottom through which the monkeys
reached their arms toward tools to collect a reward. See Fujita et
al. (2003) for a photographic view of the apparatus.
A white bubbled vinyl chloride tray was used as a substrate for
tool use, measuring 44 cm wide ⫻ 58 cm long. Three rails on the
tray, one in the center and one about 10 cm from either edge,
formed two channels and guided the manipulated tools in the
appropriate direction. A black opaque panel made of vinyl chlo-
ride, measuring 47 cm wide ⫻ 60 cm long, was used to block the
monkey’s view when the experimenter prepared food, tool, and
hindrance 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 a
straight stick with a curved top like an inverted J (see Figure 1 in
Fujita et al., 2003, for an image). The scoop had three rectangular
corners 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, its
function is a little more complicated than the hook. Two identical
tools of each kind were used. Their approximate width, length,
diameter, and weight were as follows: hook, 6.5 cm, 22 cm, 10
mm, 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 third
element (environment) mentioned in the introduction. Obstacles
were rectangular plastic erasers wrapped in yellow-green vinyl
tape, 2 cm wide ⫻ 4 cm long ⫻ 1 cm high, that were stuck with
double-face tape to the substrate tray. Traps were visible pitfalls, 4
cm wide ⫻ 3 cm long, on the substrate tray. All of the traps were
located within 19 to 41 cm of the edge of the substrate tray
adjacent to the experimental box.
Problems
Each problem provided two alternatives for the monkeys on the
right and the left sides of the substrate, each of which had a
combination of a food reward (a 5-mm cube of sweet potato), a
tool, and a hindrance (obstacle or trap). The grips of the tools were
located within reach of the monkeys about 16 cm distant from the
sliding door of the experimental box. In one of the two alterna-
tives, simply pulling the tool allowed the monkey easy access to
the reward. In the other, however, the food was arranged so that it
would not get hooked by the pulled tool, the obstacle would block
the path of the pulled tool, or the food would fall into the trap.
Although skillful or random maneuvering of the tool in the latter
alternative could occasionally lead to obtaining a reward, only
pulling 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 pairs
of spatial arrangements of food, tool, and hindrance, each pre-
sented once in a random order in each session. The arrangements
were all different except that those in Problems 1⬘ through 6⬘ in
each set were right–left switches of Problems 1 through 6. See the
Method section and figures of each experiment for the sets used in
each 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 the
monkey’s view. E then arranged two combinations of food, tool,
and hindrance on the substrate tray. The panel was then removed
and, after about 6 s, E opened the sliding door by 3 cm to allow the
monkey to choose a tool. E closed the door as soon as the monkey
pulled the appropriately arranged tool and obtained the reward
(defined as correct trials) or pulled the inappropriately arranged
tool, which did not yield the reward (defined as incorrect trials).
Intertrial intervals were about 30 s. Each session consisted of 12
trials throughout the present series of experiments, as in Fujita et
al. (2003). One session was run each day. All sessions were
videotaped. E recorded the monkeys’ first pull of the tool as their
choice. Although the monkeys’ responses were obvious, an assis-
tant coded the monkeys’ choice in randomly chosen three sessions
 TOOL USE BY CAPTIVE CAPUCHINS 13

of the recovery phase described below. The interobserver matching 1 2 3 4 5 6

of the recorded choice was 100%.
(a) obstacle set A
The subjects were tested for their long-term retention of the
previously trained performances on the 12 two-term problems
involving food and hook tool used in Experiment 1 of Fujita et al.
(2003) after 2 years 5 months with no relevant experience. We (b) obstacle set B
planned to repeat sessions until the monkeys reached the original
criterion (Fujita et al., 2003) of 10 or more correct trials of 12 in
two consecutive sessions. In fact, all four monkeys immediately (c) trap set A
performed almost perfectly and required only two sessions, the
minimum number, to reach the criterion. Heiji showed 12 and 11
correct choices of 12 in the first and the second sessions, respec- (d) trap set B
tively; Zilla showed 10 and 10; Kiki showed 11 and 12; Pigmon
showed 12 and 12. Thus, it is evident that tufted capuchin monkeys
obst obst obst trap
seem to possess robust and impressive long-term memory for this (e) 㪈㪉
type of cognitive skill. They went to Experiment 1 immediately p<0.05 (/12 trs.)
㪈㪇
after this recovery phase.

No. of Correct Choice

㪏
1st session
Experiment 1: Three-Term Training 㪍

This experiment aimed to train the monkeys on three-term
problems 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 failure
was 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 previously
extensively trained strategy with the two-term spatial relationship
required in the original problems. If the former is true, tufted
capuchin 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 novel
problems. Alternatively, if the latter is true, the monkeys would
learn three-term problems without much difficulty and, once
learned, they would show good generalization to novel problems.
Procedure
The hook was used as a tool as in the recovery phase. The
problems were the four sets shown in Figures 1a–1d, two of which
were for the obstacle condition and the other two were for the trap
condition. All sets were those used in Fujita et al. (2003).
The four sets were each assigned to each individual: Obstacle
Set 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 Figure
1c) to Pigmon. Training continued until the monkeys reached the
same criterion as in the recovery phase, 10 or more correct of 12
trials in two consecutive sessions.
Because Zilla did not reach this criterion after 25 sessions, she
was 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 given
Obstacle Set B (11 sessions).
㪋 2nd session
㪉
㪇
㪟㪼㫀㫁㫀 㪱㫀㫃㫃㪸 㪢㫀㫂㫀 㪧㫀㪾㫄㫆㫅
Subjects
Figure 1. (a)–(d) Arrangement of food, hook, and hindrance (obstacle or
trap) in Experiment 1: the obstacle condition Set A (a) and Set B (b) and
the trap condition Set A (c) and Set B (d). These arrangements are the same
as those in Fujita et al. (2003). (e) The number of correct choices of 12 by
each monkey in each session of the generalization test in Experiment 2.
Heiji, Zilla, and Kiki were tested in new arrangements of the obstacle task
and Pigmon was tested in those of the trap task.
In Fujita et al. (2003), selection of correct options in three-term
problems was not above chance level in 24 unique test trials. In
this experiment, however, the same monkeys easily learned to
select an appropriate alternative in the three-term task. This sug-
gests that training on two-term problems did not lead to insight
into three-term relationships involved in these types of tool tasks.
This training on the three-term task was in fact faster than their
first training on the two-term task, which took 15–19 sessions.
This finding implies that this species is indeed able to process such
higher order, more complicated, causal relationships. However, it
was necessary to test whether this learning would generalize to
novel situations before concluding that a simple learning set can-
not account for success with the three-term task. The following
experiments addressed this question using variously modified
novel problems.
Experiment 2: Generalization to New Arrangements of
the Same Type of Hindrance
Although the capuchin monkeys learned to perform well on
three-term problems, they could have learned each single problem
without understanding a general rule leading to success. This
experiment was designed to test whether the monkeys would
generalize their three-term performances to untrained problems.
14 FUJITA, SATO, AND KUROSHIMA
The monkeys were tested with the other set of the same type of
hindrance used in Experiment 1.
Procedure
The same tool (hook) was used as in Experiment 1, and the
monkeys were presented with the problem sets not used during
training in the first experiment: Obstacle Set A (see Figure 1a) for
Heiji and Zilla, Obstacle Set B (see Figure 1b) for Kiki, and Trap
Set B (see Figure 1d) for Pigmon. We conducted two sessions of
12 trials as a generalization test.
Results and Discussion
All of the monkeys showed good generalization to untrained
problems. Figure 1e shows each monkey’s number of correct
choices. 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 it
in the second session. If we combine the two sessions, all monkeys
performed 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 to
perform on each arrangement in Experiment 2. That is, they are
likely to have learned some more general rule about how to solve
the problems presented in training that was applicable to novel
situations where the spatial relationship among food, tool, and
hindrance was altered.
Experiment 3: Generalization to a New Type of
Hindrance
In this experiment, we further examined what the monkeys had
learned in the preceding experiments; specifically, the possibility
of hindrance-specific learning was examined. The monkeys were
presented the same type of hindrance throughout Experiments 1
and 2 (obstacle for Heiji, Zilla, and Kiki, and trap for Pigmon), but
in this experiment, obstacle sets and trap sets were switched (trap
for 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 in
two consecutive sessions. This additional session was unnecessary
for Heiji and Kiki, who immediately reached this criterion during
the two test sessions in Experiment 2.
The hook was used in this confirmation phase and the following
test phase. Before the test phase, we presented one obstacle set or
one trap set to confirm the performance shown so far by each
monkey. The obstacle set was the 12 problems extracted from the
two sets, which were assigned odd numbers in Figures 1a and 1b;
the trap set was the 12 extracted problems, assigned odd numbers
in Figures 1c and 1d. Heiji, Zilla, and Kiki received the obstacle set
because they were given the obstacle condition in Experiments 1
and 2, and Pigmon received the trap set. In this phase, we relaxed
criterion to 18 or more correct choices in 24 trials during two
consecutive 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 Sets
A and B (see Figures 1c and 1d) for Heiji, Zilla, and Kiki, who had
been tested on the obstacle condition, and to Obstacle Sets A and
B (see Figures 1a and 1b) for Pigmon, who had been tested on the
trap 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, as
is shown in Figure 2.
Results and Discussion
Confirmation phase. All of the monkeys immediately
reached criterion. Heiji, Zilla, Kiki, and Pigmon chose correctly in
22, 20, 21, and 22 trials, respectively, of 24 trials.
Test phase. Figure 2 shows each monkey’s number of correct
choices in each session of the test phase. Three of the monkeys
(Heiji, Kiki, and Pigmon) showed good scores in the test, although
they may not have attained statistical significance in the very first
session. However, there appears to have been no improvement in
the 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, all
performances were above chance (binomial tests: p ⫽ .029 for
Zilla, p ⬍ .001 for Heiji, Kiki, and Pigmon).
As the monkeys committed more errors than in the previous
experiment, we looked into each configuration of problems. Three
monkeys tested in trap sets performed poorly in two types of
problems: 3 and 3⬘ in Trap Set A (6 correct/12 trials for the data
for three monkeys summed) and 4 and 4⬘ in Trap Set B (5/12).
However, they performed much better in similar problems: 6 and
6⬘ 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 only
one option had a hindrance (1, 1⬘, 2, and 2⬘ in each set) and four
more difficult problems having a hindrance in each option (all
trap obst
㪈㪉 * + obst-A
* * *
* + * p<0.05
No. of Correct Choice
㪈㪇 obst-B
(/12 trs.)
㪏 trap-A
trap-B
㪍
㪋
* : p<0.05 (/24 trs.)
㪉
+: p<0.10 (/24 trs.)
㪇
1234 1234 1234 1234
㪟㪼㫀㫁㫀 㪱㫀㫃㫃㪸 㪢㫀㫂㫀 㪧㫀㪾㫄㫆㫅
Heiji Zilla Kiki Pigmon
Subjects & Test Sessions
Figure 2. The number of correct choices of 12 by each monkey in each
session of the generalization test in Experiment 3. Heiji, Zilla, and Kiki
were tested for their generalization to the trap task and Pigmon was tested
for his generalization to the obstacle task.
 TOOL USE BY CAPTIVE CAPUCHINS 15

others). Three monkeys tested in trap sets were correct in 15 1 2 3 4 5 6

(93.8%), 13 (81.3%), and 14 (87.5%) trials of 16 trials for the (a) obstacle set A
one-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 in (b) obstacle set B
obstacle sets was correct in 13 (81.3%) of 16 for one-hindrance
problems and 22 (68.8%) of 32 trials for two-hindrance problems.
(c) trap set A
Although the monkeys’ accuracies were in general better for
one-hindrance problems than two-hindrance problems, none of the
comparisons for each subject between one- and two-hindrance
(d) trap set B
problems 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 comparable * *
(e) 㪈㪉 * * * * * *
regardless of the number of hindrances in each problem.
obst-A

No. of Correct Choice

One should note that the two kinds of hindrance, obstacle and 㪈㪇 p<0.05
(/12 trs.) obst-B
trap, are different in how to hinder the monkeys from collecting the 㪏
reward. An obstacle blocks the tool; a trap captures the reward into trap-A
㪍
itself. In other words, the same arrangements of food, tool, and trap-B
hindrance sometimes lead to different results. In particular, the 㪋

vertical location of food and hindrance is critical only for traps 㪉

(e.g., Problems 3 and 3⬘ in Trap Set A), whereas the horizontal
location of food and hindrance inside the tool never matters (i.e.,
always makes an incorrect option) for obstacles (e.g., Problems 2
and 2⬘ for Obstacle Set A).
To check whether and how the monkeys recognized the function
of the two types of hindrance, we compared performances between
the problems in which a different hindrance changes or obscures
the correct option as noted above (i.e., trial Types 3 and 3⬘ of the
Trap 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 of
trials was only eight for each monkey, the data were summed
across monkeys. The monkeys in total answered correctly in 16
(66.7%) of 24 trials for the former and 130 (77.4%) of 168 for the
latter. These two proportions were comparable ( p ⫽ .184, Fisher’s
exact test). This shows that it is unlikely for the monkeys to
confuse the two types of hindrance. It should be noted, however,
that the evidence was not the strongest because 16 of 24 in these
most 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 during
training on one type of hindrance to the other suggests that they
registered the necessity of taking a third environmental element
into account in order to collect the food inside the tool and, at least
to some degree, the different functions of different types of hin-
drances. However, it is still possible for the monkeys to have
learned some unidentified simple rules. Experiment 4 examined
such possibilities using a different tool.
Experiment 4: Generalization to a New Tool
Experiment 4 further investigated the generality of what the
monkeys learned in the preceding experiments. In this experiment,
a new but familiar tool, the scoop, replaced the hook (see Figures
3a–3d). The monkeys had experienced this tool in the two-term
context with success (Fujita et al., 2003), but had never experi-
enced it in the three-term context.
*: p<0.05 (/48 trs.)
㪇
12345678 12345678 12345678 12345678
㪟㪼㫀㫁㫀 㪱㫀㫃㫃㪸 㪢㫀㫂㫀 㪧㫀㪾㫄㫆㫅
Heiji Zilla Kiki Pigmon
Subjects & Test Sessions
Figure 3. (a)–(d) Arrangement of food and tool in the generalization test
of Experiment 4: the obstacle condition Set A (a) and Set B (b), and the trap
condition Set A (c) and Set B (d). (e) The number of correct choices of 12
by each monkey in each session of the generalization test in Experiment 4.
Procedure
Confirmation phase. To confirm the monkeys’ performances
on the hindrance tasks, we trained the monkeys on all of the four sets
shown in Figures 1a–1d until they scored 32 or more correct choices
on 48 trials, a statistically significant score at the 5% level, within four
sessions in which all of the four sets were presented once.
We then examined the monkeys’ performances on the two-term
problems using the scoop. We used the two sets from Experiment
4 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) had
no incorrect option, performance on those trials was omitted from
the scores, leaving a maximum of 20 correct choices.
Test phase. The three-term arrangements with the scoop
shown in Figures 3a–3d were presented. The two sets of the
obstacle and trap conditions were each tested twice in sequence.
Between the tests with different sets, we conducted at least one
session using the 12 arrangements extracted from those in the
confirmation phase of Experiment 3 using the hook.
Here, we summarize the testing procedure: first, confirmation on all
of the hindrance task sets with the hook until reaching the criterion;
second, two sessions of two-term problems with the scoop; third, at
least one session on the extracted hindrance (obstacle or trap) set;
fourth, two sessions of one of the hindrance (obstacle or trap) set
shown in Figure 9 in Fujita et al. (2003). The third and the fourth
phases were repeated four times, once for each hindrance set. The
order of testing for each monkey was as shown in Figure 3e.
16 FUJITA, SATO, AND KUROSHIMA
Results and Discussion
Confirmation phase. All monkeys immediately completed
the confirmation phase of the three-term problems with the hook in
four sessions.
The performance in the two-term problems with the scoop
was also good for all monkeys; it was above chance for all
monkeys: Heiji (19 correct of 20, binomial test: p ⬍ .001) and
Pigmon (20 of 20, p ⬍ .001), and for Zilla and Kiki (16 of 20,
p ⫽ .012 for each). The results suggest that the monkeys
maintained good performances on two-term problems with the
scoop.
Test phase. Figure 3e shows each monkey’s number of cor-
rect choices in each test session. The monkeys showed good
generalization to new problems, although not all monkeys reached
statistical significance in the very first session of each test. The
maximum number was 48 for each condition (obstacle or trap).
The performance in each condition for each monkey was above
chance (binomial tests: p ⫽ .006 for Zilla in the trap condition, p ⫽
.002 for Kiki in the trap condition, and p ⬍ .001 elsewhere). To
estimate whether the ratio of correct choices varied across condi-
tions (obstacle or trap), we applied Fisher’s exact tests to the data
and failed to find a significant difference for any monkey ( p ⫽
.261 for Heiji, p ⫽ .137 for Zilla, p ⫽ .208 for Kiki, and p ⫽ .317
for Pigmon).
We again looked into each configuration of problems as in
Experiment 3. For obstacle sets, monkeys in total were worst
for 2 and 2⬘ in Set A and 6 and 6⬘ in Set B: 10 correct of 16
trials. For trap sets, monkeys were worst for 5 and 5⬘ in Set A
and for 4 and 4⬘ in Set B: 9 correct of 16 for the former and 10
of 16 for the latter. For three of these problems, the distance
between the reward and the functional hindrance was greater
than for most of the other problems. Thus, the monkeys might
have had difficulty in avoiding options with such configura-
tions.
We again compared two types of seemingly easy problems in
which only one option had a hindrance (1, 1⬘, 2, and 2⬘ in each
set) and the remaining four types of more difficult problems
having a hindrance in each option (all others). For obstacle sets,
the monkeys were correct in 14 (87.5%), 11 (68.8%), 14 (87.5%), and
15 (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 the
two-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%), and
27 (84.4%) trials of 32 for the two-hindrance problems for Heiji,
Zilla, Kiki, and Pigmon, respectively. None of these differences
reached statistical significance: ps ⫽ .272, .462, .144, and .571 for
Heiji, Zilla, Kiki, and Pigmon, respectively. Thus, the monkeys’
performances were mostly comparable regardless of the number of
hindrances in each problem.
The results suggest that the monkeys solved the three-term tasks
in Experiments 1 to 3 in a way not specific to the task with the
hook. In other words, the monkeys had learned a rather general
rule that allowed them to perform correctly on three-term problems
involving food, tool, and hindrance, irrespective of the shape of the
tool.
General Discussion
In the recovery phase, despite a break of almost 2.5 years, all
four tufted capuchin monkeys maintained their good performance
on the basic tool task. This result shows impressively persistent
long-term memory in this species of New World monkeys.
In Experiment 1, all monkeys learned to choose the correct
alternative in three-term problems incorporating food, tool, and
hindrance. In subsequent experiments, the monkeys showed pos-
itive transfer to novel types of spatial arrangements of the three
terms (Experiment 2), to different types of hindrance (Experiment
3), and to a new familiar tool (Experiment 4). These results clearly
demonstrate that failure by the same capuchins to generalize their
performance on two-term tasks to three-term tasks in the previous
study (Fujita et al., 2003) was not due to a cognitive limitation but
to a task requirement in the original training. It may be noted that
one monkey, Zilla, failed to learn the trap task at first, but after-
ward she showed a positive transfer to the trap task after learning
the obstacle task. Thus, the ability to process three elements at a
time may be universal in this species.
Our results suggest that the capuchin monkeys learned a general
rule of how to select a correct option in this complex tool use task
involving three items, namely food, tool, and hindrance. This
performance shows an excellent capacity to handle physical chal-
lenges in this New World monkey species. The transfer of the
monkeys’ 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 not
limited to the hindrance the monkeys tackled. Thus, the rule that
the monkeys abstracted seems to have been general enough to be
successfully applied to different types of hindrance, which may be
spelled out as (a) no part of the tool is on the other side of the
obstacle, so that it would not block the tool; and (b) the food is
neither in alignment with the trap or on the other side of it, so that
the food would not come over the trap.
Although our series of experiments may not completely reject a
possibility of a simple stimulus generalization, our demonstration
is consistent with the idea that tufted capuchin monkeys have a
rudimentary understanding of the causality in tool use involving
the three terms, food, tool, and environment. These findings are
consistent with the nut-cracking behavior reported by Fragaszy,
Izar, et al. (2004) and Moura and Lee (2004), which also involves
three-term spatial relationships among a nut, a hammer, and a hard
substrate. Capuchins are in fact even selective in using hammers of
various weights (Visalberghi, Addessi, et al., 2009), although such
excellent performances still could be a result of individual trial-
and-error experience.
It is more difficult to reconcile the present findings with the
failure 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, we
propose a few possible reasons why monkeys failed in the trap
tube task. One is that the trap tube apparatus may have looked
more complicated than our two-choice situations to the monkeys
 TOOL USE BY CAPTIVE CAPUCHINS
because the tube was supported by poles and the food was located
inside the transparent tube, which made the view of the food
indirect. Another possibility is that the monkeys had to push the
food away and out the other side, which may have required greater
self-control. It should be noted that apes performed better when
they raked in the reward in the tube than when they pushed it out
(Mulcahy & Call, 2006). Finally, in the two-choice task, the
monkeys were able to compare the probability of success between
two visible options, whereas in the trap tube task they could not.
These factors might have concealed the capuchins’ fine sensitivity
to spatial relationships.
An interesting future study may ask whether capuchin monkeys
are able to create arrangements that allow smooth collection of
food by the use of tools. The two-choice task used in this series of
experiment asked their recognition of successful and unsuccessful
arrangements. In situations that require creating arrangements, we
may be able to know their understanding of causality in much
more detail. Important issues may be whether they displace the
obstacles, whether they put a cap on the trap, or whether they place
a tool of a suitable shape and size in a good orientation at a good
location.
Another question may be whether capuchin monkeys predict the
movement of the tool and the reward. Recent studies suggest that
humans, when they recognize the goal of the moving object, move
their 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 reward
if they predict the result. This finding would provide stronger
evidence for understanding causality.
The two-choice method like the one conducted in this study has
various 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, various
experimental modifications in numbers, types, and arrangements
of tool and hindrance revealed excellent physical cognition by
capuchin monkeys. Seed et al. (2006) pointed out that transfer
tasks would form an important paradigm for investigating the
nature of animal physical cognition, as opposed to tests for all-or-
none possession of intelligence such as causal understanding. The
two-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 to
pull one of the tools. This is an operation that even birds and fish
can manage using their mouth. The behavior involved—
pulling—is also naturalistic and this factor may make the task even
easier to handle for many species. We should test not only primates
but also birds such as corvids, which show excellent tool-using and
tool-making skills sometimes almost comparable to those of apes
(Chappell & Kacelnik, 2002, 2004; Kenward, Weir, Rutz, &
Kacelnik, 2005; Weir, Chappell, & Kacelnik, 2002; see also
Emery & Clayton, 2004; Kacelnik et al., 2006). Such a compara-
tive analysis should shed light on how this important cognitive
ability might have evolved.
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Received January 6, 2010
Revision received May 12, 2010
Accepted May 12, 2010 䡲

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