Gorillas’ use of the escape response in object choice memory tests

ORIGINAL PAPER

Gorillas’ use of the escape response in object choice memory tests

Chikako Suda-King • Amanda E. Bania •

Erin E. Stromberg • Francys Subiaul

Received: 7 May 2012 / Revised: 31 July 2012 / Accepted: 7 August 2012 / Published online: 25 August 2012

� Springer-Verlag 2012

Abstract The ability to monitor and control one’s own

cognitive states, metacognition, is crucial for effective

learning and problem solving. Although the literature on

animal metacognition has grown considerably during last

15 years, there have been few studies examining whether

great apes share such introspective abilities with humans.

Here, we tested whether four gorillas could meet two cri-

teria of animal metacognition, the increase in escape

responses as a function of task difficulty and the chosen-

forced performance advantage. During testing, the subjects

participated in a series of object choice memory tests in

which a preferable reward (two grapes) was placed under

one of two or three blue cups. The apes were required to

correctly select the baited blue cup in this primary test.

Importantly, the subjects also had an escape response (a

yellow cup), where they could obtain a secure but smaller

reward (one grape) without taking the memory test.

Although the gorillas received a relatively small number of

trials and thus experienced little training, three gorillas

significantly declined the memory tests more often in dif-

ficult trials (e.g., when the location of the preferred reward

conflicted with side bias) than in easy trials (e.g., when

there was no such conflict). Moreover, even when objective

cues were eliminated that corresponded to task difficulty,

one of the successful gorillas showed evidence suggestive

of improved memory performance with the help of escape

response by selectively avoiding trials in which he would

be likely to err before the memory test actually proceeded.

Together, these findings demonstrate that at least some

gorillas may be able to make optimal choices on the basis

of their own memory trace strength about the location of

the preferred reward.

Keywords Metacognition � Ape � Gorillas � Escape

response

Introduction

Metacognition, the ability to reflect on our knowledge, is

essential for learning and problem solving (Nelson and

Narens 1990, 1994; Dunlosky and Metcalfe 2009). Imagine

a student preparing for a test. While reading the textbook,

the student will know what material is familiar and known

and what material requires more time for studying, allo-

cating her time and effort accordingly. During the test, the

student might skip difficult questions for which she does not

remember correct answers and might try to complete easy

questions first. After the test, the student will be able to

accurately judge the accuracy of her answers and might try

to improve her future grade by spending more time studying

the topics where she performed poorly. Such introspective

cognitive monitoring and control is called metacognition, or

C. Suda-King � A. E. Bania � E. E. Stromberg � F. Subiaul

Think Tank at the Smithsonian’s National Zoological Park,

Washington, DC, USA

C. Suda-King (&)

Center for Animal Care Sciences, Smithsonian Conservation

Biology Institute, PO Box 37012, MRC 5507,

Washington, DC 20013-7012, USA

e-mail: [email protected]; [email protected]

F. Subiaul

Department of Speech and Hearing Science, GW Mind-Brain

Institute and Institute for Neuroscience, The George Washington

University, Washington, DC, USA

F. Subiaul

Department of Anthropology, Center for the Advanced Study

of Human Paleobiology, The George Washington University,

Washington, DC, USA

123

Anim Cogn (2013) 16:65–84

DOI 10.1007/s10071-012-0551-5

thinking about thinking (Dunlosky and Metcalfe 2009;

Nelson and Narens 1990, 1994). Adult humans can accu-

rately judge their own memory prospectively, simulta-

neously, and retrospectively. They are also able to employ

appropriate strategies (e.g., seeking for information) on the

basis of such awareness to achieve better task performance

(Dunlosky and Metcalfe 2009). This skill, however,

develops gradually throughout childhood continuing well

into adolescence (Schneider 2008); though, children as

young as preschool age may have implicit awareness of

their own memory (e.g., Balcomb and Gerken 2008). The-

oretically speaking, the human metacognition model con-

sists of the object level and the meta-level, with the latter

monitoring and controlling the former (Nelson and Narens

1990, 1994). Because the model assumes that the meta-level

acts as executive functioning on the basis of secondary

representations (metarepresentations) of object-level rep-

resentations, metacognitive abilities have been associated

with both consciousness and self-awareness (e.g., Shea and

Heyes 2010).

Given that subjective introspection implies such higher

cognitive faculties, a fascinating question is whether non-

human animals share metacognitive skills with humans.

Since the pioneering work by Smith et al. (1995) exam-

ining a dolphin’s use of the uncertainty response in an

auditory discrimination task, comparative psychologists

have developed innovative nonverbal procedures in order

to assess subjects’ metacognitive abilities. In many com-

parative metacognition paradigms, animals are tested on a

primary task such as a perceptual discrimination or mem-

ory task. During testing, subjects are required to make a

perceptual (e.g., respond to largest item) or memory (e.g.,

respond to familiar item) response. Importantly, the sub-

jects are also allowed to make a secondary response, the

metacognitive response. Here, they can decline the current/

future test, seek for task-related information before taking

the test, or make a retrospective confidence judgment about

their own performance. The logic is this: Subjects should

use the metacognitive response based on the awareness of

their own cognitive states, such as uncertainty or the

strength of the memory trace. Accordingly, two standard

criteria inferring animal metacognition are as follows: (1)

Subjects should use the metacognitive response more

during difficult than during easy trials (for retrospective

judgments, subjects should rate difficult trials as low con-

fidence while rating easy ones as high confidence), and (2)

the subjects’ primary task performance should be better

when the subjects are given the option to make the meta-

cognitive response than when they are not (i.e., are forced

to take the test) (Hampton 2001; Inman and Shettleworth

1999; Sutton and Shettleworth 2008). Rhesus monkeys,

orangutans, and rats have met both of these criteria

(Hampton 2001; Hampton et al. 2004; Call and Carpenter

2001; Call 2005; Suda-King 2008; Foote and Crystal

2007), while the dolphin in Smith et al.’s (1995) study has

produced evidence meeting the first criterion only. Capu-

chin monkeys and birds have yielded mixed results. Results

suggest that these species’ functional use of the metacog-

nitive response might be restricted to specific circum-

stances (Fujita 2009; Beran and Smith 2011; Paukner et al.

2006; Basile et al. 2009; Inman and Shettleworth 1999;

Sutton and Shettleworth 2008; Nakamura et al. 2011). So

far, dogs have failed to show any convincing evidence of

metacognitive abilities (Brauer et al. 2004; McMahon et al.

2010).

Although the literature on animal metacognition con-

tinues to grow, the question of how to interpret the previous

data on animal metacognition remains a subject of consid-

erable debate, and alternative nonmetacognitive interpre-

tations have been proposed for the animals’ apparently

effective use of the metacognitive response (e.g., Hampton

2009). First, in many previous studies, observable cues have

been correlated with task difficulty (e.g., Smith et al. 1997).

Consequently, subjects may associate these cues with an

optimal response strategy that resembles metacognition. For

instance, in perceptual discrimination tasks, which typically

include numerous testing trials, the subjects might learn that

stimuli near their perceptual threshold result in poor per-

formance and consequently might avoid those stimuli

without any understanding of their own uncertainty. Sec-

ond, some studies have presented the primary responses

with the metacognitive response simultaneously, putting

these responses in direct competition with one another (e.g.,

Beran et al. 2006). As a result, subjects may learn which

primary response is most attractive and might learn to opt

for the metacognitive response when the degrees of attrac-

tiveness are roughly equal among primary responses. In

other words, the subjects could learn to select the secondary

response when they find themselves wavering between the

primary responses. Similarly, the response strength model

argues that the metacognitive response creates constant

attractiveness when the secondary response is plotted

against the test stimulus continuum, whereas each of the

primary responses produces different degrees of response

strength across the continuum, with the degree of attrac-

tiveness determined through previous reinforcement his-

tory. According to this model, the animals compare the

degrees of response strength for all the available responses

(both primary and secondary) and choose the one that is

most attractive without any awareness of their uncertainty

or confidence (Smith et al. 2008; Crystal and Foote 2009).

In an attempt to control for these confounds, various

experimental modifications have been introduced to animal

metacognition research. These modifications are the fol-

lowing: (1) introducing a small number of testing trials to

minimize learning effect (Hampton et al. 2004; Call and

66 Anim Cogn (2013) 16:65–84

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Carpenter 2001; Suda-King 2008), (2) designing a primary

task so that its difficulty is determined by subjective states

(such as memory strength) rather than objectively acces-

sible cues (i.e., perceptual discrimination cues) to avoid

associative learning (Hampton 2001; Kornell et al. 2007),

(3) arranging the presentation of the metacognitive

response temporarily distant from (either before or after)

the primary responses to avoid response competition

(Hampton 2001; Suda-King 2008; Kornell et al. 2007;

Smith et al. 2006; Fujita 2009; Son and Kornell 2005), (4)

introducing different tasks or new sets of stimuli to

examine whether the animals’ effective use of the meta-

cognitive response transfers without additional training to

further exclude the possibility of associative learning

(Kornell et al. 2007; Smith et al. 2010), (5) dissociating

reinforcement histories from task performance to refute the

response strength model (Smith et al. 2006), and (6) using

the pure escape response that simply generates a new trial

without direct rewards (Beran et al. 2006). Overall, accu-

mulating evidence has shown that rhesus monkeys continue

to effectively use the metacognitive response once all these

controls have been adopted (see a review by Terrace and

Son 2009). In contrast, there have been only three studies

examining great apes’ metacognitive abilities (Call and

Carpenter 2001; Call 2005; Suda-King 2008), only one of

which tested gorillas as subjects. Furthermore, this study

examined only the first criterion of animal metacognition,

that is, whether the gorillas would seek for information

more often in difficult trials (when they did not know the

location of hidden food reward) than in easy ones (when

they knew where the food was) (Call 2005). It is therefore

necessary to test whether this species of great ape can also

meet the second criterion of the chosen-forced performance

advantage. The investigation of gorillas’ potentially meta-

cognitive skills seems to be especially important because

gorillas were once considered to show little evidence of

mirror self-recognition (Suarez and Gallup 1981; Ledbetter

and Basen 1982; Shillito et al. 1999), a skill associated with

self-awareness (Gallup 1998). Although it has been even

argued that this species of great ape has lost their capacity

for self-recognition after splitting from a common ancestor

with the other great ape species (Povinelli 1993; Gallup

1997), more recent studies have revealed that at least some

gorillas may recognize themselves in mirrors (Parker 1994;

Patterson and Cohen 1994; Swartz and Evans 1994; Posada

and Colell 2007). Evidence of metacognition in gorillas

may provide additional evidence consistent with self-

awareness in this species and help paint a more complete

picture of the origins of these skills in great apes.

Here, we examined whether gorillas could decline dif-

ficult trials on the basis of their own memory trace strength

about the location of a food reward in a relatively small

number of trials. We tested four gorillas using the proce-

dure developed by Suda-King (2008). Using this paradigm

Suda-King (2008) demonstrated orangutans’ functional use

of a metacognitive ‘‘escape’’ response in a series of object

choice spatial memory tasks. In this study, orangutans met

the first criterion of metacognition, declining the test more

often in difficult trials than in easy trials. One of the

orangutans tested also met the second criterion of meta-

cognition, performing significantly better in a memory test

that she had agreed to take (i.e., free-choice trials) than

when forced to take the memory test (i.e., forced trials).

The gorillas’ primary task in the current study was to

remember the location of a preferred reward (i.e., two

grapes) hidden under one of several blue cups. On some

trials, the subjects also had an option of declining trials and

gaining a secure, but less preferable reward (i.e., one grape)

placed inside a yellow cup. We tested the two specific

predictions of metacognition: (1) The subjects should use

the escape response more often during difficult trials than

during easy trials, and (2) subjects should be more accurate

in the primary task during free-choice trials where they can

choose to take the test or not than during forced trials

where they are forced to take the test.

In order to examine the first criterion, we adjusted the

task difficulty by manipulating the visibility of baiting

(Visible vs. Hidden conditions in Experiment 1) and the

subjects’ visual access to the testing stimuli (Cover vs. No

Cover tests in Experiment 3). To test the second criterion,

we manipulated the availability of the escape response and

examined whether the gorillas were more accurate in the

memory test in free-choice trials than in forced-choice

trials (Free vs. Forced conditions in Experiments 2 and 3).

Also, in an attempt to rule out the response competition

account, we presented the escape response prior to the final

configuration of the memory test (in Experiments 2 and 3)

and introduced a new test in which the test stimuli (the blue

cups) were temporarily occluded from the subjects while

they decided to either take the test or escape (in Experi-

ment 3).

Due to the small sample size, we used nonparametric

tests for all subsequent analyses. All analyses were two-

tailed. All P values were exact, and the probability of a

type I error was maintained at 0.05.

Experiment 1

The purpose of this experiment was to examine whether

gorillas could effectively escape a memory test based on

the presence/absence of memory about the location of

preferred reward. The gorillas were tested using the same

procedure used in Suda-King (2008, Experiment 2). The

Anim Cogn (2013) 16:65–84 67

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subjects were first presented with a pair of identical blue

cups. The experimenter then hid a highly preferred reward

(two grapes) beneath one of them. The baiting procedure

was visible in half of the trials. In the other half, cups were

baited behind an occluder. The experimenter then placed a

yellow cup—the escape response—between the blue cups.

If it was chosen, subjects would obtain a guaranteed but

less preferred food reward (i.e., one grape). Selecting a

blue cup resulted in either a highly preferred food reward

or no reward at all. If the gorillas could tell when they had

not seen the location of the preferred reward, they should

choose the escape response more often in difficult trials,

when the baiting procedure is hidden, than in easy trials

when the baiting is visible.

Methods

Subjects

Four gorillas housed at the Smithsonian’s National Zoo-

logical Park served as subjects: one adult male (Baraka,

16 years old at the time of testing), two juvenile males

(Kojo and Kwame, 7 and 9 years old, respectively), and

one adult female (Mandara, 26 years old). The female is

the mother of the two juveniles. Although the adult male

was related to neither the female nor her offspring, the

female gorilla adopted him shortly after his birth and raised

him. When this male was 12 years old, he was transferred

to another facility for breeding, but a few years later

returned to the National Zoo as an adult during the course

of the current study. The subjects had previously partici-

pated in a computerized memory task (Subiaul unpublished

data), but had never participated in metacognition research.

The subjects lived with two other adult females in a social

group in indoor and outdoor compounds. These subjects

showed little interest in research and thus did not partici-

pate in the current study. Diets consisted of monkey chow,

fruits, greens, and vegetables, and several smaller enrich-

ment feedings were offered throughout the day, including

various types of browse and forage type foods. Testing

sessions occurred during normal daily separations of the

animals from their group, when individuals were separated

in their indoor enclosures for the afternoon diets. Water

was available ad libitum, and the subjects were not food

deprived during the testing.

Apparatus

The apparatus used in the current study were identical to

those used by Suda-King (2008, Experiment 2). Two opaque

blue plastic cups (7 cm top diameter 9 6 cm bottom diam-

eter 9 10 cm in height) and two opaque yellow plastic cups

(7 cm top diameter 9 6 cm bottom diameter 9 10 cm in

height) were used as hiding locations of rewards. The blue

cups were paired with two blue plastic dishes (9 cm top

diameter 9 7.5 cm bottom diameter 9 1.5 cm in height),

so that two grapes could be placed on a dish and covered with

a cup positioned upside down. One of the yellow cups was

filled with grapes and covered with a yellow plastic lid

(7.8 cm diameter 9 0.7 cm in height). This procedure pre-

vented the subjects from seeing the contents in the cups. The

other yellow cup was paired with a yellow dish (9 cm top

diameter 9 7.5 cm bottom diameter 9 1.5 cm in height),

so that one grape could be placed on it and covered with the

cup. In addition, two green plastic dishes (9 cm top diame-

ter 9 7.5 cm bottom diameter 9 1.5 cm in height) were

used to present two grapes and one grape in order to assess

the subjects’ reward preference. A four-sided wooden barrier

(34.5 cm width 9 19.5 cm depth 9 20 cm in height) was

used to visually block the baiting procedure from the subjects

on some trials (see below). The cups were placed on a

Plexiglas platform (94 cm length 9 25.5 cm width 9

2.5 cm in height), which rested on a wooden table (94 cm

length 9 61 cm width 9 83–92 cm in height) that was

positioned in front of a Plexiglas panel (either 112 cm 9

92 cm, 135 cm 9 92 cm, or 145 cm 9 92 cm, depending

on the cage used during testing; cages were at different

heights from the floor). The removable panel was attached to

the cage mesh with hooked metal bolts prior to the start of

testing. Each panel had three circular holes (3.3 cm in

diameter and 18.5 cm apart from each other) lined up near

the bottom, so that the subjects could indicate their choices

by inserting their fingers through one of them. The platform

had two plastic handles that allowed the experimenter to

easily slide it back and forth on the table. The height of the

table could be adjusted appropriately such that the platform

was positioned just below the holes in the Plexiglas panel.

All the testing trials were filmed with a Panasonic video

camera. The experimenter wore an earphone metronome to

count the length of each testing trial, and she also wore a

baseball cap throughout testing in an attempt to prevent the

subjects from using any social cues. When the subjects

were making their choice, she looked down at the center of

the platform such that the cap partially blocked her upper

face from their perspective.

Procedure

The procedure of the current experiment was identical to

those of Suda-King (2008, Experiment 2).

Training Prior to the testing, the experimenter trained the

subjects to point at a grape that was placed in front of a

hole in the Plexiglas panel. The subjects readily learned to

request a reward by inserting their finger through a corre-

sponding hole.

68 Anim Cogn (2013) 16:65–84

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Pretest Having completed the training phase, the subjects

proceeded to a pretest phase. The pretest phase consisted of

three tests: (a) Preference Test, (b) Low-Value Food

Association, and (c) Memory Test. The Preference Test was

conducted to make sure that the gorillas preferred two

grapes over one. The experimenter stood in front of each

subject, positioned the platform about 36 cm away from

the Plexiglas panel, and presented a pair of the green dishes

side by side on the center of the platform. While making

sure that the subject was paying attention, she placed two

grapes and one grape, respectively, on the dishes. She then

slid the dishes from the center to opposite sides of the

platform and positioned them in front of the far right and

left holes in the Plexiglas panel. Finally, the experimenter

pushed the platform against the Plexiglas panel, so that the

subject could choose one of the dishes. The subjects

received the contents of the selected dish. The locations of

the two different quantities were counterbalanced and

randomized across trials with a restriction that two grapes

did not appear in the same location in more than two

consecutive trials. The subjects were given 4–10 sessions

of 24 trials each, and they all came to prefer the larger

quantity of reward ([83 %).

The Low-Value Food Association was conducted to

facilitate the subjects’ learning of the contingency between

choosing the yellow cup and receiving one grape. The

experimenter presented the yellow cup with a lid filled with

grapes in front of one of the holes in the Plexiglas. Once the

subject chose the yellow cup, the experimenter lifted the lid,

picked up one grape, and gave it to the subject. Subjects

received 24 trials and always pointed at the yellow cup to

receive one grape.

The Memory Test was conducted to assess the subjects’

performance in a memory task in which two grapes were

hidden underneath one of the two blue cups. The experimenter

placed a pair of the blue dishes side by side on the center of the

platform and covered them with a pair of the upside-down

blue cups. While making sure that the subject was paying

attention, she then lifted one of the cups, placed two grapes on

the dish underneath, and hid the reward by covering it with the

cup. The experimenter slid the cups from the center to the

opposites of the platform such that the cups came in front of

the far right and left holes in the Plexiglas panel. Finally, she

pushed the platform against the Plexiglas panel to allow the

subject to make a choice. The subject received two grapes

only when it selected the baited blue cup. One session con-

sisted of a random mixture of 18 memory trials, six preference

trials, and six low-value association trials. All subjects pro-

ceeded to testing as they reached the criteria of performing

significantly above chance in the memory trials (C14/18,

P \ 0.031, Binominal test) within two sessions.

Test Experiment 1 had the following four conditions. The

(?) and (-) in the condition names indicate whether the

contents of the escape option were revealed or remained

concealed before the subjects made a choice (see below).

Visible (-) The procedure was identical to the Memory

Test described above where the experimenter hid two

grapes underneath one of the blue cups and placed them in

front of the far right and left holes. She then placed the

covered yellow cup filled with grapes in front of the center

hole in the Plexiglas panel such that it was located between

the blue cups. Finally, the experimenter pushed the plat-

form against the Plexiglas panel to allow the subject to

choose one of the cups. The subject received the corre-

sponding contents of the selected cup. The subject received

two grapes only upon choosing the baited blue cup,

whereas the selection of the empty blue cup led to no

reward. If the subject chose the yellow cup instead, the

experimenter lifted its lid and gave one grape to the sub-

ject. The yellow cup thus served as the escape response

with which the subject could receive a less preferable but

secure reward. Each trial was timed by the metronome and

lasted about 10 s from the moment when the experimenter

covered two grapes with the blue cup until the platform

touched against the Plexiglas panel (retention inter-

val = about 10 s).

Hidden (-) This condition was identical to the Visible

(-) condition except that the baiting of two grapes was

hidden from the subject. After presenting the two blue cups

with a dish underneath each on the center of the platform,

the experimenter covered the test stimuli with the wooden

box such that its opening sides faced down and toward the

experimenter. She then showed two grapes to the subject,

and surreptitiously hid the grapes under one of the blue

cups out of the subject’s view by lifting each cup behind

the barrier. The experimenter removed the box, and the rest

of the procedure was identical to the Visible (-) condition.

Each trial was timed by the metronome and lasted about

10 s from the moment when the experimenter removed the

wooden barrier until the platform touched against the

Plexiglas panel (retention interval = about 10 s).

Visible (?) The procedure was the same as in the Visible

(-) condition except that the subjects could see the con-

tents of the escape response. After hiding two grapes under

one of the blue cups and placing them in front of the far

right and left holes of the Plexiglas panel, the experimenter

presented the yellow dish containing one grape in front of

the center hole of the panel such that it was located

between the two blue cups. She then immediately covered

the grape with the yellow cup. Finally, the experimenter

pushed the platform against the Plexiglas panel to allow the

Anim Cogn (2013) 16:65–84 69

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subject to choose one of the cups. The subject received the

corresponding contents of the selected cup.

Hidden (?) The procedure was the same as in the Hidden

(-) condition except that the subject could see the contents

of the escape response. After removing the wooden barrier

and sliding the blue cups from the center to opposite sides

of the platform, the experimenter placed the yellow dish

containing one grape between the blue cups such that it was

located in front of the center hole of the Plexiglas panel.

She then immediately covered the grape with the yellow

cup and pushed the platform against the Plexiglas panel to

allow the subject to choose one of the cups. The subject

received the corresponding contents of the selected cup.

We conducted 24 trials for each condition per subject.

Besides the testing trials, 48 pretest preference trials were

interspersed among the trials of the four testing conditions

in order to assess the gorillas’ preference for the larger

quantity of grapes and maintain the subjects’ motivation

throughout the testing. Each subject received eight sessions

consisting of 18 trials each, for a total of 144 trials. Each

session was a random mixture of 12 testing trials (three

trials per condition) and six preference trials. Each session

started with three low-value food association trials, which

was designed to be as warm-up and a reminder of the

contingency between selecting the lidded yellow cup and

receiving one grape. The position of two grapes was

counterbalanced and randomized with a restriction that

they did not appear in the same position in more than two

consecutive trials.

Results

Memory performance and escape response

Table 1 presents the performance of each subject in the

four testing conditions and preference trials. All subjects

showed a significant preference for two grapes over one

grape in the preference trials, P \ 0.001, Binomial test.

When taking the memory test (i.e., when choosing a blue

cup), all subjects performed significantly above chance in

both of the Visible conditions, whereas none of them sig-

nificantly exceeded chance level in either of the Hidden

conditions (Visible conditions, P \ 0.005; Hidden condi-

tions, P [ 0.15, Binomial test). Therefore, the gorillas

were skillful at selecting a baited blue cup when they could

see the experimenter placing two grapes underneath one of

the blue cups, whereas they guessed the location of the

preferred reward when they had not seen the baiting.

In order to examine whether the gorillas were able to use

the escape response differentially among the four testing

conditions, we conducted a Cochran’s Q test on each

individual. Only one juvenile male, Kojo, differentially

used the escape option at a statistically significant level

(P = 0.001). Overall, he selected the yellow cup 10 times

in the Hidden conditions and 6 times in the Visible con-

ditions. Post hoc paired comparisons revealed that Kojo

chose the yellow cup significantly more often in the Hidden

(?) condition than in the Visible (-) condition (P = 0.008,

McNemar test). Kojo’s results of the both tests remained

significant even when the P values were corrected for

multiple comparisons (P = 0.004, P = 0.032, Sidak cor-

rections). No other significant differences were found for

the other comparisons examining the effect of baiting

visibility (Visible (?) vs. Hidden (?), P = 0.69, Visible

(-) vs. Hidden (-), P = 0.50, Visible (?) vs. Hidden (-),

P = 0.13, McNemar tests). Hence, there was some evi-

dence that Kojo avoided the memory test more often when

he had not seen the location of the preferred reward. Two

other subjects, Baraka and Kwame, also used the escape

response more often in the Hidden conditions than in the

Visible conditions although these differences only

approached statistical significance (P = 0.063, P = 0.32,

respectively, Cochran’s Q tests). Baraka selected the yel-

low cup 3 times in the Hidden conditions, whereas he never

used it in the Visible conditions. Kwame declined the

memory test 12 times in the Hidden condition, whereas he

only declined the memory test 6 times in the Visible con-

ditions. The remaining subject, Mandara, showed the

opposite pattern, selecting the yellow cup 7 times in the

Hidden conditions and 12 times in the Visible conditions

although no significant difference was detected in her use

of the escape option among the four testing conditions

(P = 0.061, Cochran’s Q test).

Further analyses revealed that Mandara had a strong

side bias and she used the escape option when she had seen

the location of the two grapes was opposite to her bias.

Table 2 shows Mandara’s performance as a function of the

position of the two grapes. The conditions were collapsed

into two according to the baiting visibility in the current

analyses. In the Hidden conditions, Mandara was signifi-

cantly more likely to select the baited blue cup when it was

on her left side than when on her right side (P \ 0.001,

Fisher’s exact test). This result indicates that she strongly

preferred the left cup over the right when she had not seen

the location of the two grapes, and trials were more dif-

ficult when the reward was placed under the right cup. She

also showed the same bias in the Visible conditions, per-

forming better in the memory test when the two grapes

were placed under the left cup than under the other cup,

although the difference was only marginally significant

(P = 0.051, Fisher’s exact test). We further compared

Mandara’s memory performance against chance. When the

two grapes were placed under the left cup, Mandara’s

memory performance was significantly above chance both

in the Visible and in the Hidden conditions (P \ 0.001,

70 Anim Cogn (2013) 16:65–84

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binomial test). In contrast, her success rate was signifi-

cantly below chance when the preferable reward was

placed under the right cup behind the barrier (P = 0.017,

binomial test), an indication of her bias for the left side.

Mandara’s memory performance was marginally above

chance when she had seen the experimenter placing the

two grapes under the right blue cup (P = 0.057, binomial

test). As for the use of the escape response, Mandara was

significantly more likely to choose the yellow cup when

she had seen the experimenter placing the two grapes

under the right blue cup (difficult trials) than when she had

seen the two grapes being placed under the left blue cup

(easy trials) (P = 0.017, Fisher’s exact test). Such a dif-

ferential use of the escape option was not found for the

Hidden conditions, presumably because she could not tell

where the experimenter placed the two grapes behind the

barrier (P = 0.42, Fisher’s exact test). Altogether, these

findings imply that Mandara selectively used the safe

choice when she had seen that the position of the prefer-

able reward conflicted with her side bias and she was

consequently able to improve her memory performance by

avoiding trials that were specifically difficult for her.

Therefore, Mandara met the first criterion of animal

metacognition by demonstrating the increased use of

escape option as a function of task difficulty.

Learning effect

Finally, we examined whether the gorillas changed their

escape strategies during the course of the experiment by

dividing the 8 sessions into 2 phases and comparing the

subjects’ performance between the first and second phases.

Specifically, we conducted Fisher’s exact test on a 2 9 2

table (Take test vs. Escape, 1st phase vs. 2nd phase) for

each condition type per subject. The four conditions were

collapsed into two according to the visibility of the baiting.

None of the subjects except for Kwame showed significant

differences in their use of escape response between the first

and second phases both for the Visible and for the Hidden

conditions (P [ 0.096). Only Kwame showed some evi-

dence of learning, using the escape response significantly

less often in the second phase than in the first phases of the

Visible conditions (P = 0.022). His use of the escape

response did not differ between the first and second phases

of the Hidden conditions (P = 0.32). Considering that

Mandara’s escape strategy was affected by the reward

Table 1 Subjects’ performance in the four testing conditions of Experiment 1

Subject Frequency Success (%) Escape (%) Preference (%)

Correct Wrong Escape

Baraka 91.7**

Visible (?) 22 2 0 91.7** 0.0 –

Hidden (?) 10 11 3 47.6 12.5 –

Visible (–) 21 3 0 87.5** 0.0 –

Hidden (-) 8 16 0 33.3 0.0 –

Kojo 97.9**

Visible (?) 16 2 6 88.9** 25.0 –

Hidden (?) 7 9 8 43.8 33.3 –

Visible (-) 21 3 0 87.5** 0.0 –

Hidden (-) 12 10 2 54.5 8.3 –

Kwame 100**

Visible (?) 17 3 4 85.0** 16.7 –

Hidden (?) 8 10 6 44.4 25.0 –

Visible (-) 19 3 2 86.4** 8.3 –

Hidden (-) 8 10 6 44.4 25.0 –

Mandara 87.5**

Visible (?) 14 2 8 87.5** 33.3 –

Hidden (?) 10 8 6 55.6 25.0 –

Visible (-) 19 1 4 95.0** 16.7 –

Hidden (-) 13 10 1 56.5 4.2 –

Success (%) = a percentage of trials in which the subjects selected the baited blue cup when they selected one of the two blue cups; escape

(%) = a percentage of trials in which the subjects selected the yellow cup; preference (%) = a percentage of trials in which the subjects selected

two grapes instead of one in the preference trials

** P \ 0.01, above chance (Binomial tests)

Anim Cogn (2013) 16:65–84 71

123

location when she could see the baiting, we also conducted

Fisher’s exact test on her 2 9 2 table (Take test vs. Escape,

1st phase vs. 2nd phase) for each reward location of the

Visible conditions in order to examine whether she learned

her functional use of the escape response during the testing.

There was little evidence of her learning across the first and

second phases for each reward location (P = 1.00), for

both right and left. Therefore, Mandara’s escape strategy

remained unchanged during testing. She selectively

declined difficult trials in which she had seen the reward

location conflicted with her side bias from the beginning of

testing.

Discussion

In general, the gorillas were very skillful at remembering

the location of the preferable reward when they could see

the experimenter placing it under one of the blue cups,

whereas their accuracy in the memory test did not differ

from chance when the baiting took place out of their sight.

As predicted, three out of the four subjects selected the

escape response more often when the baiting of the pref-

erable food was hidden than when it was visible, although

only one of them, Kojo, demonstrated statistically signifi-

cant results. These findings suggest that at least one subject

seemed to be able to avoid the memory test effectively

based on the absence/presence of his memory about the

reward location. The remaining one subject, Mandara,

showed an unpredicted yet functional use of the safe

choice. She was more likely to select the escape response

when she had seen the actual location of the two grapes

conflicted with her side bias (difficult trials) than when she

had seen there was no such conflict (easy trials). These

findings are consistent with a metacognitive interpretation

by showing that gorillas like orangutans (Suda-King 2008)

are able to quit a memory test when they have not seen or

are uncertain of the location of a preferable reward. Note

also that the current study administered the small number

of trials (only 24 trials for each condition per subject) in an

attempt to minimize the opportunity of learning. In fact,

none of the gorillas except for Kwame showed significant

evidence of learning in their use of the escape response

during the course of the current experiment. However,

given that the two types of conditions (Visual vs. Hidden)

differed from each other and task difficulty corresponded

with external cues such as the presence/absence of the

occluder (i.e., choosing the baited blue cup was more dif-

ficult when the barrier was presented) or the location of the

preferable reward (i.e., choosing the blue cup on the right

was more difficult than choosing the other cup), we cannot

totally rule out the possibility that the apes used such visual

cues to decline the memory test without monitoring their

own memory or uncertainty.

In Experiment 2, we tested gorillas’ use of the escape

response in the absence of such cues that may be used as

discriminative stimuli. Task difficulty was determined only

by the subjects’ memory about the location of the preferred

reward, rather than external cues such as the presence of

the physical barrier. The escape option was presented to the

gorillas on some trials, whereas it was unavailable on other

trials. If the gorillas can base their judgments on their own

memory trace strength, they should perform better in the

primary memory task when the escape option is available

than when it is not, because they should be able to improve

their memory performance with the help of the escape

response by selectively avoiding trials in which they are

likely to err.

Experiment 2

The previous experiment had shown that two of the gorillas

were able to use the escape response effectively in the

object choice memory task in which the visibility of the

baiting was systematically manipulated. However, even

with the small number of trials, the previous experiment

could not refute the possibility of associative learning

because visual cues corresponded to the task difficulty. In

order to rule out this alternative possibility, we further

examined whether the gorillas could selectively decline

difficult trials even without obvious external cues indicating

the difficulty of task. The gorillas were tested in the same

procedure as that of Experiment 4 of Suda-King’s (2008)

study, which was designed to eliminate the association

between visual cues and task difficulty. As in Experiment 1,

the two grapes were placed under one of the blue cups.

Subjects had the option to escape trials by choosing the

yellow cup. But unlike the previous experiment, the escape

Table 2 Mandara’s performance in Experiment 1 as a function of

reward location

Reward

position

Frequency Success

(%)

Escape

(%)Correct Wrong Escape

Visible

Right 11 3 10 78.6 41.7

Left 22 0 2 100.0** 8.3

Hidden

Right 5 17 2 22.7– 8.3

Left 18 1 5 94.7** 20.8

Success (%) = a percentage of trials in which the subject selected the

baited blue cup when she selected one of the two blue cups; escape

(%) = a percentage of trials in which the subject selected the yellow

cup; reward position = the position of two grapes from the subject’s

perspective

** P \ 0.01, above chance; – P \ 0.05, below chance (binomial tests)

72 Anim Cogn (2013) 16:65–84

123

response was available only in some trials, and the sub-

jects could always see the baiting. Thus, there were no

objective differences between easy and difficult trials, and

the task difficulty was determined solely by the apes’

subjective strength of their own memory trace about the

reward location. Moreover, the apes had to decide whether

they would like to take the memory test or escape it before

the memory test proceeded to the final stage. That is,

subjects had to decide before the two blue cups were

moved to the final configuration, which means that the

gorillas had to predict their memory performance before

testing. The metacognition model predicts that the gorillas

should avoid the memory test when their memory trace

strength about the location of preferred reward is weak.

Consequently, their memory performance should be better

when the escape response is available than when it is not,

because they should decline trials in which they are more

prone to err and should subsequently improve their

memory performance with the help of the escape response:

the second criterion of the chosen-forced performance

advantage.

Methods

Subjects

The same subjects as in Experiment 1 participated in the

current experiment.

Apparatus

We used the same apparatus as in Experiment 1 (blue cups,

blue dishes, yellow cups, yellow lid, yellow dish, green

dishes, platform, wooden table, and Plexiglas panels).

Procedure

The procedure of the current experiment was identical to

that of Experiment 4 of Suda-King’s (2008) study.

Experiment 2 had the following three conditions. The (?)

and (-) in the condition names indicate whether the con-

tents of the escape option were revealed or remained

concealed before the subjects made a choice (see below).

Free (-) The experimenter stood in front of each subject

and placed the platform approximately 36 cm away from

the Plexiglas panel. She placed a pair of the blue dishes

such that they were adjacent to each other and lined up on

the center line of the platform and then covered them with

the blue cups. Both of the blue cups were perpendicularly

positioned in front of the center hole of the Plexiglas panel.

The experimenter next hid two grapes under one of the blue

cups in full view of the subject and placed the covered

yellow cup full of grapes inside in front of either the left or

right hole of the panel. She finally pushed the platform

against the Plexiglas panel and allowed the subject to insert

its finger through one of the Plexiglas holes and make a

choice. If the subject chose the yellow cup, the experi-

menter lifted the lid, picked up one grape, and handed it to

the subject, upon which the trial was terminated and the

memory test did not proceed. The yellow cup thus served

as an escape response with which the subject could

immediately gain a secure but less preferable reward.

If the subject inserted its finger through the center hole

of the Plexiglas panel instead, the following memory test

proceeded: The experimenter pulled back the platform,

removed the yellow cup, and slid the blue cups from the

center to the both ends of the platform such that each blue

cup came in front of the right and left holes of the Plexiglas

panel. There were two types of the cup movements: (1) The

front cup moved toward right with the back cup moving

toward left from the subject’s perspective, and (2) the front

cup moved toward left with the back one moving toward

right from the subject’ perspective. Finally, the experi-

menter pushed the platform against the Plexiglas panel for

the subject to select one of the blue cups. If the subject

chose the baited blue cup, it received the two grapes. If the

subject selected the empty blue cup, it was shown the

location of the two grapes but did not receive any reward.

Each trial was timed by the metronome such that 6 s

elapsed from the moment when the experimenter covered

the two grapes with the blue cup until the platform touched

against the Plexiglas panel for the subject to make its first

choice. When the subject inserted its finger through the

panel’s center hole, 10 s elapsed from the moment when

the experimenter pulled back the platform until it touched

the panel again for the subject to make its second choice.

Therefore, each trial lasted for about 6 s when the subject

avoided the memory test by selecting the yellow cup,

whereas it lasted for about 16 s when the memory test

proceeded.

Free (?) The procedure was identical to that of the Free

(-) condition except that the subject was allowed to see the

contents of the yellow cup. Having hidden two grapes

under one of the blue cups in full view of the subject, the

experimenter placed a yellow dish containing one grape in

front of either the left or right holes of the Plexiglas panel.

She next placed the yellow cup on the dish, covering the

grape inside, and pushed the platform against the panel for

the subject to insert its finger through one of the holes and

make a choice. If the subject chose the yellow sup, the

experimenter lifted the yellow cup and gave its contents

(i.e., one grape) to the subject. If the subject inserted its

finger through the center hole, the memory test proceeded.

The experimenter pulled back the platform, removed the

Anim Cogn (2013) 16:65–84 73

123

yellow cup together with the dish underneath, and the rest

of the procedure was the same as in the Free (-) condition.

Forced The procedure was identical to that of the Free

(?) condition except that the escape option was taken away

from the subject before its first choice. Immediately after

placing the yellow dish containing one grape on the plat-

form, the experimenter removed the dish and its contents.

She then pushed the platform against the Plexiglas panel

for the subject to insert its finger through one of the holes

and make a choice. In this condition, the escape response

was not available, and the subject was forced to take the

memory test. Once the subject inserted its finger through

the center hole, the experimenter pulled back the platform

and the memory test proceeded. The rest of the procedure

was the same as in the previous two conditions.

We conducted 72 trials for each condition per subject. In

order to assess the gorillas’ preference for two grapes and

maintain their motivation throughout the testing, we also

interspersed 72 pretest preference trials among the trials of

the three testing conditions. Each subject received 18 ses-

sions consisting of 16 trials each, for a total of 288 trials.

Each session was a random mixture of 12 testing trials

(four trials per condition) and four preference trials. The

subjects also received three low-value food association

trials prior to each session as a warm-up and a reminder of

the contingency between the choosing the lidded yellow

cup and receiving one grape. The beginning and final

positions of the two grapes were counterbalanced and

randomized with a restriction that the preferred reward did

not appear in the same position in more than three con-

secutive trials.

Results

Table 3 shows the subjects’ performance in the three

testing conditions and preference trials. Gorillas main-

tained their preference for the two grapes over one

(P \ 0.001, binomial test). Only two of the subjects, Ba-

raka and Kwame, performed significantly better than

chance in the Forced condition (Baraka, P = 0.013;

Kwame, P \ 0.001; binomial test). Kwame’s memory

performance was also significantly above chance in the

Free (?) condition (P = 0.028, binomial test), whereas the

others’ performance in this condition did not significantly

differ from chance level. None of the subjects’ perfor-

mance significantly exceeded chance in the Free (-) con-

dition (P [ 0.086, binomial test).

There was no statistically significant difference between

the two Free conditions in the subjects’ memory perfor-

mance (P [ 0.16, for all the subjects, Fisher’s exact test),

so for subsequent analysis we combined them to reduce the

number of comparisons. In order to examine whether the

gorillas were significantly more successful in the memory

test when the escape option was available than when it was

not, we conducted Fisher’s exact test on each subject’s

2 9 2 table (Free vs. Forced, Correct vs. Wrong), with the

two Free conditions combined. Trials in which the subjects

chose the yellow cup were excluded from the current

analysis. Contrary to the prediction, the gorillas’ memory

performance was not affected by the availability of the

escape option (Baraka, P = 0.79; Kojo, P = 0.75; Kwame,

P = 0.18; Mandara, P = 0.81). That is, there was little

evidence that the gorillas were able to improve their

memory performance by selectively avoiding difficult

trials.

Discussion

Contrary to the second metacognitive prediction, the

gorillas failed to avoid the memory test selectively when

their memory trace strength about the location of the

preferable reward was weak. None of the gorillas were

significantly more successful when they had an option of

escaping the memory test as compared to when they were

forced to take the test. One possible explanation for the

current results is that the subjects did not use the escape

response carefully because they had a substantial proba-

bility of gaining the two grapes (i.e., 50 %) even when they

could only guess the location of the high-value reward.

Consequently, in the next experiment, we reduced the

probability of receiving the two grapes to encourage the

gorillas to use the escape response.

Experiment 3

The current experiment was newly designed to encourage

the effective use of the escape response in the gorillas.

Three blue cups, instead of two, were used as potential

hiding locations for the two grapes, which reduced the

chance of obtaining the high-value food from 50 to 33 %.

As in Experiment 2, the subjects were given an option of

declining the memory test before the memory test pro-

ceeded on two-thirds of trials, whereas they were forced to

take the test on the remaining one-third of trials. Unlike in

Experiment 2, the blue cups were temporarily covered with

a box when the subjects were deciding whether or not to

take the memory test on half of trials. Therefore, the sub-

jects had to predict their future memory performance

without seeing the final configuration of the memory test.

Moreover, on some trials, they also had to make a pro-

spective judgment without the direct visual access to the

test stimuli. If the gorillas can make optimal choices based

on their own memory trace strength about the location of

the preferred reward, they should perform better in the

74 Anim Cogn (2013) 16:65–84

123

memory test when they choose to take the test than when

forced to do so. That is, they should selectively avoid trials

in which they forget the correct reward location (i.e., the

second criterion of the chosen-forced performance advan-

tage). Moreover, it is expected that the memory test is more

difficult when the blue cups are temporarily occluded as

compared to when they remain visible. Therefore, the

gorillas should use the escape response more often in the

former trials than in the latter (i.e., the first criterion of the

increase in the escape use as a function of the task

difficulty).

Methods

Subjects

The same subjects as in the previous experiments, except

for Baraka, participated in the current experiment. He lost

his interest during the early stage of the current experiment

and refused to participate further.

Apparatus

We used the same apparatus as in the previous experiments

(blue cups, blue dishes, yellow cups, yellow lid, yellow

dish, green dishes, platform, wooden table, and Plexiglas

panels). In addition, we used a four-sided cardboard box

(11.5 cm 9 30.5 cm 9 12 cm) on some trials to cover the

blue cups when the subject was making a decision on

whether or not to take the memory test.

Procedure

Experiment 3 consisted of two sets of tests: (1) Cover and

(2) No Cover. The two tests were identical to one another

except that the blue cups were temporarily covered with a

cardboard box in the Cover test whereas they remained

visible in the No Cover test.

(1) Cover test

The first test had the following three conditions (Fig. 1).

The (?) and (-) in the condition names indicate whether

the contents of the escape option were revealed or

remained concealed before the subjects were allowed to

make a choice (see below).

Free (-) The experimenter stood in front of the subject

and placed the platform approximately 36 cm away from

the Plexiglas panel. She placed three blue dishes such that

they were adjacent to each other and lined up perpendic-

ularly in front of the center hole of the Plexiglas panel, and

covered them with three blue cups. In order to ensure that

the subject could see the baiting of the two grapes, the blue

cups were positioned slightly angled with the front cup

slightly off centered to right, the middle cup on the center

line of the platform, and the back cup slightly off centered

to left, from the subject’s perspective. The experimenter

next hid two grapes underneath one of the blue cups in full

view of the subject and covered the blue cups with the

cardboard box. She then placed the covered yellow cup

containing grapes in front of either the left or right hole of

the panel. She finally pushed the platform against the

Table 3 Subjects’ performance

in the three testing conditions of

Experiment 2

Success (%) = a percentage of

trials in which the subjects

selected the baited blue cup

when they selected one of the

two blue cups; escape (%) = a

percentage of trials in which the

subjects selected the yellow

cup; preference (%) = a


subjects selected two grapes

instead of one in the preference

trials

* P \ 0.05, ** P \ 0.01, above

chance (binomial tests)



Baraka 97.2**

Free (?) 2 4 66 33.3 91.7 –

Free (-) 10 4 58 71.4 80.6 –

Forced 47 25 – 65.3* – –

Kojo 97.2**

Free (?) 1 1 70 50.0 97.2 –

Free (-) 4 5 63 44.4 87.5 –

Forced 38 34 – 52.8 – –

Kwame 100**

Free (?) 28 13 31 68.3* 43.1 –

Free (-) 19 9 44 67.9 61.1 –

Forced 57 15 – 79.2** – –

Mandara 90.3**

Free (?) 5 6 61 45.5 84.7 –

Free (-) 8 4 60 66.7 83.3 –

Forced 37 35 – 51.4 – –

Anim Cogn (2013) 16:65–84 75

123

Plexiglas panel for the subject to make its first choice. If

the subject chose the yellow cup, the experimenter lifted

the lid and gave one of the grapes to the ape. Thus, this

choice served as an escape response with which the subject

could obtain the secure but less preferable reward without

taking the memory test. If the subject selected the card-

board box instead, the memory test proceeded. The

experimenter pulled back the platform and simultaneously

removed the box and the yellow cup. She then slid two of

the blue cups (with the dishes underneath) further apart so

that each one of them came in front of either the right or

left hole of the Plexiglas panel and adjusted the position of

the remaining blue cup so that it was in front of the center

hole. There were six types of cup movements: (1) The front

cup moved to right with the middle cup remaining at the

center and the back cup moving to left, (2) the front cup

moved to right with the middle cup moving to left and the

back cup remaining at the center, (3) the front cup moved

to left, with the middle cup moving to right and the back

cup remaining at the center, (4) the front cup moved to left

with the middle cup remaining at the center and the back

cup moving to right, (5) the front cup remained at the

center with the middle cup moving to left and the back cup

moving to right, and (6) the front cup remained at the

center with the middle cup moving to right and the back

cup moving to left. Finally, the experimenter pushed the

platform against the Plexiglas panel for the subject to select

one of the blue cups. If the subject selected the baited blue

cup, they received two grapes. If the subject chose an

empty blue cup, it was shown the correct location of the

two grapes but did not receive any reward. Each trial was

timed by metronome such that 8 s elapsed from the

moment when the experimenter covered the two grapes

with one of the blue cups until the platform touched against

the Plexiglas panel for the subject’s first choice. When the

subject chose to take the memory test, 12 s elapsed from

the moment when the experimenter pulled back the plat-

form until it was pushed back against the panel for the

subject’s second choice. Hence, each trial lasted for about

8 s when the subject declined the memory test, whereas it

lasted for about 20 s when the ape decided to take the

memory test.

Cover test

ForcedFree (-) Free (+)

1 grape(No test) Memory test

1 grape(No test) Memory test Memory test

2 grapes No reward 2 grapes No reward 2 grapes No reward

Fig. 1 Examples of trials from

the cover test of Experiment 3.

Each subject received 36 trials

per condition

76 Anim Cogn (2013) 16:65–84

123


(-) condition except that the subject was allowed to see the

contents of the yellow cup. Having hidden two grapes

under one of the blue cups in full view of the subject and

placed the cardboard box over the blue cups, the experi-

menter put a yellow dish containing one grape in front of

either the left or right holes of the Plexiglas panel. She next

placed the yellow cup on the dish, covering the grape

inside, and pushed the platform against the panel for the

subject to make its first choice. If the subject chose the

yellow cup, the experimenter lifted the yellow cup and

gave its contents (i.e., one grape) to the subject. If the

subject pointed at the cardboard box, the memory test

proceeded. The experimenter pulled back the platform and

simultaneously removed the box and the yellow cup

together with the dish underneath, and the rest of the

procedure was the same as in the Free (-) condition.

Forced The procedure was identical to that of the Free

(?) condition except that the escape option was taken

away from the subject before its first choice. Immediately

after placing the yellow dish containing one grape on the

platform, the experimenter removed the dish and its

contents. She then pushed the platform against the

Plexigas panel for the subject to insert its finger through

one of the holes and make a choice. In this condition, the

escape response was unavailable, and the subject was

forced to select the cardboard box. Once the subject

inserted its finger through the center hole, the experi-

menter pulled back the platform and the memory test

proceeded. The rest of the procedure was the same as in

the previous two conditions.

We conducted 36 trials for each condition per subject. In

order to assess the gorillas’ preference for two grapes and

maintain their motivation throughout the testing, we also

interspersed 24 pretest preference trials among the trials of

the three testing conditions. Each subject received six

sessions consisting of 22 trials each, for a total of 132 trials.

Each session was a random mixture of 18 testing trials (six

trials per condition) and four preference trials. The subjects

also received three low-value food association trials prior

to each session as a warm-up and a reminder of the con-

tingency between choosing the covered yellow cup and

receiving one grape. The beginning and final positions of

the two grapes, as well as the movement of the blue cups,

were counterbalanced and randomized with a restriction

that the preferred reward did not appear in the same posi-

tion in more than three consecutive trials.

(2) No Cover test

After the completion of the previous test, the subjects

proceeded to the second test. The No Cover test had three

conditions, which were identical to those of the Cover test

except that the cardboard box was not presented and the

blue cups remained visible throughout the trials (Fig. 2).

Free (-) The procedure was identical to that of Free (-)

of the Cover test except that the cardboard box did not

occlude the blue cups. After the experimenter hid two

grapes under one of the three blue cups, which were lined

up in front of the center hole of the Plexiglas panel, the

experimenter placed the covered yellow cup containing

grapes in front of either the right or left hole of the panel.

She then pushed the platform toward the subject allowing

them to make a choice. If the subject selected the yellow

cup, the experimenter lifted the lid and gave one grape to

the subject. If the subject inserted its finger through the

center hole of the panel instead, the memory test pro-

ceeded. The experimenter pulled back the platform and

removed the lidded yellow cup, and the rest of the proce-

dure was the same as in Free (-) of the Cover test.


(-) condition in the Cover test described above except that

the cardboard box was not used and the blue cups remained

visible. Having hidden two grapes under one of the blue

cups in full view of the subject, the experimenter placed a

yellow dish containing one grape in front of either the left

or right holes of the Plexiglas panel. She next placed the

yellow cup on the dish, covering the grape inside, and

pushed the platform against the panel for the subject to

make its first choice. If the subject chose the yellow cup,

the experimenter lifted the yellow cup and gave its contents

(i.e., one grape) to the subject. If the subject inserted its

finger through the middle hole of the platform, the memory

test proceeded. The experimenter removed the yellow cup

(with the dish and the grape underneath), and the rest of the

procedure was the same as in Free (?) condition in the

Cover test.

Forced The procedure was identical to that of Forced

condition in the Cover test except that the cardboard box

was not used. After hiding two grapes under one of the

three blue cups, the experimenter placed the yellow dish

containing one grape in front of either the right or left hole

of the panel and immediately removed it. She then pushed

the platform for the subject to make a choice. Once the

subject inserted its finger through the center hole of the

Plexiglas panel, the experimenter pulled back the platform

and moved the blue cups in a previously determined con-

figuration. The rest of the procedure was the same as in the

Forced condition of the Cover test.

Each trial lasted about 8 s when the subject chose the

escape option, while it lasted about 20 s when the ape

chose to take the memory test. We conducted 36 trials for

each condition per subject. In order to assess the gorillas’

preference for two grapes and maintain their motivation

Anim Cogn (2013) 16:65–84 77

123

throughout the testing, we also interspersed 24 pretest

preference trials among the trials of the three testing con-

ditions. Each subject received six sessions consisting of 22

trials each, for a total of 132 trials. Each session was a

random mixture of 18 testing trials (six trials per condition)

and four preference trials. The subjects also received three

low-value food association trials prior to each session as a

warm-up and a reminder of the contingency between

choosing the covered yellow cup and receiving one grape.

The beginning and final positions of two grapes, as well as

the movement of the blue cups, were counterbalanced and

randomized with a restriction that the preferred reward did

not appear in the same position in more than three con-

secutive trials.

Results

(1) Cover test


testing conditions and preference trials for the Cover test.

The gorillas maintained their preference for the larger

amount of reward (P \ 0.003, binomial test). Despite the

seemingly complicated movements of the cups as well as

the temporary visual occlusion of the test stimuli, one of

the gorillas, Kwame, performed significantly above chance

in all of the conditions (Free (-): P = 0.002; Free (?):

P = 0.018; Forced: P = 0.008, binomial test). Kojo’s

result approached the significance level in the Forced

condition only (P = 0.051, binomial test), while Mand-

ara’s performance failed to differ from chance level in any

of the conditions (P [ 0.20, binomial test). Consistent with

these individual differences in memory performance, Kojo

and Mandara declined the memory test in a large propor-

tion of Free trials ([90 %), whereas Kwame used the

escape response in less than 40 % of Free trials.



mance (P [ 0.55, for all the subjects, Fisher’s exact test),

so for subsequent analysis we combined them to reduce the




not, we conducted Fisher’s exact test on each subject’s

No cover test

ForcedFree (-) Free (+)

1 grape(No test) Memory test

1 grape(No test) Memory test Memory test

2 grapes No reward 2 grapes No reward 2 grapes No reward

Fig. 2 Examples of trials from

the No Cover test of Experiment

3. Each subject received 36

trials per condition

78 Anim Cogn (2013) 16:65–84

123

2 9 2 table (Free vs. Forced, Correct vs. Wrong). Trials in

which the subjects chose the yellow cup were excluded

from the current analyses. None of the gorillas as an

individual showed a significant difference in the memory

performance between the two types of conditions (Kwame,

P = 0.51; Kojo, P = 0.24; Mandara, P = 0.33). However,

all of the subjects showed the predicted behavioral pattern,

demonstrating higher memory accuracies in the Free con-

ditions than did in the Forced condition (see Table 4).

(2) No Cover test


testing conditions and preference trials for the No Cover

test. The gorillas continued to prefer the larger amount of

reward over the smaller one (P \ 0.001, Binomial test).

One of the gorillas, Kwame, who was the most successful in

the Cover test, performed significantly above chance in all

of the conditions (P \ 0.001, binomial test). Kojo’s per-

formance significantly exceeded chance level in the Forced

condition only (P = 0.004, binomial test). Mandara’s

performance failed to differ from chance level in any of the

conditions (P [ 0.21, binomial test). Again, consistent with

these individual differences in memory performance, Kojo

and Mandara declined the memory test in a large proportion

of Free trials ([88 %), whereas Kwame used the escape

response in less than 17 % of Free trials.



mance (P [ 0.48, for all the subjects, Fisher’s exact test), so

for subsequent analysis we combined them to reduce the




not, we conducted Fisher’s exact test on each subject’s 2 9 2

table (Free vs. Forced, Correct vs. Wrong). Trials in which

the subjects chose the yellow cup were excluded from the

current analyses. The gorillas’ memory performance did not

significantly differ by condition type (Kwame, P = 0.099;

Kojo, P = 1.00; Mandara, P = 0.41), although Kwame

showed the predicted performance pattern.

Table 4 Subjects’ performance

in the cover and No Cover tests

of Experiment 3

Success (%) = a percentage of

trials in which the subjects

selected the baited blue cup

when they selected one of the

three blue cups; escape (%) = a


subjects selected the yellow

cup; preference (%) = a


subjects selected two grapes

instead of one in the preference

trials

* P \ 0.05; ** P \ 0.01, above

chance (Binomial tests)



Kojo

Cover 100**

Free (?) 2 0 34 100 94.4 –

Free (-) 1 0 35 100 97.2 –

Forced 18 18 – 50.0 – –

No Cover 100**

Free (?) 1 2 33 33.3 91.7 –

Free (-) 1 0 35 100 97.2 –

Forced 21 15 – 58.3** – –

Kwame

Cover 95.8**

Free (?) 14 10 12 58.3* 33.3 –

Free (-) 15 7 14 68.2** 38.9 –

Forced 20 16 – 55.6** – –

No Cover 91.7**

Free (?) 29 1 6 96.7** 16.7 –

Free (-) 29 1 6 96.7** 16.7 –

Forced 31 5 – 86.1** – –

Mandara

Cover 83.3**

Free (?) 1 0 35 100 97.2 –

Free (-) 2 1 33 66.7 91.7 –

Forced 16 20 – 44.4 – –

No Cover 91.7**

Free (?) 1 2 33 33.3 91.7 –

Free (-) 3 1 32 75.0 88.9 –

Forced 13 23 – 36.1 – –

Anim Cogn (2013) 16:65–84 79

123

Overall analyses

The previous analyses of the two tests in Experiment 3

revealed that one of the three tested gorillas, Kwame,

generally showed the predicted pattern, performing better

in the memory test when he had the option of declining the

memory test than when he was forced to take the test. The

same subject was also the only animal whose escape fre-

quency was at a middling level, whereas the remaining two

subjects, Kojo and Mandara, almost always avoided the

memory tests, yielding a very small number of data points

for memory performance in the Free conditions. We

therefore focused on Kwame’s data and combined

Kwame’s data across the two tests and conducted Fisher’s

exact test on his 2 9 2 table (Free vs. Forced, Correct vs.

Wrong). Kwame demonstrated the pattern of performing

better in the memory test in the Free conditions than in the

Forced condition, although the result failed to reach sig-

nificance (P = 0.10).

We further compared Kwame’s memory performance

between the Free conditions and the Forced condition

across the sessions. Table 5 shows the subjects’ success

rates in the memory test for the Free conditions and the

Forced condition across 12 sessions (6 sessions 9 2 tests).

In order to examine whether the predicted behavioral pat-

tern was detected for Kwame, we conducted a sign test on

his memory performance across all the sessions. Kwame

showed the predicted pattern in 8 sessions, whereas he did

the opposite only in 1 session and his memory performance

was the same between the two types of conditions in 3

sessions (see Table 5). A sign test confirmed that he was

significantly more successful at selecting the baited blue

cup in the Free conditions than in the Forced condition

(P = 0.039). These findings suggest that at least one sub-

ject showed the statistically significant evidence of the

chosen-forced performance advantage (i.e., the second

criterion of animal metacognition) by declining the mem-

ory test when his memory trace strength about the location

of the preferred reward was weak. However, the results

should be interpreted with caution because if Mandara and

Kojo were included in the analyses and we had to correct

Kwame’s P value for multiple comparisons, the corrected

P value was not significant (P = 0.11, Sidak correction).

The discrepancy in the results between the two tests

might have partly come from the fact that Kwame’s

memory performance in the Forced trials reached 100 %

correct in the last two sessions of the No Cover test (see

Table 5). Once his baseline performance reached 100 %

correct in the Forced trials, there should not be any chosen-

forced performance advantage, and this was exactly what

we found. Kwame scored 100 % correct both in the Free

and in the Forced trials in the last two sessions of the No

Cover test. When we conducted Fisher’s exact test, the data

from these sessions were included, which might have

reduced the likelihood of obtaining statistically significant

results. On the other hand, the sign test naturally excluded

ties from the analyses (which seems more appropriate in

the current context because of the ceiling effect in the last

two sessions), which might have led to the significant

results.

We also compared the subjects’ performance across the

two tests. First, we examined whether trials were more dif-

ficult when the blue cups were temporarily covered with the

box than when they remained visible by conducting Fisher’s

exact test on each subject’s 2 9 2 table (Correct vs. Wrong,

Cover vs. No Cover) for the Forced trials. Only one subject,

Kwame, was significantly more successful at selecting the

baited blue cup in the No Cover test than in the Cover test.

The two tests were equally difficult for the remaining two

subjects (Kwame, P = 0.009; Kojo, P = 0.64; Mandara,

P = 0.63). We further conducted Fisher’s exact test on each

subject’s 2 9 2 table (Take test vs. Escape, Cover vs. No

Cover) for the Free trials in order to examine whether the

subjects showed differential use of the escape response

across the two tests. As predicted, Kwame was significantly

more likely to use the escape response in the Cover test

(difficult trials) than in the No Cover test (easy trials)

(Kwame, P = 0.013; Kojo, P = 1.00; Mandara, P = 0.53).

His results remained significant even when the P value was

corrected for multiple comparisons (P = 0.038, Sidak cor-

rection). Altogether, one subject demonstrated significant

evidence of the increase in the use of the escape response as a

function of task difficulty (i.e., the first criterion of animal

metacognition).

Discussion

Overall, one of the tested gorillas fulfilled the first behav-

ioral criterion of animal metacognition by using the escape

response significantly more often in the Cover test—

objectively difficult trials—than in the No Cover test—

objectively easy trials. The same subject’s response pattern

was also consistent with the chosen-forced performance

advantage, and he met the second criterion at the statisti-

cally significant level but only when the P value was not

corrected for multiple comparisons. It is important to note

that when we conducted the sign test to compare Kwame’s

memory performance between the Free and Forced trials,

the comparisons were made within each session. Unlike in

Experiment 1 in which the presence of the barrier was

associated with difficult trials, each session of Experiment 3

included only one type of test (Cover or No Cover), and

thus, there were no external cues that could potentially

indicate the task difficulty of trials. The difficulty within

each session was solely determined by the subject’s mem-

ory trace strength. The memory task was difficult when the

80 Anim Cogn (2013) 16:65–84

123

subject forgot, whereas it was easy when he remembered. In

other words, Kwame had to discriminate difficult trials (in

which he forgot) from easy ones (in which he remembered)

without discriminative or associative cues. Therefore, the

chosen-forced performance advantage demonstrated by this

subject cannot be explained by associative learning alone,

and the performance difference between the Free and

Forced trials seemed to emerge because the ape selectively

declined the memory test when he forgot.

Response competition is unlikely to explain Kwame’s

chosen-forced performance advantage, because he had to

decide whether or not to take the memory test before the

memory test actually proceeded to the end stage. When the

subjects were making a choice between taking the test and

escaping, the blue cups were still lined up in the middle of

the platform and they were blind as to the final location of

the cups. Furthermore, on the first half of the testing trials

(i.e., in the Cover test), the test stimuli were temporarily

blocked from the subjects’ view, and the apes had to make

prospective judgments on whether or not to take the

memory task. Note here that Kwame’s behavioral pattern

followed the second metacognitive prediction even in the

Cover test alone. Taken together, most parsimonious

explanation for his performance in the current testing

seems to be that he used his own memory trace about the

location of the preferable reward and effectively avoided

trials in which he would likely make an error.

General discussion

In the current research, we evaluated whether gorillas

selectively declined a spatial memory test when they did

not remember the location of a preferred reward. Results

showed that at least three gorillas showed significant

results consistent with one or both of the two criteria of

animal metacognition. In Experiment 1, one subject, Kojo,

demonstrated evidence of being more likely to decline the

memory test when the baiting of the preferred reward was

visually blocked as compared to when it remained visible,

while another subject, Mandara, selectively used the escape

option more often when she had seen that the actual

location of the two grapes conflicted with her side bias.

These findings are consistent with the first metacognitive

criterion of using the escape option more often in difficult

trials than in easy ones. In Experiment 3, one subject,

Kwame, was able to improve his memory performance by

avoiding trials in which he would perform poorly despite

the fact that he had to make a choice between taking the

test or escaping before the memory test was introduced.

That is, he was significantly more accurate when he had the

option to escape than when he did not (but only if the

P value was not corrected for multiple comparisons), thus

demonstrating evidence suggestive of fulfilling the second

criterion of the chosen-forced performance advantage. The

same subject was also significantly more likely to decline

Table 5 Subjects’ success rate in the cover and No Cover tests of Experiment 3 across sessions

Session Kojo Kwame Mandara

Free Forced ± Free Forced ± Free Forced ±

Cover

1 N 83.3 (5/6) NA 71.4 (5/7) 66.7 (4/6) ? N 16.7 (1/6) NA

2 100 (2/2) 50.0 (3/6) ? 70.0 (7/10) 66.7 (4/6) ? 100 (1/1) 16.7 (1/6) ?

3 N 50.0 (3/6) NA 62.5 (5/8) 33.3 (2/6) ? 100 (1/1) 66.7 (4/6) ?

4 N 66.7 (4/6) NA 40.0 (2/5) 83.3 (5/6) - N 50.0 (3/6) NA

5 100 (1/1) 33.3 (2/6) ? 50.0 (4/8) 50.0 (3/6) 0 N 50.0 (3/6) NA

6 N 16.7 (1/6) NA 75.0 (6/8) 33.3 (2/6) ? 50.0 (1/2) 66.7 (4/6) -

No Cover

1 100 (1/1) 50.0 (3/6) ? 100 (10/10) 66.7 (4/6) ? 66.7 (2/3) 33.3 (2/6) ?

2 0.0 (0/1) 66.7 (4/6) - 100 (10/10) 83.3 (5/6) ? 0.0 (0/1) 33.3 (2/6) -

3 100 (1/1) 50.0 (3/6) ? 90.0 (9/10) 83.3 (5/6) ? 66.7 (2/3) 50.0 (3/6) ?

4 N 66.7 (4/6) NA 90.0 (9/10) 83.3 (5/6) ? N 33.3 (2/6) NA

5 0.0 (0/1) 33.3 (2/6) - 100 (8/8) 100 (6/6) 0 N 33.3 (2/6) NA

6 N 83.3 (5/6) NA 100 (12/12) 100 (6/6) 0 N 33.3 (2/6) NA

Trials in which the subjects chose the escape response were excluded from the analyses. Bold numbers indicate the percentages of correct choices

(i.e., choosing the baited blue cup) made by the subjects in the memory test. Numbers in parentheses indicate the frequency of correct choices

divided by that of take-test responses. Free = Free (-) and Free (?) conditions combined; Forced = Forced condition; ± = direction of

memory performance; ? = a session in which the subject’s memory performance in the Free conditions exceeded that in the Forced condition as

predicted; - = a session in which the subject’s memory performance in the Forced condition exceeded that in the Free condition; 0 = a session

in which the subject’s memory performance did not differ between the Free and Forced condition; N no data available as the subjects never chose

to take the memory test within a session; NA not applicable because no data were available for the Free conditions

Anim Cogn (2013) 16:65–84 81

123

difficult trials (the Cover test) than easy trials (the No

Cover test) even with the corrected P value, hence meeting

the first criterion.

Several nonmetacognitive models have been previously

proposed for the effective use of the metacognitive response

in animals, and the current study was designed to rule out

such lower-level models. First, associative learning seems

not to explain the gorillas’ performance given that the apes

received relatively few trials. In fact, only one subject

showed some effect of learning in Experiment 1, whereas

all the others’ performance remained statistically unchan-

ged throughout testing. Moreover, within each session of

Experiment 3, there were no obvious objective cues avail-

able (e.g., presence/absence of the occluder) that corre-

sponded to task difficulty. As such, the present study was

designed to remove these discriminative cues and force

subjects to rely on their own memory trace strength in order

to selectively decline difficult trials appropriately.

Second, response competition is an unlikely mechanism

for Kwame’s performance in Experiment 3 because he had

to make prospective judgments on whether or not to take

the memory test before the test actually proceeded. He

could not see the final configuration of the blue cups (i.e.,

the apes had no idea into which directions cups would

move) at the time of the take-test/escape choice, and

therefore, the primary responses were not in direct com-

petition with the escape response. Additionally, in half of

the trials, he was even temporarily prevented from seeing

the blue cups at the moment when he made the prospective

judgments, which makes the response competition account

even more unlikely. Taken together, Kwame’s perfor-

mance pattern in Experiment 3 appears to imply that he

was able to make the optimal decision of avoiding difficult

trials on the basis of his own memory trace strength about

the location of the preferred reward. It should be still noted

here that Smith et al.’s response strength model can be

applied to Kwame’s chosen-forced performance advantage.

That is, Kwame might have acquired a certain level of

attractiveness toward the escape response during the

experiment and consequently might have compared the

strength of such attractiveness with his own memory trace

strength about the location of the preferred reward. The

attractiveness of the escape option might have determined

the trade-off between the delay length to reinforcement and

the amount of reinforcement.

Although the current experiments demonstrated the

effective use of the escape response in some gorillas for the

first time, we recognize that there are some limitations in

the current study. First, we tested only four subjects, and

only one subject at the individual level showed the chosen-

forced performance advantage, and that only when the

P value was not corrected for multiple comparisons. The

remaining subjects declined the memory test in a majority

of trials, yielding a very small number of data points for the

free-choice trials, which hindered statistical analyses of the

second criterion on these individuals. It is therefore nec-

essary to modify the testing procedure, so that the subjects’

frequency of the escape use can be kept to a middling level.

Second, the very important question of how much the

gorillas’ use of the escape response depends on explicit

memory exceeds the scope of the current study. Future

research should examine the degree of flexibility this spe-

cies can demonstrate in their use of the escape response.

Specifically, it would be important to investigate whether

gorillas can use different kinds of metacognitive responses

not only prospectively but also retrospectively under vari-

ous kinds of conditions, as has been demonstrated for

rhesus monkeys did.

Finally, the current findings also converge with the

recent positive results of mirror self-recognition in some

gorillas. It would be interesting to examine whether the

ability to recognize oneself is actually correlated with

metacognitive skills in this species. If those who are more

competent at using the metacognitive response also per-

form better in the mirror test, a plausible conclusion would

be that these two kinds of tests actually tap into the same

cognitive faculty. Whether the awareness of one’s own

body is integrated with that of their own cognition in great

apes is a fascinating question, but further research is

required to address such a question. Here, we want to

advance the possibility that metacognition and self-

awareness may originally have been mediated by distinct

neural-cognitive systems as evidenced by the likely dis-

sociations between metacognition and self-awareness in

monkeys who evidence metacognition but not mirror self-

recognition (Anderson and Gallup 2011). However, these

two systems may have converged in the course of hominid

evolution, where the more ancestral metacognitive system

responsible for the representation of internal mental states

converged with the system mediating the representation of

somatosensory and proprioceptive information. To test this

hypothesis will require testing more animals where these

two systems may be dissociated. Evaluating the develop-

ment of metacognition and mirror self-recognition in typ-

ically as well as atypically developing human children may

also provide important clues into the cognitive architecture

of these skills and help answer whether they are mediated

by one system or two.

In conclusion, the current research revealed the functional

use of the escape response in gorillas for the first time. Three

of the tested gorillas were able to meet the first criterion of

animal metacognition by selectively declining the test when

the task was more difficult in a relatively small number of

testing trials with little training. One of the successful sub-

jects also demonstrated evidence suggestive of the chosen-

forced performance advantage (i.e., the second criterion).

82 Anim Cogn (2013) 16:65–84

123

The study of great apes’ introspective skills has, unfortu-

nately, lagged behind that of monkeys for which much more

evidence exists. More research focusing on the introspective

skills of our closest relatives is necessary to shed light on the

evolutionary origins of mind and self-awareness.

Acknowledgments I thank Lisa Stevens for allowing me to work

with the great apes at the Smithsonian’s National Zoological Park and

all the zookeepers of the Great Ape House for their support. I also

thank Milton Tierney for constructing the testing apparatus. This

study was supported by a research grant from the David Bohnett

Foundation, the Smithsonian Institute Fellowship to CK, and a

CAREER Grant from the National Science Foundation to FS (BCS-

0748717). All of the experiments were approved by the IACUC of the

National Zoological Park and complied with the current laws of the

country in which they were conducted.

References

Anderson JR, Gallup GG (2011) Do rhesus monkeys recognize

themselves in mirrors? Am J Primatol 73:603–606. doi:10.1002/

ajp.20950

Balcomb FK, Gerken L (2008) Three-year-old children can access

their own memory to guide responses on a visual matching task.

Dev Sci 11(5):750–760. doi:10.1111/j.1467-7687.2008.00725.x

Basile BM, Hampton RR, Suomi SJ, Murray EA (2009) An

assessment of memory awareness in tufted capuchin monkeys

(Cebus apella). Anim Cogn 12:169–180. doi:10.1007/s10071-008-

0180-1

Beran MJ, Smith JD (2011) Information seeking by rhesus monkeys

(Macaca mulatta) and capuchin monkeys (Cebus apella).

Cognition 120:90–105. doi:10.1016/j.cognition.2011.02.016

Beran MJ, Smith JD, Redford JS, Washburn DA (2006) Rhesus

macaques (Macaca mulatta) monitor uncertainty during numer-

osity judgments. J Exp Psychol Anim Behav Proc 32:111–119

Brauer J, Call J, Tomasello M (2004) Visual perspective-taking in

dogs (Canis familiaris) in the presence of barriers. Appl Anim

Behav Sci 88:299–317. doi:10.1016/j.applanim.2004.03.004

Call J (2005) The self and other: a missing link in comparative social

cognition. In: Terrace HS, Metcalfe J (eds) The missing link in

cognition: origins of self-reflective consciousness. Oxford Uni-

versity Press, New York, pp 321–341

Call J, Carpenter M (2001) Do apes and children know what they

have seen? Anim Cogn 4:207–220. doi:10.1007/s100710100078

Crystal JD, Foote AL (2009) Metacognition in animals. Comp Cogn

Behav Rev 4:1–16. doi:10.3819/ccbr.2009.40001

Dunlosky J, Metcalfe J (2009) Metacognition. Sage, Los Angeles

Foote AL, Crystal JD (2007) Metacognition in the rat. Curr Biol

17:551–555. doi:10.1016/j.cub.2007.01.061

Fujita K (2009) Metamemory in tufted capuchin monkeys (Cebusapella). Anim Cogn 12:575–585. doi:10.1007/s10071-009-0217-0

Gallup GG (1997) On the rise and fall of self-conception in primates.

Ann NY Acad Sci 818:73–84. doi:10.1111/j.1749-6632.1997.

tb48247.x

Gallup GG (1998) Self-awareness and the evolution of social intelli-

gence. Behav Process 42:239–247. doi:10.1016/S0376-6357

(97)00079-X

Hampton RR (2001) Rhesus monkeys know when they remember.

Proc Natl Acad Sci 98:5359–5362. doi:10.1073/pnas.071600998

Hampton RR (2009) Multiple demonstrations of metacognition in

nonhumans: conversing evidence or multiple mechanisms?

Comp Cogn Behav Rev 4:17–28. doi:10.3819/ccbr.2009.40002

Hampton RR, Zivin A, Murray EA (2004) Rhesus monkeys (Macacamulatta) discriminate between knowing and not knowing and

collect information as needed before acting. Anim Cogn

7:239–246. doi:10.1007/s10071-004-0215-1

Inman A, Shettleworth SJ (1999) Detecting metamemory in nonver-

bal subjects: a test with pigeons. J Exp Psychol Anim Behav

Proc 25:389–395. doi:10.1037/0097-7403.25.3.389

Kornell N, Son LK, Terrace HS (2007) Transfer of metacognitive

skills and hint seeking in monkeys. Psychol Sci 18:64–71. doi:

10.1111/j.1467-9280.2007.01850.x

Ledbetter D, Basen J (1982) Failure to demonstrate self-recognition in

gorillas. Am J Primatol 2:301–310. doi:10.1002/ajp.1350020309

McMahon S, Macpherson K, Roberts WA (2010) Dogs choose a

human informant: metacognition in canines. Behav Process

85:293–298. doi:10.1016/j.beproc.2010.07014

Nakamura N, Watanabe S, Betsuyaku T, Fujita K (2011) Do birds

(pigeons and bantams) know how confident they are of their

perceptual decisions? Anim Cogn 14:83–93. doi:10.1007/s10071-

010-0345-6

Nelson TO, Narens L (1990) Metamemory: a theoretical framework

and new findings. In: Bower GH (ed) The psychology of learning

and motivation, vol 26. Academic Press, New York, pp 125–141

Nelson TO, Narens L (1994) Why investigate metacognition? In:

Metcalfe J, Shimamura AP (eds) Metacognition: knowing about

knowing. MIT Press, Cambridge, pp 1–25

Parker ST (1994) Incipient mirror self-recognition in zoo gorillas and

chimpanzees. In: Parker ST, Mitchell RW, Boccia ML (eds) The

mentalities of gorillas and orangutans. Cambridge University

Press, Cambridge, pp 301–307

Patterson F, Cohen RH (1994) Self-recognition and self-awareness inlowland gorillas. In: Parker ST, Mitchell RW, Boccia ML (eds)

Self-awareness in animals and humans. Cambridge University

Press, Cambridge, pp 273–290

Paukner A, Anderson JR, Fujita K (2006) Redundant food searches by

capuchin monkeys (Cebus apella): a failure of metacognition?

Anim Cogn 9:110–117. doi:10.1007/s10071-005-0007-2

Posada S, Colell M (2007) Another gorilla recognizes himself in a

mirror. Am J Primatol 69:576–583. doi:10.1002/ajp.20355

Povinelli DJ (1993) Reconstructing the evolution of mind. Am

Psychol 48:493–509. doi:10.1037/0003-066X.48.5.493

Schneider W (2008) The development of metacognitive knowledge in

children and adolescents: major trends and implications for

education. Mind Brain Educ 2:114–121

Shea N, Heyes C (2010) Metamemory as evidence of animal conscious-

ness: the type that does the trick. Biol Philos 25:95–110. doi:

10.1007/s10539-009-9171-0

Shillito DJ, Gallup GG, Beck BB (1999) Factors affecting mirror

behavior in western lowland gorillas. Anim Behav 57:999–1004.

doi:10.1006/anbe.1998.1062

Smith JD, Schull J, Strote J, McGee K, Egnor R, Erb L (1995) The

uncertain response in the bottlenosed dolphin (Tursiops trunc-atus). J Exp Psychol Gen 124:391–408

Smith JD, Shields WE, Schull J, Washburn DA (1997) The uncertain

response in humans and animals. Cognition 62:75–97

Smith JD, Beran MJ, Redford JS, Washburn DA (2006) Dissociating

uncertainty responses and reinforcement signals in the comparative

study of uncertainty monitoring. J Exp Psychol Gen 135:282–297

Smith JD, Beran MJ, Couchman JJ, Coutinho MVC (2008) The

comparative study of metacognition: sharper paradigms, safer

inferences. Psychon Bull Rev 15:679–691. doi:10.3758/PBR.15.

4.679

Smith JD, Redford JS, Beran MJ, Washburn DA (2010) Rhesus

monkeys (Macaca mulatta) adaptively monitor uncertainty while

multi-tasking. Anim Cogn 13:93–101. doi:10.1007/s10071-009-

0249-5

Anim Cogn (2013) 16:65–84 83

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http://dx.doi.org/10.1007/s10071-008-0180-1

http://dx.doi.org/10.1007/s10071-008-0180-1

http://dx.doi.org/10.1016/j.cognition.2011.02.016

http://dx.doi.org/10.1016/j.applanim.2004.03.004

http://dx.doi.org/10.1007/s100710100078

http://dx.doi.org/10.3819/ccbr.2009.40001

http://dx.doi.org/10.1016/j.cub.2007.01.061

http://dx.doi.org/10.1007/s10071-009-0217-0

http://dx.doi.org/10.1111/j.1749-6632.1997.tb48247.x

http://dx.doi.org/10.1111/j.1749-6632.1997.tb48247.x

http://dx.doi.org/10.1016/S0376-6357(97)00079-X

http://dx.doi.org/10.1016/S0376-6357(97)00079-X

http://dx.doi.org/10.1073/pnas.071600998

http://dx.doi.org/10.3819/ccbr.2009.40002

http://dx.doi.org/10.1007/s10071-004-0215-1

http://dx.doi.org/10.1037/0097-7403.25.3.389

http://dx.doi.org/10.1111/j.1467-9280.2007.01850.x


http://dx.doi.org/10.1016/j.beproc.2010.07014

http://dx.doi.org/10.1007/s10071-010-0345-6

http://dx.doi.org/10.1007/s10071-010-0345-6

http://dx.doi.org/10.1007/s10071-005-0007-2


http://dx.doi.org/10.1037/0003-066X.48.5.493

http://dx.doi.org/10.1007/s10539-009-9171-0

http://dx.doi.org/10.1006/anbe.1998.1062

http://dx.doi.org/10.3758/PBR.15.4.679

http://dx.doi.org/10.3758/PBR.15.4.679

http://dx.doi.org/10.1007/s10071-009-0249-5

http://dx.doi.org/10.1007/s10071-009-0249-5

Son LK, Kornell N (2005) Metaconfidence judgments in rhesus

macaques: explicit versus implicit mechanisms. In: Terrace HS,

Metcalfe J (eds) The missing link in cognition: origins of self-

reflective consciousness. Oxford University Press, New York,

pp 296–320

Suarez S, Gallup GG (1981) Self recognition in chimpanzees and

orangutans, but not gorillas. J Hum Evol 10:175–188. doi:

10.1016/S0047-2484(81)80016-4

Subiaul F (unpublished data) Serial lists learning in gorillas.

CAREER: evolution of cultural learning. National Science

Foundation (BCS-0748717)

Suda-King C (2008) Do orangutans (Pongo pygmaeus) know when

they do not remember? Anim Cogn 11:21–42. doi:10.1007/

s10071-007-0082-7

Sutton JE, Shettleworth SJ (2008) Memory without awareness:

pigeons do not show metamemory in delayed matching to sample.

J Exp Psychol Anim Behav Proc 34:266–282. doi:10.1037/

0097-7403.34.2.266

Swartz KB, Evans S (1994) Social and cognitive factors in

chimpanzee and gorilla mirror behavior and sef-recognition.

In: Parker ST, Mitchell RW, Boccia ML (eds) Self-awareness in

animals and humans. Cambridge University Press, Cambridge,

pp 189–206

Terrace HS, Son LK (2009) Comparative metacognition. Curr Opin

Neurobiol 19:67–74. doi:10.1016/j.conb.2009.06.004

84 Anim Cogn (2013) 16:65–84

123

http://dx.doi.org/10.1016/S0047-2484(81)80016-4

http://dx.doi.org/10.1007/s10071-007-0082-7

http://dx.doi.org/10.1007/s10071-007-0082-7

http://dx.doi.org/10.1037/0097-7403.34.2.266

http://dx.doi.org/10.1037/0097-7403.34.2.266

http://dx.doi.org/10.1016/j.conb.2009.06.004

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