Reaching around barriers: the performance of the great apes and 3

Anim Cogn (2010) 13:273–285

DOI 10.1007/s10071-009-0265-5

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ORIGINAL PAPER

Reaching around barriers: the performance of the great

apes and 3–5-year-old children

Petra H. J. M. Vlamings · Brian Hare · Josep Call

Received: 17 April 2009 / Revised: 13 July 2009 / Accepted: 15 July 2009 / Published online: 4 August 2009

Abstract Inhibitory control has been suggested as a key

predictive measure of problem-solving skills in human and

nonhuman animals. However, there has yet to be a direct

comparison of the inhibitory skills of the nonhuman apes

and their development in human children. We compared

the inhibitory skills of all great ape species, including

3–5-year-old children in a detour-reaching task, which

required subjects to avoid reaching directly for food and

instead use an indirect reaching method to successfully

obtain the food. We tested 22 chimpanzees, 18 bonobos, 18

orangutans, 6 gorillas and 42 children. Our sample included

chimpanzees, bonobos and orangutans housed in zoos

(N = 27) and others housed in sanctuaries in their native

habitats (N = 37). Overall, orangutans were the most skilful

apes, including human children. As expected older children

outperformed younger children. Sanctuary chimpanzees

and bonobos outperformed their zoo counterparts whereas

there was no diVerence between the two orangutan samples.

Most zoo chimpanzees and bonobos failed to solve the

original task, but improved their performance with addi-

tional training, although the training method determined to

a considerable extent the level of success that the apes

achieved in a transfer phase. In general, the performance of

the older children was far from perfect and comparable to

some of the nonhuman apes tested.

Keywords Problem solving · Inhibitory control ·

Reaching · Detour

Introduction

Everyday animals face countless problem-solving situa-

tions. One of the key ingredients of successful problem-

solving is the inhibition of certain prepotent responses that

exist because they are either preprogrammed or have been

extensively reinforced in the past. Developmental studies

on animals and children have shown that inhibitory

problems, rather than a lack of conceptual comprehension,

can often prevent subjects from solving certain tasks

(e.g., Deacon 1997; Diamond 1990).

Numerous species have been observed to perform well

on detour tasks in which they have to walk around a barrier

(e.g., fence) to obtain food or a social reward (chimpanzees:

Köhler 1925; Kellog and Kellog 1933; chicks: Regolin

et al. 1994, 1995a; cats: Poucet Thinus-Blanc and Chapuis

1983; dogs: Pongracz et al. 2001; quokkas: Wynne and

Leguet 2004; quails, canaries and herring gulls: Zucca et al.

2005; Wsh: Bisazza et al. 1997; snails: Atkinson 2003). It is

very likely that species diVer in the way they solve this

task. Snails, for example, rely on sensory feedback while

moving along a barrier, whereas 2-day-old chicks have

been reported to solve detour tasks in their initial choice,

although some evidence suggest that they may perform bet-

ter in seeking social partners than prey (Regolin et al.

1995b). Nevertheless, there are some task features to which

various species respond in similar ways. Thus, comparisons

P. H. J. M. Vlamings · J. Call (&)

Max Planck Institute for Evolutionary Anthropology,

MPI-EVA, Deutscher Platz 6, Leipzig 04103, Germany

e-mail: ca[email protected]

P. H. J. M. Vlamings

Department of Neurocognition,

University of Maastricht, Maastricht, The Netherlands

B. Hare

Department of Evolutionary Anthropology,

Duke University, Durham, NC 27708, USA

274 Anim Cogn (2010) 13:273–285

123

of the behavior in front of transparent and opaque barriers

with various species (chicks: Regolin et al. 1994; cats:

Poucet et al. 1983; dogs: Chapuis et al. 1983) have con-

Wrmed an early Wnding of Köhler (1925) with chimpanzees,

that transparent barriers pose a more diYcult problem than

opaque ones.

In contrast to detour problems in which subjects have to

move around a barrier themselves, Köhler (1925) showed

that chimpanzees perform poorly when pushing an object

around a barrier. However, later studies have found that

chimpanzees and other primates can solve mechanical

mazes, computerized mazes, and bent-wire detour prob-

lems that require the inhibition of direct solutions and the

activation of alternative indirect routes (Bingham 1929;

Guillaume and Meyerson 1930; Davis et al. 1957; Davis

1958, 1968; Washburn and Rumbaugh 1992; Washburn

et al. 1991). One of the tasks that has received considerable

research attention in connection to the ability to inhibit pre-

potent responses is the detour-reaching task or object

retrieval task. In this task, a toy is placed into a plexiglass

box, with an opening only to one side only (Diamond

1981). When 7–9-month-old human infants see the toy

through the closed plexiglass side of the box, they will

reach straight for it, despite tactile feedback from the plexi-

glass. In contrast to 9-month-olds, older infants Wnd the

opening of the box (Diamond 1990). When tested with

an opaque box, 7–9-month-old infants perform better

(Diamond 1981, 1990), suggesting that the visibility of the

attractive toy evokes the urge to reach for it directly. In

several studies Diamond has shown that performance on the

object retrieval task is linked to maturation of the dorsolat-

eral prefrontal cortex (e.g., Diamond and Goldman-Rakic

1986; Diamond 1991a, b).

Adult rhesus monkeys, marmosets and vervet monkeys

easily Wnd the opening of the object retrieval box (Diamond

and Goldman-Rakic 1989; Roberts et al. 1991; Taylor et al.

1990a, b). In contrast, cotton-top tamarins fail to perform

above chance in this task (and continue reaching directly)

even after 24 trials (Santos et al. 1999). However, given

suYcient experience that included a training phase with an

opaque box, tamarins were also able to overcome their ini-

tial diYculties and solve the reaching problem.

Surprisingly, performance in object-reaching tasks has

yet to be examined in the great apes. This lack of informa-

tion about humans’ closest living relatives is particularly

puzzling because increases of prefrontal cortex have been

postulated in human evolution as key development in exec-

utive problem-solving and forward-planning. Crucially, the

great apes, rather than the monkeys that have been tested,

are the group that displays the largest prefrontal cortex in

nonhuman primates (see Semendeferi 1999). Therefore,

data on great apes’ performance is crucial to make infer-

ences about the evolution of inhibitory skills in humans.

Moreover, obtaining data from all great ape species, not

just one species (e.g., chimpanzees) is essential to make

inferences about the evolution of human and ape cognitive

skills (see Beck 1982; Parker et al. 1999). A joint appraisal

could help to infer points where this capability may have

increased.

Some authors have suggested that orangutans rather than

our closest relative, the chimpanzee, possess greater inhibi-

tory skills. For instance, Shumaker et al. (2002) found that

two orangutans solved a reversed contingency task that

chimpanzees had systematically failed (Boysen and

Berntson 1995; Boysen et al. 1996). However, the study by

Shumaker et al. (2002) has been criticized because orangu-

tans showed no initial preference for the larger quantity,

and, therefore, they did not have to inhibit reaching for the

larger quantity of food (Kralik et al. 2002; Vlamings et al.

2006). Moreover, Vlamings et al. (2006) (see also Uher and

Call 2008) tested all the great apes in a reverse contingency

task and found no evidence of the putative diVerences

between chimpanzees and orangutans. Some orangutans

(and chimpanzees) passed the task while some orangutans

(and chimpanzees) failed it. Note that some monkeys, if

given enough trials, can also pass this task even without

using correction procedures (Albiach-Serrano et al. 2007;

Murray et al. 2005).

The aim of the current study was to compare the ability

of great apes to solve a modiWed version of the classical

detour-reaching task taking great care to use the same

method with all species. This is important because

although data from multiple species is available, for

instance in the case of the classical detour task, quite often

inter-species comparisons are diYcult to interpret because

the methods used to study each species also diVer substan-

tially. Upon completing our Wrst experiment, we con-

ducted a follow-up with those apes that initially failed the

task to assess the reasons for their failure and to see if a

minimum amount of training would help them overcome

their initial bias. Since the current study also included

apes from two diVerent captive populations (zoo and

sanctuary), we investigated whether the origin of the apes

had an eVect on performance. This comparison is impor-

tant to map the inter-population diVerences in cognition—

a topic that has received relatively little research attention

(but see Bania et al. 2009; Call and Tomasello 1996; Fur-

long et al. 2008). Finally, we tested 3–5-year-old children

on the same task as this age represents a key transition

period as evidenced by neurological and behavioral stud-

ies. Neurological studies reported that the prefrontal

lobe—an area implicated in the inhibition of prepotent

responses, shows an important growth spurt between the

age of 4 and 4 years (Luria 1973; Huttenlocher 1979;

Thatcher 1992). Among the major changes detected

during this period are the development in the size and

Anim Cogn (2010) 13:273–285 275

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complexity of cells, which include myelinisation, Wssura-

tion and synaptic density (Carver et al. 2001a).

Behavioral studies have indicated that 3–4-year-old chil-

dren perform poorly on a variety of tasks requiring inhibi-

tory control, including the day–night task (Gerstadt et al.

1994; Diamond et al. 2002), the tapping-imitation task

(Luria 1973; Diamond and Taylor 1996), the delay of grati-

Wcation task (Mischel and Mischel 1983; Mischel et al.

1989) and the dimensional card-sorting task (Frye et al.

1995). However, there is a marked improvement in inhibi-

tory control between 3 and 5 years of age (Carlson and

Moses 2001; Kopp 1982; Zelazo and Frye 1998). Livesey

and Morgan (1991) administered a go/no-go task to 4- and

5-year-old children, and found that performance was near

perfect in latter age group. Further it has been reported that

the preschool period is an important period for the develop-

ment of inhibitory skills as measured by the stop-signal task

(Carver et al. 2001a, b) in which subjects have to inhibit

their responses following an auditory signal in a forced

choice discrimination task. Even the youngest age group

(children between 4- and 9-year-old were tested) had some

capacity of withholding responses, and performance

improved signiWcantly with age, in particular in the youn-

gest age group. According to Bell and Livesey (1985)

inhibitory behavior is linked to self regulation, the develop-

ment of which is reported to be an important milestone in

the young child (Kopp 1982; Lee et al. 1983). As far as we

know, there have been no studies that investigate inhibitory

control in preschool children in a problem-solving setting.

Additionally, except for the study of Carlson et al. (2002)

there have been no studies that directly compare inhibitory

skills among 3-, 4- and 5-year-olds. Based on the previous

studies we expected older children to show superior perfor-

mance than younger children in the detour-reaching task

used in this study.

Experiment 1: zoo apes

Methods

Subjects

We tested 27 great apes housed at the Wolfgang Köhler Pri-

mate Research Center (WKPRC) in Leipzig (Germany).

There were 6 gorillas (Gorilla gorilla; age range 5–25 years;

2 males, 4 females), 7 orangutans (Pongo pygmaeus; age

range 5–33 years; 2 males, 5 females), 4 bonobos (Pan

paniscus; age range 6–20 years; 3 males, 1 female) and

10 chimpanzees (Pan troglodytes; age range 5–27 years;

3 males, 7 females). All animals had participated in

various experimental cognitive studies at the WKPRC (see

http://wkprc.eva.mpg.de). Subjects were not food deprived

prior or during the experiment and water was available

ad libitum during the experiment. We included all subjects

older than 3 years of age that were available for testing at

the time.

Materials

The apparatus consisted of a bottomless opaque wooden

box (50 £ 53 £ 30 cm) resting on a platform and attached

to the mesh by a metal frame (see Fig. 1

a). The front panel

of the box had two transparent Plexiglas doors

(18 £ 18 cm

) suspended by hinges and that opened

inwards when pushed. We used transparent doors because

several studies had shown that several species Wnd transpar-

ent barriers more challenging than opaque ones (e.g.,

Chapuis et al. 1983; Diamond 1990; Regolin et al. 1994). The

mesh contained two large holes that coincided with the box

doors through which the animal could stick his or her entire

arm. A 5-cm piece of banana could be placed right behind

one of the hinged doors via one of two lateral trap doors,

which were out of reach of the subject. An opaque plexi-

glass panel (80 £ 90 cm) blocked the subject’s access to

the hinged doors during baiting. This prevented the subject

from seeing where the food was placed. In one of the condi-

tions, the banana was covered by a small opaque cup (5 cm

in diameter and 6 cm in height). If the subject tried to reach

for the food directly, the door pushed the food away and the

reward fell out of reach from the subject. To get the reward,

subjects had to reach indirectly, through the empty door

and grab the reward from behind (see Fig. 1b). Two

cameras recorded testing. One camera was placed under-

neath the box, the other one at the side. The signal of both

cameras was fed to a single tape in a DV-walkman.

Procedure

Each subject was tested individually in an observation

room, except for one orangutan and three chimpanzees that

were accompanied by their young oVspring. At the begin-

ning of each trial, the experimenter installed an opaque

panel and placed a piece of banana behind either the left or

right door of the box. In the visible condition the reward

was fully visible whereas in the invisible condition, the

experimenter covered the reward with an upside down

opaque cup. Including trials in the visible and invisible con-

ditions allowed us to assess whether seeing the reward

made the problem harder than not seeing it. After baiting

was completed, the experimenter removed the opaque panel

and sat down approximately 1 m behind the box. Subjects

were allowed to approach the box and take the food by

reaching through the doors (see Fig. 1b). The trial ended

when subjects got or lost the food. Then the opaque panel

was lowered again and the next trial was conducted. If

276 Anim Cogn (2010) 13:273–285

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subjects failed to respond to the box, they were vocally

encouraged to do so. If subjects did not respond after 5 min,

the session was terminated. Testing stopped after subjects

became unwilling to participate on three consecutive ses-

sions. All sessions were videotaped.

Design

We used a 4 (species) £ 2 (condition: visible/invisible)

split plot, with species as the between and condition as the

within subjects factor. The order, in which the conditions

were presented, was counterbalanced within species. Each

condition consisted of ten trials [5 trials for each food loca-

tion (left/right)]. The order of food location was counterbal-

anced across trials using a randomization program, with the

obligation that food was never on the same location three

times in a row. Subjects were tested in two sessions (one

per condition), each run on a diVerent day. The median

number of days between conditions was one.

Data scoring and analyses

We scored from the videotapes whether subjects obtained

the reward. A second observer coded 20% of the sessions.

Inter-observer reliability was excellent (Cohen’s kappa =

0.94). We analyzed the percent of correct trials as a func-

tion of species, condition and sex. We used nonparametric

statistics because the assumption of homogeneity of vari-

ance was not met. We corrected multiple pair-wise compar-

isons with the Bonferroni–Holm procedure (Holm 1979).

Results

Two chimpanzees and one bonobo were dropped from the

analysis because they did not complete the two sessions.

Figure 2 presents the percentage of correct trials as a func-

tion of species. There were no signiWcant diVerences

between conditions. Consequently, we collapsed this vari-

able in subsequent analyses. There were signiWcant diVer-

ences between species (Kruskal–Wallis test: 

= 17.52;

df =3; P = 0.001). Pairwise comparisons revealed that

orangutans outperformed all other species (Mann–Whitney

tests: Z > 2.71; P < 0.01 in all cases). Males and females

performed at comparable levels (Mann–Whitney test:

Z=0.59; P = 0.55). Unlike other species, orangutans sig-

niWcantly improved their performance during testing from

29% correct in the Wrst 5-trial block to 91% correct in the

last 5-trial block (Friedman test: 

=14.22; df =3;

P = 0.003). Only one out of seven orangutans solved the

problem in the Wrst trial, although she subsequently missed

other trials (no subject from any other species solved the

problem on their Wrst trial). We found no evidence that age

aVected performance in orangutans (Spearman r =0.07;

P =0.88; N =7).

Discussion

Orangutans outperformed all other great ape species.

Although initially they also performed poorly, unlike other

species, they learned to inhibit reaching directly for the

reward within 20 trials. It is conceivable that this reXects the

more developed inhibitory skills of orangutans as some

authors have suggested (Shumaker et al. 2002, but see

Vlamings et al. 2006). Perhaps the reason for their success is

Fig. 1 Experimental setup (a) and solution to the task (b)

Fig. 2 Mean percentage (+SEM) of correct trials as a function of spe-

cies in “Experiment 1”

% correct

orangutansgorillaschimpanzees bonobos

Anim Cogn (2010) 13:273–285 277

123

due to the fact that they were not pulled as strongly by the

food as their African counterparts which face stronger food

competition with group mates (Shumaker et al. 2002). Addi-

tionally, orangutans’ more deliberate means of locomotion in

the canopy (see Povinelli and Cant 1995) may have contrib-

uted as well. However, the fact that orangutans also made

numerous mistakes in the initial trials shows that at least they

showed the same initial pull as the other ape species.

Unlike previous studies with human infants and mon-

keys (e.g., Diamond 1990; Santos et al. 1999) the visibility

of the reward had no eVect on performance. However, the

barrier in the current study was always transparent whereas

other studies made the barrier opaque, which may explain

the diVerences between studies.

Although the species diVerences reported here may rep-

resent a genuine species diVerence, caution is required for

two reasons. First, our sample size is small, and therefore

the impact of large inter-individual diVerences on the group

comparisons should not be underestimated. It is conceiv-

able that the origin of our subjects (zoo) may have had an

important eVect on performance, although we can rule that

a diVerential experimental history was responsible for the

observed diVerences between orangutans and other apes

because all species routinely received the same tests. Sec-

ond, even if the species diVerences were genuine, the

strength of the prepotent response in unsuccessful subjects

is unknown. It is conceivable that unsuccessful subjects

could learn to overcome their responses if provided with

some sort of training. In the next two experiments, we

addressed these two open questions.

Experiment 2: two training regimes for apes

In this experiment, we investigated whether subjects could

learn to refrain from reaching directly for the reward, after

implementing a special training that consisted of blocking

the baited door so that subjects were forced to use the other

door and grab the reward from behind. We divided the sub-

jects that had failed “Experiment 1” into two groups. Each

group received one of two training regimes. The Wxed

regime taught subjects to always reach through the same

door to get the reward, while the variable training regime

trained subjects to reach from both doors alternatively.

Once training was completed, we presented the visible con-

dition of “Experiment 1”.

Methods

Subjects

We included all subjects that had failed “Experiment 1”

except one gorilla and one chimpanzee that were dropped

because of their extreme side-biased responding. Thus, the

Wnal sample consisted of 5 gorillas (age range 5–25 years),

4 bonobos (age range 6–20 years) and 9 chimpanzees (age

range 5–27 years).

Materials

We used the same box and setup as in “Experiment 1” with

two exceptions. First, baiting took place behind a transpar-

ent (not an opaque) panel (80 £ 90 cm) placed between the

mesh and the box. Second, we used a piece of opaque plexi-

glass (5 £ 30 cm) placed vertically behind the door where

the reward was located to block the door movement during

training (Fig. 3).

Procedure

The basic testing procedure was the same as in “Experiment

1” except that there were two phases: training and testing.

During training, the experimenter inserted the transparent

panel between the apparatus and the subject. Then the

experimenter captured the subject’s attention, placed the

reward behind one of the doors and blocked the door verti-

cally by sliding down a piece of opaque plastic in full view

of the subject. Upon removal of the transparent panel, the

subject was allowed to approach the apparatus and take the

food by reaching through the unblocked door. As soon as

the subject acquired the food, the safety panel was lowered

and the procedure was repeated for a total of six trials. In the

Wxed training regime, the reward was always placed behind

the same door (with left/right side counterbalanced across

subjects) whereas in the variable regime, the reward

appeared equally often behind each door.

Upon completing the six training trials, subjects received

six test trials which were identical to visible trials in

Fig. 3 Picture showing the plastic piece blocking the movement of

the door to train subjects to reach indirectly for the reward

278 Anim Cogn (2010) 13:273–285

123

“Experiment 1”, except that we used a transparent rather

than an opaque panel to prevent subjects from reaching

before baiting was completed. On the Wrst test trial, the

reward always appeared on the opposite side from where it

was placed on the last training trial. In the rest of the trials

the order of the food location was counterbalanced across

trials. If subjects did not respond or retrieve the food during

training or test trials, the experimenter encouraged them

vocally. If subjects did not respond after 5 min, the session

ended. When subjects were not able to retrieve the food or

became unwilling to be tested on six consecutive sessions

testing stopped. All sessions were videotaped.

Design

We used a between subjects design with training condition

(Wxed/variable) as the between subjects factor. Each train-

ing condition consisted of six trials. Half of the subjects

were presented with the Wxed condition, the other half with

the variable condition. Participants were matched across

conditions on the basis of sex, age and species so that there

were no signiWcant diVerences between groups in any of

these variables.

Data scoring and analyses

We scored from the videotapes whether subjects kept

knocking against the blocked door during training and

whether they obtained the reward in the test. A second

observer coded 20% of the sessions for each of these two

variables. Inter-observer reliability was excellent for

knocking (Cohen’s kappa = 1.0) and success (Cohen’s

kappa = 0.94).

We compared the percent of correct trials before and

after training. To do so, we selected the last six trials of

“Experiment 1” and compared them to the six test trials of

the current experiment. Additionally, we compared the

overall percent of correct trials in the test as a function of

the training regime. Finally, we correlated the percent of

correct trials in the test with the percentage of trials in

which subjects knocked on the door during training for

each of the training regimes. Due to our reduced sample

size, we were unable to analyze species diVerences and

consequently, pooled all species together. We used non-

parametric statistics because the assumption of homogene-

ity of variance was not met.

Results

Two gorillas failed to learn during training and another one

quit responding during testing, and they were dropped from

subsequent analyses. Figure 4 presents the percentage of

correct trials prior and after training in the remaining

subjects. Subjects improved their performance in the test

compared to the pretest both in the Wxed (Wilcoxon test:

Z=2.41; P = 0.016) and variable condition (Wilcoxon test:

Z=2.54; P = 0.011). Additionally, there were no signiW-

cant diVerences in the test between the two training meth-

ods (Mann–Whitney test: Z=0.81; P = 0.42). However,

the distribution of responses diVered substantially between

training regimes. Subjects in the Wxed training showed a

more restricted distribution of responses with the values

clustered around the median (inter-quartile range 50–67%;

kurtosis 3.17) whereas subjects in the variable training

showed a greater dispersal in their responses (inter-quartile

range 12.5–70%; kurtosis 1.04). We found no evidence that

either sex (Mann–Whitney test: Z=0.68; P =0.50) or age

(Spearman r = 0.33; P =0.20; N = 17) signiWcantly aVected

performance.

Training regimes also di

Vered in the percentage of trials

in which subjects knocked against the plexiglass during

training. Subjects with variable training knocked the plexi-

glass signiWcantly more often than subjects with Wxed train-

ing (Mann–Whitney test: Z=2.75; P = 0.006).

Interestingly, the percent of knocking during training pre-

dicted success during the test for the variable training regime

(Spearman r = ¡0.83; P = 0.003; N = 10). Subjects who

knocked less often against the plexiglass during training per-

formed better in the test than those who knocked frequently

against the plexiglass during training. In contrast, subjects in

the Wxed training regime showed no relation between knock-

ing against the plexiglass during training and test perfor-

mance (Spearman r = ¡0.11; P = 0.81; N =7).

Discussion

Most subjects could learn to overcome their prepotent

responses with little additional training (six forced trials)—

only two gorillas failed to beneWt from this training. Both

Fig. 4 Mean percentage (+SEM) of correct trials before and after

training as a function of training regime

% correct

pre-training

post-training

fixedvariable

TRAINING REGIME

Anim Cogn (2010) 13:273–285 279

123

training regimes resulted in comparable overall levels of

eVectiveness but diVerent distributions. On the one hand,

the Wxed regime trained subjects to always reach through

one of the doors and when presented with the test, in which

the location of the reward changed from trial to trial, sub-

jects got about 50% of the trials correct because they

always reached through the same door—the one they had

been trained to use. On the other hand, the variable regime

did not train subjects to reach through one particular door,

but required the subjects to reach through diVerent doors in

diVerent trials depending on the position of the reward.

Some subjects seem to have understood this because they

did well in the test, better in general than most subjects in

the Wxed training regime. Interestingly, those successful

subjects were also those who knocked less on the blocked

door during training. In fact, those subjects who knocked

on the door more often during training not only performed

worse than the other subjects in the variable training regime

but also generally worse than most subjects in the Wxed

training regime.

Thus, the Wxed regime trained subjects to produce a sin-

gle response and therefore was easier to acquire—all sub-

jects except one scored 50% or above. The downside of

this regime, however, was that only one subject (14%)

scored above 50%. In contrast, the variable regime trained

Xexibility, and therefore it was more eVective in the test

phase in which 40% of the subjects scored above 50% cor-

rect, but its downside was that another 40% of the subjects

scored below 20% correct. Taken together, these results

indicated that subjects could be trained to overcome their

prepotent reaching response toward the reward in a few

trials, but the training regime had a profound impact on the

Xexibility that subjects displayed during the test. In the

next experiment, we returned to the question of species

diVerences by testing additional groups of apes in the orig-

inal problem.

Experiment 3: sanctuary apes

In this experiment, we sought to conWrm the species

diVerences found in “Experiment 1” with another sample

of great apes. In this case, the apes came from sanctuaries

located in countries with wild ape populations. Unlike zoo

apes, sanctuary apes had been born in the wild and had

been transferred to sanctuaries after they became

orphaned or conWscated from humans who kept them ille-

gally as pets. At the sanctuaries, apes had the opportunity

to join other apes in social groups and spend some time

roaming the forest habitat surrounding the sanctuaries.

The inclusion of apes with diVerent rearing histories

allowed us to investigate the eVects of ape origin on

performance.

Methods

Subjects

We tested 14 bonobos (8 males and 6 females; mean age

5.5 years; range 4–8 years), 12 chimpanzees (6 males and

6 females; mean age 6.8 years; range 4–15 years), and 11

orangutans (6 males and 5 females; mean age 6.4 years;

range 4–10 years). The bonobos were housed at the Lola

Ya Bonobo sanctuary in Democratic Republic of Congo,

the chimpanzees at the Ngamba Island sanctuary in

Uganda and the orangutans belonged to the orangutan

care center and quarantine in Pasir Panjang, Kalimantan,

Indonesia. We dropped one orangutan that, instead of

reaching for the food, destroyed the testing unit. Subjects

were tested individually and they were not food- or water

deprived during testing. We included all subjects older

than 3 years of age that were available for testing at the

time.

Materials

We used the same apparatus as in “Experiment 1”.

Procedure

The procedure was identical to that of “Experiment 1”

except that we only used visible trials. After subjects had

entered the testing unit, the experimenter showed a food

reward to the subject and placed it behind one of the swing-

ing doors. In order to get the reward, subjects had to intro-

duce their arm through the empty door and grab the food

from behind. Subjects received one 10-trial session with the

food appearing the same number of times to the left and

right of the subject with the restriction that it never

appeared more than two times in a row on the same side.

We scored and analyzed the data in the same way as in

“Experiment 1”. In addition, we directly compared the per-

formance of zoo and sanctuary apes. To do so, we calcu-

lated the percentage of correct trials for the Wrst ten trials of

the zoo apes and compared them to the ten trials adminis-

tered to sanctuary apes.

Results

Figure 5 presents the percentage of correct trials for each

species housed at the sanctuaries. Contrary to our expec-

tations, species did not diVer signiWcantly in their ability

to obtain the reward (Kruskal–Wallis test: 

=1.69;

df =2; P = 0.43). Similarly, there were no signiWcant sex

(Mann–Whitney test: Z=0.91; P = 0.36) or age diVer-

ences (Spearman r = ¡0.002; P =0.99; N = 37). How-

ever, we found important individual diVerences. One

280 Anim Cogn (2010) 13:273–285

123

bonobo, two orangutans, and no chimpanzees got the

reward more often than would be expected by chance (at

least 9 out of 10 times). Furthermore, three bonobos, two

orangutans and four chimpanzees got the reward in the

Wrst trial. Only one bonobo and one orangutan solved the

problem on the Wrst trial and were above chance in the

whole session.

Sanctuary apes performed signiWcantly better than zoo

apes (Mann–Whitney test: Z=3.07; P = 0.002) although

such a diVerence depended on the species. Sanctuary chim-

panzees and bonobos performed signiWcantly better than

their zoo counterparts (Mann–Whitney test: chimpanzees:

Z=3.05, P = 0.002; bonobos: Z=2.43, P = 0.015). In con-

trast, there were no signiWcant diVerences between the two

orangutan samples (Mann–Whitney test: Z=0.64;

P = 0.52). Combining the data from both samples revealed

a signiWcant diVerence between species (Kruskal–Wallis

test: 

=6.79; df =2; P = 0.034). Orangutans performed

signiWcantly better than chimpanzees and bonobos. There

were no sex diVerences (Mann–Whitney test: Z=1.01;

P =0.31).

Discussion

We partially conWrmed the results of “Experiment 1”.

Orangutans performed at comparable levels to those

observed in “Experiment 1”, thus showing good inhibitory

skills. In contrast, the chimpanzees and the bonobos in the

current experiment performed better than those included in

“Experiment 1”. Combining the data from both samples

revealed that orangutans outperformed chimpanzees and

bonobos. In general, subjects did not perform above 50%

correct, and only a minority of subjects mastered the task

by the end of testing. This attests to a considerable level of

task diYculty. In the next experiment we tested 3–5-year-

old children. These ages are particularly interesting in chil-

dren because they represent an important transition period

for inhibitory and executive function abilities (e.g., Carlson

et al. 1998; Kopp 1982).

Experiment 4: children

Methods

Subjects

Fifty-Wve children from eight schools in Leipzig partici-

pated in this experiment. These children were drawn from

the participant database from the department of develop-

ment psychology of the Max Planck institute for Evolution-

ary Anthropology. Children came from families of mixed

socio-economic backgrounds. Thirteen of these children

were dropped from the study because they did not respond

to the task or refused to be tested after a few trials. Thus,

the Wnal group consisted of 42 children: fourteen 3-year-

olds (M = 3.0; range 35–37 months), fourteen 5-year-olds

(M = 4.0; range 47–49 months) and fourteen 5-year-olds

(M = 5.0; range 59–61 months). There were equal numbers

of boys and girls in each age group.

Materials

The apparatus was identical to the one used with apes, but it

was painted diVerently (and had stickers glued on the top

and sides) to make it more attractive to children (Fig. 6).

Additionally, the door openings were padded to prevent

potential injuries. A yellow curtain with printed bears was

hanging in front of the box to prevent the child seeing the

box being baited. We used six diVerent toys as rewards that

were exchanged for small stickers that children could keep.

A pilot study showed that children in this age range were

very motivated to obtain those stickers.

Procedure

Children were tested individually by two experimenters in a

quiet room at their own school. During the walk to the test

room, both experimenters talked to the child to make her

feel comfortable with the experimenters and the new situa-

tion. Experimenter 1 asked whether the child wanted to

play a game and went inside the room and took his position

behind the box while Experimenter 2 waited outside with

the child. Upon being called by Experimenter 1, the child

and Experimenter 2 entered the room and approached the

box. The Experimenter 1 said: “Watch this (name of the

child). I am going to hide this

(name of the toy). If you are

able to retrieve the (name of the toy), and bring it to Exper-

imenter 2, Experimenter 2 will give you a sticker”. While

Experimenter 1 put the toy behind one of the doors, Experi-

menter 2 kneeled down, presented the child with the stick-

ers and asked which sticker would like to have.

After the child had chosen a sticker, Experimenter 1

said: “Ok, you will get this sticker if you can bring me the

Fig. 5 Mean percentage (+SEM) of correct trials as a function of spe-

cies in “Experiment 3”

% correct

orangutanschimpanzees bonobos

Anim Cogn (2010) 13:273–285 281

123

toy”. Experimenter 2 immediately opened the curtain and

the child was allowed to approach the box and attempt to

get the toy by reaching through the doors. After the subject

got the toy, Experimenter 1 closed the curtain while saying:

“Perfect, you really did a good job”. Experimenter 2

rewarded the child by saying: “Perfect, you really did a

good job, now you will get the sticker”. If the subject lost

the toy, Experimenter 1 closed the curtain while saying:

“Ooohh, it does not work”. Experimenter 2 said: “Ooohh,

now you won’t get a sticker.” Then Experimenter 1 asked

whether the child wanted to try again and put a new toy

behind one of the doors. If the child solved the task on the

previous trial, it was allowed to choose a new sticker. If

children did not respond to the box or kept telling the

experimenter that they could not get the toy, Experimenter

1 encouraged them by saying: “Just try, try to get the toy”.

If the subject did not respond after approximately 5 min,

the trial ended. Experimenter 1 asked whether the child

wanted to try with a diVerent toy. When the child refused to

retrieve the toy on three consecutive trials, testing stopped.

All sessions were videotaped.

Design

We used a between subjects design with age as factor. Each

subject received one session of six trials [3 trials for each

toy location (left/right)]. The order of the location at which

the toy was placed was counterbalanced across trials using

a randomization program.

Data analysis

We used the same scoring procedure and analyses as in

“Experiment 3”. A second observer coded 20% of the

sessions. Inter-observer reliability was excellent (Cohen’s

kappa = 1.0). Additionally, we also scored the time it took

subjects to solve each trial. Inter-observer reliability was

again excellent (r = 0.93). Based on the data available in

the literature, we expected older children to perform better

than younger ones. Therefore, we used one-tailed nonpara-

metric statistics.

Results

Figure 7 presents the percentage of correct trials for each

age group (N = 14 for each group). As predicted, older chil-

dren performed signiWcantly better than younger ones

(Kruskal–Wallis test: 

= 4.75; df =2; P = 0.047, one-

tailed). However, this diVerence was most clearly shown

when comparing 3-year-olds to 4- and 5-year-olds pooled

together (Mann–Whitney test: Z=1.91; P = 0.028). Five

4-year-olds (36%) and three 5-year-olds (21%) solved the

task whereas only one 3-year-old (7%) did so.

Analysis of the latencies indicated a signiWcant

diVerence in the time it took subjects to make a choice

Fig. 6 Testing setup for chil-

dren. The top row of pictures

depicts a child reaching directly

for the reward and losing it. The

bottom row depicts a child

reaching indirectly and getting

the reward

Fig. 7 Mean percentage (+SEM) of correct trials as a function of age

in “Experiment 4”

% correct

5-year-olds3-year-olds 4-year-olds

282 Anim Cogn (2010) 13:273–285

123

[²(2, N = 42) = 15.69; P = 0.001]. Three-year-old children

needed signiWcantly more time in comparison to 4- (68 vs.

8 s, Mann–Whitney: Z=3.81; P = 0.001) and 5-year-old

children (68 vs. 25 s, Mann–Whitney: Z=2.99; P = 0.003).

Additionally, 75% of the 3-year-old children missed 1–3

trials because they were unable to solve the task after

approximately 5 min or indicated that it was not possible to

get the toy and refused to be tested. In contrast, only one

4-year-old child and no 5-year-old child had a trial missing.

Discussion

As expected older children outperformed younger ones in

this task. These data Wt well with other results on inhibitory

control that the age between 3 and 5 years is an important

transition period for the acquisition of inhibitory control.

Numerous studies have reported 3-year-olds having motor-

and cognitive inhibition problems in a variety of tasks

(Carlson and Moses 2001; Diamond and Taylor 1996; Frye

et al. 1995; Gerstadt et al. 1994; Mischel and Mischel

1983). However, even the performance of the older chil-

dren was quite low (between 20 and 30%) which again con-

Wrms previous studies reporting far-from-perfect

performance in these age groups (Carver et al. 2001a, b;

Carlson et al. 2002; Mischel and Mischel 1983; Mischel

et al. 1989).

We also noted that 3-year-old children needed more time

to complete a test trial. The majority of 3-year-old children

passed the 5-min limit on 1–3 test trials or indicated that

they were unable to solve the task and refused to be tested

further. At Wrst all 3-year-olds tried to reach for the toy

directly. When this strategy failed, they often stopped try-

ing and kept repeating that it was impossible to get the toy.

Others just kept looking through the door behind which the

toy was placed or tried to somehow lift it. These Wndings

might indicate that in comparison to 4- and 5-year olds,

3-year-olds might have been less able to cope with the frus-

tration of ‘losing a sticker’. Unable to activate any eYcient

solution they might have stopped trying. In contrast 4- and

5-year-olds kept trying and completed test trials more

quickly.

It is conceivable that the test setting, including being

watched by two experimenters while being unable to solve

a task might have put extra pressure on participants,

decreasing the likelihood of producing the detour-solution.

This explanation, however, cannot easily explain the

observed age diVerences. Future studies could investigate

whether children show similar performance when left alone

in the room. Being alone may have alleviated some of the

social pressure that they may have felt and additionally, not

being able to relate their failures to experimenter may have

helped them to better monitor and evaluate their own

actions.

General discussion

We found some evidence that great apes could solve the

detour-reaching task, thus inhibiting their initial tendency

to reach directly for the food. Orangutans were generally

the more skilful than the other species although unsuccess-

ful subjects showed notable improvement after minimal

training. However, the type of training substantially

aVected the subsequent task performance. Sanctuary chim-

panzees and bonobos outperformed their zoo counterparts,

but this was not the case for orangutans. Four- and 5-year-

old children outperformed 3-year-olds even though the per-

formance of the older children was far from perfect and

comparable to some of the ape groups tested.

Orangutans were the species that performed best in this

task. They appeared better able to take into account the

larger picture, generate the detour-solution and inhibit their

prepotent responses than the other species. One possible

explanation is due to the fact that they are more deliberate

than the other apes due to their means of locomotion in the

canopy. Additionally, the diVerences may have been accen-

tuated by their unique social organization based on a dis-

persed social system that reduces direct individual food

competition. As a consequence they might be less impul-

sive, less focused and better able to overview

certain situations than the other species. It is worth noting

that the orbital frontal cortex of orangutans, an area com-

monly associated with inhibitory skills, deviates from the

other species (Semendeferi et al. 1997; Semendeferi 1999).

However, other tests for inhibitory control have found no

evidence of species diVerences between orangutans, chim-

panzees and bonobos (Amici et al. 2008; Vlamings et al.

2006). Interestingly, all three species display high levels of

Wssion–fusion, a social organization in which party mem-

bership changes constantly. In contrast, gorillas, which

have a more stable social organization, showed lower levels

of inhibitory control than those species with higher levels

of Wssion–fusion (Amici et al. 2008). Note that gorillas

were also the species that displayed more diYculties during

the training phase of “Experiment 2”, but our small sample

does not allow us to draw Wrm conclusions on this point.

Despite the great diYculty that some subjects experi-

enced with the task, they were able to improve their perfor-

mance after some minimal remedial training. The results of

this training suggested that most unsuccessful apes experi-

enced cognitive rather than motor inhibition problems. Due

to the salience of the food item subjects might have been so

focused on the door behind which the food was placed that

they were unable to detach their attention from it and take

into account other aspects of the task (the other door) that

would have allowed them to solve the task. It is important

to emphasize that the type of training had a profound

impact of the subsequent task performance. Those subjects

Anim Cogn (2010) 13:273–285 283

123

trained to reach through one particular door continued to do

so during the test, which means that they failed all those tri-

als in which the food appeared in the nontrained side. Thus,

this kind of Wxed training fostered motor inXexibility

whereas training alternation between doors fostered Xexi-

bility; but this worked only for those individuals that could

inhibit reaching directly toward the reward during training.

Recall that knocking against the door during training pre-

dicted was inversely correlated with success during the sub-

sequent test phase but only for those subjects that were

trained with the alternation regime.

Research on frontal patients has indicated that insuY-

cient inhibitory control can lead to two diVerent outcomes:

(a) the inability to focus on just one thing (as measured in

for example the Stroop Test) and (b) the opposite, the

inability to expand one’s attention beyond one thing

(Diamond 1990). Frontal patients can be so focused on a

salient stimulus that they fail to take into account the larger

picture, for example alternative routes to solve a task (Luria

1973; Diamond 1990). The children and apes tested in the

present study seemed to have problems with taking into

account the larger picture too. They seemed to be so

focused on the door behind which the toy was presented

that they failed to take into account that the solution

involved the other door. Unlike apes, however, children

made no mistakes after they found the correct solution. In

pure cognitive inhibition problems, like the nine-dot prob-

lem (Maier 1930), subjects usually do not make mistake

once they know the solution. It is therefore suggested that

in contrast to the apes, children are facing pure cognitive

inhibition problems in the present detour-reaching study.

To further investigate the nature of the inhibitory prob-

lems of the children who were unable to solve the task, it

would be interesting to present children with the training

blocked condition. If performance reached perfection after

blocking, failures in the original task are likely due to cog-

nitive inhibition problems: the inability to activate a detour-

solution due to the salience of the toy. If children increased

performance but kept making mistakes, this is likely due to

motor inhibition problems: being unable to inhibit the pre-

potent direct-reaching response. In addition it would be

interesting to test older children. As reported earlier, inhibi-

tory skills continue to develop in childhood (Kopp 1982;

Mischel and Mischel 1983; Mischel et al. 1989; Carver

et al. 2001a, b; Carlson et al. 2002). Children become cog-

nitively more Xexible and are better able to disengage from

salient objects. Future studies on inhibitory skills in typi-

cally developing children are important, as inhibitory skills

are good predictors of cognitive as well as social compe-

tence, scholastic performance and the ability to cope with

stress and frustration (Mischel et al. 1989). Given the cur-

rent interest in theory of mind development, investigation

of inhibitory skills is relevant too, as theory of mind and

inhibitory skills seem to be closely related (Perner and

Lang 2002; Carlson et al. 2002; Zelazo et al. 2002).

Chimpanzees and bonobos housed in sanctuaries clearly

outperformed their counterparts housed in zoos, although

this was not true for orangutans. These diVerences are

intriguing and potentially important (Boesch 2007). How-

ever, caution is needed when trying to extrapolate these

results to the whole population of zoo or sanctuary apes

because our samples are small and come from particular

origins. Caution should also be applied with the human

sample because it may only reXect the performance of mid-

dle-class western children, and it may not be representative

of other human populations that diVer with regard to the

experiences that children are exposed to (e.g., schooling).

Moreover, the ape populations themselves are not so homo-

geneous since there are large inter-individual diVerences

within populations regarding the rearing histories of the

individuals and also potentially important genetic di

Ver-

ences. For instance, all zoo chimpanzees were descendants

of individuals that came from Liberia whereas all sanctuary

chimpanzees came from Eastern wild populations. Future

studies could include multiple groups that vary systemati-

cally in certain factors (e.g., rearing practices or cultural

background) to assess their impact on inhibitory control.

There is another issue that recommends caution when

making broad generalizations. Although sanctuary chim-

panzees and bonobos outperformed their zoo counterpart

on a detour-reaching task, there are other tasks in which the

pattern is reversed and these same zoo apes outperformed

sanctuary apes. For instance, zoo apes outperformed sanc-

tuary apes in quantity estimation and gaze following (com-

pare Hanus and Call 2007; Bräuer et al. 2005 with

Herrmann et al. 2007). Nevertheless, the potential diVer-

ences between populations is an important issue that

deserves careful scrutiny as it may provide important clues

regarding the epigenesis of cognitive skills in the great

apes. Documenting the diVerences is important but not less

important is documenting the similarities. In fact, there are

some tasks in which no diVerences were apparent between

zoo and sanctuary apes (e.g., quantity estimation, object

tracking tasks, see Herrmann et al. 2007; Barth and Call

2006). This means that what is required to assess the status

of various populations is a battery of multiple tasks and a

balanced consideration of the similarities and diVerences

between populations. At the very least, this manuscript

should contribute to dispel the myth that sanctuary apes are

a nonviable research population due to their origin as we

have seen that they are capable of solving tasks that chal-

lenge the inventiveness of 4- and 5-year-old children.

In summary, we found that some great apes were capa-

ble of solving a detour-reaching task after only a few trials

and those that failed could be trained to solve the task after

minimal training. However, the training regime had a

284 Anim Cogn (2010) 13:273–285

123

substantial eVect on how Xexibly subjects could deploy

their training in the original situation. In general, orangu-

tans outperformed other ape species, but there were also

important diVerences between groups depending on the

apes’ origin. Namely, sanctuary chimpanzees and bonobos

outperformed their zoo counterparts. Four- and 5-year-old

children performed better than 3-year-old children. Finally,

the performance of the older children was roughly equiva-

lent to that of sanctuary apes.

Acknowledgments We are grateful to the sanctuaries for hosting our

research, At Lola ya Bonobo Sanctuary (www.friendsofbonobos.org).

We are thankful to Claudine Andre, Dominique Morel, Crispin

Kamate Mahamba and Pierrot Mbonzo for their enthusiasm and

support for our research in collaboration with the Ministry of Environ-

ment. At Ngamba Island Chimpanzee Sanctuary (www.ngambaisland.

org) we thank Lilly Ajarova, Debby Cox, Richard Ssunna and the trust-

ees for their help and support in collaboration with the Ugandan

National Council for Science and Technology and the Uganda Wildlife

Authority. At the Orangutan Care Center and Quarantine in Pasir Panj-

ang, Indonesia we thank B. M. Galdikas and the staV for their great

help and support in collaboration with the Indonesian Institute of

Sciences (LIPI) and the Indonesian Ministry of Forestry for allowing

us to conduct our research in their country. We deeply appreciate the

hard work of the animal caregivers from the three sanctuaries: J.C.

Nzumbi, S. Mokando, C. Paluku, A. Kisungu, P. Kunaka, N. Luvualu,

K. Manzambi, M. Gum, P. Kibirege, I. Mujaasi, L. Mugisha, M. Mus-

umba, G. Muyingo, A. Okello, R. Okello, S. Nyandwi, Pak Mekok,

Pak Usai and Pak Yoyong. The research of B.H. was supported by a

Sofja Kovalevskaja award received from The Alexander von Hum-

boldt Foundation and the German Federal Ministry for Education.

Experiments 1, 2 and 4 were part of PHJM Vlamings diploma thesis.

We thank three anonymous reviewers for their helpful comments on an

earlier version of this manuscript.

Open Access This article is distributed under the terms of the Crea-

tive Commons Attribution Noncommercial License which permits any

noncommercial use, distribution, and reproduction in any medium,

provided the original author(s) and source are credited.

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