Primates (2007) 48:303–309
DOI 10.1007/s10329-007-0044-3
ORIGINAL ARTICLE
Development of the visual preference of chimpanzees
(Pan troglodytes) for photographs of primates:
effect of social experience
Masayuki Tanaka
Received: 21 August 2006 / Accepted: 21 February 2007 / Published online: 27 March 2007
Japan Monkey Centre and Springer 2007
Abstract In a study by Tanaka (2003) five captive
chimpanzees preferred photographs of humans to those of
chimpanzees. All the subjects were raised by humans and
lived in captivity for many years. This suggests their
preference might have developed through social experience. In this study examined this hypothesis by using three
young chimpanzees raised by their mothers in a captive
chimpanzee community. The young chimpanzees were
tested four times before six years of age. I also tested eight
adult chimpanzees that had been in captivity for more than
20 years. Each subject was presented with digitized color
photographs of different species of primates on a touchsensitive screen. The subjects received a food reward when
they touched a photograph, irrespective of which photograph they touched. All the adult chimpanzees touched
photographs of humans more frequently than those of any
other species of primate. Two of the young chimpanzees
showed no species preference before reaching 5 years of
age, when they started to show preference for humans. The
remaining young chimpanzee consistently preferred chimpanzees. These results suggest that development of visual
preference of chimpanzees is affected by social experience
during infancy.
Keywords Visual preference Chimpanzee Free-choice
task Social influence
M. Tanaka (&)
Language and Intelligence Section,
Department of Behavioral and Brain Sciences,
Primate Research Institute, Kyoto University,
41-2 Inuyama, Aichi 484-8506, Japan
e-mail: [email protected]
Introduction
In a study by Tanaka (2003) five adult chimpanzees preferred photographs of humans rather than conspecifics,
presented among different species of primates. Each subject was shown twelve photographs, which included
chimpanzees, humans, gorillas, orangutans, and other primate species. The subjects could touch three photographs
in a trial and were given a food reward with a probability of
60–66%, irrespective of which images they touched. The
results showed that all the five chimpanzees touched the
photographs of humans significantly more frequently than
those of other primate species. These chimpanzees had
been in captivity for many years and had been looked after
by humans since their early childhood. Tanaka (2003)
proposed that early social experience may affect chimpanzees’ visual preferences. In this study, this hypothesis
was examined by testing young chimpanzees who had been
reared by their mothers and had grown up in a chimpanzee
community.
Fujita and Matsuzawa (1986), developed a sensory
reinforcement procedure in a chimpanzee. Using the procedure, Fujita and his colleagues demonstrated that macaque species tend to show greater interest in images of
monkeys of their own species (Fujita 1987, 1990, 1993a;
Fujita and Watanabe 1995; Fujita et al. 1997). In some of
these studies Fujita (1990, 1993b) controlled the subjects’
social experience in infancy, to examine its effect on visual
preference. These studies revealed that rhesus macaques
tend to view rhesus macaques for longer than other species
of macaques, irrespective of their age or social experience.
A visual conspecific preference may be genetically programmed in rhesus macaques. Fujita and his colleagues
suggested that such a preference might help prevent
interbreeding among neighboring species.
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In studies of great apes the effect of social experience
has been examined from the perspective of ‘‘enculturation’’. Tomasello et al. (1993) found more highly developed imitative behavior in human-reared than motherreared captive chimpanzees. According to the ‘‘enculturation hypothesis’’ (Tomasello et al. 1997; Tomasello and
Call 1997), social cognitive abilities are enhanced in human-reared great apes. There are several criticisms of the
enculturation hypothesis, however (for example Bering
2004), and researchers are still arguing about cognitive
developmental changes in human-reared great apes.
Tanaka (2003) did not examine social cognition in
chimpanzees, but the finding that photographs of humans
attracted the chimpanzees’ attention could be taken as
support for the enculturation hypothesis. In the study by
Tanaka (2003) all the subjects were human-reared chimpanzees and had been familiar with many aspects of human
behavior; social experience in infancy might therefore have
led to the preference for humans in that study. In this study
I further examined the effect on chimpanzees of social
experience in infancy by assessing the visual preference of
three young chimpanzees who had been reared by their
mothers and who had lived in a chimpanzee community in
captivity. For comparison, eight adult chimpanzees were
also tested. Five of the eight adults were those studied by
Tanaka (2003). They were included to assess the consistency of their previously established preference.
Methods
Subjects
The subjects were three young and eight adult chimpanzees.
The profiles of the subjects are summarized in Table 1. Four
of the adults were born in the wild (wild-born), but raised by
humans from 1 or 2 years of age. They had been in captivity
for more than 25 years. The other four adults were born in
captivity (captive-born) and raised by humans immediately
after birth. They had previously participated in a variety of
experiments on cognitive ability (Kawai and Matsuzawa
2000; Matsuzawa 2003; Tanaka 2001; Tomonaga 2002).
The young chimpanzees were born at the Primate Research
Institute (PRI), Kyoto University, and raised by their own
mothers. None was weaned by the end of this study, although they could eat anything the adults ate. At two months of age each young chimpanzee, with its mother, had
been placed in a captive group. The young chimpanzees had
also previously participated in a variety of cognitive,
behavioral, and morphological studies (Matsuzawa et al.
2006; Tomonaga et al. 2004). Among the adults, Ai, Mari,
Pendesa, Popo, and Pan had participated in the visual
preference study by Tanaka (2003) and had shown a strong
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Primates (2007) 48:303–309
preference for photographs of humans. All the subjects are
currently members of a captive community in the PRI,
housed in an enriched outdoor compound and an attached
indoor residence (Ochiai and Matsuzawa 1998). The subjects were usually with the other members of the community. They spontaneously entered the experimental booth
when the researcher called them. The young chimpanzees
always came with their mothers. The five adults other than
the mothers came to the experimental booth individually.
They were not deprived of food at any time during the
study. Treatment of the chimpanzees adhered to the
Guidelines for the Care and Use of Laboratory Primates of
the Primate Research Institute, Kyoto University (2002).
Apparatus
Each chimpanzee was trained and tested in an experimental
booth (1.8 m W, 1.8 m D, and 2.0 m H). Two sets of 15-inch
liquid crystal displays (LCD) with touch-sensitive screens
(Pro-Tect PD-105TP15), 1024 · 768 pixels, 32-bit color)
were installed on the wall of the booth. A universal feeder
(Biomedica, BUF-310) was attached to each monitor and
delivered small pieces of a food reward (apple or raisins) into
a food tray below the display. The equipment was controlled
by means of a personal computer running Windows.
Stimuli
The stimuli were 5.6 cm · 5.6 cm digitized color images
(198 · 198 pixels, 24-bit color jpeg file) made from color
photographs. The stimulus set was composed of four genera
and two taxonomic families of primates: Homo, Pan,
Gorilla, Pongo, Hylobatidae, and Cercopithecidae. Each
category consisted of 20 different images, that is, a stimulus
set consisted of 120 images. The species used in a stimulus
set are shown in Table 2. The images of humans (Homo)
were highly varied in terms of race, age, and sex, because
the focus of the study was preference based on biological
category. None of the images had been presented to the
subjects before this study. There were some images of
Asian people but no images of people seen by the subjects
every day. Six of the images of humans were those of one or
more toddlers. Three of the images of humans were those of
old people. Among the images of the other species or taxonomic families, some were those of infants, juveniles, or
mother-infant pairs of those genera or families.
Procedure
A trial began with the appearance of a starting stimulus (a
gray solid square, 3.5 cm · 3.5 cm) at a random position
on the display. After the subject touched the starting
stimulus six images were presented in six cells randomly
Primates (2007) 48:303–309
305
Table 1 Subjects and their profiles
Name
Sex
Age at testa
Birth place
Age at the PRIb
Note
Adult chimpanzees
Gon
Male
38
Wild
13
Raised by humans as a pet until coming to the PRI.
Father of Popo and Pan.
Ai
Female
27
Wild
1:01
Raised by humans, in the PRI, with Mari and Akira. She
bore a son, Ayumu, by artificial insemination.
Akira
Male
27
Wild
1:06
Raised by humans, in the PRI, with Mari and Ai. Father
of Ayumu and Pal.
Mari
Female
27
Wild
1:06
Moved to JMC at the age of 9 and lived in the
chimpanzee group of the JMC. Returned to the PRI at
the age of 19.
Pendesa
Female
26
JMC (Captive)
2:09
Born on February 2, 1977. Raised by humans
immediately after birth. She lived with the other
chimpanzees in the PRI community.
Chloe
Female
23
Paris (Captive)
4:01
Born on December 12, 1980. Raised by humans
immediately after birth. She bore a daughter, Cleo,
by natural mating.
Popo
Female
22
PRI (Captive)
0:00
Born on March 7, 1982. Raised by humans and lived
with her brother and sister (Pan) during infancy.
Pan
Female
20
PRI (Captive)
0:00
Born on December 7, 1983. Raised by humans and lived with
her brother and sister (Popo) during infancy.
She bore a daughter, Pal, by artificial insemination.
3:08
4:02
PRI
0:00
Born on April 24, 2000. Raised by his mother, Ai,
and joined the PRI community at 2 months of age.
PRI
0:00
Born on June 19, 2000. Raised by her mother, Chloe,
and joined the PRI community at 2 months of age.
PRI
0:00
Born on August 9, 2000. Raised by her mother, Pan,
and joined the PRI community at 2 months of age.
Young chimpanzees
Ayumu
Male
5:00
6:00
Cleo
Female
4:00
4:06
5:00
6:00
Pal
Female
3:04
3:11
5:00
6:00
PRI, Primate Research Institute, Kyoto University; JMC, Japan Monkey Center, Inuyama, Aichi, Japan
a
Age at which the subject was tested, in years: months
b
Age at which the subject arrived at the PRI, in years: months
selected within a three row by four column matrix on the
display. Each image belonged to one category. In a trial a
subject was given two opportunities to touch the images
(Fig. 1). Each touch was followed by a 2-s chime and the
disappearance of the other images. Food reward was
delivered with a probability of approximately 60% irrespective of the image the subject touched. After a 2-s
chime, the six images appeared again. Any image touched
by the subject was highlighted, and touching the same
image had no scheduled consequence. When the subject
touched another image, the same feedback was again presented, and all images disappeared from the monitor. The
next trial started after a 1-s inter-trial interval. One session
consisted of ten trials. The subjects underwent one or two
sessions a day and eight sessions in total. Each image was
presented in each of two sessions run four times for a total
of eight sessions. The combination of images presented
was changed in every trial. Each young chimpanzee performed the task independent of his/her mother. While the
young chimpanzees were tested their mothers were performing other tasks.
Data analysis
In addition to summing the number of choices at each
opportunity, each image was scored according to the order
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Primates (2007) 48:303–309
Results
Table 2 Species contained in stimulus set
Pan
Homo
Gorilla
Pan troglodytes Homo sapiens Gorilla gorilla
Pan paniscus
Hylobatidae
Pongo
Pongo pygmaeus
Gorilla beringei Pongo abelii
Cercopithecidae
Hylobates agilis
Cercopithecus ascanius
Hylobates hoolock
Cercopithecus diana
Hylobates klossii
Chlorocebus pygerythrus
Hylobates lar
Colobus guereza
Hylobates moloch
Erythrocebus patas
Hylobates pileatus
Macaca assamensis
Hylobatis meulleri
Macaca fascicularis
Nomascus concolor
Macaca fuscata
Nomascus gabriellae
Macaca maura
Nomascus leucogenys
Macaca mulatta
Symphalangus syndactylus
Macaca radiate
Macaca sylvanus
Mandrillus sphinx
Papio hamadryas
Papio papio
Papio ursinus
Presbytis francoisi
Presbytis phayrei
Rhinopithecus bieti
Semnopithecus entellus
Fig. 1 Video print showing the experimental procedure. The subject
touches one of six images presented on a touch-sensitive screen
of choice in a trial. The first choice was given two points,
and the second choice was given one point. The image the
subjects chose first in a trial was taken as the preferred
image.
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Although the chimpanzees randomly received a food reward irrespective of the image they touched, they all
showed marked differences in the number of choices and
the stimulus category selected. Because there was a marked
difference between adult and infant chimpanzees, their results are shown separately. Figure 2 shows the mean scores
of an image in each category for the wild-born and captiveborn adults. The sum of scores for each image presented
four times was determined and shown as the mean of 20
images. It is clear that images in the Homo category (i.e.
humans) obtained the highest score for all adult chimpanzees. In subsequent analysis the scores of Homo (the category with the highest score) and of Pan (the genus to which
the subjects belonged) were selected. ANOVA using stimulus category (Pan or Homo) and site of birth (wild or
captive-born) as the variables revealed a significant main
effect of stimulus category (F(1, 316) = 109, P < 0.001). The
effect of birth was not significant (F(1, 316) = 1.49,
P = 0.22), and the interaction between category and birth
was also not significant (F(1, 316) = 0.182, P = 0.67).
The results for the infant chimpanzees were different
from one another. Figure 3 shows developmental change of
the mean scores of an image in each category for each
subject. Each subject was tested four times at different ages.
ANOVA using stimulus category (Pan or Homo) and age
(4) as variables was conducted for each subject. For Ayumu,
the Homo score was the highest among the categories at
each testing time. ANOVA revealed a significant main
effect of stimulus category (F(1, 38) = 5.59, P = 0.023), but
the effect of age was not significant (F(3, 114) = 1.71,
P = 0.17). There was no significant interaction between
stimulus category and age (F(3, 114) = 0.61, P = 0.61).
Ayumu chose images belonging to the Homo category
much more frequently than those belonging to the other
category at 6 years of age. A one-way ANOVA using
stimulus category (Pan or Homo) as the variable was conducted for Ayumu at different ages; this revealed a significant effect of category at 6 years of age (F(1, 38) = 6.71,
P = 0.014), but the effect was not significant before 6 years
of age (3 years 8 months: F(1, 38) = 1.57, P = 0.22; 4 years
3 months: F(1, 38) = 2.36, P = 0.13; 5 years: F(1, 38) = 0.56,
P = 0.46).
For Cleo, the scores of each category were not significantly different from one another before 5 years of age, but
the score for Homo was highest at 5 and 6 years of age.
ANOVA using stimulus category (Pan or Homo) and age
(4) as the variables revealed a significant main effect of
stimulus category (F(1, 38) = 4.74, P = 0.036) and a
significant interaction between stimulus category and age
(F(3, 114) = 3.79, P = 0.012). The effect of age was not
significant (F(3, 114) = 1.87, P = 0.14).
Primates (2007) 48:303–309
307
By use of a free-choice task, eight adult and three infant
chimpanzees were examined for their visual preference for
photographs of different categories of primate. The results
showed a clear difference between adult and young
chimpanzees in visual preference. For all adult chimpanzees the score of Homo (humans) was highest among the
six primate categories, irrespective of whether or not the
subjects were born in the wild or in captivity. The adult
chimpanzees chose the images of humans more often, and
such images tended to be their first choice. These results
are consistent with those of Tanaka (2003) and provide
stronger evidence that the visual preference of the adult
chimpanzees for images of humans is consistent.
In contrast, none of the young chimpanzees initially
showed preference for images of humans. Two infants
(Ayumu and Cleo) formed a preference for images of humans with age. For neither of these young chimpanzees
was there a significant difference between their choice of
categories or a clear preference for images of humans until
they were 5 years old. For the remaining young chimpanzee, Pal, selectivity among categories was significant, with
a preference for images of the Pan genus at the first presentation, that is, when she was 3 years and 4 months old.
Pal’s preference was consistent until 6 years of age. The
Fig. 2 Mean scores of images in each category for wild-born (left)
and captive-born (right) adult chimpanzees. Each open symbol
indicates the mean score of images for each subject. Bars indicate
the mean score for each category. Each image was presented four
times, so the highest possible score was 8 (i.e. this score indicated the
image was always touched as the first choice in each presentation).
Differences between the scores for the Pan and Homo categories were
significant (P < 0.001)
Pal was the only chimpanzee who most frequently selected images belonging to the Pan category; this was
consistent from 3 years and 4 months of age. In particular,
the score of the Pan category was much higher than those
of the other categories from 3 years and 11 months of age.
The Homo category ranked second at each age for Pal.
ANOVA using stimulus category (Pan or Homo) and age
(4) as the variables revealed a significant main effect of
category (F(1, 38) = 5.75, P = 0.022), but no significant
effect of age (F(3, 114) = 0.15, P = 0.93) and no significant
interaction between category and age (F(3, 114) = 0.83,
P = 0.48).
Discussion
Fig. 3 Developmental changes
of mean scores of images in
each category for three young
chimpanzees. Each line
indicates the stimulus category.
The X-axis indicates the age in
years:months at which the
subject participated. Each image
was presented four times, so the
highest possible score was 8
(i.e. this score indicated the
image was always touched as
the first choice in each
presentation)
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308
mean score of the Homo category for Pal always ranked
second and was not significantly different from that of the
Pan category.
As expected before this study, there was a clear difference between the visual preferences of the adult and young
chimpanzees in the PRI community. Irrespective of whether the adult chimpanzees were born in the wild or captivity, all had been separated from their mothers in their
infancy and raised mainly by human caretakers or
researchers. Some had been raised with peers of approximately the same age, but not in a seminatural community
such as the current community at the PRI. Humans may
have always been very important for the adult chimpanzees
because the humans feed them, train them, often play with
them, or sometimes order them to do something. In contrast, the young chimpanzees had been raised by their own
mothers and had grown up in a seminatural community.
The young chimpanzees may therefore have a qualitatively
different social experience in infancy from that of the adult
chimpanzees. Pal, who preferred images of the genus Pan,
was the youngest of the three young chimpanzees. Pal had
experience of interacting with other chimpanzees of different ages from infancy to old age. She also had opportunities to play with other infants and adults other than her
mother, from approximately 1 year of age. Such social
experience might have promoted Pal’s visual preference
for her genus. Ayumu and Cleo, however, developed a
preference for images of humans as they grew up. These
young chimpanzees have been fed by humans from
approximately 6 months of age. They have been trained in
a variety of experimental situations from approximately
1 year of age. It is not surprising that humans became
increasingly important to the young chimpanzees as they
grew up. Food sharing and mother-to-infant food transfer
have, on the other hand, often been observed in the three
mother–infant pairs of chimpanzees (Ueno and Matsuzawa
2004). In particular, Pal had often attempted to take the
food from her mother’s hand, and succeeded. In contrast,
Cleo almost always failed to take the food from her mother
and, since infancy, had been more dependent on humans
for feeding than Ayumu and Pal. Such interactions between
mothers and infants might have made a difference to
preference among the young chimpanzees. The visual
preference for humans may not be based on the quantity of
human encounters the chimpanzees have experienced but
on the quality of their relationship with humans.
In previous studies Fujita (1990, 1993b) found that social
experience in infancy might affect the visual preference of
Japanese macaques. He used animals with variously
restricted social experience (reared either by humans or
with conspecific heterospecific peers). In these studies
rhesus macaques tended to visually prefer rhesus macaques,
irrespective of age or social experience. Japanese macaques
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Primates (2007) 48:303–309
with restricted experience tended to visually prefer rhesus
macaques to Japanese macaques, however. Fujita discussed
the preference of Japanese macaques and suggested that
geographical isolation does not promote the ‘‘psychological
isolation mechanism (Yoshikubo 1987)’’, which is conspecific preference and leads to reproductive isolation.
Chimpanzees have a closely related species, bonobo (Pan
paniscus), but these species are geographically isolated.
The same factors as those in Japanese macaques might
therefore have affected the formation of visual preference of
chimpanzees.
The results for the young chimpanzees also suggest that
early visual preference may not be determined by an
imprinting phenomenon but may develop after the age of 5
or more. Ayumu and Cleo did not show any tendency to
choose images of a specific species/family for the first time
of this task. In this free-choice task the probability of
obtaining a food reward did not depend of the species/
family of the image the subject touched. When the young
chimpanzees were 3 or 4 years old they preferred a specific
position (i.e. they often touched the images in a corner of
the lower row); this resulted in a food reward as often as if
they selectively touched the images of specific categories.
At 5 years of age, however, Ayumu and Cleo selectively
touched the images of humans and Pal selectively touched
images belonging to the Pan category. The results for
adults born in the wild may support this hypothesis. They
had been reared by their own mothers and with other
community members for several months after birth. The
preference of the wild-born individuals, however, was not
different from that of the captive-born individuals who
were reared by humans immediately after their birth. The
results suggest that visual preference gradually develops
during infancy in chimpanzees. Furthermore, because the
visual preference of the adult chimpanzees that participated
in the previous study (Tanaka 2003) remained the same,
visual preference seems to remain unchanged in chimpanzees after having developed in infancy.
The chimpanzees rarely used in previous cognitive
studies (e.g. Gon) showed the same preference as the other
adult chimpanzees, which suggests that preference for
images of humans may not depend on daily experimental
procedures but instead may be formed through daily life in
captivity over a prolonged period.
Tanaka (2003) has suggested that some visual features
of humans might particularly attract the subjects’ attention.
For example, human eyes are exceptionally conspicuous in
both shape and coloration (Kobayashi and Koshima 1997,
2001). In this study, one young chimpanzee (Pal) showed a
stronger preference for conspecific images whereas two
other young chimpanzees at first showed no preference
for images of humans. These results suggest that
visual features of humans may not automatically attract
Primates (2007) 48:303–309
chimpanzees’ attention but that the chimpanzees spontaneously select images of species that psychologically attract their attention.
In studies of preference, including this study, choice of a
particular stimulus in preference to one or more other
stimuli is often interpreted as suggesting the subject
‘‘likes’’ that stimulus more than nonchosen alternative
stimuli. It is, of course, unclear whether the stimulus is
more pleasing or more threatening to the subjects. Curiosity occasionally gets the better of fear. In any case, more
frequent selection of a stimulus indicates that some stimuli
can attract the attention of the subjects more than other
types of stimulus. This study suggests that early social
experience the may affect the visual preference of chimpanzees. This may have relevance to changes in social
cognitive abilities in great apes as proposed in the enculturation hypothesis (Tomasello et al. 1997; Tomasello and
Call 1997). That is, if humans can spontaneously elicit
more attention from human-reared great apes than motherreared ones, the human-reared great apes will be of greater
advantage in social cognitive experiments.
Acknowledgements This study was supported by the MEXT
Grants-in-Aid for Scientific Research, nos. 15730334 and 16002001,
and by the 21st Century COE Program for biodiversity (A14). I wish
to thank Mr S. Nagumo for technical help in programming and
interfacing, and laboratory staff members for assistance. I also thank
the staff members of the Center for Human Evolution Modeling
Research, Primate Research Institute, Kyoto University, for their
management of the subjects’ health.
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