Multiple levels of categorization in long tailed macaque (Macaca fascicularis)

ISSN 0912-4047

PRIMATE RESEARCH

Symposium of Primate Society of Japan, July 7th-8'\ Japan.

1

MULTIPLE LEVELS OF CATEGORIZATION IN LONG TAILED
MACAQUE (Macaca fascicularis)
Kanthi Arum Widayati 1, Bam bang Suryobroto 1, Achmad Farajallah 1,
Akichika Mikami2
1. Bogor Agricultural University, Indonesia

2. Chubu Gakuin University, Japan.

INTRODUCTION

We live in a world full of ever-changing objects. It is impossible for us to
memorize each and every new individual we encounter. One way to overcome the
memory storage constraint is to represent factual objects as conceptualized mental

images. A concept concludes a lot of informations that had been collected at the
time we perceive the object and abstracts them to assist the process of grouping
individuals or events into different categories (Rosch et a/. 1976). There are
several levels of categorization and within a taxonomy the levels are nested
(Rosch et al. 1976). At the most concrete level of categorization, all or most
members of the category shared common physical attributes that differ from other
category. The higher the level of category, the fewer common attributes between
members of the group.
In addition to humans, the ability to categorize has also been proposed for
animals. Being able to identify, visually or otherwise, a new object as a member of
a category is an advantage for animals. It should help them to distinguish between
food or non-food, and to discriminate between species of animal. This species
discrimination is important to prevent hybridization among species (Yoshikubo
1985, Fujita and Watanabe 1995, Fujita eta/. 1997).
Present experiment aims to test the ability of species discrimination by M
fascicularis in discriminating dichotomous-stimuli of two different classes of

animal. Previous studies showed that monkeys able to see photos as
representations of real objects (Kyes et al. 1982, Dasser 1987). We therefore used
photos of various human, monkey and other animal as stimuli to infer their

categorization ability. We did three major experiments. First, we tested whether

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Symposium of Primate Society of Japan, July 7th-8th, Japan.

monkeys are able to categorize monkey individuals as a class against human
individuals as another class. Second, we tested whether they able to discriminate
between their conspecific from other macaque species. Third, we tested their
ability to categorize animal as non-human class against human individuals as
human class.

METHODS

Using operant conditioning method Reynolds (1975), we trained monkeys
to associate sample and matching stimuli against distractor stimulus. First, we
showed monkeys a sample stimulus as reference to be matched (Figure la). To
ensure that the subjects paid attention to the sample stimulus, they had to touch
the sample stimulus and for this they received reward that they may find beneath
the stimulus. Next, we presented side-by-side matching and distractor stimuli

which one had to be chosen by the subjects. When the subjects chose the
matching stimulus, they received food as a reward; the response was counted as a
correct one. When they chose the distractor, they did not get any rewards.
Subject's motivation for reward warranted the choice of the matching stimulus.

a Baseline trial

b. Test trial

Figw-e I. Schematic diagram of operant conditioning match-1(}-sample task of the experiment in
baseline (a) and test trials (b). First, we showed sample stimulus to subject; after that, we
showed a pair of stimulus consists of matching and distractor, respectively. Subject need
to choose matching stimulus to get a rewanl In baseline trials, matching stimuli is the
same sample stimulus; in test trials, they were different

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Symposium of Primate Society of Japan, July 7th-8th, Japan.

We repeated the trials consecutively with inter-trial intervals for about 30 second.

The location of matching and distractor stimuli on the tray was arranged
pseudorandomly. We blocked every 20 trials into one session and measured their
correct rate. If the subject chose the matching stimuli higher than 90% in a
session, it means they were able to associate matching to sample stimuli.
Human vs Macaques

a

b

c

d

e

f

g

h

Figure 2. Example of stimuli used for Human vs Macaques experiment. a and b were a pair of
stimuli used in baseline trials. Both photos could be sample and matching stimuli,
depended on the trials. These stimuli were also used as sample stimuli in test trials. c
to h were example of matching stimuli in test trials. c, e and g were the example of
human stimuli. d, f and h were example of monkey stimuli. d was example of photos
of M. fascicularis, while f and h were example of M. mulatta and M. foscata,
respectively.

For training phase, sample and matching stimuli were the same and
monkey's stimuli were always M fascicularis (see figure 2b and 2d). To test if a
subject could apply the learned concept of human and monkeys to new
individuals, we changed the pictures of matching stimulus with different
individuals that belonged to the same category as the sample stimuli (ex: figure
2c , 2e, 2g). To test whether the subjects have multilevel abstraction, we deviced
extended experiments that stripped off certain visual information from the stimuli.
First, we took color off the photos and presented it in black and white. In the next
step, we reduced the size of the stimuli to one quarter of the original and showed
it to monkeys. In this case, we tested them using pairs of photos of colored human

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Symposium of Primate Society of Japan, July 7th-8th, Japan.

and M fascicularis. We continued our test by giving the subjects the blurred,
black and white, original size photos of human and macaques. In our last attempt
to ascertain whether the subjects could categorize human differently from
macaques, we reduced the size of the black and white, blurred photos of human
and monkeys to one quarter of the original size. Thus, by comparing subject's
responds to complete and reduced information stimuli, we may interprete their
level of categorization. In total, we used 82 photos as the stimuli for the test.

M. fascicularis vs Other Macaques
In this experiment, we assesed categorization ability of M fascicularis to
discriminate their own species from other species of macaques. In this
experiment, we used several facial photos of M fascicularis, M mulatta and M

foscata. We did this in two conditions, that is in color and black and white. Same
as the first experiment, the test session consisted of certain proportion of baseline

and test trials. In baseline trials of both paradigms, the photos of matching stimuli
were the same to sample stimuli. In total, we used 40 photos as the stimuli for the
test.

Human vs Non-Human
In this experiment, we assesed categorization ability of M fascicularis to

a

b

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Figure 3. a to h were example of stimuli used in human vs non-human experiments.

Symposium of Primate Society of Japan, July 7th-8'h, Japan.

5

discriminate various kinds of animals from human using facial features. In this
experiment, we used several photos of human (see the first experiment) and nonprimate animals, such as mammals, reptiles and amphibians (Figure 3). As in the
second experiment, we did this in color and black and white. In test trials, we
changed the pictures of matching stimulus with different individuals that belonged
to the same category as the sample stimuli; for example, if the sample stimulus
was monkey 2b then the matching stimulus was animal 3a. The subject should
compare the novel matching stimulus to the available distractor. If the subject
could associate the sample and the different-picture of matching stimuli, we may
infer that they put those two pictures into one class that dichotomically differs
from the class of distractor. This would mean they are able to categorize nonhuman animals

differently from human. The baseline stimuli were the same

stimuli used in Human vs Macaques experiment (see Figure 2). In total, we used
68 photos as the stimuli for the test.

Subjects
The subjects were two adult M fascicularis males, named Ucok and
Sukhoi and one female named Kerok. Both male monkeys were maintained at the
Department of Biology of Bogor Agricultural University. The female monkey was
maintained at Primate Researh Institute, Kyoto University. They were reared in
individual cages and tested in the same cage. Experiments were conducted
according to the Guide for the Care and Use of Laboratory Animals by the
National Institute of Health, U.S.A. (1985), and the Guide for the Care and Use of
Laboratory Primates by the Primate Research Institute, Kyoto University (1986,
2002). The training phase was held about two years for Ucok and one year for
Sukhoi and two months for Kerok depend on the ability of learning of the
monkeys. The test phase was conducted for few months for all monkeys.

Data Analysis
In this experiment, monkeys have to respond to particular stimuli. We
defined the response of monkeys as correct when they choose matching stimulus,

Symposium of Primate Society of Japan, July 7th-8'\ Japan.

6

and false when they choose distractor stimulus. This binomial responses were
dependent on stimuli presented in baseline and test trials; we therefore treat
baseline and test trials as independent variables and the effect of individuals in the
analysis as random effect. Thus, we used Generalized Linear Mixed Model
(GLMM, Venables and Ripley 2002) using R software version 2.10.1 (R
Development Core Team 2010) to analyze our discrete, binomial data.

RESULTS

Human vs Macaques

In this experiment, all subjects could associate matching to sample stimuli.
They showed high performance of choosing the correct stimuli at the proportion
around 90% of the trials. Because the matching stimuli were always of a different
category to the distractor stimuli, it might mean they developed different and
mutually exclusive concepts of human and monkeys. These results provided a
reference to test whether subjects could transfer the newly developed mental
concepts to identify new individuals. We did this by changing the matching
stimulus with pictures of different humans and different kinds of monkeys. In this
test, we found that all subjects associate sample stimuli to new individuals of
matching stimuli (Figure 4). This same result to baseline (glmmPQL, p=O.l5;
Venables and Ripley 2002) would indicate that subjects were able to correctly
identify new individuals as members of its own class or of human class. This
would mean that monkeys categorized humans differently from monkeys. To test
whether the subjects have multilevel abstraction, we deviced three experiments
that stripped off certain visual information from the stimuli. First, we took color
off from the photos and presented it in black and white. We found that the
subject's performance in both baseline and test phases were the same (glmmPQL,
p=0.19) (Figure 5). This result indicates that even without color, the subjects
categorized humans differently from monkeys. In the next step, we tested whether
size of the stimuli could affect the performance of the subjects in categorizing
humans differently from monkeys. We found that the subject's performance in
both baseline and test phase were the same (glmmPQL, p=0.85)(Figure 6). It

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Symposium of Primate Society of Japan, July 7th-8'\ Japan.

means the subjects did not affected by the reduction in size of the stimuli.
We continued our test by giving the subjects the blurred and black and
white original size photos of human and macaques. We found that the subjects
were able to categorize human separately from monkeys. Their performance in
both baseline and test phases were the same (glmmPQL, p=0.53) (Figure 7).
In our last attempt, we reduced the size of the black and white, blurred
photos of human and monkeys to one quarter of the original size. We found that
even in condition lacking important physical informations, such as color, shape
and size, their performance in both baseline and test phases were the same

Ucok

Sukhoi
Human

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Figure 5. Monkeys performances in categorizing human and monkeys using black
and white stimuli. The vertical lines show the 95% confidence level in
the binomial test The performance levels of both monkeys at test trials
were not significantly different from the baseline trials (glmmPQL,
p=0.19).
SukhOi

Ucok

Kerok

Hu"""'
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Figure 6. Monkeys performances in categorizing human and monkeys using
resized stimuli. The vertical lines show the 95% confidence level in
the binomial test. The performance levels of both monkeys at test
trials were not significantly different from the baseline trials
(glmmPQL, p=0.85).

9

Symposium of Primate Society of Japan, July 7th-8'\ Japan.

Sukhoi
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Figure 7. Monkeys performances in categorizing human and monkeys using
black and white blurred stimuli. The vertical lines show the 95%
confidence level in the binomial test. The performance levels of both
monkeys at test trials were not significantly different from the
baseline trials (glmmPQL, p=0.53).
Sukhoi
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Figure 8. Monkeys performances in categorizing human and monkeys using
resized, blurred, black and white stimuli. The vertical lines show the
95% confidence level in the binomial test. The performance levels of
both monkeys at test trials were not significantly different from the
baseline trials (glmmPQL, p=0.57).

Symposium of Primate Society of Japan, July 7th-8'\ Japan.

10

M. fascicularis vs other macaques
This experiment aimed to test the ability of monkeys in categorizing M

fascicularis differently from other macaque species. In this experiment we used
two paradigms, that is, M fascicularis vs M mulatta and M fascicularis vs M

fuscata. In baseline trials of both paradigms, the photos of matching stimuli were
the same to sample stimuli. We found that all subjects associate sample stimulus
to new individuals of matching stimuli (Figure 9). This same result to baseline
(glmmPQL, p=1) indicate that subjects were able to correctly identify new
individuals as members of their respective class. This would mean that the
subjects categorized M fascicularis differently from the two other macaques.
As in the first experiment, we ascertained this categorization ability by
taking color off the photos. We found that all subjects associate sample stimulus to
black and white version of the matching stimuli (Figure 10). This same result to
baseline (glmmPQL, p= 1) would indicate that even without color, the subjects
could also categorize M fascicularis differently from other macaques.

Human vs Non-Human

This experiment aimed to test ability of monkeys in categorizing human
differently from non-primate animals. In this experiment, we used several photos
of human and non-primate animals, such as mammals, birds and reptiles and
amphibians. We tested the subject using both color and black and white photos.
For baseline trials, we used same photos of human and M fascicularis that used in
baseline trials of Human vs Macaques experiment. We found that our subjects did
high performance in test trials, similar to that in baseline trials (glmmPQL,
p=0.65for colored stimuli and p=O. 70 for black and white stimuli) (Figure 11 ). It
means that they were able to maintain concept of human and developed new
concept about non-human.

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Symposium of Primate Society of Japan, July 7th-8'\ Japan.

Sukhoi

l

g

!

::1

E
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Ucok

M.fasdcurarill

M.fasdcurarill

MJasci-

ｾ＠

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0

10

-

Figure 9. Monkeys performances in categorizing conspecific and other monkeys
using colored stimuli. The vertical lines show the 95% confidence
level in the binomial test. The performance levels of both monkeys at
test trials were not significantly different from the baseline trials
Sukhoi

Ucok

Figure 10. Monkeys performances in categorizing conspecific and other monkeys
using black and white stimuli. The vertical lines show the 95%
confidence level in the binomial test. The performance levels of both
monkeys at test trials were not significantly different from the baseline
trials (glmmPQL. p=l).

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Symposium of Primate Society of Japan, July 7th-8'\ Japan.

Sukhoi

Ucok
!Jlad( and Whit& Sbmuo

r---- -1

Figure 11. Monkeys performances in categorizing human and non-human using
colored and black and white stimuli. The vertical lines show the 95%
confidence level in the binomial test. The performance levels of both
monkeys at test trials were not significantly different from the baseline
trials (glmmPQL, p=0.65 for colored stimuli and p=0.70 for black and
white stimuli).

Symposium of Primate Society of Japan, July 7th-8'\ Japan.

13

DISCUSSION

Our first experiment to show the ability of categorization in M
fascicular is was the discrimination of human vs monkey. In the training phase, we
introduced pictures of human and monkey to subjects. There were consistent
similarities and differences of physical properties between human and monkey
pictures. It is not unreasonable to conclude that our subjects used these similarities
and differences to create a conceptualized mental image of human that differs to
that of monkey. There are some physical properties that provide information to
create concepts. First is shape. The global and local shapes of human's and
monkey's faces are very different. While human faces are oval, monkey's faces are
rounded with hair on it. Another possibility is that the subjects detected the
presence of the eye. This mechanism, called "eye direction detector", is important
to understand facial emotion (Farroni et al. 2002, Baron-Cohen et al. 1999).
Given the eyes, its angles with nose and lips of both species are different. The
second is color. In this experiment, we used colored photographs. As seen in
stimulus photos (Figure 2), compared to uniformly presented background color,
the global color of the monkeys was different to that of human. Indeed, this had
been shown by Santos (200 1) that colors are used as information to categorize
object. Those informations may help subjects to recognize and discriminate
between categorically human and monkey.
The resulting concepts of human and monkey developed from training
phase were used by our M fascicularis individuals as basis to categorize pictures
in the test phase. In every trial of test phase we changed the baseline pictures with
new ones. This would prove the ability of subjects to transfer its concepts to
respond to novel stimuli. For monkey pictures, we used three different species of
macaques. We found that proceeding from baseline to test trials performance of
our subjects remained the same. These indicate that our subject categorized
monkey as monkey and human as human. It is interesting to note that although
two of our subjects (M fascicularis) never saw other species (M fuscata and M
mulatta) for their entire life, they categorize photos of those species as monkey

Symposium of Primate Society of Japan, July 7th-8 1\ Japan.

14

instead of human which in captivity they see everyday. It might be concluded that
they had concepts of human and monkey based on different color and shape of the
stimuli. We may interprete this fact as the monkeys recognized natural
discontinuity between the two class; Rosch et al. 1976 called this as basic level of
abstraction. As this kind of categorization ability was based on perceptual
similarity of physical attributes of the photos discussed above we may also
describe this as the concrete level of abstraction (Vonk and MacDonald
2002,2004).

In nature, sometimes there are conditions (such as at long distance or less
light conditions) where monkeys could not see detailed information of object to
do categorization. Thus, they have to be able to categorize objects based on broad,
generalized concept that is developed on concept with complete and detailed
physical percepts. According to Rosch et al. (1976), the world is structured
because real-world properties do not occur independently of each other. Because
of this correlation, few properties of an object would suffice to predict the whole
properties. After seeing the results of the above test (which were positive), we
wondered whether the subjects would still have the ability to identify objects if
the informations on the physical properties of the stimuli were reduced. This
would simulate natural conditions and further proof the ability to transfer the
learned concept in our subjects. We then manipulated the stimuli by taking color
off the matching and distractor stimuli. The result showed that the ability of all of
our subjects to categorize between human and monkey was not hampered. They
could successfully transferred their mental image to the black and white photos.
This fact showed that the subjects did not depend on color and use other
informations to discriminate the stimuli. Some studies showed that monkey may
use global shape (Dittrich 1994) and local features (Demaria and Thierry 1988) of
object as informations in categorizing object. Jitsumori and Matsuzawa (1991)
showed that M mulatta and M cyclopsis able to classify human shilouettes as
human and assume that monkeys used global shape to recognize human. Rosch et
al. (1976) explained that levels of abstraction are nested. At the basic level,
objects within category shared most similarity in concrete properties. When it

Symposium of Primate Society of Japan, July 7th-8'\ Japan.

15

goes to the more abstract levels, it share less properties among each other. Thus,
we may follow that the use of global shape is one way monkey used to generalize
the physical properties of an object. To test whether our subjects might be able to
generalize their physical percepts, we blurred or resized the stimuli to reduce
and/or to change the local shape informations carried by the stimuli. Again, in all
of these extended tests, our M fascicularis subjects showed high performance of
discrimination. This ability to classify blurred or resized photos of human as
human and blurred or resized photos of monkey as monkey demonstrated that the
subjects were looking for features of blurred or resized matching stimulus that
have common properties with those of sample stimulus. It seemed that our
subjects substracted the local shape differences to get a generalized concept of
object. Our experiment showed that our subjects performs at least two levels of
categorization by learning from their experience in training and test phases.
For second experiment, we tested the ability of M fascicularis m
discriminating M fuscata or M mulatta against their conspecific. Those macaques
belong to fascicularis group (Fooden 1969) so they shared many similar physical
properties of face, such as the existence of facial hair and other local shapes. Thus,
the monkeys have to extract the differences from total facial properties to get the
uniqueness of each species. Result of the experiment showed that monkeys could
discriminate their conspecific from other species. They may used color as
information, since the hair color of M fascicularis in the stimuli were lighter than
that of M mulatta and darker from M fuscata. More over, the facial color of M

fascicularis is relatively brownish while M mulatta paler and M fuscata reddish.
In Human vs Macaques experiments, when color information was discarded, our
monkeys used (whether global or local) shape informations to categorize the two
different classes. Thus, we took the color off the stimuli and found that our
subjects again showed high performance of discriminations. This adds to our
conclusion that the subjects able to detect the differences in physical properties of
each species and use it as basis in discrimination. This experiment showed the
categorization ability the other way around from the first experiment; that is, the
transfer of concept from general to specific.

Symposium of Primate Society of Japan, July 7th-8'\ Japan.

16

The Human vs Macaques and M fascicularis vs Other Macaques
experiments showed that our M fascicularis able to develop concept using
informations from similarity and difference of physical properties to put objects
into one particular class. However, in some conditions, it takes more than physical
similarity to put objects into one group. One object may relate to others based on
relations that could not be detected easily by sensory properties. Thus, in this case,
subjects need the ability to associate different conceptualized mental images to
discriminate stimuli lacking in physical clues. The class that is created does not
rely on perceivable features and may reflect a more conceptual understanding of
category belongingness. This kind of concept assisted higher level of
categorization. To test whether our M fascicularis were able to create such a more
abstract concept, we did Human vs Non-Human experiment. In two previous
experiments, there are physical similarities between all sample and matching
stimuli. In Human vs Non-Human experiment, we dismissed physical similarities
within one category; that is, Non-Human class consisted of photos of animals
such as mammal, bird, reptile and amphibian which were different in many ways.
At first we tested them with colored stimuli. Our subjects showed high
performance in discriminating between human and non-human classes. Since
there are no similarity within non-human category, we may suspect that our
subject use color information to do categorization. Still, if we took color off the
stimuli, our subjects discriminated non-human from human. We assumed that the
monkeys created a new concept, that is concept of non-human that differ from
concept of human. Thus, the result clearly showed that our subjects could perform

higher level of abstraction.

CONCLUSION

Our studies showed that our M fascicularis able to discriminate several
species of animal. They did it by creating concepts that were based on concrete
and non-percepts informations represented in the stimuli. Thus, we concluded that

M fascicularis able to perform basic and abstract level of categorizations.

Symposium of Primate Society of Japan, July 7th-8'\ Japan.

17

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