Macaca fascicularis vs other macaques

36 Appendix 4 Test of the similarity of the monkey performances between baseline and test trials Tabel 4 Test of the similarity of the monkey performances shown in Appendix 1 to Appendix 3 between baseline and test trials GLMM, Venables and Ripley 2002. Values indicate statistical probability that performances in test trials were the same as in baseline trials. All values are higher than 0.05, it means the monkeys performances in both baseline and test trials are the same. . Experiment Values

1. Human vs Macaques a. Colored stimuli

0.15 0.52 0.76 0.88

b. Black and White 0.19

0.17 0.53 0.29

c. Resized stimuli 0.86

d. Blured Black and White stimuli 0.53

1.00 0.59 1.00

e. Blurred, Small, Black and White stimuli 0.57

1.00 1.00 1.00

a. Colored stimuli

1.00 0.31 1.00

b. Black and White stimuli 1.00

1.00 1.00

3. Human vs Non Human a. Colored stimuli

0.66

b. Black and White stimuli

0.71 1. Human vs M. fascicularis 2. Human vs M. mulatta 3. Human vs M. fuscata 1. Human vs M. fascicularis 2. Human vs M. mulatta 3. Human vs M. fuscata 1. Human vs M. fascicularis 2. Human vs M. mulatta 3. Human vs M. fuscata 1. Human vs M. fascicularis 2. Human vs M. mulatta 3. Human vs M. fuscata

2. Macaca fascicularis vs other macaques

1. M. fascicularis vs M. mulatta 2. M. fascicularis vs M. mulatta 1. M. fascicularis vs M. mulatta 2. M. fascicularis vs M. mulatta ABSTRACT KANTHI ARUM WIDAYATI. Categorization in Macaca fascicularis. Supervised by BAMBANG SURYOBROTO, AKICHIKA MIKAMI, ACHMAD FARAJALLAH. Categorization is an ability to group individuals or events into different classes mediated by conceptualized mental images. There are several levels of categorization and within a taxonomy the levels are nested. At the most concrete level of categorization, all or most members of the category shared common physical attributes that differ from other categories. 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 in animals. One example of categorization in animal is species discrimination. Using matching-to- sample task, present experiment tested ability of the long-tailed macaque Macaca fascicularis in discriminating dichotomous-stimuli of different animals. The species has been shown to be able to see photos as representations of real object so I used facial photos of humans and animals for the stimuli. First, I tested their ability to classify humans and macaques into separate group. Second, I tested their ability to discriminate their conspecific from other macaques. And the last, I tested whether the subjects were able to discriminate non-human animals from humans. In all of these experiments I found that the subjects showed high performance in categorizing objects, even when I discarded details of visual informations, such as color and local shapes. The ability to identify objects with reduced representation of physical properties means the subjects were able to generalize attributes of members of the group. This would indicate that the subjects created a higher level abstraction. On the other hand, in discriminating intrageneric macaque species I found that they were able to extract uniqueness of each species. More over, I also found that the subjects were able to put photos of non-human animals that shared very few similarities in physical percepts into one group. I suggested that the subjects could create a more abstract concept based on non-percepts relations as a basis to put the objects into one category. Thus, I concluded that M. fascicularis were able to perform multiple levels of categorizations. Key Words: Categorization, Conceptualized mental image, Species discrimination, Macaca fascicularis, Matching-to-sample task 1 INTRODUCTION We live in a world full of ever-changing objects. It is impossible for us to memorize each and every new individuals we encountered. Our brain need to have an ability to deal with infinite informations that is continuously coming from the surrounding environment. 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 al. 1976. These categories reduce the number of bits of information to manageable classes. 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 in the animals. Being able to identify, visually or otherwise, a new object as a member of a category is an advantage for the 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 1987, Fujita and Watanabe 1995, Fujita et al. 1997. Present experiment aims to test the ability of species discrimination by primates. I did three major experiments. First, I tested whether the monkeys were able to categorize monkey individuals as a class against human individuals as another class. Second, I tested whether they were able to discriminate their conspecific from other macaque species. Third, I tested their ability to categorize non primate animal as non-human class against human individuals as human class. Previous studies showed that monkeys were able to see photos as representations of real objects Kyes et al. 1982. I therefore used photos of various humans, monkeys and other animals as stimuli to infer their categorization 2 ability. The stimuli consisted of information on physical properties of the object. The physical properties represented in photos may be modified in many ways to alter the amount of information in the stimuli. These modified photos provide a way to deduce levels of categorization of the monkey. Some experiments found that the monkeys look to their conspecific longer than to non-conspecific so they used duration of visual fixation to indicate this discriminative capability Demaria and Thierry 1988, Fujita 1993, Fujita and Watanabe 1995, Fujita et al. 1997. However, although counting the fixation time is easy to be described quantitatively, it is uncertain as to what the reaction time measures. For instance, the longer the time could represent two facts; the monkeys likes the picture in the stimuli, or it can be the opposite. In fact, in agonistic bouts, the amonkeys tend to look longer to their opponent de Waal et al. 1976. Thus, the reaction time may better be interpreted as a measure for the attention of the monkeys and may not carry information about species discrimination. Moreover, it is not clear whether the monkeys are truly able to distinguish between species or their familiarity with their own species due to experience in their life history made them see conspecific longer. Instead of counting fixation time of each stimulus, present experiment test their categorization ability in discriminating dichotomous-stimuli of two different classes of animal. 3 LITERATURE STUDY Categorization in Humans Categorization is the ability to put an object to a group based on some internal representations of the group Rosch et al. 1976. The ability to categorize objects and events and extending this behavior to new instances is fundamental to many human activities. I sort the objects and events around us into categories, while still being able to recognize some or all of the individuals. In general, categorization could be divided into two levels Behl-Chadha 1996. If the detected physical properties of the individuals within a category are mostly similar, we call it as basic level of abstraction Rosch et al. 1976. For example; we could put Asians, Africans and Caucasians into one group; that is a human group. If the connection between members of one category is not only based on perceptual similarity but more on relations between concepts, we call it as abstract level of categorization Mervis and Rosch 1975. For example, we can put rice, bread and fruit into the food or edible group and put a chair, a plane and a soap into the non-food group. Although it is basically divided into two levels, the relation between each class often overlap and sometimes it is very difficult to differentiate between classes. These levels of categorization are basic to understand language, number and social relationship with other humans. This ability obviously needs memory, learning and reasoning. In humans, categorizing behavior was predicted to start at infantile age. Quinn 1993, 2002 found that the 3-4 month old infants attended to natural objects as though they belong to groups of basic level. The experiments used the preferential looking procedure and measure the looking time of the pictures. The infants tended to look at the picture of a new categories for longer period of time. Their ability was regarded as in the basic-level of categorization. Categorization in Animal The field of research on the ability of animals to categorize objects was opened by the pioneering study of Herrnstein and Loveland 1964. They showed 4 that the pigeon were able to sort photographs on the basis of whether the image contained human being or not. It means the pigeon were able to make a class of human and a class of non-human, which is the definition of categorization. Since then, several studies have demonstrated categorization in other animals, most of them used primates as models ex: Tanaka 2001, Jitsumori and Matsuzawa 1991, Santos 2000. Some of the researches aimed to know whether categorization processes in the animal is based on similar processess compare to human ex: Farbe-Thorpe 2003, Freedman et al. 2002,2003, Hampson et al. 2004. In other case, some studies wanted to find out the levels of categorization that could be performed by the animals ex: Tanaka 2000, Jitsumori and Matsuzawa 1991, Santos 2000, Inoue et al. 2008, Vonk McDonald 2002; Vonk McDonald 2004. In both cases, the studies used photos of biologically significant objects, such food vs non food, animals vs non-animals, and the last is own species vs non-own species or species discrimination Tanaka 2001, Jitsumori and Matsuzawa 1991, Santos 2000, Inoue et al. 2008, Fujita et al 1995, 1997, Vonk McDonald 2002; Vonk McDonald 2004. Species discrimination is important to prevent hybridization among species Yoshikubo 1985, Fujita 1995, Fujita et al. 1997. Some studies were conducted to find out which part of the body are really important to identify and categorize the species. Those studies found that face provide information about species, sex, age and emotion of an individual Pascalis and Bachevalier 1988, Tomonaga 2007. Fujita et al. 1995 demonstrated that Sulawesi macaques performed basic level of categorization in identifying their conspecific. The stimuli used in that experiment were photos of monkey presented sequentially. By counting the fixation time of each stimulus, they found that the Sulawesi macaques see their conspecific longer than non-conspecific. Thus, the photos carry specific information which could be categorized by conspecific or non-conspecific Fujita et al. 1995, Pascalis and Bachevalier 1988, Tomonaga 2007. However, although the fixation time is easy to be described quantitatively, it is difficult to draw conclusion from it. For example, the longer reaction time could mean that monkey likes the picture in the stimuli, or it could be the opposite. In fact, in agonistic bout, the monkeys tend to 5 look longer to hisher opponents de Waal et al. 1976. Looking at previous work in primates, there are some data on categorization in great apes, M. mulatta, M. fuscata and Sulawesi macaques but not really in long-tailed macaques M. fascicularis. A few studies showed that M. fascicularis were able to see photos as a representations of the real objects Dasser 1987, Kyes et al. 1982. More over, some studies also found that those monkeys were able to identify individual within species Dasser 1987, read facial expression from the drawing and could discriminate between drawings of some bodies of old world primate species Dittrich 1994. However, there were no direct experiment to infer the level of categorization in this species. Operant Conditioning Behavior In this experiment, I used the operant conditioning methods which refers to process in which the frequency of occurrence of the particular type of behavior was modified by the consequences of the behavior Reynolds 1975. In operant conditioning, the behavior called operant came from animal motivation to response to a given stimulus. The stimulus used in operant conditioning is discriminative. In this particular experiment, monkeys were trained to choose a specific stimulus the plus stimulus, S+ from another alternative to get a reward. If they choose the other the minus stimulus, S-, they would not get any rewards. The behavior to choose a specific card is an operant. The reward is the consequences of the behavior and it should increase animal motivation to choose the plus stimulus. The specific task in this operant conditioning method is matching to sample Miller et al. 1996 with photographs of human, macaques and other animals as stimuli. 6 METHODS Subjects The subjects were two adult M. fascicularis males, named Ucok and Sukhoi and one female named Kerok. Ucok were born in Pangandaran National Park, with present age at least 19 years old. Kerok and Sukhoi were born in Department of Biology, Bogor Agricultural University with ages are 14 and 9 years old, respectively. Both male monkeys were maintained at the Department of Biology of Bogor Agricultural University. The female monkey was maintained at Primate Research 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 phases were held about two years for Ucok and one year for Sukhoi and two months for Kerok depended on the ability of learning of the monkeys. The test phase was conducted for few months for all monkeys. Apparatus A modified version of the Wisconsin General Test Apparatus WGTA was used for the presentation of stimuli to the macaques. The apparatus used consisted of a horizontal tray containing three shallow food-wells mounted on a portable shelf. A sample stimulus and a matching stimulus were placed over the food-wells so that they always associated with a food reward beneath. When setting up the food reward between trials, an opaque screen was placed between the cage and the experimenter to prevent animals from seeing the process. The eye of the experimenter was covered with sunglasses, so the monkey could not use eye direction of the experimenter as cue to find the matching stimulus. To control the animal’s motivation level, animals were deprived of food after 5 pm until the next morning before the day of a training session or a test session. Foods were provided either during or after the experiments . 7 Stimuli and Procedure I assessed the ability of M. fascicularis in categorizing objects by conducting three experiments. First, Human vs Macaques experiment, aimed to test the ability of M. fascicularis in categorizing monkeys and humans into two different conceptual classes. Second, M. fascicularis vs Other Macaques experiment, to test the ability of M. fascicularis in categorizing conspecific differently from M. mulatta or M. fuscata. And the last one, Human vs Non Human experiment, to test the ability of M. fascicularis in categorizing various kinds of animal differently from human. Fujita et al. 1995 demonstrated the ability of species discrimination of Sulawesi macaques using photos as stimuli. Other studies of categorization also used photos Demaria and Thierry 1988, Fujita 1993, Fujita and Watanabe 1995, Fujita et al. 1997 but those former studies did not control feature of the photos so it is difficult to delineate which component of the photo provides informations to do categorization. Each species of the animal possess distinctive non-facial, physical features; for instance, posture and proportion of legs which may or may not be present at the photo frames. For that reason, I used facial photos and controlled the background color by changing it into green. Because of limitation of visual fixation time to infer species discrimination as noted in Introduction, present experiments tested their categorization ability based on dichotomic discrimination of one species against other. To do this, I employed match-to- sample task that often were used in working memory experiments Miller et al. 1996, Rao et al. 1997 and later to study categorization experiments Freedman et al. 2002; Hampson et al. 2004; Inoue et al. 2008; Tanaka 2001. Using operant conditioning method, at first, the monkeys were trained to respond only to particular stimulus, not based on previous experience in their life. Every trial consisted of two presentations. The first presentation shows sample stimulus, and the second matching and distractor stimuli side by side. The sample and matching stimuli always belonged to a same category that dichotomically differ to the distractor Figure 1. I assumed that each stimulus was independent from each other so a stimulus could be defined as a matching stimulus in one trial and could 8 be a distractor in other trial depended to the sample stimulus. I trained the monkeys to associate sample and matching stimuli against distractor stimulus. First, I showed the monkeys a sample stimulus as reference to be matched Figure 1a. 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, I 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. Subjects motivation for reward warranted the choice of the matching stimulus. I 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. I blocked every 20 trials into one session and measured their correct rate. If the subjects chose the matching stimuli higher than 90 in a 9 session, it means they were able to associate matching to sample stimuli. Then I introduced a set of new photographs of the same human and the same monkey. I repeated this training until the same criterion was reached 90 correct rate in 3 continuous sessions. After the monkey cleared the criterion of third set, I introduced the photographs of a different human and a different monkey. This procedure was repeated for six set of new humans and monkeys. After the monkey cleared all of these training phases, I started the test session. At this stage, logically, this may be inferred as the subjects had developed dichotomic concepts of matching against distractor. When they showed this competence, they went to test phase see below for details where the matching photos were new ones. If the subjects were able to transfer the learned concept to novel stimuli, it proved that they could categorize. 10

a. Human vs Macaques