Visual Preference in a Human-Reared Agile Gibbon (Hylobates Agilis)
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Primates (2010) 51:63–67 DOI 10.1007/s10329-009-0175-9 ORIGINAL ARTICLE Visual preference in a human-reared agile gibbon (Hylobates agilis) Masayuki Tanaka • Makiko Uchikoshi Received: 6 August 2009 / Accepted: 6 October 2009 / Published online: 31 October 2009 Ó Japan Monkey Centre and Springer 2009 Abstract Visual preference was evaluated in a male agile Introduction gibbon. The subject was raised by humans immediately after birth, but lived with his biological family from This study assessed visual preference for photographs of one year of age. Visual preference was assessed using a primate species in a human-reared agile gibbon. Fujita and free-choice task in which five or six photographs of dif- colleagues revealed that macaque species generally show ferent primate species, including humans, were presented greater interest in images depicting their own species (e.g., on a touch-sensitive screen. The subject touched one of Fujita 1987, 1993a; Fujita and Watanabe 1995; Fujita et al. them. Food rewards were delivered irrespective of the 1997). Using cross-fostered macaques, they demonstrated subject’s responses. We prepared two types of stimulus that such a preference is genetically programmed (Fujita sets. With set 1, the subject touched photographs of 1993b). In contrast, Tanaka (2003, 2007) revealed that humans more frequently than those of other species, visual preference in chimpanzees might develop through recalling previous findings in human-reared chimpanzees. social experience in infancy. With set 2, photographs of nine species of gibbons were Gibbons, members of the Hominoidea, are distributed presented. Chimpanzees touched photographs of white- throughout the tropical rain forests of southeast Asia, and handed gibbons more than those of other gibbon species. form socially monogamous and territorial family groups. The gibbon subject initially touched photographs of agile Gibbon species that live in adjacent or overlapping areas gibbons more than white-handed gibbons, but after one and can be from different genera (Symphalangus and Hylobates two years his choice patterns resembled the chimpanzees’. lar/agilis), and it is now known that the different genera of The results suggest that, as in chimpanzees, visual prefer- gibbon are as distinct from one another as are Homo from ences of agile gibbons are not genetically programmed but Pan (Roos and Geissmann 2001). Studies of wild gibbons develop through social experience during infancy. have addressed topics such as vocal communication, social structure, and feeding ecology (e.g., Chivers 1976; Mitani Keywords Agile gibbon Á Sensory reinforcement Á 1988; Oyakawa et al. 2007). There are some developmental Visual preference Á Social experience studies in captive gibbons (e.g., Uchikoshi and Matsuzawa 2002, 2007), but there are relatively few behavioral and cognitive studies (e.g., Beck 1967; Cunningham et al. 2006; Horton and Caldwell 2006; Hyatt 1998; Inoue et al. 2004; Myowa-Yamakoshi and Tomonaga 2001; Ujhelyi M. Tanaka Á M. Uchikoshi et al. 2000). Here, we extend the use of the free-choice task Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan as a means of studying the perceptual and cognitive abili- ties of gibbons. The subject was reared by humans M. Tanaka (&) throughout infancy, but had extensive contact with his Wildlife Research Center, Kyoto University, brother and parents from the age of one year. The objective 2-24 Tanaka-sekiden-cho, Sakyo-ku, Kyoto 606-8203, Japan was to assess whether visual social preference in this gib- e-mail: [email protected] bon appeared genetically programmed, as in macaques, or 123 64 Primates (2010) 51:63–67 whether it was influenced by experience, as in running the WindowsÒ OS. We used this booth and some chimpanzees. other similarly equipped booths to test the chimpanzees. Stimuli Methods The stimuli were 5.6 9 5.6 cm digitized color images Subject (198 9 198 pixels, 24-bit color jpeg file) created from color photographs. We prepared two types of stimulus sets The subject was a male agile gibbon (H. agilis) named that differed in their taxonomic categories. Tsuyoshi, housed at the Primate Research Institute of Kyoto University (KUPRI). He was born on 9 June 1998. Stimulus set 1 Because of persistent abusive behavior by his mother, nursery rearing was instigated eight days after birth. Stimulus set 1 was composed of four genera and two tax- Tsuyoshi was raised by one of the authors (MU) and other onomic families of primates: Homo, Pan, Gorilla, Pongo, members of the KUPRI staff. He also had daily visual Hylobatidae, and Cercopithecidae. Each category consisted contact with four adult gibbons—his parents and a pair of of 20 different images; that is, a stimulus set consisted of white-handed gibbons (H. lar)—who were housed in dif- 120 images. The images of humans (Homo) were highly ferent cages in the same room. That is, two species of varied in terms of race, age, and sex. Gaze direction was gibbons and humans were familiar to the subject since not controlled, but not all photographs were face-on. Pic- infancy. When he was one year of age, his younger brother tures of humans and other species included examples of Raja was born. The two have lived together since that time. both direct and averted gaze. None of the images had been When Tsuyoshi was 2.5 years old, he and Raja were presented to the subject before this study. The images of returned to their mother’s cage. Although permanently nonhuman primates included infants, juveniles, and housed with gibbons, Tsuyoshi and Raja continued to have mother–infant pairs. Since these images had previously daily contact with humans for husbandry training, behav- been used in a study investigating visual preferences in ioral observations, and enrichment purposes (Uchikoshi chimpanzees (Tanaka 2007), stimulus set 1 was only used and Matsuzawa 2002, 2007). Although we trained both for the gibbon subject. Tsuyoshi and Raja, only Tsuyoshi continued to participate in the present study. Nine chimpanzees (Pan troglodytes) Stimulus set 2 (three juveniles and six adults) also participated in the study. The chimpanzees lived together in KUPRI. They Stimulus set 2 was composed of nine species of gibbons had participated in many previous cognitive studies, (Hylobates agilis, H. lar, H. moloch, H. pileatus, Bunopi- including touch screen tasks (e.g., Matsuzawa 2003; thecus hoolock, Nomuscus concolor, N. gabriellae, N. leu- Matsuzawa et al. 2006), and in visual preference studies cogenys, and Symphalangus syndactylus). Each species (Tanaka 2003, 2007). Because the gibbons were housed on was represented by 15 different images; that is, a stimulus a different floor from the chimpanzees, the latter had little set contained 135 images. None of the images had been visual contact with gibbons in their daily lives. presented to the subjects previously. All procedures adhered to the Guidelines for the Care We conducted the experiment with stimulus set 1 when and Use of Laboratory Primates of the Primate Research Tsuyoshi was 6 years 3 months, 8 years 8 months, and Institute, Kyoto University, 2nd ed. (2002). 9 years 8 months of age. We conducted the experiment with stimulus set 2 when Tsuyoshi was 6 years 5 months, Apparatus 8 years, and 9 years of age. The gibbon subject was trained and tested in an experi- Procedure mental booth (1.8 m W, 1.8 m D, and 2.0 m H) that was originally designed for chimpanzee studies. Several 1700 The general procedure was the same as that described in liquid crystal display (LCD) touch-sensitive screens (IO- Tanaka (2007). The subject faced a touch-sensitive screen data Device Inc., LCD-AD172F-T, 1280 9 1024 pixels, in an experimental booth (see Fig. 1). The procedure was 32-bit color) were installed along one wall of the booth. A slightly modified for the gibbon: one of the authors (MU) universal feeder (Biomedica, BUF-310-P50) was attached stayed near the subject but remained passive throughout. A to the display and delivered small pieces of food as rewards trial began with a warning stimulus (a gray solid square (e.g., blueberry, grape, and pineapple) in front of the sub- 3.5 9 3.5 cm) appearing in a random position on the dis- ject. The entire system was controlled by a personal PC play. After the subject had touched the warning stimulus, 123 Primates (2010) 51:63–67 65 Fig. 1 The subject, Tsuyoshi, facing the display (left) and touching an image of a human (right) as a second choice stimulus images were presented, each one in a cell ran- Results domly located within a three-row-by-four-column matrix. Each image belonged to one category. In each trial the The mean scores for images in each category of stimulus subject was given two opportunities to touch an image. The set 1 are shown in Fig. 2. The gibbon subject showed first touch was then followed by a 2 s chime, and then only marked differences in the stimuli selected. The sum of the touched image was presented on the monitor for 2 s. A scores for the four presentations of each image was food reward was delivered with a probability of approxi- calculated and is shown as the mean of 20 images. mately 60% irrespective of the image selected. After the Whereas images of Homo (i.e., humans) obtained the 2-s presentation the six images reappeared. Any image highest scores every time, those of Hylobatid, which touched by the subject was highlighted, and touching the contained the closest species to the subject, obtained same image as during the previous presentation resulted in much lower scores. Moreover, the difference between no special feedback. The next trial started after a 1 s inter- them increased with the age of the subject.