Primates (2010) 51:63–67 DOI 10.1007/s10329-009-0175-9

ORIGINAL ARTICLE

Visual preference in a human-reared agile ( 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 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 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 Sensory reinforcement 1988; Oyakawa et al. 2007). There are some developmental Visual preference 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 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 (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. Two-way trial interval. ANOVA, using age (3) and category (Homo vs. In the experiment with stimulus set 1, six images were Hylobatid) revealed a significant effect of category presented in a trial. One session consisted of ten trials, and (F(1,38) = 130, P \ 0.001) but no significant age effect one or two sessions were run each day, for a total of eight (F(2,76) = 0.20, p = 0.82). The interaction between age sessions. Each image was presented in two sessions, each and category was statistically significant (F(2,76) = 14.5, of which was run four times, for a total of eight sessions. p \ 0.001). The combination of images presented changed on every Figure 3 shows the gibbon subject’s mean scores for the trial. In the experiment with stimulus set 2, five images different gibbon species at three different ages. For easy were presented. One session consisted of nine trials. The comparison, the chimpanzees’ mean scores are plotted on subjects received one or two sessions a day, and a total of the right hand side of the graph. Tsuyoshi did not touch the 12 sessions. Each image was presented in three sessions, images of H. agilis more frequently than those of other each run four times, for a total of 12 sessions. species. He touched H. agilis images relatively frequently in the first test compared to the second and third tests, by Data analysis which time the score for H. agilis had decreased markedly. In contrast, H. lar was touched increasingly frequently In addition to the total number of times chosen, each image across the tests. A two-way ANOVA using age (3) and was scored according to the order of choice in a trial. The category (H.agilis vs. H.lar) revealed a significant effect of

first choice was given two points and the second choice category (F(1,28) = 5.27, p = 0.04) but no age effect was given one point. The image the subjects chose first in a (F(2,56) = 1.74, p = 0.18). The interaction between age trial was deemed the preferred image. The score was and category was statistically significant (F(2,56) = 12.0, summed for each image. p \ 0.001).

123 66 Primates (2010) 51:63–67

6 chimpanzees with that of the gibbon’s score at different ages. The chi-square test revealed a significant difference 5 in the distribution of each category’s score between chimpanzees and the gibbon on the first test (df = 8, v2 = 26.3, p \ 0.001), but no significant difference during 4 subsequent tests (8 years 0 month: v2 = 7.76, p = 0.46; 9 years 0 month: v2 = 10.2, p = 0.25). 3

2 Discussion MEAN SCORE The results of the free-choice presentation of two stimulus 1 sets failed to show any visual preference for photographs of conspecifics in an agile gibbon. The human-reared gibbon 0 7:02 8:00 9:08 chose human photographs more frequently than other pri- AGE mate categories. This preference grew stronger with age. These results suggest that early and extensive postnatal Pan Homo social experience with humans affected the subject’s Gorilla Pongo preference. Previous studies have shown that human-reared Hylobatid Cercopithecid chimpanzees also show a bias for photographs of humans (Tanaka 2003, 2007). Fig. 2 Mean scores for images in each category of stimulus set 1 at Our gibbon subject had been reared by humans for each age of the gibbon subject. Age is indicated as (years: months) one year after his birth, but subsequently lived with his brother and had extensive visual contact with his parents 4.5 and white-handed gibbons. Nevertheless, he preferentially selected images of humans over those of other primates. 4 The results suggest that, in gibbons, as in chimpanzees, 3.5 H. agilis social experience in infancy affects an individual’s visual H. lar preference. 3 H. moloch Stimulus set 1 was the same as that used by Tanaka 2.5 H. pileatus (2007). In this set, 11 species of gibbons were grouped into B. hoolock one category, Hylobatids. Therefore, we prepared photo- 2 N. concolor graphs of nine species of gibbons from four genera of the

MEAN SCORE N. gabriellae 1.5 N. leucogenys Hylobatidae (i.e., stimulus set 2). Additionally, chimpan- 1 S. syndactylus zees were tested for comparison. Because there should be no features predisposing chimpanzees to prefer a particular 0.5 species of gibbon, the chimpanzees’ data would reflect the 0 relative perceptual salience of the images used. The results 6:05 8:00 9:00 Chimp suggest that the agile gibbon did not prefer images of AGE conspecifics over other gibbon species. The gibbon subject Fig. 3 Mean scores for images of each gibbon species in stimulus set showed a different pattern of choices in the first test, 2 at each age of the gibbon subject. Age is indicated as (years: touching H. agilis images more than H. lar, which was one months). Mean scores for chimpanzees are plotted on the right hand of the species preferred by the chimpanzees. However, the side gibbon subject touched H. lar images more frequently when the test was repeated. Because the distributions of the The distribution of Tsuyoshi’s scores at 8 years 0 month scores were not different between the chimpanzees and or 9 years 0 month was similar to the mean score of Tsuyoshi at 8 years or 9 years of age, Tsuyoshi’s visual chimpanzees, in contrast to Tsuyoshi’s first test (at 6 years preference may had shifted to one based on perceptual 5 months). We calculated the mean score of the chim- features, which the chimpanzees probably also used. panzees for each image category, and summed the score of Studies have found commonalities in physical devel- each image for each category in the chimpanzees and the opment between gibbons and macaques, and in some gibbon at different ages. We used a chi-square test to aspects of behavioral and cognitive development between compare the distribution of total scores for each category in gibbons and great (Uchikoshi and Matsuzawa 2002, 123 Primates (2010) 51:63–67 67

2007). The present study further suggests similitudes in the Fujita K (1993a) Role of some physical characteristics in species development of visual preferences between gibbons and recognition by pigtail monkeys. Primates 34:133–140 Fujita K (1993b) Development of visual preference for closely related chimpanzees. species by infant and juvenile macaques with restricted social All species of gibbons produce species-specific vocal- experience. Primates 34:141–150 izations that are often referred to as ‘‘songs.’’ It is likely Fujita K, Watanabe K (1995) Visual preference for closely related that vocal communication plays an important role in species by Sulawesi macaques. Am J Primatol 37:253–261 Fujita K, Watanabe K, Widarto TH, Suryobroto B (1997) Discrim- mate-choice in gibbons. However, our present study also ination of macaques: the case of Sulawesi species. Primates suggests a role for visual features. Indeed, studies have 38:233–245 confirmed the presence of mixed groups of H. agilis and Gittins SP (1978) Hark! The beautiful song of the gibbon. New Sci H. lar, and of hybrids in the north-western part of Peninsular 80:832–834 Horton KE, Caldwell CA (2006) Visual co-orientation and expecta- Malaysia (Brockelman and Gittins 1984; Gittins 1978), tions about attentional orientation in pileated gibbons (Hylobates while H. agilis 9 H. muelleri hybrids can also be found in pileatus). Behav Proc 72:65–73 Kalimantan (Brockelman and Gittins 1984; Marshall and Hyatt CW (1998) Responses of gibbons (Hylobates lar) to their Sugardjito 1986; Mather 1992). These findings give further mirror images. Am J Primatol 45:307–311 Inoue Y, Inoue E, Itakura S (2004) Use of experimenter-given support to the view that gibbon visual preferences may be directional cues by a young white-handed gibbon (Hylobates flexible and influenced by several factors. lar). Jpn Psych Res 46:262–267 Since the present study was based on data from a single Marshall JT, Sugardjito J (1986) Gibbon systematics. In: Swindler subject, it is clear that more studies are urgently needed to DR, Erwin J (eds) Comparative primate biology, vol 1: systematics, evolution, and anatomy. Alan R. Liss, New York, validate our results and to advance our understanding of the pp 137–185 perceptual and cognitive abilities of gibbons. The present Mather R (1992) A field study of hybrid gibbons in central study shows that, as with macaques and chimpanzees, free- Kalimantan, Indonesia (Ph.D. thesis). Department of Veterinary choice tasks using a touch screen can be an effective Anatomy, Cambridge University, Cambridge Matsuzawa T (2003) The Ai project: historical and ecological method for such investigations in gibbons. contexts. Anim Cogn 6:199–211 Matsuzawa T, Tomonaga M, Tanaka M (eds) (2006) Cognitive Acknowledgments The first author has now moved to the Wildlife development in chimpanzees. Springer, Tokyo Research Center, Kyoto University. This study was financially sup- Mitani JC (1988) Male gibbon (Hylobates agilis) singing behavior: ported by MEXT Grants-in-Aid for Scientific Research (Nos. natural history, song variations and function. Ethology 79:177– 20002001, 19530653), the Global COE Programs A06 and D07 to 194 Kyoto University, and a research fellowship to M. Uchikoshi from Myowa-Yamakoshi M, Tomonaga M (2001) Development of face JSPS (No. 171163). We thank the members of the Language and recognition in an infant gibbon (Hylobates agilis). Infant Behav Cognition Section of KUPRI for technical assistance and encour- Develop 24:215–227 agement. We also thank the staff members of the Center for Human Oyakawa C, Koda H, Sugiura H (2007) Acoustic features contributing Evolution Modeling Research, KUPRI, for taking care of the subjects’ to the individuality of wild agile gibbon (Hylobates agilis agilis) health. songs. Am J Primatol 69:1–14 Roos C, Geissmann T (2001) Molecular phylogeny of the major Hylobatid divisions. Mol Phylogen Evol 19:486–494 References Tanaka M (2003) Visual preference by chimpanzees (Pan troglo- dytes) for photos of primates measured by a free choice-order task: implication for influence of social experience. Primates Beck BB (1967) A study of problem solving by gibbons. Behavior 44:157–165 28:95–108 Tanaka M (2007) Development of the visual preference of chimpan- Brockelman WY, Gittins SP (1984) Natural hybridization in the zees (Pan troglodytes) for photographs of primates: effect of Hylobates lar species group: implications for speciation in social experience. Primates 48:303–309 gibbons. In: Preuschoft H, Chivers DJ, Brockelman WY, Creel N Uchikoshi M, Matsuzawa T (2002) Behavioral development of agile (eds) The lesser apes. Evolutionary and behavioral biology. gibbons: the first four years after birth (in Japanese with English Edinburgh University Press, Edinburgh, pp 498–532 summary). Jpn Psych Rev 45:483–499 Chivers DJ (1976) Communication within and between family groups Uchikoshi M, Matsuzawa T (2007) Tooth eruption in two agile Symphalangus syndactylus of ( ). Behaviour 57:116–135 gibbons (Hylobates agilis). Gibbon J 3:66–73 Cunningham CL, Anderson JR, Mootnick AR (2006) Object manip- Ujhelyi M, Merker B, Buk P, Geissmann T (2000) Observations on Bunopithe- ulation to obtain a food reward in hoolock gibbons, the behavior of gibbons (Hylobates leucogenys, H. gabriellae, cus hoolock. Anim Behav 71:621–629 and H. lar) in the presence of mirrors. J Comp Psych 114:253– Fujita K (1987) Species recognition by five macaque monkeys. 262 Primates 28:353–366

123