Developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus) possible signals in visual communication.код для вставкиСкачать
American Journal of Primatology 65:353–376 (2005) RESEARCH ARTICLE Developmental Changes in the Facial Morphology of the Borneo Orangutan (Pongo pygmaeus): Possible Signals in Visual Communication NOKO KUZE1n, TITOL PETER MALIM2, AND SHIRO KOHSHIMA1 1 Department of Biological Sciences, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Tokyo, Japan 2 Sabah Wildlife Department, Sabah, Malaysia Orangutans display remarkable developmental changes and sexual differences in facial morphology, such as the flanges or cheek-pads that develop only on the face of dominant adult males. These changes suggest that facial morphology is an important factor in visual communication. However, developmental changes in facial morphology have not been examined in detail. We studied developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus) by observing 79 individuals of various ages living in the Sepilok Orangutan Rehabilitation Centre (SORC) in Malaysia and in Japanese zoos. We also analyzed photographs of one captive male that were taken over a period of more than 16 years. There were clear morphological changes that occurred with growth, and we identified previously unreported sexual and developmental differences in facial morphology. Light-colored skin around the eyes and mouth is most prominent in animals younger than 3 years, and rapidly decreases in area through the age of ~7 years. At the same time, the scattered, erect hairs on the head (infant hair) become thick, dense hairs lying on the head (adult hair) in both sexes. The results suggest that these features are infant signals, and that adult signals may include darkened face color, adult hair, whiskers, and a beard, which begin to develop after the age of B7 years in both sexes. In females, the eyelids remain white even after 10 years, and turn black at around the age of 20; in males, the eyelids turn black before the age of 10. The whiskers and beards of adults are thicker in males than in females, and are fully developed before the age of 10 in males, while they begin to develop in females only after B20 years. White eyelids and undeveloped whiskers and beards may be visual signals that are indicative of young adult females. Our results Contract grant sponsor: Shikata Memorial Trust for Nature Conservation; Contract grant sponsor: Tokyo Zoo Conservation Fund; Contract grant sponsor: Sumitomo Foundation. n Correspondence to: Noko Kuze, Department of Biological Sciences, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 2-12-1-W3-43 Ookayama Meguro-Ku, Tokyo 1528551, Japan. E-mail: firstname.lastname@example.org, email@example.com Received 5 December 2003; revised 20 August 2004; revision accepted 27 November 2004 DOI 10.1002/ajp.20121 Published online in Wiley InterScience (www.interscience.wiley.com). r 2005 Wiley-Liss, Inc. 354 / Kuze et al. also show that the facial morphology of the unflanged male is similar to that of the adult female, although it has also been pointed out that unflanged males resemble younger individuals. Am. J. Primatol. r 2005 Wiley-Liss, Inc. 65:353–376, 2005. Key words: Borneo orangutan; Pongo pygmaeus; facial morphology; infant signal; visual communication; developmental change INTRODUCTION Orangutans are the only great apes that live in Asia, and their characteristics differ greatly from those of other great apes. Among these distinctive characteristics are their highly solitary social system and almost completely arboreal lifestyle in tropical rainforests. Remarkable sex-specific differences and developmental changes in morphology have also been noted [Uchida, 1996]. The flanges (or cheek-pads) that develop on the face of dominant adult males are the most well-known example of developmental changes in orangutan morphology [Mackinnon, 1974; Rijksen, 1978; Rodman & Mitani, 1987]. The development of flanges has been reported to be arrested by the presence of other dominant males, even though flanges usually develop as a secondary sexual characteristic in mature males [Galdikas, 1985a, b; Maggioncalda et al., 1999; Schürmann & van Hooff, 1986; Utamia et al., 2002]. Unflanged males are reportedly able to avoid attack by dominant flanged males, but are completely capable of reproduction [Kingsley, 1982; Maggioncalda et al., 1999, 2000; Utamia et al., 2002]. Thus, flanges on the male face probably function as a visual signal to display dominance in social interactions. Flange development in male orangutans is not the only developmental or sexual change that occurs in the morphology of this species. Morphological changes in such things as the color of the face skin and body hair have also been reported in immature individuals and females [Mackinnon, 1974, 1975; Rijksen, 1978; Schultz, 1941]. It may be that these morphological changes also function as visual signals in orangutan social interactions. However, there have been no detailed or quantitative studies of developmental changes in orangutan facial morphology. In this study, we aimed to clarify and quantify the developmental changes in the facial morphology of Borneo orangutans by analyzing facial images collected at the Sepilok Orangutan Rehabilitation Centre (SORC) in Malaysia and in Japanese zoos. In addition, we examined photographs of a captive male that were taken over a period of more than 16 years. Our results revealed clear developmental changes in facial morphology, as well as previously unreported sexual and developmental differences. We discuss the potential relationship between these morphological changes and the life history of this species, and the possible functions of these face morphologies in visual communication. We examined the facial morphology of only the Borneo orangutan (Pongo pygmaeus) in this study, because various morphological differences (e.g., in face shape, beard, flange size, and the density and length of body hair) have been reported between the Borneo orangutan and Sumatra orangutan (Pongo abelii) [Courtenay et al., 1988; Mackinnon, 1975]. Changes in Orangutan Facial Morphology / 355 MATERIALS AND METHODS Study Animals We observed a total of 79 Borneo orangutans at SORC in Sabah, Malaysia, and in seven Japanese zoos (Tama Zoological Park, Yokohama Zoological Gardens, Chiba Zoological Park, Tennouji Zoo, Oji Zoo, Kyoto City Zoo, and Ueno Zoo). Demographic data for the observed animals are shown in Tables I–III. At SORC, we studied 58 Borneo orangutans (24 males and 34 females) in June 2000. Their estimated ages at the time of observation ranged from 3 months TABLE I. Age and Sex Distribution of Sampled Orangutans North Borneo (Sabah) Age Borneo Island (unknown region) Male Female Male Female Total 15 5 4 19 9 4 1 1 34 1 1 1 4 2 9 1 1 3 7 12 35 16 10 8 10 79 0–3 years 4–7 years 8–10 years 11–20 years 21–years Total 24 All individuals from SORC were originally from northern Borneo. All zoo animals were identified as Borneo orangutans by chromosomal examination. TABLE IIa. Demographic Data of Male Sampled Animals From SORC ID Age (year) Date of arrival at SORC Development of flange 0 1 2 2 2 2 2 2 3 3 3 3 3 3 3 4 6 6 6 7 8 9 9 10 21-Apr-2000 14-Aug-1999 10-Jun-1999 25-Apr-1999 20-Sep-1998 8-Apr-1998 26-Oct-1997 1-Feb-1999 3-Apr-1998 3-Mar-1998 19-Jul-1996 12-Apr-1998 28-Nov-1997 9-Oct-1997 2-Aug-1997 5-Apr-1998 4-May-1995 18-Dec-1994 25-Aug-1994 26-Aug-1993 30-Mar-1992 15-Dec-1990 18-Apr-1991 27-Nov-1990 None None None None None None None None None None None None None None None None None None None None None None None None n PP624 PP610n PP605 PP602 PP593n PP569n PP538n PP600 PP566n PP552n PP483 PP572n PP543 PP537 PP532n PP567n PP437n PP412 PP393n PP352n PP304 PP272 PP279n PP255n n Used in image analysis. 356 / Kuze et al. TABLE IIb. Demographic Data of Female Sampled Animals From SORC ID Age (year) Date of arrival at SORC Number of births 0 0 0 1 1 1 1 1 1 1 2 2 2 2 2 2 3 3 3 4 4 6 6 6 6 6 7 7 8 8 8 10 16 22 15-Jun-2000 24-May-2000 22-Aug-1999 27-Nov-1999 24-Nov-1999 17-Nov-1999 24-Oct-1999 24-Aug-1999 6-Jul-1999 24-Nov-1998 27-Nov-1999 27-Nov-1999 14-Sep-1998 24-Dec-1997 13-Feb-1998 8-Apr-1998 27-Oct-1997 4-Jun-1998 13-Mar-1998 19-Nov-1997 13-Apr-1996 18-Oct-1996 13-Apr-1996 30-Apr-1995 17-Nov-1994 25-Aug-1994 18-Nov-1994 28-May-1994 2-Apr-1996 25-Sep-1993 27-Nov-1992 11-Nov-1992 1-Oct-1986 8-Aug-1980 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 over 2 1 n PP627 PP625n PP614n PP618n PP617n PP616n PP615n PP611n PP606n PP598n PP621n PP619 PP592n PP544 PP554n PP568n PP539n PP581n PP559n PP542 PP474 PP498n PP475n PP435n PP405n PP392 PP406n PP384n PP473 PP358 PP332n PP330 PP193 PP103 n Used in image analysis. to 22 years (Table II). All of these animals originated from Sabah in northern Borneo, and almost all came from oil palm plantations (SORC database, unpublished). SORC was established in 1964 by the Sabah state government for the rehabilitation of orangutans that had been injured or had lost their mothers or habitats. SORC has received more than 600 orangutans, some of which have been released into the Kabili-Sepilok Forest Reserve. Several scientific studies of orangutans have been carried out at SORC [Kilbourn et al., 2003; Kuze et al., 2002; Rogers & Kaplan, 1996]. At this facility, very young orangutans (0–3 years old) are usually kept in cages, but others (43 years old) can range freely in the protected forest areas adjacent to SORC. They are fed twice daily at feeding platforms in the forest. We studied 21 Borneo orangutans (nine males and 12 females) in seven Japanese zoos during the period between June 1999 and September 2000. Their Changes in Orangutan Facial Morphology / 357 TABLE IIIa. Demographic Data of Male Sampled Animals From Japanese Zoos International studbook no. Age (year) Date of birth Development of flange Zoo 0 6 8 11 13 15 20 30 33 8-Jun-2000 12-Mar-1993 13-Feb-1991 9-Feb-1988 14-Nov-1986 25-Apr-1985 31-Aug-1980 1969 1965 None None None None Flanged Arrested Flanged Flanged Flanged Tama Zoological Park Yokohama Zoological Garden Yokohama Zoological Garden Chiba Zoological Park Tennouji Zoo Tama Zoological Park Kyoto City Zoo Tama Zoological Park Tennouji Zoo IS2954n IS2607 IS2426n IS2206 IS2080 IS2017n IS1788 IS1123n IS0919 n Used in image analysis TABLE IIIb. Demographic Data of Female Sampled Animals From Japanese Zoos International studbook no. Age (year) Date of birth Number of births Zoo 6 9 12 13 16 22 27 29 31 34 42 47 5-Sep-1992 27-Apr-1990 27-Apr-1986 14-Feb-1986 10-Aug-1983 6-Apr-1978 26-Feb-1973 1970 18-Jun-1968 6-May-1965 1956 1952 0 0 0 0 0 1 3 1 3 1 4 4 Tama Zoological Park Chiba Zoological Park Tennouji Zoo Oji Zoo Tama Zoological Park Kyoto City Zoo Tama Zoological Park Tennouji Zoo Tama Zoological Park Tama Zoological Park Tama Zoological Park Uenon Zoo IS2514 IS2378 IS2221 IS2074n IS1629n IS1643 IS1288 IS1327 IS0955 IS0726n IS0319 IS0221 n Used in image analysis. estimated ages at the time of observation ranged from 3 months to 48 years (Table III). All of the zoo animals were identified by chromosomal examination as Borneo orangutans [Hashikawa, 2001] (an inversion in the second chromosome pair is a diagnostic subspecies marker of the orangutan) [Ryder & Chemnick, 1993]. We also analyzed photographs of a male orangutan that had been kept by a Japanese family for more than 16 years, from 1969 to 1986. The orangutan, named Hitoshi, was estimated to be about 6 months old when he was given to the family by a sailor, and was about 17 years old when he died of illness on 22 October 1986. Hitoshi is thought to have come from northern Borneo. At that time (1960s–1970s), it was common for Japanese sailors to visit Borneo, especially northern Borneo, because of the flourishing timber trade. In addition, Hitoshi’s morphology was apparently similar to that of other Borneo orangutans (i.e., flanges curved outward from the face, a large throat pouch, and a less noticeable beard) [Jones, 1969]. This orangutan lived indoors in the family house until the age of B7, when he was moved to a garden enclosure. The family took more than 3,000 photographs of Hitoshi, mostly between 1970 and 1986, and selected images were used in our analysis. 358 / Kuze et al. Age Estimation Almost all of the orangutans arrived at SORC as infants. When orangutans are brought to SORC, veterinarians estimate their age by measuring their deciduous dentition, weight, and behavior [e.g., Fooden & Izor, 1983; Kaplan & Rogers, 1994]. We estimated the age of each individual at the time of our study based on its estimated age when it arrived at SORC. Since 16 of the 21 orangutans studied in the zoos were born in captivity, their absolute ages were known. The other five individuals were brought to the zoos as infants from the wild, at which time their ages were estimated by veterinarians according to body size, state of teeth, and behavioral development [e.g., Fooden & Izor, 1983]. We confirmed these original estimates by checking zoo records and photographs of these individuals. We calculated their ages at the time of our study by adding the period in captivity to their estimated ages at arrival. All five of these wild-origin orangutans had been kept in zoos for more than 20 years, and were fully mature adults at the time of this study. Hitoshi was estimated to have been B6 months old when he arrived in Japan, based on records of his deciduous dentition (none present) and weight (4.5 kg) [e.g., Fooden & Izor, 1983]. Analysis of Facial Morphology by Direct Observation For each animal, one observer scored eight morphological features: color of the skin around the eyes, color of the eyelids, color of the skin around the mouth, type of head hair, whisker density, beard density, size of flange (cheek-pad), and color of body hair (Fig. 1a). Skin color was ranked on a scale of 1–4 (1=very light, 2=light, 3=dark, and 4=very dark). Flange size was ranked on a scale of 0–2 (0=none, 1=small, and 2=large). Head hair was categorized as one of two types: infant hair (scattered, upstanding hair) or adult hair (dense, thicker hair lying down on the head). Body hair color was recorded with the use of the graduated color chart JIS Z 8102:2001 (published by the Japanese Standards Association). Lightness of body hair was ranked on a scale of 1–5 (1=orange (Munsell scale 5YR, 6.5, 13), 2=cinnamon (10R, 5.5, 6), 3=maroon (2YR, 3.5, 4), 4=chocolate (10R, 2.5, 2.5), and 5=rust (9R, 3.5, 8.5)). This ranking is comparable to that used by Mackinnon . Whisker and beard densities were ranked on a scale of 0–4 (0=none, 2=very sparse, 3=sparse, and 4=dense). Most zoo animals were observed at outdoor playgrounds under natural sunlight from a distance of 3–5 m. However, two zoo animals (adolescent females IS2221 and IS 2074; Table III) were observed in indoor exhibition rooms under artificial light from a distance of 0.5–2 m. Most SORC animals were observed at outdoor playgrounds under natural sunlight from a distance of o1 m. The exceptions were mother–infant pairs (PP193 and PP554, PP103, and PP483; Table II) that were observed at feeding platforms in the forest in sunlight from a distance of o10 m. Microscopic Observation of Head Hair The microscopic structure of infant hair (collected from infant female PP625) was compared with that of adult hair (from adult male IS1123) with the use of a Nikon OPTIPHOT-2 microscope. Changes in Orangutan Facial Morphology / 359 a Head Hair Skin around the Eye Whiskers Skin around the Mouth Beard b width of eye (=L) Original Measurement Fig. 1. a: Names of morphological features. b: Method of measurement of the light-colored area. Image Analyses For quantitative analyses of facial morphology, full face images were taken of five zoo animals and 43 SORC animals (Tables II and III) with a digital camera 360 / Kuze et al. (Ricoh RDC5500 and Olimpas Camedia 3030) and a film camera (Canon EOS1000 with Fujifilm Sensia II) under natural sunlight conditions. Images in which animals showed no obvious facial expression were processed and analyzed using software for graphical analyses (IP-Lab Spectrum TM). Two parameters were measured for each animal: the relative area of light-colored skin around the eyes (LE), and the relative area of light-colored skin around the mouth (LM). For each image, we measured the distance between the horizontal corners of the eyes (A; Fig. 1b), the area of light-colored skin around the eyes (E), and the area of lightcolored skin around the mouth (M). LE was calculated from (E)/A2, and LM was calculated from (M)/A2. The boundaries of (E) and (M) were visually determined and delineated by one person, and the areas were measured digitally by the software program. Long-Term Photographic Record of a Male From the extensive photographic collection, we selected full face images (four black and white photographs, and 26 color photographs) that showed no obvious expression, and analyzed them as previously described. Statistics We used the Mann-Whitney U-test to examine differences in morphological features between sexes and among age classes. RESULTS Light-Colored Areas of the Face There were obvious changes in the area and shade of the light-colored skin on the face in both sexes with growth. Animals aged 0–3 and 4–7 years had large areas of light-colored skin around the eyes and the mouth. These areas became darker and decreased in size as the animals grew. Coloration around the eyes. The color of the skin around the eyes darkened with age in both sexes (Fig. 2). There were significant differences in the color of this skin area between animals r10 years old and those Z11 years old (Po0.01) for both sexes. All animals aged 0–3 and 4–7 years had very light-colored skin around the eyes. In contrast, all males older than 10 years (six animals) and most females over 20 years old (seven of eight animals) had very dark or dark skin around the eyes. All males older than 12 years of age and all females older than 26 years had very dark skin around the eyes. As an animal aged, the light-colored area around the eyes tended to darken from the outer part to the inner part, near the eye. Figure 3 shows the developmental changes in the skin color of the eyelids. The eyelids also tended to be of very light coloration in males r10 years old (26 of 26 animals) and in females r20 years old (37 of 37 animals), and darkened with growth in both sexes. Eyelid color differed significantly between males younger than 10 years and males older than 11 years (Po0.01), and between females younger than 20 years and females older than 21 years (Po0.01). All males Z14 years old and all females Z31 years old had dark eyelids. For both sexes, darkening of the eyelids proceeded more slowly than did darkening of the skin around the eyes. This was particularly true of females: three of seven females Z21 years old still had light or Changes in Orangutan Facial Morphology / 361 a 20 ** Number 16 12 8 4 0 0-3 year b 4-7 year 8-10 year Male 11-20 year 21- year ** 20 Number 16 12 8 4 0 0-3 year 4-7 year very light 8-10 year Female light 11-20 year dark Fig. 2. Developmental changes in skin color around the eye. nn 21- year very dark Po0.01. very light eyelids, while the skin around their eyes was already dark or very dark. In contrast, no females Z21 years old with dark or very dark eyelids had light or very light skin around their eyes. All five 8- to 10-year-old males with dark or very dark skin around the eyes still had light or very light eyelids. In contrast, no 8- to 10-year-old animals with dark or very dark eyelids had light or very light skin around the eyes. Coloration around the mouth. The light-colored area of skin around the mouth was prominent in animals aged 0–3 years, and darkened with growth in both sexes (Fig. 4). All males Z7 362 / Kuze et al. a 18 ** 15 Number 12 9 6 3 0 0-3 year b 4-7 year 8-10 year Male 11-20 year 21- year ** 20 Number 16 12 8 4 0 0-3 year 4-7 year 8-10 year 11-20 year 21- year Female very light Fig. 3. Developmental changes in eyelid color. light nn dark very dark Po0.01. years old and all females Z9 years old had dark skin around the mouth. This skin area was light or very light in all animals aged 0–3 years, and dark or very dark in all animals Z8 years old, in both sexes (the difference between r7-year-old animals and Z8-year-old animals was significant at Po0.01). This skin area tended to darken earlier than did the skin around the eyes (Figs. 4 and 5; differences in 4- to 10-year-olds of both sexes were significant at Po0.05). Developmental changes in light-colored areas of the face. The relationship between the size of the light-colored area around the eyes (LE) and the estimated age of the animal is shown in Fig. 5. In both sexes, LE is Changes in Orangutan Facial Morphology / 363 a ** 18 15 Number 12 9 6 3 0 0-3 year b 4-7 year 8-10 year Male 11-20 year 21- year ** 20 Number 16 12 8 4 0 0-3 year 4-7 year very light 8-10 year Female light 11-20 year dark Fig. 4. Developmental changes in skin color around the mouth. 21- year very dark nn Po0.01. large until the age of 3 years, and it rapidly decreases over the subsequent 4 years of the animal’s life. LE is almost zero in males by the time they are 15 years old, while LE may remain obvious in females even after 20 years. The relationship between the size of the light-colored area around the mouth (LM) and the estimated age of the animal is shown in Fig. 6. Similar to the trend observed for LE, LM is large until the age of 3 years, and it rapidly decreases over the subsequent 4 years of the animal’s life, in both sexes. Individual variation in LM (SD=3.02) is larger than that of LE (SD=1.96). LM is reduced to almost zero in both sexes by the age of 15 years. 364 / Kuze et al. 10 N=45 8 LE 6 4 2 0 || 0 1 2 3 4 6 7 8 9 10 || 15 17 31 35 Age Fig. 5. Relationship between the size of the light-colored area around the eyes (LE) and the estimated age. Types of Head Hair Head hair type clearly changed with age in both sexes (Fig. 7). Differences (significant at Po0.01) were observed between animals of both sexes aged r7 years and Z8 years. All 0- to 3-year-old animals of both sexes (34 animals) had infant hair. Most females (nine of 10) and some males (two of five) aged 4–7 years had infant hair. In contrast, all males Z7 years old and all females Z9 years old had adult hair. Microscopic observations showed that the infant hair of PP625 had no remarkable hair pulp, while the adult hair of IS1123 had prominent dark hair pulp (55 mm in diameter). Adult hairs were much thicker (175 mm in diameter) than infant hairs (62.5 mm in diameter). Whiskers and Beard There were clear changes in whisker density with growth in both sexes (Fig. 8). Whisker density differed significantly between males of r10 years and males of Z11 years (Po0.01), and between females of r20 years and females of Z21 years (Po0.01). Most 0- to 3-year-old animals (16 of 19 females, 14 of 16 males) and 4to 7-year-old animals (nine of 10 females, three of five males) had no whiskers; Changes in Orangutan Facial Morphology / 365 12 N=45 10 LM 8 6 4 2 0 || 0 1 2 3 4 6 7 8 9 10 || 15 17 31 35 Age Fig. 6. Relationship between the size of the light-colored area around the mouth (LM) and the estimated age. most animals Z21 years old (seven of eight females, one of one male) had whiskers. In contrast, all males Z7 years old and all females Z21 years old had whiskers. Dense whiskers were observed only in males, and increases in whisker density with growth proceeded more slowly in females than in males (Fig. 8). No females aged 8–10 or 11–20 years had whiskers, though males aged 8–10 and 11– 20 years had sparse or dense whiskers. This represents a sexual difference in animals Z8 years of age (significant at Po0.05). Beard density also changed with growth in both sexes (Fig. 9). All males Z6 years old and all females Z21 years old had beards. Significant differences in beard density were observed between males r10 and Z11 years of age (Po0.01), and between females r20 and Z21 years of age (Po0.01). Dense beards were observed only on males, and increases in beard density with growth proceeded more slowly in females than in males (Fig. 9). No females r20 years of age had beards, while all males aged 11–20 years (four animals) had sparse or dense beards. This was a sexual difference in animals Z11 years in age (significant at Po0.05). A female aged 30 years still had only a little beard and sparse whiskers, although some infants and juveniles had whiskers and beards like downy hair. 366 / Kuze et al. a 20 ** Number 16 12 8 4 0 b 0-3 year 4-7 year 8-10 year Male 11-20 year 21- year ** 20 Number 16 12 8 4 0 0-3 year 4-7 year 8-10 year 11-20 year 21- year Female infant hair Fig. 7. Developmental changes in the type of head hair. adult hair nn Po0.01. There appear to be large individual differences in the degree of development of beards and whiskers. Whisker and beard development appeared to be unrelated to that of facial flanges. While all flanged males (four animals) had dense or sparse whiskers and beards, one unflanged male (14 years old) also had sparse whiskers and a dense beard. Size of Flanges (Cheek-Pads) in Males Flange size changed with growth in males (Fig. 10). Animals r7 years of age (22 animals) had no flanges, while all those Z21 years of age (two animals) had Changes in Orangutan Facial Morphology / 367 a 18 ** 15 Number 12 9 6 * * 8-10 year Male 11-20 year 3 0 b 0-3 year 4-7 year 21- year ** 20 16 Number 12 8 * 4 0 * 0-3 year 4-7 year no 8-10 year Female very sprase Fig. 8. Developmental changes in whisker density. animals 8–10 years old, 11–20 years old; nPo0.05. 11-20 year sprase nn 21- year dense Po0.01, significant sexual differences in fully matured flanges. Flange size differed significantly between animals of r10 years and those of Z21 years of age (Po0.05). All males Z11 years old observed in this study were usually kept alone in separate cages. Two males aged 11–20 years without flanges in the figure were IS2206 (11 years old) and IS2017 (15 years old). Flange development of IS2017 appeared to be arrested due to the presence of another adult male because he was living in a cage near that of another adult male (IS1123, 30 years old, no kinship with IS2017), where he could see, hear, and probably smell the other male. However, IS2080 (13 years old), who lived in a cage near that of his father (IS0910, 33 years old) had large flanges that started to develop from about 10 years of age. 368 / Kuze et al. a 18 ** 15 Number 12 9 6 * 3 0 0-3 year 4-7 year 8-10 year Male 11-20 year 21- year ** b 20 Number 16 12 8 4 0 * 0-3 year 4-7 year no 8-10 year Female very sprase 11-20 year sprase 21- year dense Fig. 9. Developmental changes in beard density. nnPo0.01, significant sexual differences in animals 11–20 years old; nPo0.05. Color of Body Hair Body hair darkened with growth in both sexes. Most animals r7 years old had light-colored body hair (orange or cinnamon) in both sexes, and most animals Z21 years old had darker body hair (maroon or rust). Body hair appeared to change in color at around the age of 7 years (differences between younger and older animals were significant at Po0.01 for males and Po0.05 for females), although there was large individual variation. For example, infant PP566 (a 3year-old male) had rust-colored hair, while adult PP103 (a 22-year-old female) still had cinnamon-colored hair. Changes in Orangutan Facial Morphology / 369 18 15 Number 12 9 6 3 0 0-3 year 4-7 year 8-10 year 11-20 year 21- year Male no little large Fig. 10. Developmental changes in flange size (males only). Long-Term Observation of a Male Changes in facial morphology observed in the captive male orangutan Hitoshi over a 16-year period (from the age of 6 months to 17 years) are shown in Fig. 11. Until the age of 3 years, light-colored areas of skin around the eyes and the mouth were noticeable and large, and the head hair was typical infant hair. Subsequently, the light areas around the eyes started to darken peripherally. The light skin around the mouth became darker more quickly and randomly, forming many dark speckles. At 6 years of age, the skin around the mouth was completely dark, and by 7 years the skin around the eyes had turned dark. At the age of 8 years, both the body hair and eyelids had darkened, the whiskers and beard had become longer and denser, and facial flanges began to develop. The head hair was entirely adult hair by the age of 9 years. Adult facial morphology apparently was achieved by the age of 10 years, since there were no subsequent changes. These observations support the pattern of developmental change in facial morphology suggested by other results of this study. In particular, these results corroborate the timing of developmental events: the light skin around the eyes and mouth changes between the ages of 3 and 7 years, and the darkening of eyelids and body hair, the development of whiskers, beard, and flanges, and the changes in head hair type that occur in males between the ages of 7 and 10 years. In the case of Hitoshi, infant hair decreased at the age of about 6 years, and dense long adult hair grew in over the subsequent 1.5 years. In the intervening 6 months his head hair was very short and sparse. By the age of 9 years all head hair had completely changed to adult hair. A similar sequence of events was observed by the authors between January 2000 and May 2003 in a female orangutan (IS2514; Table III) kept at Tama Zoo. At the age of about 8 years, her infant hair decreased and her head hair was then sparse and very short for 370 / Kuze et al. Life History First ejaculation Sexual maturation* Weaning Color around the eyes dark transition light Color around the eyelids light transition light transition dark Color around the mouth dark Head hair infant-hair transition adult-hair none transition developed none transition developed none transition developed Beard Whiskers Flange Color of body hair 0.5 Face Type light Infant-face 3 7 Juvenile-face 10 Adolescent-face dark 17 Flanged-male-face n Fig. 11. Morphological changes of Hitoshi (a male orangutan). Sexual maturation was estimated by the amount, viscosity, and color of the sperm, and the morphology and color of the penis. about 6 months. Over the subsequent year, her head hair became denser and longer. DISCUSSION Developmental Changes in Facial Morphology The typical developmental changes in facial morphology during growth in Borneo orangutans, as clarified in this study, are summarized in Fig. 12. Facial morphology and its development were similar in both sexes until the age of about 10 years. The facial morphology of animals r10 years old can be categorized into three types: infant face, juvenile face, and adolescent face. The infant face (0–3 years of age in both sexes; Fig. 13a) has large, lightcolored areas of skin around the eyes and the mouth, light-colored eyelids, and infant hair, but no whiskers, beards, or flange. The juvenile face (4–7 years of age in both sexes; Fig. 13b) is characterized by smaller, darker areas of skin (especially around the mouth), light-colored eyelids, and infant hair, and no whiskers, beards, or flanges. The adolescent face (8–10 years of age in both sexes; Fig. 13c and d) has still smaller, darker areas of light-colored skin around the eyes, light-colored eyelids, darkened skin around the mouth, infant hair changing to adult hair, developing whiskers and beard, and perhaps, in some males, developing flanges. There are clear sexual differences in facial morphology and development in animals Z10 years old. These animals can be assigned to two sex-specific categories on the basis of facial morphology: young or adult female face, and flanged or unflanged male face. The young female face (11–20 years of age, Fig. 13e) has darkened skin around the eyes and mouth, light-colored eyelids, adult hair, sparse whiskers, and beards at an early stage of development. The adult female face (420 years old; Fig. 13f) has darkened skin around the eyes and mouth, darkening or darkened Changes in Orangutan Facial Morphology / 371 a Weaning Typical Life History Independence End of body-growth Color around the eyes dark transition light Color around the eyelids transition light dark Color around the mouth light dark transition Head hair infant-hair transition adult-hair transition developed transition developed Beard none Whiskers none Flange 3 0 Face Type b Infantface Typical Life History 7 none Juvenileface Weaning 10 15 20 Adolescentface Independence 40 arrested or developed Flanged / Unflanged-male-face End of body-growth Color around the eyes dark transition light Color around the eyelids transition light dark Color around the mouth transition light dark Head hair adult-hair infant-hair transition Beard none transition developed none transition developed Whiskers Flange 0 Face Type Infantface 3 7 10 Juvenile- Adolescentface face 20 Young-female-face none 40 Adult-female-face Fig. 12. Summary of typical developmental changes in facial morphology: (a) male and (b) female. eyelids, adult hair, and sparse whiskers and beards. The eyelids continue to darken in some individuals until the age of B30 years. The flanged male face (410 years old; Fig. 13g) has darkened skin around the eyes and mouth, darkened eyelids, adult hair, well-developed beard and whiskers, and well-developed facial flanges. The unflanged male face (410 years; Fig. 13h) has darkened skin around the eyes and mouth, darkened eyelids, adult hair, and well-developed whiskers and beard, but lacks flanges. There are similarities between the unflanged male face and the adult female face (Fig. 13f and h). Although it is known that orangutan infants have large, light-colored areas of skin around the eyes and mouth [Mackinnon, 1974; Schultz, 1941], no precise research into the developmental changes of this skin had been published prior to this study. Similarly, although Jones  mentioned that ‘‘the hair of young individuals is thin,’’ no previous studies investigated the development of head and body hair, whiskers, or beards in orangutans. Galdikas  briefly stated that the face of adolescent females was whiter than that of fully adult females, but our results demonstrate for the first time that young females have a characteristic facial morphology. 372 / Kuze et al. Fig. 13. Developmental changes in facial morphology. a: Infant face. b: Juvenile face. c: Adolescent face (male). d: Adolescent face (female). e: Young female face. f: Adult female face. g: Flanged male face. h: Unflanged male face. Life History and Face Type Orangutan life history is usually classified into four stages: infant stage (0–3 years old), juvenile stage (4–7 years old), adolescent stage (8–15 years old in males and 8–10 years old in females), and adult stage (415 years old in males and 410 years old in females). This classification is based on studies of behavior and physical development in captive and wild orangutans [Fooden & Izor, 1983; Kaplan & Rogers, 1994; Mackinnon, 1974]. Orangutans are ablactated at B3 years old and become independent from their mothers at B7 years old [Mackinnon, 1974], corresponding to the infant and juvenile life history stages. Young individuals that are independent of their mother but still continue physical growth are called adolescents (8–15 years old in males and 8–10 years old in females) [Fooden & Izor, 1983; Galdikas, 1995; Mackinnon, 1974]. Females are reported to be capable of reproduction from the age of B10 years, while males are not mature until the age of B15 years in the wild [Delgado & van Schaik, 2000; Maggioncalda et al., 2000]. It has been suggested that the reproductive strategies of flanged males differ from those of unflanged males [Rodman & Mitani, 1987]. Flanged males make long calls and wait for females, while unflanged males conspicuously search for females without calling [Galdikas, 1985b; Utamia et al., 2002]. Although flanges normally develop in males 410 years old, flange development is often arrested by Changes in Orangutan Facial Morphology / 373 the presence of other flanged males [Galdikas, 1985a, b; Maggioncalda et al., 1999, 2000; Schürmann & van Hooff, 1986]. Utamia et al.  reported that flange development was arrested in a wild adult male Sumatran orangutan for more than 20 years. Our results suggest the following relationships between facial types and life stages (Figs. 12 and 13): the infant face is characteristic of the infant stage, the juvenile face is characteristic of the juvenile stage, the adolescent face is characteristic of the adolescent stage in females and young adolescent stage in males, the young female face is characteristic of young adult females (11–20 years old), the adult female face is characteristic of old adult females (4 20 years old), the unflanged male face is characteristic of young males in the late stage of adolescence (11–15 years old) and subdominant adult males, and the flanged male face is characteristic of dominant adult males. Possible Function As an Age Signal Morphological features that change during development or in sex-specific ways, and have no obvious physiological or ecological explanation may be useful as visual communication signals. It is difficult to imagine a physiological or ecological reason for the relative prominence of light-colored skin areas on the face of infants, or the observed sex-specific differences in the speed of skin darkening. The light-colored facial skin and the infant hair of infants and juveniles may be infant signals, because these visually conspicuous features are most prominent during the lactation period (0–3 years) and rapidly decrease in prominence as the animals become independent of their mothers (B7 years old). All three infants that we studied in relationship to their mothers (IS2954, PP483, and PP544: 0, 3, and 2 years old, respectively; Tables II and III) still suckled, and only one such juvenile (female IS2514, 6 years old) was no longer dependent on her mother for food. Our observations of developmental changes in orangutan infant and juvenile characteristics are similar to those reported for infant signals in chimpanzees and gorillas. Suckling chimpanzees and gorillas have conspicuous white tail tufts that rapidly decline with growth. It has been reported that adults are very tolerant of individuals with this feature [Napier & Napier, 1985]. In some primate species, the coats of infants are more conspicuous than those of adults [Hrdy, 1976; Treves, 1997]. It has been suggested that these conspicuous natal coats evolved to promote allocare by adult females [Ross & Regan, 2000]. With regard to orangutans, Mackinnon  reported that the body hair color of infants darkened with growth, though this was a qualitative rather than quantitative observation. Our study indicates that body hair color tends to be lighter in infants than adults; however, there were large individual variations in the developmental pattern in this respect. The head hair type and face coloration are more reliable indicators of life history stage. Kaplan and Rogers  noted that juvenile orangutans look at the faces of other individuals more frequently than do individuals of any other life stage. It is possible that their conspicuous infant/juvenile signals (light-colored facial skin and infant hair) make other animals tolerant of their gaze. Infant and juvenile orangutans appear to interact with their mothers almost exclusively and have few chances to use infant signals. However, it has been reported that mothers and infants are often visited and followed by juveniles and adolescents, and they sometimes move together for a few hours or days [Galdikas, 374 / Kuze et al. 1985c]. In addition, unflanged males have been observed approaching mother– child pairs to copulate with the mother [Galdikas, 1985b]. Under such circumstances, infant signals may be useful for infants and juveniles to obtain tolerance and/or protection from other individuals. Conspicuous characteristics of juvenile face, adolescent face, and young female face (such as light-colored skin around the eyes and/or eyelids) may also function in such social interactions by helping young animals to approach and contact other individuals. It has also been reported that social interactions are very intense among young orangutan females [Galdikas, 1995]. Young females often form a group of two to three individuals and follow mother–child pairs. Again, in this scenario, an obvious visual signal of age and sex could conceivably be beneficial. In Sumatran orangutans, the eyelids have been reported to remain light-colored even in adulthood, and this may reflect their apparently more intense social lives [Delgado & van Schaik, 2000; Kaplan & Rogers, 2002]. Differences in eyelid coloration between orangutans from Sumatra and those from Borneo may be an adaptation to different levels of social interaction. However, the sociability of young female Borneo orangutans is reported to decline after they commence reproduction [Galdikas, 1995], but the coloration of the eyelids of young females does not appear to be related to their reproductive experience. A young adult female (16 years old) that had already reproduced was observed to still have a young female face with white eyelids, the same as those of three other young females with no reproductive experience. Our results also reveal that the facial morphology of unflanged males is similar to that of adult females. It has been reported that flanged males are tolerant of unflanged males when they encounter each other in large fruiting fig trees [Utami et al., 1997]. It is possible that unflanged males, which lack this conspicuous secondary sex characteristic of male orangutans, are tolerated by flanged males, and can more easily approach females because their faces are similar to those of adult females. Maggioncalda and Sapolsky  pointed out that unflanged males look similar to younger individuals and are more inconspicuous. Our results show that unflanged males look like adult females rather than infants, juveniles, or adolescents. Geographical Differences in Face Morphology Many morphological and genetic differences between Borneo (Pongo pygmaeus) and Sumatran (Pongo abelii) orangutans have been reported [Groves, 1971; Janczewski et al., 1990; Jones, 1969; Mackinnon, 1974; Mallinson, 1978; Ryder & Chemnick, 1993; van Bemmel, 1968; Xu & Arnason, 1996]. Furthermore, it has been reported that there are substantial differences among populations in Borneo with regard to cranial and dental morphology [Courtenay et al., 1988; Groves et al., 1992; Uchida, 1998] and genetics [Kanthaswamy & Smith, 2002]. Given that we still have no data on interpopulation differences in the external morphology of Borneo orangutans, it is possible that the results of this study were biased by local characteristics of the animals from northern Borneo (see Materials and Methods, and Table I). CONCLUSIONS We closely examined developmental changes in the facial morphology of Borneo orangutans, and discussed the possible utility of these features in visual communication. Light-colored skin around the eyes and mouth, and scattered, Changes in Orangutan Facial Morphology / 375 standing head hair (infant hair) are likely to be infant signals. In contrast, darkened face coloration, adult hair, whiskers, and beards are probably adult signals. Light-colored eyelids and less-developed whiskers and beards may be visual signals indicating young adult females. Our results also show that the facial morphology of unflanged males is similar to that of adult females, rather than to younger individuals. ACKNOWLEDGMENTS We express our sincere thanks to the staffs of SORC in Sabah and the Sabah Wildlife Department for their kind support of our research. We also thank the staff members of Tama Zoological Park (particularly Kunio Inoue) for their kind support of our research. We are grateful to Tennouji Zoo, Yokohama Zoological Gardens, Chiba Zoological Park, Oji Zoo, Kyoto City Zoo, and Ueno Zoo in Japan for permitting our research. We gratefully acknowledge Sadako Yamakawa for providing the photos and information about Hitoshi for our analyses. Thanks are offered to Tomoko Kanamori and Jun Uetake for their help with the microscopic observations of head hair. We thank Hisahi Matubayashi and Fuyuki Nomura for their support in Sabah. We especially thank Satoru Kuze for his encouragement, advice, and criticism. We also thank the three anonymous referees who made valuable comments on this manuscript. REFERENCES Courtenay J, Groves CP, Andrews P. 1988. Inter- or intra-island variation? 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