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Developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus) possible signals in visual communication.

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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: nyasuno@bio.titech.ac.jp, nouko@mva.biglobe.ne.jp
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 [1974]. 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 [1969] 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 [1995] 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. [2002] 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 [1975] 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 [2002] 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 [2002] 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.
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