P.ZHANG: Alopecia in Japanese macaques

P. ZHANG: Alopecia in Japanese macaques

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UNCORRECTED PROOF

A non-invasive study of alopecia in Japanese macaques Macaca fuscata

Peng ZHANG1, 2, 3

1 School of Sociology and Anthropology, Sun Yat-sen University, GuangZhou, 510275, China

2 Primate Research Institute, Kyoto University, Japan

3 Japan Society for the Promotion of Science (JSPS)

Abstract This article provides information on the phenomenon of alopecia in Japanese macaques, Macaca

fuscata, in various environments and proposes a 3-step scoring system for a quantitative assessment of hair loss.

Results suggest that alopecia is commonly observed in Japanese macaques, with 20.5% of individuals showing

head alopecia and 4.7% showing back alopecia across eight study groups. Alopecia was more commonly observed

in adult females (30.8% individuals showing head alopecia and 15.3% showing back alopecia) than in other

age-sex classes. Seasonal variation of back alopecia was noted, in particular, individuals with patchy back hair

were more frequently observed in winter than in summer. Seasonal variation was not observed in head hair. The

distribution of alopecia was also different among study groups. The wild population generally had better hair

condition than provisioned populations and captive populations. The present study used a non-invasive alopecia

scoring system which can be a useful, rapid and non-invasive tool to monitor animal health and well-being at a

population level [Current Zoology 57 (1): – , 2011].

Key words Alopecia, Coat condition, Hair loss, Macaca fuscata

Alopecia (hair loss) is a common phenomenon in captive and free-ranging animals (Wolfensohn and Lloyd,

2003). Different factors contribute to excessive alopecia. Stress can play an important role in the onset of alopecia

in non-human mammals (Roloff et al., 1998; Sawyer et al., 1999; Arck et al., 2003) and humans (Gupta et al.,

1997; York et al., 1998). In primates, environmental disturbance is most likely to be responsible for observed

alopecia (Reinhardt et al., 1986). Isbell (1995) recorded seasonal hair loss in Amboseli vervet monkeys

Received May 19; 2010; accepted Aug 15, 2010.

 E-mail: zhangp99@mail.sysu.edu.cn

© 2011 Current Zoology

P. ZHANG: Alopecia in Japanese macaques

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Cercopithecus aethiops, which could be due to social stress, to feeding on Acacia tortilis seeds, or to a

combination of these. Findings from small animals and human dermatology indicate that hair growth is a cyclic

phenomenon rather than a continuous process (Rivier and Vale, 1985; Arck et al., 2003). An index of coat

condition therefore does not identify the cause of stress, and the actual time of the stress that damages hair

follicles may be as much as 2-4 months before the observed effects, e.g. the delayed effect of pregnancy on

alopecia in rhesus macaques (Macaca mulatta, Beisner and Isbell, 2009).

Another reason for alopecia in captive non-human primates might by hair pulling during overgrooming

(Beisner and Isbell, 2008). Although grooming is considered a hygienic behavior in cleaning parasites and dirty

skin (Martin and Bateson, 1993), overgrooming is defined when animals spend excessive time cleaning one

another by combing through the hair and extracting foreign objects (Reinhardt et al., 1986). In crowded conditions

female macaques are known to increase all social interactions from aggression to overgrooming (e.g. females

overgrooming their infants, PRI, 2002). Overgrooming sometimes can be very severe, resulting in extensive areas

of baldness and skin damage.

Other factors may be also related to hair loss and range from naturally occurring processes (e.g. seasonality, age,

Steinmetz et al., 2006) to various biologic dysfuctions, including vitamin and mineral imbalances (Rushton, 2002),

endocrine disorders (Diani et al., 1995), immunologic disease (Wiedemeyer et al., 2004), and genetic mutations

(Ahmad et al., 1999). A variety of skin conditions are associated with inflammation and pruritis and may also

result in hair loss, including bacterial and fungal infections (Otberg et al., 2007), parasitic infection (Martin and

Elewski, 2003), and atopic dermatitis (Ovadia et al., 2005). Some of these factors are quite rare in non-human

primates (such as mutation of hairless genes) and others are more common (Novak and Meyer, 2009). Hair loss

itself has not been the focus of much research in monkeys. However, a need to promote psychological well-being

in captive primates along with a recent focus by regulators on alopecia as an area of concern means that

understanding hair loss in these animals is now essential.

Alopecia scoring has been widely applied for captive primate welfare and has been based on present-absence

scores. Isbell (1995) used one-zero criteria for Amboseli vervet monkeys: hair loss was either present or absent as

a seasonal percentage of the population. The scoring of hair condition is suitable as a rapid non-invasive health

assessment. Recently, Honess et al. (2005) developed a five-step scoring system for back hair conditions in rhesus

macaques and used it as an index of social stress and stress related hair-picking. Berg et al. (2009) scored back and

tail hair conditions in free-ranging populations of ring-tailed lemurs Lemur catta in six steps.

Japanese macaques Macaca fuscata are amongst the most widely studied primates and raised in many research

and breeding facilities (Kawai and Ohsawa, 1983; PRI, 2002). Healthy macaques have shiny, moderately dense

hair and a thick coat in winter. Good external hair-cover may reflect resistance to parasites and good health

condition (Hamilton and Zuk, 1982). Partial or complete alopecia is commonly observed in both provisioned and

captive populations (Inagaki and Hamada, 1985). Hair loss could be a serious health problem in Japanese

macaques because hair functions as an important anatomical and physiological barrier between animals and their

environment (Wolfensohn and Lloyd, 2003). Serious alopecia might also affect thermoregulation for Japanese

macaques as this species inhabits the coldest habitats of any non-human primate. To date, here have been few

attempts to investigate and describe alopecia in this species.

P. ZHANG: Alopecia in Japanese macaques

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Here, we provide information on the phenomenon of alopecia in Japanese macaques living in the wild,

free-ranging provisioned populations and captive populations. The aims of this study were: (1) to describe

precisely the incidence of alopecia in Japanese macaques across different populations and age-sex classes; (2) to

analyze seasonal and age-sex variations of alopecia; and (3) propose a 3-step scoring system for a quantitative

assessment of hair loss.

1 Materials and Methods

1.1 Study sites and groups

The incidence of alopecia was investigated by visual inspection of eight groups living in various environments

(Table 1): a wild group at the Yakushima Island (Nina-2 group), five provisioned groups (JB group at Jigokudani

Valley, TB and TC groups at Mount Takasakiyama, SA and SB groups at Shodoshima Island) and two captive

groups (Wakasa-3 group and Takahama group at Kyoto University).

The wild Nina-2 group lives in Yakushima Island, which is in the southwest part of Japan (30oN, 131oE) and

has an area of 503 km2. More detailed information on Yakushima monkey populations is described by Yamagiwa

and Hill (1998). The monkeys were well habituated to humans and could be observed from 3–4 m away. The

investigation is based on individual identification of all 29 animals from October to November in 2006 (Table 1).

The provisioned JB group is located at the Jigokudani Monkey Park (36 º 43′N, 138 º 27′E) in Shiga Heights,

one of the coldest habitats for Japanese macaques. The group size was 178 individuals during the time of this

study (Table 1). This group visits the park every day. Food was provided to the group at 09:00, 12:00 and 15:00 in

the form of 20 kg of wheat grains and a small amount of soy beans. Forty kilograms of sliced apples were added

each day at 17:00 in summer. Food was spread widely in the park. Tourists are not allowed to feed monkeys, and

have little influence on their behavior. Monkeys also consume natural food and spend their nights in the mountain

outside the park. Monkeys were well habituated to humans and could be observed as close as 1–2 m away. Scan

sampling was conducted to investigate the hair condition of individual monkeys (Altmann, 1974), from one end of

the park to the other in order to avoid duplicate observation. The group was scanned six times during winter

(January-February) and six times during summer (August-September) in 2006. Coat condition of individuals,

age-sex class and temperature were recorded. Names of some identified individuals were also noted.

TB and TC groups are distributed at the Takasakiyama Monkey Park located on the east coast of Kyushu (33 º

25’N, 131 º 53’E). Two study groups visited the park every day and each spent half of each day around the park.

These groups have been well studied, and their social structures are characterized by rigid hierarchies (Sugiyama

and Ohsawa, 1982). The group sizes were 432 and 743 during this study (Table 1). The park provides sweet

potatoes to the TC group twice per day at 9:00 and 13:00, and to the TB group once at 14:00. Monkeys in the park

also receive 3 kg of wheat grains every 30 min from 9:00 to 17:00. The amount of food was 0.11 kg/individual for

the TB group and 0.10 kg/individual for the TC group. Tourists are not allowed to feed monkeys, and have little

influence on their behavior. Monkeys also consume natural foods and spend their nights in mountains outside the

park. They were well habituated to humans and could be observed as close as 1–2 m. Hair condition was

investigated six times during winter (January-February) and six times during summer (June-July) in 2005 using

the same scan sampling method as mentioned above.

P. ZHANG: Alopecia in Japanese macaques

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SA and SB groups are distributed at the Choshikei Monkey Park (N34o 30′, E134o 19′) located on

Shodoshima Island, the second largest island (153.5 km2) in the Setonaikai Sea. Population sizes of SA group and

SB group were around 450 and 330 respectively (Table 1). Two study groups visited the feeding site in Choshikei

Monkey Park every day and spent most of the day around the park. Wheat grain was supplied three times a day (in

total 25 kg for each group), and similar amounts of sweet potato and vegetables were also offered in the afternoon

each day. Tourists are allowed to feed monkeys, and increase social interactions among monkeys, e.g. aggressions,

proximity (Zhang and Watanabe, 2007). Monkeys also consumed food from the natural vegetation around the park.

They were well habituated to humans and could be observed from 1–2 m away. Hair condition was investigated

six times using scan sampling during winter (November-December) and six times during summer

(July–September) in 2004.

Takahama and Wakasa-3 groups are captive populations at the Primate Research Institute of Kyoto University,

Japan. Takahama group (48 individuals during this study) occupies a 960 m2 outdoor enclosure with metal

climbing structures. Wakasa-3 group (25 individuals) is housed in a 496 m2 outdoor enclosure with an 8 m high

climbing structure located in the middle of the enclosure. The structure consists of two stories with platforms and

a smaller-roofed shelter on top. The enclosure also contains a 15 m artificial stream, small pond and a patch of

grass. Both groups are provisioned daily by staff with commercial monkey chow (AS, Oriental Yeast Co. Ltd.,

Tokyo, Japan). Provisioning occurred once a day between 9:00 and 11:00. During the study period subjects were

provisioned with monkey chow, sweet potato, wheat, and occasionally cucumber and bamboo shoots. Food was

evenly dispersed in the enclosure. Water was available ad libitum. The two groups were individually identified,

and hair condition was investigated once in winter (January) and once in summer (July) in 2007, and observed

from 1–2 m away.

1.2 Development of a scoring system

Fig. 1 shows the variation of alopecia on the back and head of Japanese macaques. The score system was

developed by visual investigation of more than 2000 animals and covers a complete range of hair conditions from

perfectly fluffy to almost no-hair based on a 3-step scale for head and back hair. Head hair scores (HS) range from

HS 1 (good) to HS 3 (bald) with 1.0 point steps. Similarly, back hair scores (BS) range from BS 1 (good) to BS 3

(bald). Animals with patchy back hair (BS 2) and a bald head (HS 3) were observed, as well as good-back-hair

animals (BS 1) with a bald head (HS 3). Hair on the ventral abdomen is not included because it can be difficult to

see and seems to experience an abrupt change from furred to bald, rather than a gradual worsening. Categories of

hair scores on head (HS) and back (BS) are described as follows:

Score HS 1 (good head hair): animal shows complete, fluffy, and generally even hair cover, although one or two

small holes are allowed. These small holes are included here because they probably result from tufts pulled out

during fights rather than from a decreased health condition and therefore should be distinguished from score HS 2.

Score HS 2 (patchy head hair): animals show bare patches with good or rough surrounding hair. The patches are

larger than coin-size and thus clearly visible. It covers up to 50% of the head. Animals with large patched shaggy,

P. ZHANG: Alopecia in Japanese macaques

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slightly thinned out hair covering less than half of the head part are also classified in this category.

Score HS 3 (bald head): the animal is considered bald if half or more of the head is bare.

Score BS 1 (good back hair): in line with good head hair, animals in this category have good coat condition

with little visible coat damage.

Score BS 2 (patchy back hair): the back has several small patches of hair loss or large patches that cover less

than 50% of the back. Some animals show serious coat damage that is less than half the normal depth on large

patches of the back.

Score BS 3 (bald back): the back is counted as bald if bare skin is more apparent than haired skin.

Monkeys were classified into five age-sex classes: adult male (estimated to be more than 7 years old), adult

female (estimated to be more than 6 years old), subadult male (estimated to be 4 to 7 years old), subadult female

and juvenile (estimated to be 1 to 6 years old), and infant (estimated to be less than 1 year old). Infants less than 6

months old were excluded from sampling because their coat patterns are unstable. Age-sex classes of monkeys

were identified by their body size, facial characters such as color and wrinkles, development of external genitals

(for males) and nipple size (for females) (Zhang and Watanabe, 2007).

Distance from the target animal can bias judgment. An animal with a patchy coat may seem good from a

distance, so scores were taken principally when monkeys were within 5 m of an observer. To avoid inter-observer

bias, the author investigated and scored coat conditions of all study groups reported in this article. The research

protocol conforms to the national and institutional guidelines for the care and management of primates established

by the Primate Research Institute, Kyoto University, Japan (PRI, 2002).

1.3 mStatistical analysis

Individual identification is difficult in provisioned groups with extraordinarily large group sizes. Data from

these groups are not a completely random sample of the population since some individuals remain un-sampled and

others double-sampled in one scan. To avoid the bias of re-sampling, I made several scans in a given day and

chose to analyze only one scan from each day, e.g. the scan that had at least 90% of group members. Data may not

be independent between seasons, since most individuals are re-sampled in winter and summer. To resolve this bias,

data in summer and winter only were analyzed respectively and those of winter coat were used for inter-group

comparisons. Comparisons were done using a Mann-Whitney U test for two categories, and a Kruskal–Wallis test

for multiple categories using SPSS v16. A Wilcoxon rank test was used to analyze seasonal variation in hair

condition and a Pearson correlation test was used to look for a relationship between hair condition on the back and

head. All statistical tests were two-tailed.

2 Results

2.1 Incidence of alopecia in Japanese macaques in different populations and age-sex classes

The distribution of head alopecia was dramatically different among study groups (Kruskal-Wallis χ2=34.99, n=7,

P<0.001) (Fig. 2). Head hair in the wild Nina-2 group was the healthiest as only one adult male showed head coat

damage. Provisioned groups exhibited more serious head coat damage than the wild group, with head-alopecia

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being as frequently observed as 4.7±0.5% in JB group, 9.5±0.8% in TB group, 8.8±0.6% in TC group, 17.9±1.1%

in SA group and 20.5±1.7% in SB group. The two captive groups showed the most serious head coat damage:

alopecic individuals accounted for 12.5% in Takahama group and 40.9% in Wakasa-3 group.

Back alopecia varied among between groups (χ2=34.7, n=7, P <0.001) (Fig. 3). Back hair in the wild Nina-2

group was healthiest, with only one adult male showing mild back coat damage. Provisioned groups had more

serious back alopecia than the wild Nina-2 group, with back alopecia being as frequently observed as 4.1±0.5% in

TB group, 4.2±0.4% in TC group, 6.5±0.6% in SA group, 7.1±0.8% in TC group. Another provisioned JB group,

however, resembled the wild Nina-2 group, with no individuals showing back alopecia. In Takahama and

Wakasa-3 captive groups, individuals with back alopecia were frequently observed and accounted for 8.3% and

27.3% of group members respectively. Many individuals showed a combination of good back hair (BS 1) and

patchy head hair (HS 2) or that of patchy back hair (BS 2) and bald head hair (HS 3) in study groups. Back

alopecia was less frequently observed than head alopecia across all study groups (patchy: Z=-2.5, P <0.05; bald:

Z=-2.0, P <0.05).

2.2 Age and sex

Distribution of alopecic individuals was different among age-sex classes (Fig. 4, Friedman test, head hair:

χ2=37.3, df=4, P <0.001; back hair: χ2=26.1, df=4, P <0.001). For head alopecia, subadult males showed the best

hair condition, with 1.5±1% head-alopecia individuals, followed by juveniles with 6.9±4.4% head-alopecia

individuals (n=72, z=-2.8, P <0.01). Bald-headed sub-adult males or juveniles were not observed, but adult

females (7.2±8.4%), adult males (2.3±4.6%) and infants (3.8±5.5%) were bald-headed. Adult males and infants

had more serious head alopecia than subadult males and juveniles, with 11.3±4.9% (n=72, z=-5.1, P<0.001) and

13.6±10.5% head-alopecic individuals respectively (n=72, z=-7.3, P <0.001). Adult females showed the most

serious head alopecia (30.8±14.1%, n=180, z=-7.2, P <0.001).

With respect to back alopecia, few alopecic juveniles (0.5±1.5%), and some subadult males (6.5±17.6%, n=84,

z=-4.9, P <0.001) were found. Adult males, infants and adult females had the worst hair condition as 11.3±8.1%

(n=144, z=-7.3, P <0.001), 13.6±6.8 (n=84, z=-5.3, P <0.001) and 15.3±15.4% (n=144, z=-4.9, P <0.001)

individuals show back coat damage respectively. Bald back individuals were observed in adult females

(7.6±0.9%), infants (2.4±3.7%) and adult males (2.3±4.6%) but were not observed in other age-sex classes.

2.3 Variation of coat condition between summer and winter

The condition of back hair varied significantly between summer and winter. In particular, animals with patchy

back hair were more frequently observed in winter than in summer (Fig. 5b, Wilcoxon Test, patchy: z=-2.52, P

<0.05; Bald z=-0.41, P >0.05). Seasonal variation was not observed in head alopecia (Fig. 5a, Patchy: z=-0.84, P

>0.05, Bald: z=-0.11, P >0.05). In some individuals, regrowth of head hair was not observed across seasons, and

serious alopecia conditions continued over years.

3 Discussion

The present study suggests that alopecia is rarely found in wild Japanese macaques, but frequently observed in

provisioned and captive animals. This condition has also been observed in several other provisioned populations,

Arashiyama group (western Japan), Mino group (western Japan), Koshima group (southern Japan), and many zoo

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populations (Zhang P, unpublished data). Compared to wild populations, primates in provisioned and captive

groups suffer from crowding, frequent competition and conflict, abnormal group size and composition

(Wolfensohn and Lloyd, 2003; Zhang, 2008). Psychological stress could be a primary causal factor in triggering

hair loss by telogen effluvium, or be a secondary factor in exacerbating hair loss due to a preexisting disorder,

such as endocrine imbalance, toxin exposure, nutrient deficiency, or autoimmune disease (Hadshiew et al., 2004).

Steinmetz et al. (2006) noted that rhesus macaques in indoor groups have poorer hair condition than out-door

groups. Hair condition may change with changing housing environments and husbandry in captive animals. For

example, captive rhesus macaques with grass vegetation (a foraging substrate) have less alopecia than groups

without any vegetation (Beisner and Isbell, 2008; 2009). My results suggest alopecia is more common in the

captive Wakasa-3 group than captive Takahama group, probably because the former has less living space and there

was lack of a shelter colony for subordinates to avoid aggressions from dominants.

Macaques in the Choshike Monkey Park and the Takasakiyama Monkey Park suffered higher rates of alopecia

than those at the Jigokudani Monkey Park. Over 700 animals reside within Chosike, 1100 in Takasakiyama and

less than 200 at Jigokudani. Animals in these groups spent a large amount of time within 200 m of the

provisioning site during the day. Available space or disturbances in environmental factors are like to be

responsible for the observed alopecia, and populations that demonstrate frequent alopecia are assumed to be under

particular stress. Nevertheless, populations at Shodoshima Island suffered alopecia more seriously than those of

other habitats despite similar provisioning and group composition (cf. Takasakiyama populations). It is known that

Shodoshima populations have more tolerant social organization than other populations (Zhang and Watanabe,

2007). For example, they display highly tolerant inter-individual interaction, frequent social grooming, high

tolerance between dominants and subordinates and the habitual formation of clusters of more than 50 individuals,

traits not found in other populations off the island (Kawai et al., 1967; Yamada, 1971; Kawamura et al., 1974).

The nature of Shodoshima populations may further increase the possibility of inflammatory hair loss within

groups caused by bacterial infections, parasitic infections or allergic processes (Goto, personal communication).

This study suggests that hair condition is worse in females, adult males and infants, and best in young

individuals. This pattern was also found in ring-tailed lemurs (Jolly, 2009b). Frequent alopecia in adult females

may reflect either costs of pregnancy or an unexpected cost for matrilineal interactions (raising young, social

interactions and dominance), or both (Steinmetz et al., 2006). In Takahama and Wakasa-3 groups back alopecia

occurred in 30% and 100% of adult females with a dependent infant, respectively. Many adult females visibly lose

hair during early lactation, and may develop bare racing stripes where infant hands and feet cling to their sides, as

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well as holes on the back and thighs.

The results I present here are different from findings in rhesus macaques (Steimatz et al., 2006) that alopecia

significantly increases with age and is absent in infants. The present data suggest that infants have worse hair

condition than sub-adult males and juveniles have the best hair conditions, except for the Nina-2 group, where

only one individual (a male) had alopecia. Alopecia in captive primates most commonly results from the

pathological intensification of grooming behavior such as hair plucking followed by ingestion (rhesus monkeys,

Reinhardt et al., 1986; long-tailed macaques, M. fascicularis, Slively et al., 2002). Reinhardt et al. (1986)

examined hair-pulling and eating captive macaques and found that it is unlikely to result from nutritional or

toxicological factors, but possibly related to psychological stress. In provisioned groups at Shodoshima and

Takasakiyama adult females spent 19.1% and 14% of their active time in social grooming, and frequently focused

on their infants (Zhang and Watanabe, 2007). Frequent alopecia in infants may result from overgrooming and

hair-pulling by other individuals. The influence of self-grooming or hair-pulling was ignored here, because the

head and back are seldom reached in self-grooming. In socially housed macaques, alopecia is almost exclusively

due to allogrooming in more than 97% of instances, rather than self-grooming (Reinhardt et al., 1986).

The distribution of head alopecia and back alopecia is different to a certain degree in Japanese macaques. First,

head alopecia is more frequently observed than back alopecia in study groups. Between 4.7% to 20.5% of animals

exhibited head alopecia, and 2% to 7.1% were found to have back alopecia. Many individuals with bald heads

may show no or only mild damage to their back hair. Secondly the condition of head hair showed few seasonal

changes, while back hair condition was influenced by season. Crockett et al. (2009) also suggested a variation of

alopecia condition in body parts of laboratory primates. Factors influencing the difference between head alopecia

and back alopecia in Japanese macaques are as yet unknown. In ring-tail lemurs, foraging leucaena Leucaena

leucocepahala may cause alopecia, especially in tails (Jolly, 2009a). Influence of feeding ecology in Japanese

macaques should be investigated further.

The reliability in using an alopecia scoring system for primates has been tested by several researchers

(Steinmetz et al., 2006; Honess et al., 2005; Berg et al. 2009). Their findings have suggested alopecia scores of the

same group are in agreement by different observers and that reliability increased if the study groups were

individually identified. Berg et al. (2009) however noted that to distinguish between ‘good’ and ‘pointy’ could be

confused when using a 6-step scoring systems for ring-tailed lemurs, especially from a distance. Honess et al.

(2005) developed a five-step scoring system using photographs of sedated captive rhesus macaques, and found

there are small differences between scoring from photographs and direct observation. In particular the boundaries

in some categories are blurred under different body postures and lighting conditions. Based on my previous

experience, I developed this three-step scale for Japanese macaques. This system has the following benefits: it was

developed based on an assessment of a large population across various living environments; it scores hair

condition on the back and head whereas previous measures relied on the back alone; the three-step scale is

practical for free-ranging and wild populations; it considers variation across seasons and age-sex classes. It may

be possible to use an modified scoring system for other species. The chief adjustment for other species might be in

the location of hair loss. The current scale refers to head and back, while ring-tail lemurs often lose hair on back

and tail (Berg et al, 2009), vervet monkeys instead often loss hair on the abdomen, knees, elbows and inner thighs

(Isbell, 1995).

P. ZHANG: Alopecia in Japanese macaques

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In general, this study suggests that alopecia is rare in wild populations, but frequently observed in captive and

provisioned populations of Japanese macaques. Social stress under high population densities and disturbed

environments may be chief factors responsible for alopecia in captive and provisioned populations. Environmental

enrichment and quality of available living space should be improved for captive animals. Hair and skin condition

should be routinely assessed as part of regular health exams. Quantifying hair loss and evaluating the skin may be

useful to determine whether the condition is improving or deteriorating from one health exam to the next. In

free-ranging populations, chronic social stress could be reduced by improved management of the population, such

as spreading food across a wide area and discouraging tourists to feed monkeys. While this study cannot

differentiate between various potential causes of stress or the time of suffering, the repeated and sequential use of

the scoring system presented here will enable researchers and animal care staff to carry out simple, quantifiable

and non-invasive assessments of well-being.

Acknowledgments The study was supported by the Hundred Scholar Program (090013) of Sun Yat-sen

University in China, Fund-In-Aid of JSPS (P09103). I am grateful to the Choshikei Monkey Park, the

Takasakiyama Monkey Park, Jigokudani Monkey Park and Kyoto University for granting permission to carry out

this research. I thank Mr Sam Hodgson from Tigress Productions for revising English. I thank all members of the

Social Ecology Department and Center for Human Evolution Modeling Research at the Primate Research Institute,

Kyoto University who gave helpful comments on the manuscript.

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