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The Japanese Macaque

Brian Pochinski

UW-Milwaukee

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The Japanese macaque, Macaca fuscata, is an old world monkey that was first studied in

1948 in Japan. The genus Macaca arose in Africa approximately seven to eight million years ago

and migrated out into Eurasia between five and six million years ago. Rhesus macaques, Macaca

mulatta, are ancestral to Japanese macaques. Today, Japanese macaques are only found in Japan.

They range from the Shimokita peninsula in the North to the Yakushima Islands in the south

approximately spanning from 31 to 40 degrees North latitude. The large range in latitudes means

that Japanese macaques inhabit a wide range of climates and vegetation (Nakagawa, Nakamichi,

and Sugiura, 2010).

Despite the high degree of variability, only Macaca fuscata yakui is considered to be

morphologically distinct enough to be considered its own separate sub-species. M. fuscata yakui

lives on Yakushima Island. They became separated from other populations of Japanese

macaques 178,000 years ago. Population genetics has revealed that they went through a

bottleneck due to their low level of genetic variability. In general, Japanese macaques have less

genetic variability that other species of macaque (Nakagawa, Nakamichi, and Sugiura, 2010).

M. fuscata yakui tend to have a small body, a long tail, long fur, and dark colored fur.

This does not fit the type morphology of Japanese macaques in southern Japan. Typically

northern populations of Japanese macaques have longer fur, shorter tails, and small bodies than

Japanese macaques in southern Japan. In general, Japanese macaque populations fit Bergman’s

rule so that the body size is correlated with the lowest monthly average temperature. The

untypical morphology seen in M. fuscata yakui may be due to the bottleneck that occurred after

they became separated from other populations of Japanese macaques (Nakagawa, Nakamichi,

and Sugiura, 2010).

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Japanese macaques eat a variety of different foods. They eat leaves, fruit, seeds, flowers

and insects (Nakagawa, Nakamichi, and Sugiura, 2010) although they may resort to fallback

foods such as bark when temperatures are cold (Richard, Goldstein, and Dewar, 1989). The

proportion of food items can vary depending on the region. Japanese macaques in Kinkazan rely

on seeds for their primary source of food. Japanese macaques found in coniferous forests of

Yakushima rely on mature leaves for their primary food source whereas Japanese macaques in

the lowlands of Yakushima primarily rely on fruits. Interestingly, these two locations are only

seven kilometers apart from each other. Even in a relatively small spatial range, Japanese

macaques display a highly flexible diet (Nakagawa, Nakamichi, and Sugiura, 2010).

The flexibility in the Japanese macaque diet allows them to move in and utilize human

settlements and other modified environments for food resources. Japanese macaques will

typically ignore items not recognized as food items, but as human settlements encroach Japanese

macaque habitats, Japanese macaque are given increasing opportunities to learn about new food

sources provided by people. It was once thought that crop raiding by Japanese macaques had

ceased due to human intolerance and population pressure (Richard, Goldstein, and Dewar, 1989).

However, more recent studies have found that Japanese macaques in areas low in food resources

will resort to raiding crops and gardens near human settlements (Yamada and Muroyama 2010).

Given the opportunity to eat a food item, Japanese macaques will eat almost anything that is not

too hot or bitter. Their behavior flexibility displayed in a broadly ranging diet means that as

Japanese macaques have more exposure to human settlements and food resources, and thus more

learning experiences human food resources, they will likely rely on a wider range of human food

resources (Nakagawa, Nakamichi, and Sugiura, 2010).

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Perhaps the most intriguing learned foraging behavior in Japanese macaques is sweet

potato washing. Sweet potato washing was first observed in Japanese macaques in 1953. By

1962 almost all Japanese macaques in that group born after 1950 were washing sweet potatoes.

Interestingly, all the Japanese macaques that were born after 1950 that were not washing sweet

potatoes were the offspring of adults that did not wash sweet potatoes. This suggests that social

learning pertaining to foraging behavior is heavily modulated by parent-offspring relationships

and observations (Kawai 1965).

Social bonds and kinship is crucial in troops of Japanese macaques. Sleeping patterns are

heavily influenced by kinship and social affiliation. When it is not too cold, Japanese macaques

tend to huddle together and sleep with close kin and social affiliates. However, if temperatures

drop too low, Japanese macaques will huddle with other troop members that they do not have

strong social bonds with. Colder winter temperatures lead to an increase in group size at sleeping

sites and an increase in mutual physical contact. The increased group size and closer physical

contact serves the physiological function of warmth for the huddling group. The huddling of

Japanese macaques that do not normally have strong social bonds shows behavioral flexibility

(Takahashi, 1997). Sleeping patterns can also be influence by the seasonal availability of food

sources, strong winds, and the availability of shelter from sources such as rock formations and

fallen trees (Tsuji, 2011).

Sweet potato washing has at least three variations in the method used remove the dirt.

The primary method relies of holding the sweet potato with one hand while using the other hand

to manually brush the sand off. Sweet potato washing occurs in both salt and fresh water but

Japanese macaques tend to prefer eating sweet potatoes washed in salt water. Subordinates have

a greater tendency to use fresh water which may be due to food competition with higher ranking

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individuals. Japanese macaques will also use fresh water if the sweet potatoes are found much

closer to fresh water than salt water (Kawai 1965).

Since the initial reports of sweet potato washing, Japanese macaques have also been

observed to wash grass roots (Nakamichi, Kato, Kojima, and Itoigawa, 1996). Grass washing has

only been observed in higher ranking females. Only seven percent of the group members were

observed washing grass. Some of the females observed washing grass would gather several

grassroots before going to wash them. The ability to plan ahead in order to make foraging more

efficient may suggest a high level of cognition. Japanese macaques have also been observed

grabbing numerous pieces of wheat at a single time and throwing them in to water in order to

wash them (Kawai 1965).

The developmental stages in Japanese macaques are categorized as infantile, juvenile,

adolescent, sub-adult, adult, and elderly. Japanese macaques exhibit seasonal breeding patterns.

Mating occurs in during the fall and winter which leads to infants being born from spring

through summer (Nakagawa, Nakamichi, and Sugiura, 2010). Multiparous mother will give birth

successive years but primiparous mothers do not give successive births (Hiraiwa 1981). It is not

uncommon for a female to have other group members in close proximity while the birthing

process is occurring. After the birth is complete, the mother may either focus all of its attention

on the newborn infant or she may solely focus on eating the placenta. Multiparous mother are

more likely to eat the placenta than primiparous mothers (Turner et al. 2010).

The infantile stage lasts for approximately the first year of life and is considered to be

over when the infant begins weaning. Parity is the best predictor of mother-infant relationships in

Japanese Macaques (Nakagawa, Nakamichi, and Sugiura, 2010). By the time the infant is one

month old, primiparous mothers are less likely to reject infants from suckling than multiparous

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mothers. Primiparous mothers are also less likely to force independence upon their infant prior to

seven months old (Tanaka 1989). All mothers however are likely to reject infant suckling by the

time the infant is seven months old. Primiparous mothers do not allow allo-mothering of their

infant but multiparous mothers do allow allo-mothering of their infants. The infant’s gender has

no apparent impact on mother-infant relationships and the mother’s rank only appears to have a

slight effect very early in infancy. It does appear that high ranking mothers put more restrictions

on their infant during the first month. The observed differences in mother-infant relationships

related to parity tend to disappear during the juvenile period (Hiraiwa 1981).

The juvenile period begins with weaning and ends with the beginning of reproductive

maturation. The juvenile period ends at around four and a half years of age for males and at

about three and a half years in females. Although the offspring no longer relies on the mother for

suckling, the juvenile and the mother still have a close and important relationship (Nakagawa,

Nakamichi, and Sugiura, 2010). Mothers are able recognize the vocalization of her own offspring

compared to vocalizations of other infants. Mothers are initially responsive to the coo

vocalization of all juvenile Japanese macaques but when an offspring does not belong to the

mother she quickly shifts her attention elsewhere (Pereira 1986).

Adolescence begins with reproductive maturity. Secondary sexual characteristics develop

such as the growth of teat and skin swelling and reddening. Females reach menarche and males

see a rapid growth in the testes. During adolescence males typically beginning foraging alone or

they forage with a separate all male group. Females give birth to their first offspring during

adolescence. Most females are five years old when they have their first infant but some females

give birth by four years of age (Nakagawa, Nakamichi, and Sugiura, 2010).

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The solitary foraging seen in males is thought to limit food competition with females and

adult males. Males of low and middle ranking females tend to be smaller at both three years of

age and six years of age than males of high ranking females. Males begin solitary foraging

around six years of age. The solitary foraging can occur until the male is fifteen years of age. By

the age of fifteen, the males of high ranking, middle ranking, and low ranking females do not

show any significance in body size (Mori and Watanabe 2003).

Adulthood is considered to be reached physical growth no longer occurs. Adulthood is

generally considered to occur at age seven but the exact age is uncertain due to the variability in

size of an adult throughout their life and because of the size variability seen between different

individuals (Nakagawa, Nakamichi, and Sugiura, 2010). Even in adulthood, Japanese macaques

have been observed engaging in social play. Social play in adults is observed more often in

males than in females and adults are more likely to play with immature group members than with

other adults in the group (Ciani, Dall’Ollio, Stanyon, and Palagi, 2012).

Female Japanese macaques typically begin to experience a decline in ovarian function

after the seventeen years of age but physical signs of aging in the musculoskeletal system occur

between the ages of ten and fifteen. The maximum lifespan of a female is thirty years of age and

males will typically live less than twenty-five years. Many females have a few years of post-

reproductive life. Estrous and mating may occur for a couple years of post-reproductive life but

they will gradually diminish and will eventually not occur at all (Nakagawa, Nakamichi, and

Sugiura, 2010).

Although it is uncertain what type of role in any post-reproductive females have in the

group, observations are beginning to determine if there are any benefits of having a post-

reproductive female in the group. The results of Pavelka, Fedigan, and Zohar (2002) suggest that

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post-reproductive grandmothers no not play a crucial role in their daughter’s reproductive

success but they do have an effect on young grandchildren. Post-reproductive grandmothers are

only significantly associated with a grandchild’s survival for its first year of life. Daughters with

a living mother regardless of her reproductive status are more likely to give birth one year earlier

than daughters without a living mother (Pavelka, Fedigan, and Zohar, 2002).

Japanese macaques are highly intelligent and cultural non-human primates. Sweet potato

washing is one well known cultural innovations observed in Japanese macaques. Another well-

known cultural innovation is hot spring bathing. Hot spring bathing is most common in high

ranking females. Adult females are more likely to bath in the hot springs during the winter when

air temperatures are lower than in summer. Adults bathe more in winter despite that fact the

water temperatures are maintained to be very similar in the winter and summer. In contrast to

adults, juvenile Japanese Macaques tend to bathe in the hot springs more in the summer. Infants

of mother who habitually bathe in the hot springs are more likely to bathe in hot springs than

infants of mothers who are not habitual hot spring bathers (Zhang, Watanabe, and Eishi 2007).

Stone handling is another cultural behavior observed in Japanese Macaques. At least

forty-five different stone handling behaviors have been observed in Japanese Macaques. Stone

handling behaviors include throwing stones, rubbing stones, clacking stones together, and

pounding stones onto hard surfaces. Because stone handling in Japanese macaques does not

appear to have any direct adaptive value, it is still uncertain why such a behavior exists and even

persists in groups of Japanese macaques (Nakagawa, Nakamichi, and Sugiura, 2010). Stone

handling is however linked to visual cues that promote stone handling. Japanese macaques are

more likely to display stone handling behavior where there are piles of stones present compare to

areas where stones are randomly scattered. Indirect social inputs in the environment help to

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provide stone handling cues which help to maintain stone handling traditions in troops of

Japanese macaques (Leca, Gunst, and Huffman, 2010).

The Japanese macaque is a highly intelligent and cultural non-human primate. Cultural

innovations such as sweet potato washing, hot spring bathing, and stone handling show that

Japanese macaques’ have a high degree of behavioral flexibility and innovation. If a Japanese

macaque cannot find a preferred food source such as fruits or leaves, they will resort to fallback

foods such as bark or even resort to raiding crops and gardens when they are in close proximity

to human settlements. Mothers play a crucial role in social learning for infants and juveniles.

Although females will stay in the troop, males will typically leave the troop sometime after their

juvenile period is over. The maximum life span of a Japanese macaque is approximately twenty-

five years for males and approximately thirty years for females. Females will typically have a

few years of post-reproductive life but this does not appear to be in accord with the grandmother

hypothesis.

Socioecology

Socioecology examines the relationship between social structure and an organism’s

environment. Social structure and environment form an interdependent relationship. Factors in

the environment including cold weather and an abrupt food shortage can act as immediate and

proximate mechanisms causing changes in an organism’s social structure. Long term

environmental change can change learned social behavior and these changes tend to occur more

slowly. Natural selection at the genetic level will then come about even more slowly than long

term environmental changes (Crook and Goss-Custard, 1972).

There are two crucial factors that shape an animal’s social structure. The first factor is

predation. Predation can have an especially major effect on helpless infants which is particularly

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common in mammals including primates. The second major factor is the abundance and location

of necessary resources such as food, water, and shelter. A limited supply of resources means

there is a limited population or social group that can be supported by the available resources.

Competition for these limited resources helps shape social structure because these limited

resources are mainly obtained through social behavior. Dispersion patterns in animals reflect an

adaptive relationship between obtaining necessary resources and social behavior. Animals will

tend to space themselves out in order to maximize their reproductive value (Crook and Goss-

Custard, 1972).

Crook and Gartlan (1966) offer an analysis based on ethological and ethological results

from field studies. The small size in the groups of frugivorous primates seems likely to be due to

the limiting factor of food availability. A non-seasonal climate with a stable availability of fruit

allows the group size to reach a ceiling. The ceiling is limited by shortage of food due to plant

failure and thus a limited food supply. This limit in the food supply then limits the number of

new infants which can enter the group. When a group of animals leaves the forest and moves

onto the open Savannah social groups become larger. The increased group size is due to open

conditions of predation and food supply for animals that must spend their time on the ground as

opposed to up in the trees of the forest. High levels of dispersed individuals in these conditions

would increase the risk of predation on single individuals. Large groups would be advantageous

in dealing with terrestrial predators. One consequence of the large group size is an increase in

competition in males for females (Crook and Gartlan, 1966).

Ecology can have an especially profound impact the social relationships in female-

bonded primates. The ultimate cause of female-bonded primates is believed to be because of

competition for high quality food patches such as fruit that that have a limited number of feeding

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sites. Cooperative relationships between females allow them to displace others from their

preferred food patch. Ecological data supports this idea for many female-bonded primates except

for when they do not have high quality food sources that only have a limited number of feeding

sites. In addition, multi-male groups tend to be found in female-bonded primate species when

they are not territorial. Having several males in a troop can help aid in aggressive inter-group

encounters (Wrangham, 1980).

Spuhler and Jorde (1975) conducted a large multivariate analysis of nineteen

demographic, ecological, and social behavioral variables in order to determine how the impacts

of phylogeny and the environment compare with each other. Twenty-nine population samples

from twenty-one primate species were analyzed. The results show that phylogenetic and

environmental variables were approximately equal in influencing social behavior. The main

variable that was significantly correlated with phylogeny was learning in great apes,

cercopithecoids, ceboids, and gibbons. Other variables were much more equally influenced by

phylogeny and the environment. The time spent navigating the environment can be just as

different in two species of macaques as it can be between one of the macaque species and a

species of lemur. Other variables that appear to be influenced roughly the same by phylogeny

and the environment are aggression, play, group size, home range, arborearlity, and group

composition (Spuhler and Jorde, 1975).

The study of socioecology has received both support and criticism. Socioecological

models for are interspecific differences in social relations between females, female dominance

relations, and kinship between group members may need to be abandoned because these

variables appear to be better predicted through life history models. However, socioecological

models can still support the idea that large groups possess a benefit for between group

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encounters. The notion that food distribution and feeding competition are important constraints

in tolerance of breeding females can also still be adequately explained with socioecological

models (Clutton-Brock and Janson, 2012).

Living in social groups has major advantages for Japanese macaques. Social learning has

allowed for behavioral innovations such as sweet potato washing, stone handling, and even the

use of medicinal plants to help fight off parasites. Social play in Japanese macaques can provide

cues to others in the group that they are safe from predation. Mothers provide the most social

learning and support for young Japanese macaques. The social groups of Japanese macaques can

also provide support during inter-troop encounters and can aid in obtaining resources.

Japanese macaques have been observed to display a variety of stone handling behaviors

including pulling stones, pushing stones, gathering stones into a pile, clacking stones, striking

stones (Huffman, Nahallage, and Leca, 2008), biting stones, carry stones in their mouth,

cuddling stones, washing stones in water, and wrapping stones in leaves (Nahallage and

Huffman, 2007). Stone handling can be observed as early as six weeks old but most infants do

not acquire stone handling until two to three months of age (Huffman, Nahallage, and Leca,

2008). Complex stone handling such as clacking stones typically does not occur until after six

months. The number of stone handling behaviors increases until age four and then eventually

begins decreasing into adulthood. The infant’s mother appears to be the most important social

model for learning stone handling behavior. Infants of mothers exhibiting a high frequency of

stone handling tend to exhibit more stone handling themselves. Mother’s that were observed to

be high frequency stone handlers were also more likely to have an infant that began stone

handling earlier than mothers that were observed to be low frequency stone handlers. High

frequency stone handling mother’s infants observed a greater percentage of their mother’s total

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time stone handling than low frequency mother’s infants. High frequency mothers were also

more likely to try and take the stones away from her while she was stone handling. Infants with

exposure to peers that displayed stone handling behavior were not more likely to display stone

handling. Exposure to stones in the environment did not have any effect on infants acquiring

stone handling behavior (Nahallage and Huffman, 2007).

Stone handling in Japanese macaque troops varies depending on the group size and age

distribution of the troop. Troops that are missing an age group tend to have less stone handling

patterns. Adults have more complex stone handling behaviors and younger macaques have a

shorter duration for their stone handling bouts. Larger groups of Japanese macaques have more

simultaneous stone handling. Observing other troop members stone handling may provide a

visual cue that the environment is currently free of predators and it is safe to play (Leca, Gunst,

and Huffman, 2007). Stone handling follows the ratchet effect. Having more time and experience

with stone handling leads to a greater variety of stone handling behavior. Observations at

Arashiyama and Takasakiyama show that the variety of stone handling behaviors has nearly

doubled over period and thirteen and fifteen years, respectively (Huffman, Nahallage, and Leca,

2008).

Aside from the various forms of stone handling already mentioned, Japanese macaques in

the Takh troop have been observed throwing stones. Stone throwing typically occurs in response

to a disturbance such as loud Japanese military aircrafts and intra-group aggression. The

response to intra-group aggression was never directed at the initiator or the recipient of

aggression. Stone throwing does not seem to be aimed at any particular target because no

Japanese macaques were ever hit by a stone nor were any near the area where a stone was

thrown. Stone throwing occupies almost every social layer in the Takh troop. Males and females

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of all ranks ranging between one year of age and twenty-two years of age have been observed

throwing stones. Stone throwing typically occurs from a tripedal position and is then followed by

multiple vertical leaps (Leca, Nahallage, Gunst, and Huffman, 2008).

Like other Old World Monkeys, Japanese macaques engage in play fighting. During play

fighting, macaques will gently bite or defend the upper arm, shoulder, and the side of the neck.

Juveniles tend to play with partners that are from the same matriline and of the same social rank.

Due to their low social tolerance, Japanese macaques tend to have more competitive play

fighting. In contrast, Tonkean macaques have high social tolerance and more cooperative play.

Mounting behavior is also incorporated into play fighting adaptation (Leca, Huffman, and Vasey,

2012).

Female mounting behavior is highly correlated with hormone fluctuations that occur

during the ovarian cycle. This applies to both heterosexual mounting behavior as well as

homosexual mounting behavior. High levels of mounting behavior tend to occur during the

follicular phase and periovulatory phase but not with the luteal phase (O’Neill, Fedigan, and

Ziegler, 2004). The follicular phase is the most fertile stage during the ovulatory cycle (Puts et

al., 2012).

Having high rank in the social group can have its benefits but also brings certain costs.

These costs however can be offset by ecology. High ranking females receive grooming from

more grooming partners than middle and low ranking females and are more central members of

the group. As a cost, high ranking females also have higher levels of nematode parasites

(MacIntosh et al., 2012). To offset consequences of parasite infection, Japanese macaques have

been found to consume plants with medicinal value. At least 135 species of plants eaten by

Japanese macaques have some medicinal value. Some plants eaten by Japanese macaques have

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even been used by humans for their antibacterial properties, their antifungal properties, their

antiviral properties, and their anthelmintic properties. Plants with anthelmintic properties are able

to kill parasites. Interestingly, some of the medicinal plants are only consumed seasonally. In the

spring, Japanese macaques will eat a toxic plant that can kill them by its actions on sodium-

potassium pumps which leads to cell death in the macaques. This toxic plant is however able to

kill the parasites that are most prevalent to infect Japanese macaques during the spring time

making consuming the toxic plant an advantageous behavioral adaptation (Leca, Huffman, and

Vasey, 2012).

Social grooming in Japanese macaques has been shown to be associated with grooming

related-feeding behavior. Grooming related-feeding behavior is when one monkey uses its

forefinger and thumb to comb through the fur of another monkey. Increased grooming duration

is significantly correlated with increased grooming related-feeding behavior (Onishi, Yamada,

and Nakamichi, 2013). As much as 98.9% of what Japanese macaques pick and eat while

grooming another troop member are lice eggs. This makes social grooming an advantage to the

groomee in the form of lice removal. The groomer receives an advantage by gaining the

opportunity to eat a high protein food source. The lice eggs are an easy source of food despite

their small size because Japanese macaques don’t have to worry about the eggs moving or

avoiding them (Tanaka and Takefushi, 1993).

Japanese macaques exploit a variety of food sources other than lice eggs and these food

sources are partially dictated by the age of the animal. In a non-predatory environment, male

juveniles tend to eat more animal matter than male adults but male adults tend to eat more

fibrous food sources such as mature leaves. Animal matter is a high energy food source rich in

protein and mature leaves are low quality food sources. Juveniles also engage in more time

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foraging during mating season because the adults spent time trying to mate. There is no

difference in the daily travel observed in adults and juveniles while foraging. Adults tend to

forage at a faster rate but this is offset the smaller metabolic demands of juveniles. This is

inconsistent with the idea that juvenile males are more prone to starvation than adult males

(Hanya, 2003).

Abundant resources are necessary for the survival of the offspring of Japanese macaques.

Because Japanese macaques are seasonal breeders, a low availability of fruit can have a major

impact on the birth rate in a troop. Low fruiting years can lead to a reduced number of new

offspring born into the troop compared to high fruiting years. The low fruiting years are

especially hard on smaller troops. A high level of inter-troop competition tends to lead to a lower

birth rate in small troops than in large troops. The discrepancy in the birth rate between large

troops and small troops is not observed during high fruiting years (Suzuki, Noma, and Izawa,

1998).

Dental flossing is a spontaneous innovation behavior associated with social grooming

that has been observed in at least one Japanese macaque. Chompe-69-85-94 is a central group

member, middle aged, and middle ranked female. Dental flossing was observed sixty-three times

during 17.8 hours of focal sampling of Chompe-68-85-94. Dental flossing involves inserting hair

between the teeth and performing repeated teeth chattering to remove food items. After flossing,

the hair is usually examined and then the saliva is licked off. Observations have found that

between one and six pieces of hair are used for dental flossing. Hair used for dental flossing can

come from any region of the body. Fingers or non-hair objects have never been observed being

used for dental flossing. 71.6% of dental flossing observed during allo-grooming whereas only

28.4% of dental flossing has been observed during self-grooming. Chompe-68-85-94 was

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observed dental flossing during social grooming with seven out of her eleven grooming partners.

Less dental flossing was observed with high ranking troop members. This may be because

sometimes dental flossing during social grooming is followed by aggression presumably because

it causes pain for the groomee (Leca, Gunst, and Huffman, 2010).

Although infanticide is rare in Japanese macaques, it has been observed at least once in a

wild non-provisioned troop. Eight adult males were observed to attack unweaned infants in pre-

mating season and early mating season. Only one infant died as a result of male aggression. The

attacks near mating season are inconsistent with the social pathology hypothesis, the side effect

of male aggression hypothesis, the cannibalism hypothesis, or the resource defense hypothesis of

infanticide. Instead the aggression near mating season is consistent with the sexual-selection

hypothesis of infanticide. The male attackers had recently risen in rank due of other high ranking

males leaving the troop. Most males had been observed to mate with the mother of the attack

victims. DNA analysis showed that none of the males attacked their own offspring. Males were

eight times more likely to attack an infant of a female he had not previously mated with. Females

mating with multiple males can inhibit male aggression towards the mother’s infant. It appears

that sexually selected infanticide can occur in seasonally mating, multi-male, multi-female

groups (Soltis, Thomsen, Matsubayashi, and Takenaka, 2000).

High ranking Japanese macaque males do not always have the most sexual partners.

Younger males that have not achieved the highest rank in the troop can have a high number of

sexual partners during mating season. The mating success observed in younger males may be

due to the female’s aversion to mate with males she has previously mated with. Furthermore, low

and middle ranking males may copulate in view of the highest ranking male without facing

aggression from the highest ranking male. Successful males tend to show more affiliative

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behavior towards females regardless of whether or not the two mate with each other. Successful

males also tend to show more aggression towards other males in the troop. Courtship displays

don’t appear to impact a male’s success at acquiring mating partners (Leca, Huffman, and Vasey,

2012).

The highest ranking male in the troop tends to keep his rank for several years. High

ranking males tend to mate with high ranking middle aged females. Young males typically mate

with young and low ranking females. Low ranking females will often mate with low ranking

males when they are between the ages of three to seven but will then mate with high ranking

males when they are between the ages of eight and thirteen years. 56% of high ranking female’s

mates are middle ranking males, low ranking males, sub-adult males, and solitary males. Re-

copulations between mates are common when looking at three year intervals but not when the

interval is expanded to four years (Leca, Huffman, and Vasey, 2012).

Examining the relationship an organism’s social structure and environment can provide

crucial insight into their behavior. Predation and the availability of resources such as food, water,

and shelter are two of the most important factors in shaping an animal’s social structure. Stone

handling behavior in Japanese macaques provides cues to the rest of the group that it is safe for

social play and that there are no immediate predators nearby. Living in social groups allows for

learned cultural behaviors including sweet potato washing, the use of medicinal plants, hot

spring bathing, and stone handling.

Object Handling

Object handling and manipulation requires a high degree of cognition. While

manipulating the external world is a crucial aspect of human behavior it is also seen in other

animals. Animals capable of using tools typically begin manipulating objects at a young age

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despite there being no immediate goal for manipulating the object. Object manipulation is also

dependent on social or observational learning. Tools are particularly common in primates, but

dolphins have also been observed using a sponge as a tool to help aid in foraging. Crows have

also been observed using a probe as a tool for foraging (Seed and Byrne, 2010).

Humans display incredibly complex object manipulation and tool use. Complex

manipulation requires complex activity and coordination in the central nervous system. Even

stone tools require a neurological capacity that is absent in non-human primates. Stout, Toth,

Schick, Chaminade (2008) conducted an experiment using positron emission tomography (PET)

to examine brain activity involved in the production of Oldowan and Acheulean tools by three

expert subjects. Each subject made Oldowan and Acheulean tools. Acheulean stone tools are

more complex and require more coordination and planning than the simpler Oldowan stone tools.

Brain activity for Oldowan and Acheulean tool making only overlapped in the lateral and ventral

precentral gyrii of the left hemisphere. The precentral gyrus is the primary motor cortex. The

orbitofrontal cortex was activated in Oldowan tool production, but not Acheulean tool

production. This region is involved in behavioral regulation (Stout, Toth, Schick, and

Chaminade, 2008).

Data was also compared between novice and expert stone tool makers. Novice tool

makers had more activity in the frontal cortex. This implies more executive function is needed to

learn how to make a stone tool than is required to make a tool after an individual is already

experienced with stone tool making. Expert tool makers had more activity in the supramarginal

gyrus (SMG), and experts had a posterior shift in a portion of the superior parietal lobe. Only

expert toolmakers had activity in the right occipital cortex. All brain activity that increased in

novice Oldowan tool making compared to control also increased in expert Oldowan tool makers.

20

Torigoe (1985) conducted an extensive experiment that showed at least seventy-four

species of non-human primates are capable of using tools. The experiment included twenty-four

genera and six families. Objects given to the primates were a nylon rope and a wooden cube. The

size of both objects varied depending on the size of the primate. For example, the objects given

to a chimpanzee would be larger than the objects given to a marmoset. A total of 506 behavioral

patterns using the objects were observed. Two-hundred and fifty-four of the manipulation

patterns used the rope, 157 used the cube, and 95 used both the rope and the cube. The

manipulation patterns were categorized based on the actions performed, the body parts used, and

the relationships to other objects in the environment (Torigoe, 1985).

An inter-specific comparison yielded three different groups of primates based on their

behavioral patterns. The first group consisted of lemurs, marmosets, spider monkeys, and

folivores. This first group had a small repertoire of manipulation patterns. They had few different

actions and only used a few body parts to perform these actions. The second group consisted of

the lesser apes, macaques, guenons, mangabys, and baboons. The second group had a greater

number of manipulations than the first group, but the second group had a lot of variation between

species. The third group contained the great apes and the cebus monkeys. Group three had the

most varied repertoire of object manipulation patterns with the nylon rope and the wooden box

(Torigoe, 1985).

Some the manipulation patterns observed were far more common in certain species while

other patterns were common to all species. Among the 506 manipulation patterns observed

across the seventy-four species of non-human primates, a few patterns were observed in all the

species. Every species in the experiment was observed to pick up the objects, place an object into

their mouth, and transport and object. This suggests that these manipulation patterns are common

21

to all primates. Object manipulation by lemurs and marmosets were most likely to involve

manipulations using the mouth. Lesser apes were far more likely to manipulate and object using

their feet than any of the other primates. Macaques, guenons, mangabeys, baboons, lesser apes,

and great apes commonly used fine control of their fingers to manipulate an object (Torigoe,

1985).

Among primates, tools are especially common in the great apes. Gorillas will use a stick

to measure water depth when they are wading through. Orangutans will use piles of leaves to

muffle their calls giving them a deeper sound. Chimpanzees may have the most extensive tool

use of any non-human primate. Perhaps one of the more human-like tools used and manufactured

by chimpanzees are spears. Chimpanzees make the spears from sticks they find in their

environment and use them to hunt bushbabys. Chimpanzees also use stick to dig into the ground

for tubers and underground beehives. Despite the fact the termites and ants are both small

insects, different models of a similar tool are required to access them. Chimpanzees will use a

leafy vine to make a flexible probe for termite fishing but they will use a much stiffer probe

when foraging for ants. There are even signs that chimpanzees will think about and plan future

tool use. Termite fishing can require two tools. The first tool is used to puncture the ground

making a hole near a termite nest. The second tool is the flexible probe that can then be used to

gather termites. The interesting part the two tools used is that although the second tool is taken

with the chimpanzee after they are done foraging, they will leave the first stick at the site so it

can be used again in the future (Seed and Byrne, 2010).

Rocks and stones are common objects used by primates. The earliest evidence for

modified objects by early hominins comes through stone tools. Non-human primates have never

been observed to manufacture and use a modified stone tool. Although an unmodified stone is a

22

simple tool, it can still be effective. Chimpanzees and capuchins have both been observed using

stones to crack open nuts. Capuchins are also known to use rocks to dig into the ground.

Baboons will throw rocks at predators to deter them (Seed and Byrne, 2010).

Sweet potato washing seen in Japanese macaques was one of the first observations of

object manipulation. Sweet potato washing has at least three variations in the method used

remove the dirt. The primary method relies of holding the sweet potato with one hand while

using the other hand to manually brush the sand off. Sweet potato washing occurs in both salt

and fresh water but Japanese macaques tend to prefer eating sweet potatoes washed in salt water

(Kawai 1965). Aside from sweet potato washing, Japanese macaques have also been observed to

wash grass roots (Nakamichi, Kato, Kojima, and Itoigawa, 1996).

Stone handling is another cultural behavior involving object manipulation that has been

observed in Japanese Macaques. Stone handling in Japanese macaques has been defined as the

“spontaneous stone-directed manipulative behavior, and comprised of multiple one-handed and

(a)symmetrical/(un)coordinated two-handed patterns” (Leca, Huffman, and Gunst, 2011: p. 63).

At least forty-five different stone handling behaviors have been observed in Japanese Macaques.

Stone handling behaviors include throwing stones, rubbing stones, clacking stones together, and

pounding stones onto hard surfaces. Because stone handling in Japanese macaques does not

appear to have any direct adaptive value, it is still uncertain why such a behavior exists and even

persists in groups of Japanese macaques (Nakagawa, Nakamichi, and Sugiura, 2010). Stone

handling is however linked to visual cues that promote stone handling. Japanese macaques are

more likely to display stone handling behavior where there are piles of stones present compare to

areas where stones are randomly scattered. Indirect social inputs in the environment help to

23

provide stone handling cues which help to maintain stone handling traditions in troops of

Japanese macaques (Leca, Gunst, and Huffman, 2010).

Leca, Gunst, and Huffman (2007) conducted video recording observations on ten troops

of Japanese macaques including one troop of Macaca fuscata yakui at six different sites in Japan.

Almost 1300 bouts of stone handling behavior were analyzed. Of the forty-five different stone

handling patterns that were observed, many of these stone handling patterns showed

geographical distribution. The geographical distribution of stone handling patterns has been

referred to as local variants or local stone handling traditions. A positive correlation was found

between geographical proximity and cultural similarity in stone handling patterns. No difference

was found however when comparing the stone handling patterns between the two subspecies

Macaca fuscata fuscata and Macaca fuscata yakui (Leca, Gunst, and Huffman, 2007).

Leca, Gunst, and Huffman (2010) examined stone handling behavior in eighty-four

Japanese macaques to determine if there was a laterality bias in stone handling. Of the 84

subjects, eighteen showed a left handed bias while twenty-two had a right hand bias. The other

forty-four Japanese macaques did not show a laterality bias. Older adults ages twenty-one years

and older were more likely to have a laterality bias than infants and juveniles. A negative

correlation was found between age and stone handling diversity with older Japanese macaques

displaying less stone handling diversity. There was also a negative correlation between stone

handling diversity and laterality. Older Japanese macaques displayed less diversity but more

laterality (Leca, Gunst, and Huffman, 2010).

Leca, Huffman, and Gunst (2011) conducted a cross-sectional analysis of stone handling

in Japanese macaques. They focused on bimanuality, coordination, and symmetry in hand use.

Japanese macaques were found to display more bimanual stone handling patterns than unilateral

24

stone handling patterns. Among bimanual patterns, most of them were coordinated as opposed to

uncoordinated. Four types of bimanual stone handling were observed. Both hands could be used

to perform the same task (uncoordinated symmetrical) or a different task (uncoordinated

asymmetrical) simultaneously. Both hands could also be used to perform the same task

(coordinated symmetrical) or different task (coordinated asymmetrical) simultaneously and

jointly to perform a single stone handling pattern. Some Japanese macaques were even observed

using their feet to handle stones although this is much rarer than using hands to handle stones

(Leca, Huffman, and Gunst, 2011).

Although stone handling shares some similarities with tool making and tool use, stone

handling does not appear to be as complex as tool making and tool use. Many of the motor

patterns that are required for stone handling are already present in Japanese macaques’ foraging

behavior. Among bimanual patterns, coordinated symmetrical patterns were far more common

than coordinated asymmetrical patterns. Bimanual symmetrical stone handling patterns requires

less cerebral asymmetry than bimanual asymmetrical patterns which means which means the

symmetrical patterns do not require as complex of a motor pattern. Older Japanese macaques

have even less complex stone handling patterns than younger adults. Older macaques typically

displayed unimanual stone handling patterns that usually occur while sitting down. It appears

that the older macaques require one free hand to assist with postural support while stone

handling. Among the older Japanese macaques, the females display more bimanual stone

handling patterns than the males. This could be because the estrogen in females has a

neuroprotective role that helps prevent the decay of fine motor control (Leca, Huffman, and

Gunst, 2011).

25

Stone handling is believed to have three separate stages. The first stage is the

transmission phase followed by the tradition phase and finally the transformation phase. During

the transmission phase, a young Japanese macaque collects stones and begins to manipulate

them. The infant will do so repeatedly for extended periods of time. Observational learning is

crucial in this early period. As the young stone handler gets older, their social networks will

expand. This creates new social peers and siblings who can observe the stone handling patterns

and incorporate them into their stone handling repertoire. The second stage is the tradition phase.

This occurs when females in the group reach reproductive maturity. At this time, the rate of

Japanese macaques leaving the troop is roughly equal the birth rate in the troop. Males who leave

the troop can pass on learned stone handling patterns to other troops. New infants being born into

the troop can learn stone handling behavior by observing their mother. Infants can also learn

stone handling patterns from an older sibling or one of their playmates whom likely learned from

their mother. Infants as young as three weeks old will show interest in stones. The young infants

will show interest in stones by grabbing them and sometimes putting them in their mouth. The

final stage in stone handling is the transformation phase. Living with a troop that has numerous

stone handling patterns allows newer members in the troop to acquire a variety of patterns

through observational learning. Familiarity and practice with stones may then extend the number

of stone handling patterns in the troop. Younger monkeys are likely to be crucial to innovating

new patterns because the older troop members typically have more difficulty acquiring new

behaviors and modifying existing behaviors (Huffman and Quiatt, 1986).

Aside from the stone handling that has been observed in Japanese macaques, stone

handling has also been observed in rhesus macaques Macaca mulatta (Nahallage and Huffman,

2008). The shared stone handling behavior between Japanese macaques and rhesus macaques

26

should probably come as no surprise due to the close genetic similarity and fairly recent

divergence between the two species. Depending on the dating technique used, estimates for the

divergence between rhesus macaques and Japanese macaques ranges from 310,000 years ago to

880,000 thousand years ago. Genetic analysis has estimated a six percent to thirteen percent

sequence divergence. The six to thirteen percent difference is actually less than the sequence

divergence found in the subspecies of the Borneo orangutans Pongo pygmaeus pygmaeus and the

Sumatran orangutans Pongo pygmaeus abelli This had led to questioning whether or not rhesus

macaques and Japanese macaques should be considered a single species (Marmi, Bertranpetit,

Terradas, Takenaka, and Domingo-Roura, 2004).

Despite the shared behavior of stone handling in Japanese macaques and rhesus

macaques, their stone handling behavior is not identical. Rhesus macaques only have twenty-

three stone handling patterns compared to the forty-five patterns exhibited by Japanese

macaques. All the stone handling patterns observed in Rhesus macaques have already been

observed in Japanese macaques with the exception of one new pattern. Five rhesus macaques

have been observed placing a stone into a cavity or a pipe. Despite the simplicity of this object

manipulation, Japanese macaques are yet to be observed utilizing this stone handling behavior in

their repertoire. When comparing the two species, Japanese macaques have a stone handling rate

a little more than twice that seen in rhesus macaques. Japanese macaques have seven customary

stone handling behaviors compared to three seen in rhesus macaques. Japanese macaques and

rhesus macaques both have five habitual stone handling patterns. Japanese macaques display

more complex stone handling patterns than rhesus macaques. Japanese macaques have twenty-

seven complex patterns and eighteen simple patterns. Rhesus macaques only have seven

complex patterns and sixteen simple patterns. Rhesus macaques spend more of their time stone

27

handling above ground on climbing structures. Rhesus macaques also spend more of their stone

handling time in a group as a communal activity. One explanation for the discrepancy seen in the

comparison of stone handling patterns in Japanese macaques and rhesus macaques is that the

Takeshima troop was observed for Japanese macaques. The Takeshima troop has the most stone

handling patterns observed among any troop of Japanese macaques. The Takeshima troop

actually displays all of the stone handling behaviors known to Japanese macaques (Nahallage

and Huffman, 2008).

Like Japanese macaques, rhesus macaques display age related differences in stone

handling behavior. Although rhesus macaques have no stone handling patterns that are unique to

adults aged five years or older, there are several patterns that are unique to young rhesus

macaques. Some of these patterns require a higher degree of physical force than other patterns

which may explain why they are not seen in the older adults, although not all the patterns unique

to the younger monkeys require physical force. Moving and pushing stones across the ground

requires a high level of force but cuddling and clacking stones does not. These patterns are not

observed in adult rhesus macaques despite the fact that they do not require a high degree of

physical force (Nahallage and Huffman, 2012).

The average number of stone handling patterns exhibited by rhesus macaques is 7.9.

Males tend to have slightly more patterns than females but this difference does not reach

statistical significance. Young rhesus macaques do however exhibit a significantly greater

number of stone handling patterns than older rhesus macaques. Stone handling is significantly

more likely to occur on sunny days. No stone handling has been observed on rainy days. Stone

handling is most commonly observed in rhesus macaques when at least forty percent of the troop

is resting. Common activities before stone handling include feeding, grooming, locomotion, and

28

playing. Aggression is incredibly rare before stone handling behavior (Nahallage and Huffman,

2008).

Although object handling and tool use in the animal kingdom are not as complex as they

are in humans, primates and especially the great apes display an impressive variety of object

handling and tool use. Perhaps some of the most well documented examples of object handling

in old world monkeys are sweet potato washing and stone handling seen in Japanese macaques.

With forty-five different stone handling patterns observed in Japanese macaques, they display a

wide variety of behavioral flexibility and innovation.

Dominance and Priority of access in Japanese Macaques

Because the dominant male was easily distinguishable due to a large patch of hair

missing, it was possible to compare the behaviors of the dominant male and the other Japanese

macaques that were not the dominant male. Comparisons were made during focal sampling.

Because dominant individuals often get priority of access to resources (Pusey, Williams, and

Goodall, 1997), it was hypothesized that the dominant male would be observed eating more,

getting groomed more, and grooming others less than the other Japanese macaques.

Methods

Subjects

Subjects were eight captive Japanese macaques at the Milwaukee County Zoo who had

spent their whole life in captivity at the Milwaukee County Zoo. All eight belonged to the

subspecies Macaca fuscata fuscata. Five of the Japanese macaques were females’ ages 25, 24,

23, 21, and 19 years old. The other three were males’ ages 23, 19, and 19 years old. Due to a lack

of experience with the Japanese macaques in conjunction with the relatively far observation

distance, it was not possible to distinguish between the individual Japanese macaques with the

29

exception of the dominant male because he was missing an extensive are of fur on his back.

Slightly more than fifty percent of the fur on his back was gone. The zookeeper on site suggested

the hair loss was due to excessive grooming. The zookeeper also mentioned that he was the first

one to eat when feeding time occurred and he was the boldest macaque when interacting with the

zookeepers. The dominant male was twenty-three years old.

Procedure

All data was collected on April 30, 2013. A series of sampling procedures were used to

record data. All observations were made on the macaques’ island and the bridge which connects

the island to an indoor enclosure. The Japanese macaques had free access to the indoor enclosure

and the island. No spatial dimensions were available for the island, but dimensions were

available for the indoor enclosure. The first room was 24.5 feet X 10.5 feet, the second room was

19 feet X 13.5 feet, and the third room was 19 feet X 9.5 feet. Zoo patrons are not allowed in the

indoor enclosure so no observations could be made there.

Scan sampling

Scan sampling was conducted at five and ten minute intervals. At the designated time

periods, the behavior of all observable Japanese macaques was recorded. Scans were conducted

at five minute intervals between 11:05 AM and 12:30 PM and between 3:20 PM. Ten minute

scan intervals were conducted between 1:00 PM and 2:30 PM. Data from a total of twenty-nine

scan samples were collected.

Focal sampling

Focal sampling was also conducted to determine the numerous different behaviors that an

individual engages in during a designated time period. Because the dominant male was of

30

particular interest, five ten minute samples for a total of fifty minutes were recorded. For the

other Japanese macaques, eight five minute samples were recorded for a total of forty minutes.

Ad libitum

Free note taking was also used to help gather as much interesting data as possible. Ad

libitum sampling was recorded in between scan samples.

Results

Ad libitum sampling

A total of 103 behaviors were observed during ad libitum sampling. Eating was the most

common behavior observed with 44 observations. The second most common behavior observed

was digging in the ground with twenty observations which was followed by grooming one’s self

with eleven observations. The rest of the data for ad libitum sampling can be found in table one

and figure one.

Table 1

Ad libitum sampling data for the number times behaviors were observed

Groom self Groom other Drink Eat

11 5 6 44

Itch Itch with hind leg Vocalize Dig

7 7 3 20

31

Figure 1

Graph for ad libitum sampling data depicting the number of times behaviors were observed

0 5 10 15 20 25 30 35 40 45 50

digvocalizeitch with hindlegitcheatdrinkgroom otherGroom self

A handful of unique or unexpected behaviors were recording during ad libitum sampling.

Perhaps the most unexpected observation was watching one Japanese macaque leap

approximately fifteen feet from a tree on the island to the structure located in the center of the

island. No other observations involving leaping or jumping were made during any of the other

sampling techniques although one Japanese macaque was observed walking across a rope that

was tied up between two trees on the island.

With respect to the observations recorded eating, two of them were peculiar. One

Japanese macaque was observed eating a loose piece of paper that had ended up on the island.

The piece of paper was saturated with water from the stream that surrounds the island. It is

unclear whether or not the paper was purposefully dipped into the stream or if the paper had

accidently fallen in the stream. Before eating the paper, the macaque would rip thin strips off the

32

sheet of paper. Some of the thin strips were simply discarded into the stream while other strips

were eaten. It is unclear why the Japanese macaque would resort to eating such a low quality

food source when there is no need to rely on any type of fall back food.

The macaques were not only fed by the zoo keepers, but also were able to find their own

food sources on the island. Although it was not possible to clearly view what was being eaten,

many of the macaques were observed digging in the ground and then eating whatever is was that

was that was found in the ground. It is likely that whatever was being dug out of the ground was

some type of insect. It was also quite common to observe a macaque eating something after

grooming one’s self or after grooming another macaque.

Scan sampling

A total of 137 behaviors of Japanese macaques were observed during scan sampling. The

most common behavior observed was resting with a total of 77 observations. The second most

common behavior was locomotion with 33 recordings. The rest of the data for the total

observations made during scan sampling can be found in table two and figure two. A total of 76

observations were made between the times of 11:05 AM and 12:30 PM with data being collected

every five minutes for a total of eighteen recording times. Resting was the most common

behavior observed 11:05 AM and 12:30 PM followed by locomotion. Between the times of 1:00

PM and 2:30 PM, the most common behaviors observed were once again resting followed by

locomotion. Resting was not the most common behavior observed between 3:20 PM and 4:00

PM. Instead, the most common behavior observed was locomotion but locomotion was closely

followed by resting.

Table 2

33

Scan Sampling Data

Key for table two: GA = groom another, GG = get groomed, D = dig, E = eat, L = locomotion, R

= rest, S = smell hand, C = climb, X = no subject present

Time Subject 1 Subject 2 Subject 3 Subject 4 Subject 5 Subject

6

11:05 E L L X X X

11:10 R R R R X X

11:15 R R C C C X

11:20 L L R R X X

11:25 L R R R R X

11:30 L R C R X X

11:35 S R R R X X

11:40 L L C R X X

11:45 R R R R L L

11:50 R R R X X X

11:55 L R R R X X

12:00 L L R R X X

12:05 R R R X X X

12:10 R R R R R C

12:15 R R R L X X

12:20 R R R L X X

12:25 R R R L X X

12:30 R R X X X X

34

1:00 R R X X X X

1:10 R R GA GG X X

1:20 L L E R X X

1:30 GA GG R X X X

1:40 C GA GG R L L

1:50 R X X X X X

2:00 R R R L L X

2:10 R R R R R R

2:20 L X X X X X

2:30 R R R X X X

3:20 GO GG X X X X

3:25 GO GG D X X X

3:30 E GG GO L R X

3:35 L L D X X X

3:40 L R D X X X

3:45 L L L X X X

3:50 L R R R X X

3:55 R R D X X X

4:00 X X X X X X

35

Figure 2

Graph displaying the total behaviors observed during scan sampling

Key for figure two: GA = groom another, GG = get groomed, D = dig, E = eat, L = locomotion,

R = rest, S = smell hand, C = climb; no subject present is not depicted in figure 2.

GAGGDELRSC

Focal sampling

The hypothesis that the dominant male would be observed eating more, getting groomed

more, and grooming others less was supported by the data although statistical analysis was not

conducted in order to determine if any of these values reached statistical significance. Table

three shows the focal sampling data for all Japanese macaques sampled that were not dominant

male. Locomotion was the most common behavior observed followed by resting. Only one

observation was made for both eating and grooming another individual. No observations were

made of any of the non-dominant macaques getting groomed during focal sampling. Table four

shows the focal sampling data for the dominant male. The most common behavior observed was

36

resting which was followed by locomotion. The dominant male was observed eating far more

times than the other macaques. The dominant male was observed eating thirteen times. The

dominant male was never observed grooming another individual but he was observed getting

groomed by another individual twice. Figure three shows of comparison of the average number

of behavioral changes per minute for the dominant male and the Japanese macaques that were

not the dominant male. The macaques that were not the dominant male were observed changing

their behavior 0.675 times per minute whereas the dominant male was observed changing his

behavior 1.240 times per minute.

Table 3

Data for focal sampling

All focal samples in table 3 used five minute observations. Only changes in behavior were

recorded and times were excluded from data acquisition.

Focal sample 1: groom another individual, left view

Focal sample 2: rest, peer into enclosure, left view

Focal sample 3: sit on top of structure, climb down, rest, smell hand

Focal sample 4: rest, locomotion, itch hindquarters, smell hand, rest, locomotion, sit on ledge,

chew, itch arm, smell hand

Focal sample 5: sit in tree, itch, groom self, itch, groom, self, eat, climb down tree

Focal sample 6: walk across rope, sit in tree, itch, groom self, grunt

Focal sample 7: climb structure, sit on structure, climb down structure, left view

Focal sample 8: sit in tree, locomotion, climb structure, sit on structure, climb structure, sit on

structure, climb down structure, left view

37

Table 4

Data for focal sampling of dominant male

All focal samples in table 4 used ten minute observations. Only changes in behavior were

recorded and times were excluded from data acquisition.

Focal sample 1: locomotion, sit under tree, chew, locomotion, drink, rest, eat, locomotion, climb

structure, rest, eat, rest, eat, rest, eat, rest

Focal sample 2: locomotion, rest, locomotion, drink, locomotion, rest, eat, rest, eat, rest, eat, rest,

eat, rest, left view

Focal sample 3: get groomed, rest, eat, rest, get groomed, eat, rest

Focal sample 4: locomotion, dig, eat, locomotion, climb structure, rest, eat, rest, eat

Focal sample 5: rest, left view, locomotion, climb structure, rest, climb down structure,

locomotion, rest, left view, locomotion, climb structure, rest, left view, climb structure, rest

Figure 3

Number of behavioral changes per minute for focal sampling

Figure 3 depicts the number of behavioral changes per minute that were observed in the

dominant male and the other non-dominant members. The dominant male averaged and the non-

dominant members averaged 1.240 and 0.675 behavioral changes per minute respectively.

Dominant male

non-dominant

0 0.2 0.4 0.6 0.8 1 1.2 1.4

38

Discussion

The hypothesis in the present study was that the dominant male would be observed eating

more, getting groomed more, and grooming others less during focal sampling. All three points of

the hypothesis were confirmed although no statistical analysis was conducted to determine

whether or not the data reached statistical significance. Despite confirming the hypothesis, the

data from the current study cannot draw definitive conclusions. The dominant male was observed

for a total of fifty minutes during focal sampling whereas the non-dominant macaques were only

observed for forty minutes. The observations were relatively short and were of unequal duration.

It should also be noted that although eating was the most common behavior observed during ad

libitum sampling with a total of 44 observations, during focal sampling only one observation was

made of a non-dominant macaque eating and thirteen observations were made of the dominant

male eating. More conclusive results may be yielded by observing the Japanese macaques at

feeding time. According to the zoo keeper on site, during feeding time the dominant male has

priority of access to the food but no data was available to confirm this. All of the foraging

behavior that was observed occurred in the context of finding food sources that were already

available to the macaques on the island. The food items that were eaten were not observable. It

could be that certain macaques on the island are able to acquire higher quality food sources than

others but this speculation cannot be confirmed by the present study.

The most common behavior observed during scan sampling was resting followed by

locomotion. Resting and locomotion were the most common and second most common

behaviors observed respectively between the times of 11:05 AM and 12:30 PM as well as

between 1:00 PM and 2:30 PM. This pattern was reversed between 3:20 PM and 4:00 PM with

39

locomotion being the most common observation and resting being the second most common

observation.

Perhaps the most peculiar behavior observed was one Japanese macaque eating paper. It

has typically been accepted that Japanese macaques do not eat items that are not recognized as

food items. Also, Japanese macaques usually don’t resort to fall back foods unless temperatures

are very low (Richard, Goldstein, and Dewar, 1989). However, recent research has found that

when food sources are scarce, Japanese macaques will resort to raiding crops and gardens

(Yamada and Muroyama, 2010); when given the opportunity, Japanese macaques will eat almost

anything that is not too hot or bitter (Nakagawa, Nakamichi, and Sugiura, 2010).

The present study has confirmed the hypothesis that the dominant male would be

observed eating more, getting groomed more, and grooming others less during focal sampling,

although no statistical analysis was conducted to determine whether or not the data reached

statistical significance. Despite confirming the hypothesis, the data from the current study cannot

draw definitive conclusions due to the unequal time durations in focal sampling and the

relatively short observations for both the dominant male and the non-dominant Japanese

macaques. The results for grooming were also hard to assess due to the low frequency of

observations. Future research should try to conduct a more comprehensive examination of the

differences in behavior observed in the dominant male and the non-dominant macaques at the

Milwaukee County Zoo.

40

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