agonistic behavior in a transplanted troop of japanese macaques: arashiyama west

PRIMATES, 19(1): 141--151, January 1978 141

Agonistic Behavior in a Transplanted Troop of Japanese Macaques: Arashiyama West

TIM W. CLARK

University of Wisconsin, Madison

ABSTRACT. Arashiyama A troop was transplanted from Japan to Texas, U.S.A. in February 1972 and released into a large outdoor enclosure (42 ha) in a semi-free ranging condition. Agonistic behavior was quantified during the first six months after the release. Agonistic interactions occurred at about one incident per 100 monkeys every 2 to 9 minutes. In general, peaks in frequency of agonistic interactions coincided with peaks in feeding activity. 97.5 70 of all incidents were of a "mild" type, and 85.7 70 were simple one-to-one, unidirectional interactions. "Severe" forms of agonistic behavior occurred only during the first month and then only rarely. Adult females and juveniles were initiators in about 93 % of all cases. In general, the more severe the form of attack, the more pronounced was the form of submission.

I N T R O D U C T I O N

Several Japanese macaque troops have received continuous research attention over the last two decades; numerous contributions have resulted from these long-term studies (e.g., "pre-culture" : IMANISm, 1952; KAWAMURA, 1956; YAMADA, 1957 ; et al.). In 1972, one such troop, captured in its ancestral home near Kyoto, Japan, was transplanted intact to Laredo, Texas, U.S.A. and released into a large outdoor enclosure. A general overview of the troop and its history, transplant site, and some behavioral and ecological adaptations was given by CLARK and MAYO (1975) and detailed presentations by CLARK (1975) and CASEY and CLARK (1976). Agonistic behavior was part of the early post-transplant research interests. Agonistic behavior refers to all aspects of conflict behavior, i.e., all overt aggressive and submissive interactions of individuals within the group (SouTHWlCK, 1967). The purposes of this paper are: (1) to describe some changes in agonistic behavior during the first six months after the transplant, (2) to give data on the structure (number of troop members involved) and form (behavior patterns involved) of agonistic interactions, and (3) to relate these data to the Japanese macaque troop in Oregon and to other macaques.

METHODS

Agonistic interactions were examined in a series of 10-minute samples to record the frequency, structure, form, and participants. Data were gathered at hourly intervals. Each hour of the day from dawn to sunset--that is, one daily activity cycle--was covered at least once every five to 10 days (three to six times per month). Agonistic interactions were recorded using a system designed by ALEXANDER and ROTH (1970)

142 T.W. CLARK

for the Japanese macaques at the Oregon Regional Primate Research Center during their study of the relationship between crowding and aggressive behavior. (1) Structure of Aggressive Interaction:

(a) One-to-one, one-way: one monkey attacks another (using one of the forms of attack listed below); the recipient either submits or ignores the attack.

(b) One-to-one, two-way: mutual attack between two monkeys. (c) Group-to-one, one-way: a group of less than 10 attack a single individual or a

single individual attacks a group; the recipient(s) either submit or ignore the attack.

(d) Group-to-one, two-way: mutual attack between a group of less than 10 and an individual.

(e) Troop attack: Ten or more monkeys attack a single monkey which flees or submits.

(f) Shifting troop attack: Ten or more monkeys engage in attack behavior, the recipient of which changes frequently.

(2) Forms of Attack: listed in order of increasing severity. (a) Threat: a directed pursuit of more than 5 meters or any conspicuous aggressive

movement of one animal toward another (e.g., woofing, ear-flipping, gaping, pursed lips, screaming) together with a lunge sufficient to bring the recipient to his feet.

(b) Chase: both a directed pursuit and an aggressive movement. (c) Punish: aggressive physical contact that does not appear to result in tissue

damage and is brief in nature (slaps, hair pulling, quick bites). (d) Assault: aggressive physical contact that appears to inflict tissue damage

(violent biting, shaking, gnawing). (3) Forms of Submission: listed in order of increasing intensity and designated with

a letter identification. Submission was only scored in response to an attack. (a) A: no reaction or moving backwards less than one meter. (b) B: flight from attacker greater than one meter, fear grimace, cringe, no vocali-

zation other than short yips. (c) C: same as B, but with sustained screaming. (d) D: silently crouching in corner or near a wall with head toward the wall.

(4) Defense Behavior: recorded under the following condition: monkey A attacks monkey B (as defined above), and monkey C attacks monkey A immediately afterwards. In this case, monkey C defends monkey B. For each agonistic interaction, the structure, the most severe form of attack, the

most intense form of submission, and the participants were recorded where possible. Extensive, detailed field notes were made during all phases of observation. As

RIOCH (1967) points out, the importance of quantitative data is unquestionable. Nevertheless, there is still room in the field of naturalistic primate research for an- ecdotal records of unique events. Field notes covered a wide variety of behaviors and activities of the monkeys.

THE TRANSPLANTED TROOP

The Arashiyama Japanese macaques have been provisioned and under continuous

Agonistic Behavior of Japanese Macaques 143

observation since 1952 (NoRIKOSHI, 1971; GOUZOULES et al., 1975). As a result, there exists a wealth of data on troop lineage, social behavior, etc. The troop split into two parts, A and B, in 1966. A more detailed history of the troop and a list of the published studies up to the time of transplant are given by CLARK (1975). The ex- istence of a sister troop (Arashiyama B) still in the ancestral home in Japan makes Arashiyama West troop unique for scientific study. The age and sex composition of the troop is compared for two periods (start of study and shortly after its termination) by CLARK and MANO (1975).

THE TRANSPLANT SITE

The transplant site lies 48 km N of Laredo and 24 km SW of Encinal, Texas, the nearest towns. A comparative description of the transplant site and the Arashiyama evolutionary environment are given by CLARK (1975).

The climate of the transplant site is semi-arid, with an abundance of sunshine throughout the year, high summer temperatures with low humidities, and mild winters. Monthly average temperatures at Laredo (from 1931 to 1960) were 30.6~ in July through September, 14.4~ in January. The normal annual rainfall is 46.5 cm; drought is common. Snow is rare; only three measurable amounts have been recorded since 1931.

The Texas savanna ecosystem is a relatively flat plain; the maximum relief at the release site is only 12 m. Natural water is available only for a day or two after heavy rains. Four water outlets piped in from a nearby well provide a continuous flow of fresh water to the monkeys. The vegetation of the transplant site is a more or less homogeneous savanna-like mixture of shrubs, cacti, and herbs averaging about 1.5 m high. Acacia spp. are the most common shrub with mesquite (Prosopis spp.) scattered throughout. Cacti (Opuntia spp.) are abundant.

CONTAINMENT FACILITIES

In Texas, the monkeys are retained in a large outdoor enclosure (42 ha) by an electric fence; design of this facility is described by CLARK (1975). From 23 February to 25 March 1972, the troop was confined to a corral constructed near the center of the larger enclosure.

The corral encloses an area of 5575 sq. m (0.6 ha) 75 m on a side. A variety of structures was constructed in the corral--four shade platforms, two sleeping and shade towers, a holding cage, and an observation tower. Six dead mesquite trees were transplanted also. The size of the corral was designed to approximate the observed troop spread area seen between provisioning sessions in Japan. The area used in Japan was about 4000 sq. m; the corral was built about half again as large. A 3-m high electric fence bounded the corral area and prohibited monkey egress.

RESULTS

AGONISTIC BEHAVIOR RATES

Data are presented from two periods: February and March during confinement in the small corral and the other, April through August, following release into the

144 T.W. CLARK

~) 55.0

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~ g 15.c

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Fig. 1. Comparison of April through August)

FEB.- MAR.

I I I I I ) I f t I I I I I I 6 7 B 9 I0 II 12 I Z S 4 5 6 7 8

AM HOURS OF DAY PM

agonistic behavior rates for two periods (February and March, and in 1972, Arashiyama West, Texas.

larger enclosure (Fig. 1). No major difference in rates of agonistic interactions between the two periods occurred. It was thought that a combination of the newness of the transplant environment and the relatively small corral might increase agonistic rates. Agonistic interactions occurred at the rate of about one incident per 100 monkeys every 2 to 9 minutes. However, rates were not uniform over time: agonistic encounters tended to come in clumps. For example, an interaction might break out while several monkeys were resting in the shade on a tower. The incident would result in a shifting of spatial relations on the tower Which, in turn, precipitated other agonistic encounters. The next spontaneous agonistic interactions might not occur for another hour or more.

In general, peaks in frequency of agonistic interactions coincided with peaks in feeding activity. CLARK and MANO (1974) and CLARK (1975) reported that the troop tended to feed three times daily, from 7-10 a.m. then from l l a.m.-1 p.m., and finally from 4-7 p.m. The coincidence between agonistic behavior and feeding periods was clearly seen in February-March (Fig. 1), when the troop was provisioned twice daily (ca. 8 a.m. & 5 p.m.). Peaks in frequency of agonistic interactions in April- August also coincided with the single evening provisioning period as well as the morning foraging forays. Since the high midday summer temperatures tended to suppress midday feeding activity, only two daily peaks in rates of agonistic encounters clearly occurred.

STRUCTURE OF AGONISTIC INTERACTIONS

Agonistic interactions were grouped into two classes after ALEXANDER and ROTH (1970). "Mobbing" involved the more severe structure, Troop Attacks (TA), and Shifting Troop Attacks (STA). "Squabbling," the mild type of agonistic behavior, involved all other interactions. A summary of 420 agonistic encounters is given in Figure 2. Only those interactions that could easily be characterized as either mobbing or squabbling and the precise structure determined were listed in Figure 2.97.5 percent of all incidents were of a squabbling type, and 85.7 percent were simple one-to- one, unidirectional interactions.

Mobbing occurred only during the first month and then only rarely. The relatively crowded condition of the entire troop in the 0.6 ha corral, especially since some peripheral males were present, may have increased the incidence of this severe form


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4

2

o One to one, one way

1972 Feb. - Mar. Apr.- Aug.

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N N /

One toom Group toone, Group to one, Troop Shifting two way one way two way Attack Troop Attack

STRUCTURE OF AGONISTIC INTERACTIONS Fig. 2. Summary of the structure of 420 agonistic interactions between Japanese macaques of Arashiyama West.

of aggression. The peripheral males, who in Japan usually remain away from the central part of the troop, were unable to spatially segregate themselves. Within hours after the transplant, the single solitary male and several of the 17 peripheral males were recipients of aggressive attacks by central troop members and tried to leave the corral. Within the first six days after the release: (1) six of these males died, one from electrification and five from "stress" due to reduced consumption of water and food as well as harassment (the severity of none of the attacks was, in itself, sufficient to cause death); and (2) nine peripheral males were removed from the corral by the researchers. This reduced the number of peripheral males to three by day seven, but on that day one peripheral male climbed back inside--leaving four peripheral males inside for the remainder of the confinement in the corral.

Mobbing episodes lasted up to 20 minutes and involved several dozen monkeys. As in the mobbing behavior reported in the Oregon troop, the form of attack was mostly Assault; and submission was usually D.

A typical TA or STA started when a juvenile threatened a peripheral male. The juvenile was soon joined by peers, family members, central males, and others. Ten TA's were observed; they usually dissolved after a few minutes when the aggressive monkeys turned to other activities. Only one STA was observed. The members of the attacking group, after attacking the focus peripheral male, turned on each other. No one was seriously injured and the encounter lasted only a few minutes. The single

146 T.W. CLARK

STA occurred during the first week after the transplant while more than a dozen peripheral males were still in the corral. As more and more peripheral males were removed from the corral, fewer TA were seen. By the third week after the transplant, such interactions were very rare.

On one occasion, the peripheral male recipient of the TA fell motionless after a short chase--apparently uninjured. The aggressors immediately descended on him. Agonistic behavior was instantly terminated and several adult females began to groom him. The remainder of the attacking group slowly returned to other activities.

Of the 420 agonistic interactions observed in their entirety, 293 one-to-one, unidirectional encounters were categorized as to sex and age of initiators and recipients (Fig 3). Adult females and juveniles were initiators in about 93 percent of all cases. Adult males were initiators or recipients in 1 percent of all interactions. Adult females (61.3 percent) and juveniles (31.8 percent). Juveniles were not observed to

6

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Initiated b y ~ Juvenile

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Initiated by Infant

Inf.

AGE AND SEX OF RECIPIENT IN I J' 1 AGONISTIC INTERACTIONS

Fig. 3. Initiator and recipient of 293, 1--~1 agonistic encounters between Japanese macaques of Arashiyama West.


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Adu l t Moles

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AGE AND SEX OF P A R T I C I P A N T S IN ! = = 1 A G O N I S T I C I N T E R A C T I O N S

Fig. 4. Participants in 38, 1~--~1 agonistic encounters between Japanese macaques of Arashi- yama West.

direcCy any agonistic behavior to adult males and very little towards adult females (14.2 percent). Most (75.7 percent) juvenile initiated agonistic behavior was directed at other juveniles. Over all, juveniles were recipients of about 54 percent of all agonistic behavior, followed by adult females who received 35 percent. Infants were seldom involved in agonistic incidents, but occasionally a juvenile exhibited agonistic behavior towards them.

The largest single class (48 percent) of one-to-one, two-way interactions was within the juvenile age class (Fig. 4). Adult females were next with about 32 percent of all interactions. Adult females and juvenile interactions comprised 16 percent and adult males and juveniles about 4 percent.

In general, the more severe the form of attack, the more pronounced was the form of submission (Fig. 5). Simple threats were met with all four possible submissive behavioral categories: form of submission A was the response 6.7 percent of the

148 T.W. CLARK

1972 Feb.- Mar. Apr:- Auo.

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Form of attack: Threat

o ~ 14: z b.I ::)

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FORMS

Threat ~ Chase

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OF SUBMISSION

Threat, Chase a Punish

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IC

i 21 A B C D

Fig. 5. Relationship between forms of attacks and subsequent forms of submission among Japanese macaques of Arashiyama West in 1---~1 agonistic encounters.

time; B, 32.6 percent; C, 58.4 percent; and D, 2.2 percent. When a threat was com- bined with a chase, then the recipient exhibited only forms of submission B (26.1 percent) or C (73.2 percent). A combination threat, chase, and punish was met with only C-form of submission. No combination of threat, chase, punish, and assault forms of attack was observed in a one-to-one interaction.

DISCUSSION

Numerous facets and correlates of primate agonistic behavior have been investi- gated (e.g., SOUTHWICK, 1967, 1969; TO~UDA & JENSEN, 1968; ALEXANOER & ROTH, 1970; MARSDEN, 1973; BERNSTEIN & GORDON, 1974; BERNSTEIN et al., 1974; et al.). Comparisons of agonistic behavior between Arashiyama West and other primates are impossible except in a general way. The Oregon Japanese macaque troop is the only other Japanese macaque troop on this continent, but it differs from Arashiyama West in age and sex structure, size, density, ecological context, and confinement and provisioning situations. Moreover, several features of the Oregon troop make it atypical of Japanese macaque troops in general (ALEXANDER & BOWERS, 1968) and different from Arashiyama West. First, this closely confined (0.8 ha) troop lacks the general central-peripheral pattern characteristic of Japanese monkeys (MIYADI, 1964; YAMAOA, 1966; SUCIYAMA, 1960). Second is the extreme aggressiveness of its members (ALEXANOER & BOWERS, 1968; ALEXANDER & ROTH, 1970). The leader is apparently


ineffective in controlling the frequency and intensity of aggression; this seems to result in a diminished tendency for troop members to cluster around the leader in the central-peripheral pattern. It is ALEXANDER and BOWERS' (1968) hypothesis that the 0.8 ha corral deprives the troop leader of many of his normal functions such as guiding troop migrations, leading confrontations against neighboring troops, and guarding against predators (IMANISHI, 1965). Since the leader is no longer vital to the troop's well-being, the clustering tendency has gradually waned, and the troop com- mingles in small groups organized around play, grooming, and feeding. At the same time, the leader appears to have lost some of his zeal towards controlling aggression (ALEXANDER • BOWERS, 1968; ALEXANDER ~; ROTH, 1970).

ALEXANDER and BOWERS (1970) believe that, as a result of confinement, aggressive encounters probably increased in frequency of aggressive behavior in this troop in the wild prior to the transplant, it is difficult to draw any specific conclusions. However, the frequencies of TA and STA are unique to the Oregon troop.

Arashiyama West maintained the central-peripheral structure it exhibited prior to the transplant, continued normal behavior of the leader males, and exhibited no major behavioral alterations. However, during the first 30 days in Texas when peripheral males were closely confined with the central portion of the troop, some severe agonistic interactions occurred, although at a lower frequency than seen in the Oregon troop. Also, as soon as Arashiyama West was released into the 42 ha enclosure, all forms of severe agonistic behavior ceased. The Oregon troop was confined until recently to the 0.8 ha corral and severe forms of aggression continued. Nearly all agonistic interactions seen in Arashiyama West were one-to-one, unidirectional; ALEXANDER and BOWERS (1968) reported that aggression is consistently unidirectional in the Oregon troop.

An experimental study in the Oregon troop on the effect of acute crowding on aggressive behavior (ALEXANDER & ROTH, 1970) showed that both mild and severe forms of aggression occurred more frequently in the crowding pen. In the Okino- shima troop transplanted in Japan, an increase in the frequency of agonistic behavior was observed and attributed not to the effects of the move itself but to the limitation of troop movements because of the small size of the island in which it was introduced (KAwAI et al., 1967). KAWABE (1971, pets. comm.) noted an increase in agonistic behavior of the Shodoshima I troop, which he studied before and after its release. He believes that a similar phenomenon of increased agonistic behavior occurred in Shodoshima T and O troops after their release. A similar increase in frequency of agonistic interactions did not seem to occur in Arashiyama West. However, this conclusion is based on the comparison of the agonistic behavior of the first six months with only general observations in Texas two years after the transplant. The only difference in agonistic behavior at any time was the occurrence of TA and STA during the short interval the troop was confined to the corral.

In Arashiyama West, agonistic incidents clearly increased at provisioning times: rates frequently more than doubled. However, a similar high rate was also seen when the troop conducted its usually morning feeding sortie. As the exact effects of provisioning on agonistic behavior become available, a clearer understanding of aggression and its role in primate societies will no doubt emerge.

150 T.W. CLARK

Acknowledgements. Constructive comments made by DENISE CASEY, TIM JOHNSTON, and HAROLD GOUZOULES were invaluable. The encouragement of Drs. JOHN T. EMLEN and JOHN C. NEESS was essential. Support of this study was given by the Grant Foundation, National Science Foundation, Wisconsin Regional Primate Research Center and the Department of Zoology, University of Wisconsin-Madison. A great many people made the transplant and thus this study possible; to all the Japanese and Americans who helped directly or indirectly-- thank you.

REFERENCES

ALEXANDER, B. K. & J. M. BOWERS, 1968. The social structure of the Oregon troop of Japanese macaques. Primates, 8 : 333-340.

- - & E. M. ROTH, 1970. The effects of acute crowding on aggressive behavior of Japanese macaques. Behaviour, 39: 73-89.

BERNSTEIN, I. S. & T. P. GORDON, 1974. The function of aggression in Primate societies. Amer. Scientist, 62: 304-311.

- - , I. P. GORDON, & R. M. ROSE, 1974. Aggression and social controls in rhesus monkeys (Macaca mulatta) groups revealed in group formation studies. Folia primat., 21: 81-107.

CASEY, D. E. • T. W. CLARK, 1976. Some spacing relations among the central male of a transplanted troop of Japanese macaques (Arashiyama Wes0. Primates, 17: 433-450.

CLARK, T. W., 1975. Transplantation and adaptation of a troop of Japanese macaques to a Texas brushland habitat. Unpubl. 415 p.

- - & T. MANO, 1975. Transplantation and adaptation of Arashiyama A troop of Japanese macaques to a Texas brushland habitat. Contemporary Primatology, 358-361.

EATON, G., 1971. The Oregon troop of Japanese macaques, Macacafuscata. Primate News, 9: 4-9.

GARTLAN, J. S., 1968. Structure and function in primate society. Foliaprimat., 8: 89-120. GOUZOULES, H., L. M. FEDIGAN, & L. FEDIGAN, 1975. Responses of a transplanted troop of

Japanese macaques (Macaca fuscata) to bobcat (Lynx rufus) predation. Primates, 16: 335-349.

HALL, K. R. L., 1964. Aggression in monkey and ape societies. In: The Natural History of Aggression, J. D. CARTHY & F. J. EBLING (eds.), Academic Press, London. 159 p.

IMANISHI, K., 1952. Evolution of the human characteristics. In: Man, K. IMANISHI (ed.), Mainichi-shinbun-sha, Tokyo, pp. 36-94. (in Japanese).

- - , 1965. Identification: a process of socialization in the subhuman society of Macaca fuscata. In: Japanese Monkeys--A Collection of Translations, S. ALTMAN (ed.).

KAWAI, M., S. AZUMA, & K. YOSHmA, 1967. Ecological studies of reproduction in Japanese monkeys (Macacafuscata): I. Problems of the birth season. Primates, 8: 35-74.

KAWAMURA, S., 1956. Prehuman culture. Shizen, 11 : 28-35. (in Japanese). MARSDEN, H. M., 1973. Aggression within social groups of rhesus monkeys(Macaca mulatta):

effect of contact between groups. Anita. Behav., 21 : 247-249. MIYADI, D., 1964. Social life of Japanese monkeys. Science, 143 : 783-786. NORIKOSHI, K., 1971. Tests to determine the responsiveness of free-ranging Japanese monkeys

in food-getting situations. Primates, 12:113-124. RIOCH, D., 1967. Discussion of agonistic behavior. In: Social Communication Among Pri-

mates, S. A. ALTMAN (ed.), Chicago Univ. Press, Chicago, pp. 115-122. ROWELL, T., 1967. Social organization in primates. In: Primate Ethology, D. MORRIS (ed.),

Atdine, London, pp. 219-235. SOtlTHWlCK, C. H., 1967. An experimental study of intra group agonistic behavior in rhesus

monkeys (Macaca mulatta). Behaviour, 28: 182-209. - - , 1969. Aggressive behavior of rhesus monkeys in natural and captive groups. Proc.

Syrup. on the Biol, of Aggression, Milan, May 1968, Excerpta Medica, Amsteridam. SUGIYAMA, Y., 1910. On the division of natural troop of Japanese monkeys at Takasakiyama.

Primates, 2: 109-148.


TOKUOA, K. & G. D. JENSEN, 1968. The leader's role in controlling aggressive behavior in a monkey group. Primates, 9: 319-322.

YAMADA, M., 1957. A case of acculturation in the subhuman society of Japanese monkeys. Primates, 1 : 30--46 (in Japanese).

- - , 1966. Five natural troops of Japanese monkeys in Shodoshima Island (1): distri- bution and organization, Primates, 7: 315-362.

- - Received March 29, 1976; Accepted March 11, 1977

Author's Present Address: TtM W. CLARK, Department of Biology, Idaho State University, Pocatello, Idaho 83209, U.S.A.

agonistic behavior in a transplanted troop of japanese macaques: arashiyama west

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