The Expression of Aggression in Old World Monkeys. Irwin Bemstein, ~ Larry Wil]ialns) 1 and Marcy Ramsay ~. Received March 1, 1982; revised May 6, 1982.
International Journal of Primatoiogy, Vol. 4, No. 2, 1983
The Expression of Aggression in Old World Monkeys Irwin Bemstein, ~ Larry W i l ] i a l n s ) 1 and Marcy Ramsay ~ Received March 1, 1982; revised May 6, 1982
The expression o f agonistic behavior in adult and juvenile members o f both sexes was studied in groups o f from 23 to 93 animals representing Macaca mulatta, M. arctoides, M. nemestrina, M. nigra, and Cercocebus atys. Data were collected using focal animal techniques over a period o f I year f o r each group. Adult male biting was notably infrequent in all cases, and adult male participation in agonistic encounters was less frequent than f o r any other age-sex class, especially in the groups with the highest agonlstic rates. Adult male agonlstic behavior was often expressed as aggression but seldom involved contact forms o f aggression, and biting constituted the smallest proportion o f contact aggression f o r all age-sex classes. Adult males were also seldom the targets o f aggression and had the highest rates f o r shaking o f objects and bouncing displays. A tendency f o r the most severe forms o f aggressive expression to be most frequent in those animals least capable o f inflicting injury was noted in all groups, along with a tendency f o r aggression to be directed toward immature animals. Sex differences in aggressive expression and responses to aggression were noted, but the frequency o f receipt o f aggression was not directly reflected in the wounding noted. Different means to achieve the same consequence, infrequent adult male damaging attacks, are suggested to operate in the several groups studied, KEY WORDS: aggression; age-sex differences; agonistic; control of aggression; biting; cercopithecinae.
INTRODUCTION
High sociability and an aggressive temperament may seem incompatible since sociality is commonly viewed as a cohesive force, whereas aggression ~Department of Psychology, University of Georgia, Athens, Georgia 30602, and Yerkes Regional Primate Research Center, of Emory University, Atlanta, Georgia 30322. 113 0164-0291/83/0600-0113503.00/0© 1983PlenumPublishingCorporation
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is viewed as a disruptive force. Many of the most social I~ nonetheless, also recognized as the most aggressive, with cc ty to inflict serious injury. One must therefore postulate mechanisms to control the expression and limit the conseqt sion in these taxa, in addition to recognizing the complex gression in primate societies (Bcrnstein and Gordon, 19741 Theoretically there are several possible mechanisn reduce the frequency of expression of aggression behavior, forms of aggression with severe consequences. These mec individual or social and should operate most effectively on ! with the greatest potential to inflict injury. Such mechani the overall frequencies of aggression, channel expressio: damaging form, or disrupt and terminate prolonged bou more serious forms of expression. Such mechanisms may tion of aggression to extragroup targets and displacement o: other types of activities. In sexually dimorphic animals, such as the Old World males usually have the greatest potential to inflict Mechanisms which serve to reduce the consequences of at therefore operate most effectively in reducing the frequent aggression and/or in limiting adult male aggression to nonc the milder forms of contact expression. The net result shou and slashing with the canines are minimized in the adult ma although the same mechanisms may also reduce the frequ¢ aggression in other age-sex classes as well. A specific rec male aggressive participation can result from lowering th taneous expression of aggression in adult males and/or limit cy of provocations of adult males which might be expecl gressive responses. The behavioral flexibility of primates should permit t] multiple mechanisms; the identification of any one mecharL social role of control animals in limiting intragroup conflict., Bernstein (1964, 1966)] does not preclude the exist~ mechanisms. Moreover, different taxa may achieve the; reduction of individual risk of injury from adult males, th techniques. The present study reports the frequencies and expres~ sion of different age-sex categories in groups representing Macaca and one of Cercocebus. Both the frequency of exp receipt of different agonistic patterns of behavior are report¢ sex class. The four macaque species allow for tests of th mechanisms among congeneric forms in contrast to m~ tifiable in a species from a second genus in the same sut pithecinae).
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D a t a were collected over a calendar year to control for variability produced by seasonal factors. W e dealt with long-term established social groups to approximate "normal" social conditions, as opposed to the unstable conditions typical in the early stages o f group formation or the social unrest which m a y be provoked b y deliberate manipulations and challenges o f a group.
METHODS Subjects Five groups of cercopithecine monkeys served as subjects. The four m a c a q u e groups were rhesus (Macaca mulatta), stumptall (M. arctoides), pigtm.'l (M. nemestrina), and Celebes black ape (M. nigra). The fifth cercopithecine was the sooty m a n g a b e y (Cercocebus atys). Data on the rhesus and pigtail groups were collected f r o m June 1973 to M a y 1974. The stumptail and Celebes data were collected f r o m September 1974 through July 1975, and the m a n g a b e y data f r o m September 1974 through August 1975. Total group numbers fluctuated during the s t u d y due to normally occurring births and deaths. The smallest group had 23 animals and the largest had 93. Focal animal subjects were selected in each group to represent each o f the following age-sex classes--adult males, adult females, juvenile males, and juvenile f e m a l e s - a n d their numbers also varied as the animals aged. Table I shows the n u m b e r o f focal subjects. All groups had been maintained for 4 to 10 years prior to the study and multiple generations existed in each group. Juveniles were defined as those animals over 2 years o f age but less than fully adult. Inasmuch as infants (1) have the least ability to inflict inTable I. Focal Subjects by Species° Adult Males
Immature
Females Males Females
Rhesus 8 5-6 6 3-4 Stumptalls 4 6 5 2 Pigtails 6-7 6-7 2-4 2-3 Celebes 5 5 3 3 Mangabeys 5 5 5 2-3 ~Numbers varied due to deaths and age changes during the study. Numbers reflect the number of animals of each age-sex class scored at one time. The actual number of subjects in some cases exceeds the number shown, as animals entered and left the juvenile classes during the course of the study.
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juries, (2) may be ontogenetically unable to show many f~ expression, and (3) may be difficult to distinguish as the ta expressions when riding on their mothers, no data were coI A conservative criterion of 2 years of age as the end of int ensure that all juveniles would be relatively independent and unlikely to be spending any time carded by their mo~ Apparatus
The animals were maintained at the Yerkes Regio search Center Field Station. Each group lived in an outdoo~ attached indoor quarters. The largest groups were housed i~ pounds with 3 x 10-m indoor quarters. The other groups 30 x 30-m compounds with 3 x 10-m indoor quarters. All surrounded by chain-link and sheet-metal fences which from physical contact with other groups. Monkey chow available ad libitum and fresh fruits and vegetables were p: day, but not during test sessions. The groups were subjo routines of the laboratory and the males were captured om obtain a blood sample for testosterone assays. Procedure
Each of the focal animals was scored during ten 5-n month. A def'med list of responses, previously demonstrate with 90°7o or better interobserver agreement, was used t( what to whom, in any sequence involving the focal animal volvement was also scored whenever an animal interactl animal while already interacting with an animal being sco~ For purposes of analysis, the open-mouth stare was sc This threat response was combined with chases and labelec gression. Contact aggression consisted of manual forms, and pulling, and biting. Scores for contact and noncontact sion were totaled to produce a larger category, total aggress was divided into avoiding and the stronger forms which and grimacing. Scores for aggression and submission wet duce a score for total agonistic, using agonistic in the orig gression and responses to aggression. In the event of comp such as fights which involved multiple aggressive responses i the episode was scored according to the strongest form pressed.
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RESULTS Although the rate of participation in agonistic encounters varied from 1.5 t o 5.1 per subject per hr across the five groups, the hourly rate of adult male biting never exceeded one time in 5 hr (0.2/hr) and the rate at which adult males bit others in their groups tended to be the lowest among the four age-sex classes. The hourly rate of biting per subject across groups did not exceed three times per 10 hr of observation (0.3/hr). The hourly rate of adult male participation in agonistic encounters varied between 1.3 and 3.7 and tended to be lower than that of the other age-sex classes. Adult males had the lowest rates of participation in the rhesus and stumptail groups, the two groups with the highest overall mean rates of agonistic episodes. Adult male participation in these episodes was more likely to involve aggression (45 to 92070 of male participation was expressed as aggression) than was the case for the other age-sex classes (13 to 62070)~ Although adult males did express from 25 to 35°70 (median, 29070) of their aggression in forms involving contact responses, this was less than the median percentage channeled into contact forms of aggression by adult females (41070), immature males (44070), or immature females (440/0). More important, adult male contact aggression involved biting in only 17070of the cases, whereas adult females did so in 29070, immature males in 24070, and immature females in 37070 of the cases. The percentage of adult male aggression expressed as biting was therefore the lowest for all age-sex classes. One reason perhaps that adult males were less often active participants in agonistic encounters was that they were not often the targets of agonistic behavior. Agonistic responses were directed toward them at rates of 1.3 to 3.4 per hr per male, but very few were in the form of aggression; adult males received aggressive responses only one to five times for each l0 hr (0.1-0.5/hr) of observation, the lowest rates received for any of the age-sex classes. Moreover, they received the least contact aggression and, in no group, received more than one response per l0 hr of observation (0.1/hr). Adult males were also bitten least often of all age-sex classes (except in the mangabeys, where no subjects were observed to receive a bite in several age-sex classes, including the adult males). These data are summarized in Tables II-IV. Overall, immature animals were more often engaged in agonlstic encounters than were adults. In three groups (except the rhesus and pigtails), juvenile males were more aggressive than juvenile females. Juvenile females were more often the targets of aggression than were juvenile males in three groups (except the rhesus and stumptails). In all groups, however, less than one-half of the aggression involved physical contact (from 30070 in pigtails to 44070 in stumptails), and biting accounted for less than half of all contact
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Table II. Hourly Rates of Expression per Subject Agonistic Aggressive Contact aggression Biting
Rhesus 5.1 1.8 0,6 0.3
Stumptail Pigtail Celebes 4.4 1.5 2.3 2.5 0.8 1.0 1.1 0.2 0.4 0.2 0.1 0.1
aggression. Moreover, in the three groups With the highesl tact aggression, the lowest percentages involved biting. I m with the least capacity to inflict severe injury, expressed I centage o f aggression in forms involving contact (44%). In were involved as aggressors in fewer agonistic encounter~ mature males (25 and 56o70, respectively), but when i m m a pressed aggression they bit more often than did any oth~ 07°70). Although not scored as an aggressive or agonistic res shaking o f the cage wire, or other objects, was noted t o , quently among the males than among the females. Expres,, their aggressive behavior, females shook objects about 1 t aggressive expressions, whereas adult males shook objects and juvenile males shook objects more than once for ever3 responses they showed.
Summary Description of the Five Groups Rhesus The rhesus group had the highest rate o f agonistic animal/hr) but expressed only 35°7o as aggression. Rhesus lowest ratios o f aggression to total agonistic responses comp; males. As in the other groups, juvenile animals were most o: and adult males least often, but along with higher rates o f males received more aggression than in other groups. Table HI. Hourly Rate at Which Adult Males Did Each of the Indic~ Rhesus Stumptail Pigtail Celebes Agonistic 3.1 3.7 1.7 1.3 Aggressive 1.4 3.4 0.8 0.9 Contact aggression 0.4 1.2 0.2 0.2 Biting 0.2 0.2 < 0.05 < 0.05
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Table IV. Hourly Rate at Which Adult Males Received Each of the Indicated Categories Rhesus Agonistic Aggressive Contact aggression Biting
3.4 0.5 0.1 < 0.05
Stumptail 2.4 0.3 0.1 0.1
Pigtail 1.6 0.4
