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12 décembre 2002
Am J Primatol
Inhibition of social behavior in chimpanzees under high-density conditions
Aureli F, de Waal FB
Yerkes Regional Primate Research Center, Emory University, Atlanta
Maintenance behavior - Comportement substitutif


Introduction : A direct relation between population density and aggression has been proposed to explain the results of Calhoun's (1962) classic study of crowding in rodents. Calhoun reported that as population density increases, aggressive interactions increase as well. However, recent studies on nonhuman primates do not support a simple relation between available space and the level of aggression. These studies avoid potentially confounding variables, such as novelty of the social and/or physical environment. When well-established groups of primates are crowded into familiar areas, they do not uniformly react by increasing aggressive behavior. De Waal proposed an alternative to Calhoun's so-called density/aggression model. He argued that gregarious primates exhibit behavioral flexibility and social adjustment to environmental change. This resulted in a coping model according to which aggression may increase somewhat under higher density but severe forms of aggression will be limited. Recent findings suggest that at least two coping strategies may be used depending on the duration of the high-density condition.

Confinement of a well-established group of macaques into a familiar but smaller than usual area for a limited amount of time (i.e., from a few hours up to a few days) results in an increase in submissive behavior and huddling with companions and a reduction in allogrooming, play, and exploration of the environment. This short-term response to high population density has been interpreted as a conflict-avoidance strategy aimed at reducing the risk of aggression by decreasing the overall level of movement and social activity in an environment in which forced proximity and limited escape opportunities increase the likelihood of conflict. Long-term behavioral adjustment to high population density, on the other hand, develops when a group lives under high-density conditions for many years or generations. Under such conditions primates seem to adopt a more active tension-reduction strategy by increasing affiliative interactions, such as allogrooming to relieve tension due to high density and therefore reduce the risk of aggression.

Most studies on the effects of high population density have been carried out on Old World monkeys, particularly macaques. To our knowledge, only one published study has systematically investigated the effects of population density on the behavior of a well-established group of chimpanzees (Pan troglodytes). This study examined the responses of the Arnhem colony of chimpanzees to temporary confinement in their indoor enclosure during winters. This condition falls somewhere between short- and long-term confinement since the high-density condition lasted for about 6 months per year. Some of the behavioral changes under this medium-term high-density condition resemble the long-term responses of macaques to high density, namely an increase in allogrooming and only a slight increase in aggression.

Thus far, no systematic investigation of the short-term effects of high population density in chimpanzees has been carried out. The present study was designed to fill this gap as part of a large-scale project that aims to compare the behavioral adjustment of chimpanzees to environmental change with that of other primates. Five well-established chimpanzee groups of various composition were periodically confined for short periods into a familiar area. A variety of social interactions was recorded under both the high-density and control conditions. We also measured the rates of self-grooming, self-scratching, and yawning under the two conditions, as these behavior patterns may index social stress or anxiety. [...]

Discussion : This study suggests that chimpanzees cope with a short-term increase in population density. They reduce their overall activity level, as suggested by a decrease in time spent allogrooming and a lower frequency of pant-grunt greetings. Most importantly, they reduce their aggressive behavior along with hooting and bluff displays that can lead to charges against other group members. Hence, the response of chimpanzees to the temporary reduction of interindividual distance seems to be an overall inhibition of activity, including agonistic behavior. This result is quite in contrast to that predicted by the density/aggression model to explain increased aggression under high-density conditions. This difference from the "rodent pattern" is in line with other recent studies on primates that report the absence of a direct effect of high social density on aggressive behavior (see Introduction). Our study, however, goes further than that and actually demonstrates a decrease of agonistic behavior under high-density conditions when several potentially confounding variables are taken into account.

Some other studies have reported a decrease of aggression under higher density. However, as Erwin (1979) pointed out, factors other than density could explain this result. For example, the decrease in aggression among females in pigtail macaques when they had access to only one room of their two-roora enclosure was better explained by the fact that the male was more efficient in controlling female aggression when all the females were in the same room. In our study, all groups except one had access to more than one room under the high-density condition, so it is unlikely that the same explanation applies. Interestingly, the one group (i.e., group B) that experienced a housing condition similar to the pigtail macaques in Anderson (1977) study was the only one that did not reduce the rate of agonistic behavior under the high-density condition (note that no instance of bluff-charge and aggression was observed in this group).

The present study avoided group manipulations and unfamiliar environments to create a high-density condition. The high-density and control conditions did not fundamentally differ in the cage furnishing, feeding routines, level of human activity, and opportunities for most chimpanzees to visually separate themselves from others. In addition, there were no differences in ambient temperature, levels of neighbor vocalization, and number of females showing maximal genital swelling between the high-density and control conditions. Of possible confounding variables, the only one that presents itself is that only under the control condition had the chimpanzees access to the outdoor section of their runs. This could have allowed them to spend time observing the outside surroundings. If this difference had any impact on their social behavior, we would have expected a reduced rate of interaction with group members in the control condition because more time would have been devoted in observing the more pleasant surroundings (instead of the concrete walls of the inside). The opposite, however, was actually found: social activity was higher under the control condition. We are inclined, therefore, to interpret the differences in social behavior between the two conditions as a short-term response to the different amounts of available space.

What is the evidence that our chimpanzees actively inhibited agonistic behavior? Baker and Aureli found that chimpanzees housed under various conditions (including the subjects of the present study) were more likely to hoot, bluff-display, bluff-charge, and initiate aggression when neighboring groups produced loud vocalizations or other noisy display. The proportion of time in which minimally one neighbor chimpanzee vocalized was not différent under the highdensity and control conditions (see Methods), probably because of the large number of groups housed within auditory reach of one another at the Primate Center. The similarity in the level of neighbor vocalizations between the two conditions combined with the reduced rate of agonistie behavior under the high-density condition suggests that agonistic responses to neighbor vocalizations were inhibited. Our chimpanzees seem to actively suppress their tendency to respond to vocalizations from other groups in order to avoid hooting and bluff displays that could lead to bluff charges and aggression in an environment in which spacing opportunities were sharply reduced. This view is supported by a temporal analysis of the responses to neighbor vocalizations of chimpanzees living for long periods under two différent conditions. The chimpanzees living under higher density hooted or bluff-displayed less frequently in immediate response to neighbor vocalizations.

Further support for the notion of inhibition of agonistic behavior under higher density comes from a comparison of the findings of this study with those reported by Nieuwenhuijsen and de Waal for the Arnhem colony. The inhibition of aggression and related behavior may perhaps occur only under extremely high density. The density in the high-density and control conditions of our study was, respectively, ten and four times higher than that of the Arnhem chimpanzees in their indoor enclosure. In contrast with our study, the Arnhem chimpanzees showed an inerease of aggression under the high-density condition. There are undoubtedly various factors, such as group size, enclosure complexity, and duration of the high-density condition, which might have contributed to the différence in the changes of agonistic behavior under higher density between the two studies. It is possible, however, that the large différence in density between the two studies may account for some of the changes. Higher density may increase somewhat the frequency of aggression when movements are not too constrained by the presence of others, as suggested by the study in Arnhem. However, when interindividual distances are dramatically reduced, such as under the conditions of the present study, all social interactions, including agonistic interactions, may be suppressed.

The view of an actual inhibition of aggression under extreme density conditions is strongly supported by comparisons of aggression rates recorded in the two studies. Using exactly the same definition of aggression, the rates of Arnhem chimpanzees in both the indoor quarters and the outdoor large island were at least ten times higher than those of Yerkes chimpanzees in both the high-density and control conditions.

The behavior of the adult chimpanzees of the present study bas common féatures with the short-term responses of macaques to higher density. Chimpanzees seem to go a step further than macaques, however, in the reduction of social interactions. Whereas macaques manage to control severe forms of aggression but generally fail to limit mild forms, chimpanzees seem to successfülly reduce all forms of agonistic behavior, even behavior such as hooting that is only a potential for direct charges or aggression.

The conclusion that the suppression of agonistic behavior by chimpanzees goes beyond what bas been reported for macaques is further supported by our findings on pant-grunt greetings. Whereas an increase in submissive display results from high density in macaques, the opposite was found in the present study. The increase in submissive display in macaques bas been interpreted as part of a strategy to appease dominants and avoid escalation of aggression under circumstances in which interindividual distances are reduced. Among chimpanzees, such an appeasement strategy is less needed, as aggression and bluff charges are actually less common under higher density. The decrease of pant-grunt greetings can be interpreted, therefore, as a part of a general tendency to lower overall activity, including locomotion, to avoid potential conflict when space is reduced.

The reduction in allogrooming is a common short-terra response to high density for chimpanzees (this study) and macaques discussed the decrease in allogrooming as part of a general decrease in overall activity. In an environment where interindividual distances are reduced, the risk of receiving aggression by others while approaching potential grooming partners increases.

Macaques also decrease activity such as play which might accidentally lead one into proximity with other group members. The chimpanzees of this study, however, did not show such a decrease. Actually, juveniles increased their level of playing under high density. This difference may be related to interspecific différence in the degree of tolerance of adults toward juveniles playing or in the development of coping strategies, but data from the Arnhem colony suggest that the relation between play and density may be more complex.

In fact, the medium-term response of the Arnhem juveniles to higher density was a reduction of the time spent in social play from 31% to 22%. Surprisingly, these values are similar to those found in the present study under the high-density condition (26%). A possible explanation is that juvenile play may be strongly affected by adult activity levels. When interindividual distance is reduced and social interactions between adults increase as during winters at the Arnhem Zoo, juveniles may play less often to avoid getting in the way of potentially aggressive adults. This situation may reach an extreme under density conditions similar to those of our control condition in which time spent in social play is only 14%. However, when adult activity is dramatically reduced, as the decrease of social interactions under the high-density condition of the present study suggests, juveniles can restore their play habit by probably finding areas where there are no stationary adults.

The effectiveness of chimpanzees in coping with a short-term increase in density should not lead us to conclude that the chimpanzees are relaxed under this condition. The exuberant pandemonium of the Arnhem chimpanzees in response to their release from their winter quarters each spring described by de Waal is indicative of their preference for the larger outdoor enclosure. Our data on rough scratching and yawning, probably the most reliable behavioral indicators of anxiety in chimpanzees, support this view. The increase in the rate of these activities under the high-density condition strongly suggests that social tension increases when interindividual distances are reduced. The lower rate of gentle scratching under the high-density condition may be simply due to inaccuracy of data collection when the observer had to monitor more individuals for a rather inconspicuous behavior (see Data Collection). Another possibility is that gentle scratching indexes uncertainty related to interaction between group nierabers; its decrease under the high-density condition might then reflect the lower level of social interaction under this condition.

The existence of tensions under high density suggests that conflict-avoidance strategies are probably effective only in the short run. At least two conflictavoidance strategies seem to be used to cope with the short-terni effects of high density: Macaques use an appeasement strategy, whereas chimpanzees avoid conflîcts through an inhibition strategy. Both strategies, however, do not deal with the increase in social tension, only with the potentially negative consequences of high density. If high density is maintained for long periods, this situation probably cannot be sustained, and the strategy may need to change. The change should consist of an increase in social interactions, such as allogrooming, leading to an actual reduction of social tension. Based on the limited data available, chimpanzees seeni quicker than macaques in adopting such a tension-reduction strategy or affiliation strategy. In fact, the Arnhem chimpanzees increased their frequency of allogrooming as a medium-term. response to high density, whereas under comparable conditions a group of stumptail macaques (Macaca arctoides) did not show any change in allogrooming. If the high-density condition lasts longer, however, macaques too adopt an affiliation strategy. Studies on various macaque groups that have lived under their respective conditions for many years found higher rates of allogrooming in groups living under the higher density.

Conclusions :

  1. Chimpanzees suppress agonistic behavior as a short-term response to high density.
  2. Allogrooming and pant-grunt greetings are reduced in adult chimpanzees as a short-term response to high density, whereas juvenile play increases.
  3. Social tension increases under high density, as reflected in elevated rates of rough scratching and yawning.
  4. The changes in behavior listed under conclusions 1 and 2 may be interpreted as an inhibition strategy that reduces the risk of open conflict but does not eliminate social tensions (see conclusion 3).
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