Elisabeth H. M. Sterck

The evolution of female social relationships in nonhuman primates

Abstract Considerable interspecific variation in female social relationships occurs in gregarious primates, particularly with regard to agonism and cooperation between females and to the quality of female relationships with males. This variation exists alongside variation in female philopatry and dispersal. Socioecological theories have tried to explain variation in female-female social relationships from an evolutionary perspective focused on ecological factors, notably predation and food distribution. According to the current “ecological model”, predation risk forces females of most diurnal primate species to live in groups; the strength of the contest component of competition for resources within and between groups then largely determines social relationships between females. Social relationships among gregarious females are here characterized as Dispersal-Egalitarian, Resident-Nepotistic, Resident-Nepotistic-Tolerant, or Resident-Egalitarian. This ecological model has successfully explained differences in the occurrence of formal submission signals, decided dominance relationships, coalitions and female philopatry. Group size and female rank generally affect female reproduction success as the model predicts, and studies of closely related species in different ecological circumstances underscore the importance of the model. Some cases, however, can only be explained when we extend the model to incorporate the effects of infanticide risk and habitat saturation. We review evidence in support of the ecological model and test the power of alternative models that invoke between-group competition, forced female philopatry, demographic female recruitment, male interventions into female aggression, and male harassment. Not one of these models can replace the ecological model, which already encompasses the between-group competition. Currently the best model, which explains several phenomena that the ecological model does not, is a “socioecological model” based on the combined importance of ecological factors, habitat saturation and infanticide avoidance. We note some points of similarity and divergence with other mammalian taxa; these remain to be explored in detail.

Female dominance relationships and food competition in the sympatric Thomas langur and long-tailed macaque

Aggressive interactions can serve to secure resources. These interactions determine female dominance relationships, which have been related to the monopolizability of food patches. Patches of medium size, relative to group size, cause within-group contest competition which is hypothesized to produce linear, nepotistic and formalized dominance relationships. Small dispersed or very large and abundant patches lead to reduced within-group contest competition which should lead to egalitarian and individualistic dominance relationships without a formal hierarchy. This relation was investigated in two sympatric primate species at Ketambe, Northern Sumatra: the Thomas langur (Presbytis thomasi) and the long-tailed macaque (Macaca fascicularis). The female dominance relationships of the two species differed as predicted. Both species engaged in competitive interactions for food. The Thomas langurs competed in small patches, but not in large patches. These large patches could be considered abundant. About two-thirds of their food patches incited contest competition. Long-tailed macaques were aggressive in fruit patches, irrespective of size. Most food patches incited contest competition. Contest competition was probably more important for macaque females than for langur females. Outside food patches macaque females were more aggressive than langurs, whereas inside food patches aggression rates were similar.

Determinants of female dispersal in Thomas langurs

Female dispersal occurs in a number of primate species. It may be related to: avoidance of inbreeding, reduction in food competition, reduction of predation risk, or avoidance of infanticide in combination with mate choice. Female dispersal was studied for a 5‐year period in a wild population of Thomas langurs (Presbytis thomasi) that lived in one‐male multi‐female groups. Juvenile and adult individuals of both sexes were seen to disperse. Females appeared to transfer unhindered between groups, mostly from a larger group to a recently formed smaller one. They transferred without their infants and when not pregnant, and seemed to transfer preferentially during periods when extra‐group males were harassing their group. During these inter‐group encounters extra‐group males seemed to try to commit infanticide. Thus, the timing of female transfer was probably closely linked to infanticide avoidance. Moreover, females seemed to transfer when the resident male of their group was no longer a good protector. The observations in the present study suggest that females transferred to reduce the risk of infanticide. Female dispersal may have another ultimate advantage as well, namely inbreeding avoidance. Due to the dispersal of both females and males the social organization of Thomas langurs was rather fluid. New groups were formed when females joined a male; male takeovers were not observed. Bisexual groups had only a limited life span, because all adult females of a bisexual group could emigrate. This pattern of unhindered female dispersal affects male reproductive strategies, and in particular it might lead to infanticidal behavior during inter‐group encounters. Am. J. Primatol. 42:179–198, 1997.

Female dispersal, social organization, and infanticide in langurs: Are they linked to human disturbance?

Female dispersal in gregarious animals can involve the desertion of a site, desertion of a social group, or both. Group desertion may be related to inbreeding avoidance. Group fidelity may result from cooperation among females in a group. Site fidelity will be more likely when food can be monopolized and when the population density is close to habitat saturation. The degree of habitat saturation was approximated with a measure of human disturbance. The influence of these various factors on the incidence of female dispersal was investigated for langur populations using data from the literature. The results suggest that female dispersal in langurs involved site desertion, not group desertion. The incidence of female dispersal may affect the social organization of langurs. I propose that when females do not disperse, male takeovers prevail, whereas in populations where female dispersal regularly occurs bisexual groups are disbanded or new groups are formed, a process I call female split‐merger. Male takeover is thought to occur when site fidelity is high, female split‐merger when site fidelity is low. These processes were indeed found to occur in these circumstances. The dispersal of females might prevent infanticide, whereas male takeover might promote it. Indeed, in studies with male takeover, more infants fell victim to infanticide than in studies with female split‐merger. Therefore, female dispersal in langurs is an effective female counterstrategy to infanticide. The factor that had the most profound effect on female dispersal, social organization, and infanticide was habitat saturation. Habitat saturation was measured as the degree of human disturbance, and its influence on the behavior of langurs is probably of relatively recent date. This may lead to an evolutionary transient situation and may explain the discrepancy between current socioecological theories and the behavior of langurs in populations lacking female dispersal. Am. J. Primatol. 44:235–254, 1998.

Generous leaders and selfish underdogs: Pro-sociality in despotic macaques

Actively granting food to a companion is called pro-social behavior and is considered to be part of altruism. Recent findings show that some non-human primates behave pro-socially. However, pro-social behavior is not expected in despotic species, since the steep dominance hierarchy will hamper pro-sociality. We show that some despotic long-tailed macaques do grant others access to food. Moreover, their dominance hierarchy determines pro-social behavior in an unexpected way: high-ranking individuals grant, while low-ranking individuals withhold their partner access to food. Surprisingly, pro-social behavior is not used by subordinates to obtain benefits from dominants, but by dominants to emphasize their dominance position. Hence, Machiavellian macaques rule not through “fear above love”, but through “be feared when needed and loved when possible”.

HOW ADAPTIVE OR PHYLOGENETICALLY INERT IS PRIMATE SOCIAL BEHAVIOUR? A TEST WITH TWO SYMPATRIC COLOBINES

[Socio-ecological theories predict that females adapt their social behaviour to their environment. On the other hand, as a result of phylogenetic inertia, social behaviour may be slow to catch up when the environment changes. If social behaviour is adapted to the environment, competition and co-operation among females is predicted to reflect the characteristics of food sources. Contest competition both between and within groups is expected to result in alliances among related, philopatric, females. We compared social relationships and food characteristics of two sympatric and congeneric primate species, the red colobus and the black-and-white colobus of the Tai National Park, Ivory Coast. We found that affiliative interactions among females were comparable between the species. The differences in food characteristics could explain why black-and-white females competed more often than did red colobus females, both at the intra- and inter-group level. In contrast to socio-ecological theory, female inter-group aggression was not linked to female philopatry in black-and-white colobus. The species differed from each other and from other populations of the same or closely related species with respect to their inter-group behaviour which indicates that phylogenetic inertia did not constrain this aspect of social behaviour., Socio-ecological theories predict that females adapt their social behaviour to their environment. On the other hand, as a result of phylogenetic inertia, social behaviour may be slow to catch up when the environment changes. If social behaviour is adapted to the environment, competition and co-operation among females is predicted to reflect the characteristics of food sources. Contest competition both between and within groups is expected to result in alliances among related, philopatric, females. We compared social relationships and food characteristics of two sympatric and congeneric primate species, the red colobus and the black-and-white colobus of the Tai National Park, Ivory Coast. We found that affiliative interactions among females were comparable between the species. The differences in food characteristics could explain why black-and-white females competed more often than did red colobus females, both at the intra- and inter-group level. In contrast to socio-ecological theory, female inter-group aggression was not linked to female philopatry in black-and-white colobus. The species differed from each other and from other populations of the same or closely related species with respect to their inter-group behaviour which indicates that phylogenetic inertia did not constrain this aspect of social behaviour.]

Inequity aversion in relation to effort and relationship quality in long‐tailed Macaques (Macaca fascicularis)

Social animals may employ evolved implicit rules to maintain a balance between cooperation and competition. Inequity aversion (IA), the aversive reaction to an unequal distribution of resources, is considered such a rule to avoid exploitation between cooperating individuals. Recent studies have revealed the presence of IA in several nonhuman species. In addition, it has been shown that an effort is crucial for this behavior to occur in animals. Moreover, IA may well depend on the partners identity. Although dominant individuals typically monopolize food, subordinate individuals obtain less preferred food and usually do not protest. Furthermore, “friends” may pay less attention to equity than “nonfriends.” We tested whether long‐tailed macaques show IA with different cost–benefit ratios. In addition, we determined whether IA depends on relationship quality (RQ). Dominant subjects expressed IA only when a small effort was required. At a very large effort, however, long‐tailed macaques did not show IA, possibly owing to bottom effects on the number of rewards they aim to receive. Moreover, and contrary to our predictions, an individuals inequity response was similar when tested with a “friend” or a “nonfriend.” Therefore, we conclude that long‐tailed macaques show IA only in conditions of moderate effort, yet that IA seems independent of RQ. Furthermore, IA may not be domain specific. Altogether, IA may be a trait present in all species that habitually cooperate, independent of their social organization.

Food competition between wild orangutans in large fig trees

Orangutans are usually solitary. However, occasionally aggregations are formed, especially in large fruiting fig trees. Individuals in these aggregations may experience scramble or contest competition for food. We investigated the type and strength of food competition in large figs among wild Sumatran orangutans. Adult males foraged more efficiently than adult females and subadult males did. The availability of ripe fruit is positively related to the number of orangutans visiting a fig tree and their foraging efficiency. The number of orangutans in a fig tree did not affect patch residence time and foraging behavior, though orangutans spent more time feeding when aggregation size increased in a fig tree. Dominance relationships could be measured in a number of dyads. Differences in dominance did not affect foraging behavior. The patch residence time of subordinate individuals was reduced on days that a dominant individual also visited the fig. In conclusion, orangutans seem to adjust aggregation size to the number of available ripe fruits in a fig tree in such a way that scramble competition was absent. Contest competition determined access to large fig trees.

Playbacks of loud calls to wild Thomas langurs (Primates; Presbytis thomasi): The effect of familiarity

Animals may behave aggressively towards neighbours. For several bird species it has been shown that males react more vigorously towards calls of neighbours from the centre of their home range than from the edge. This is usually explained by assuming that the centre of a home range is of higher value to a male than the edge. To test these ideas for a primate species, we conducted experiments with playbacks of loud calls on wild male and female Thomas langurs (Presbytis thomasi). These animals may defend resources in their range or protect their offspring from infanticide and males may defend their females. In natural situations between-group encounters in the centre of a home range by the intruding neighbour are more often accompanied by infanticidal attempts than encounters at the edge. Loud calls of neighbours played back from the centre of the home range caused a more vigorous reaction from the resident male than calls from the edge. However, males in food-containing trees did not respond differently to edge playbacks from males in non-food-containing trees. Although males seem to defend resources and not mates, male behaviour may be best explained by defence of infants against infanticide. Female behaviour is best explained by resource defence.

Post‐conflict third‐party affiliation in chimpanzees: what's in it for the third party?

Affiliative behavior after conflicts between conflict participants and other group members is common in many primate species. The proposed functions for such triadic interactions are numerous, mostly concerning the benefit for the former conflict opponents. We investigated post‐conflict third‐party affiliation (TPA) in captive chimpanzees (Pan troglodytes) with the aim of assessing what the affiliating third parties may gain from affiliation. Specifically, we tested whether third‐party‐initiated affiliation protects the third parties from further aggression by conflict opponents. We found support for this “self‐protection hypothesis,” in that third parties selectively directed affiliation to those opponents who more often gave further aggression to them, and affiliation effectively decreased their chance of receiving aggression from these opponents. However, a subset of affiliation, provided to conflict victims by their own kin, appeared to not be self‐protective and the function of it remained open. We conclude that chimpanzee third‐party‐initiated affiliation is a more heterogeneous behavior than thus far assumed. Am. J. Primatol. 71:409–418, 2009.