David P. Watts

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.

Why do chimpanzees hunt and share meat

Wild chimpanzees, Pan troglodytes, frequently hunt and share meat. Despite widespread interest and considerable study, continued controversy exists regarding the factors that influence chimpanzee hunting decisions and meat sharing. Three hypotheses invoke the importance of ecological, reproductive and social factors. A nutritional shortfall hypothesis suggests that chimpanzees hunt to compensate for seasonal shortages in food availability. A second hypothesis argues that male chimpanzees hunt to obtain meat that they swap for matings. A third hypothesis proposes that males use meat as a social tool to develop and maintain alliances with other males. We tested these hypotheses using observations of an unusually large community of chimpanzees at Ngogo in Kibale National Park, Uganda. Results did not support the nutritional shortfall or meat-for-sex hypotheses. The Ngogo chimpanzees hunted primarily during times of food abundance rather than scarcity. The presence of oestrous females did not predict the tendency of chimpanzees to hunt. Furthermore, meat-for-sex exchanges occurred infrequently, and males did not gain a mating advantage through sharing meat. Additional observations were consistent with the male social bonding hypothesis. At Ngogo, male chimpanzees were likely to hunt when accompanied by other males. Males shared meat nonrandomly and reciprocally among themselves, and males exchanged meat for agonistic support. Although several factors are likely to affect chimpanzee hunting decisions and meat sharing, these results indicate that primary causes will not be found through invoking simple energetic or reproductive considerations.

Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution

Fossils and molecular data are two independent sources of information that should in principle provide consistent inferences of when evolutionary lineages diverged. Here we use an alternative approach to genetic inference of species split times in recent human and ape evolution that is independent of the fossil record. We first use genetic parentage information on a large number of wild chimpanzees and mountain gorillas to directly infer their average generation times. We then compare these generation time estimates with those of humans and apply recent estimates of the human mutation rate per generation to derive estimates of split times of great apes and humans that are independent of fossil calibration. We date the human–chimpanzee split to at least 7–8 million years and the population split between Neanderthals and modern humans to 400,000–800,000 y ago. This suggests that molecular divergence dates may not be in conflict with the attribution of 6- to 7-million-y-old fossils to the human lineage and 400,000-y-old fossils to the Neanderthal lineage.

Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda

Abstract Cooperative mate guarding by males is unusual in mammals and birds, largely because fertilizations are non-shareable. Chimpanzees live in fission-fusion communities that have cores of philopatric males who cooperate in inter-group aggression and in defending access to the females in their community. Male contest mating competition is restrained within communities, but single high-ranking males sometimes try to mate guard estrous females. Data from an unusually large chimpanzee commmunity at Ngogo, Kibale National Park, Uganda, that contains more males than any previously studied community show new variation in chimpanzee mate-guarding behavior. Contrary to expectation given the large number of males, mate guarding was as common as, or more common than, at other sites, and males other than the alpha male guarded more often. More strikingly, pairs or trios of top-ranking males sometimes engaged in cooperative aggression to prevent estrous females from mating with other males, but tolerated each others mating activities. Both single males and coalitions mostly guarded periovulatory females. Mate-guarding coalitions were previously unknown in chimpanzees. Coalitions occurred in large mating parties, seemingly because these often contained too many males for single males to maintain exclusive access to estrous females. Coalition members gained higher shares of copulations than they could have expected from solo mate guarding, and suffered lower per capita costs of guarding (as inferred from aggression rates). Two males who most often participated in coalitions formed two-male coalitions at about the point where the number of males present made it unlikely that either could get 50% or more of total copulations on his own, and formed trios when this value dropped below 33%. Kin selection could be a factor in cooperation among male chimpanzees, but coalition members were not necessarily close relatives and the apparent structure of payoffs fit that of mutualism. Furthermore, reliance of male chimpanzees on support from allies to maintain high rank could have led to trading of mating exclusivity for support against mating competitors.

BOUNDARY PATROLS AND INTERGROUP ENCOUNTERS IN WILD CHIMPANZEES

Summary Chimpanzees are among the few mammals that engage in lethal coalitionary aggression between groups. Most attacks on neighbors occur when parties made up mostly of adult males patrol boundaries of their community’ s range. Patrols have time, energy, and opportunity costs, and entail some risks despite the tendency of males to attack only when they greatly outnumber their targets. These factors may lead to a collective action problem. Potential benee ts include protection of community members, particularly infants; range expansion and increases in the amount and quality of food available; and incorporation of more females into the community. Males may not share these equally; for example, those able to obtain

Hunting Behavior of Chimpanzees at Ngogo, Kibale National Park, Uganda

Chimpanzees (Pan troglodytes) prey on a variety of vertebrates, mostly on red colobus (Procolobus spp.) where the two species are sympatric. Variation across population occurs in hunting frequency and success, in whether hunting is cooperative, i.e., payoffs to individual hunters increase with group size, and in the extent to which hunters coordinate their actions in space and time, and in the impact of hunting on red colobus populations. Also, hunting frequency varies over time within populations, for reasons that are unclear. We present new data on hunting by chimpanzees at Ngogo, Kibale National Park, Uganda, and combine them with earlier data (Mitani and Watts, 1999, Am. J. Phys. Anthropol. 109: 439–454) to examine hunting frequency and success, seasonality, and cooperation. The Ngogo community is the largest and has the most males of any known community. Chimpanzees there mostly hunt red colobus and are much more successful and make many more kills per hunt than at other sites; they kill 6–12% of the red colobus population annually. The number of kills and the offtake of meat per hunt increase with the number of hunters, but per capita meat intake is independent of hunting party size; this suggests that cheating occurs in large parties. Some behavioral cooperation occurs. Hunting success and estimated meat intake vary greatly among males, partly due to dominance rank effects. The high overall success rate leads to relatively high average per capita meat intake despite the large number of consumers. The frequency of hunts and of hunting patrols varies positively with the availability of ripe fruit; this is the first quantitative demonstration of a relationship between hunting frequency and the availability of other food, and implies that the chimpanzees hunt most when they can easily meet energy needs from other sources. We provide the first quantitative support for the argument that variation in canopy structure influences decisions to hunt red colobus because hunts are easier where the canopy is broken.

Lethal intergroup aggression leads to territorial expansion in wild chimpanzees

Summary Chimpanzees make lethal coalitionary attacks on members of other groups [1]. This behavior generates considerable attention because it resembles lethal intergroup raiding in humans [2]. Similarities are nevertheless difficult to evaluate because the function of lethal intergroup aggression by chimpanzees remains unclear. One prominent hypothesis suggests that chimpanzees attack neighbors to expand their territories and to gain access to more food [2]. Two cases apparently support this hypothesis, but neither furnishes definitive evidence. Chimpanzees in the Kasekela community at Gombe National Park took over the territory of the neighboring Kahama community after a series of lethal attacks [3]. Understanding these events is complicated because the Kahama community had recently formed by fissioning from the Kasekela group and members of both communities had been provisioned with food. In a second example from the Mahale Mountains, the M group chimpanzees acquired part of the territory of the adjacent K group after all of the adult males in the latter disappeared [4]. Although fatal attacks were suspected from observations of intergroup aggression, they were not witnessed, and as a consequence, this case also fails to furnish conclusive evidence. Here we present data collected over 10 years from an unusually large chimpanzee community at Ngogo, Kibale National Park, Uganda. During this time, we observed the Ngogo chimpanzees kill or fatally wound 18 individuals from other groups; we inferred three additional cases of lethal intergroup aggression based on circumstantial evidence (see Supplemental Information). Most victims were caught in the same region and likely belonged to the same neighboring group. A causal link between lethal intergroup aggression and territorial expansion can be made now that the Ngogo chimpanzees use the area once occupied by some of their victims.

Reciprocity and interchange in the social relationships of wild male chimpanzees

Social relationships in nonhuman primates result from investments that individuals make while pursuing fitness-maximizing strategies. These strategies sometimes include social exchange, either reciprocity (exchange of the same acts) or interchange (exchange of different acts). Individuals in many species may negotiate for services in biological markets, particularly grooming and agonistic support. They also may compete for access to valuable social partners. Abundant evidence for reciprocity in grooming and in support and for competition over partners exists, notably for females in some cercopithecines. However, evidence for interchange of grooming and support is scarcer, and apparent interchange may be a byproduct of correlations between grooming or support and some third variable (e.g. dominance rank). Chimpanzees have been prominent in discussions of social exchange, especially because male chimpanzees cooperate in many ways. Most analyses of interchange have used data on captive chimpanzees; these provide good evidence for reciprocity, but ambiguity with regard to interchange. Data on an unusually large chimpanzee community at Ngogo, Kibale National Park, Uganda, strongly support the argument that social exchange is prominent in social relationships among males. Males at Ngogo show reciprocity in grooming and support. They also interchange grooming given and support received, as well as grooming received and support given, independently of reciprocity in grooming and support and of correlations of support and grooming with dominance rank. However, most cooperation in contests with third parties took low risk forms (e.g. both participants outranked their opponent). In this, males at Ngogo resemble captive chimpanzees and female cercopithecines. Reciprocity and interchange in this context may be important in the maintenance of social bonds between males, and in attainment and maintenance of high dominance rank, but probably represent mutualism, not reciprocal altruism.

Demographic influences on the hunting behavior of chimpanzees.

We investigated hunting in an unusually large community of wild chimpanzees at Ngogo in the Kibale National Park, Uganda. Aspects of predation were recorded with respect to the prey, the predators, and hunting episodes. During 23 months of observation, the Ngogo chimpanzees caught 128 prey items from four primate and three ungulate species. Chimpanzees preyed selectively on immature red colobus primarily during group hunts, with adult males making the majority of kills. Party size and composition were significant predictors of the probability that chimpanzees would hunt and of their success during attempts. Chimpanzees were more likely to hunt red colobus if party size and the number of male hunters were large; party size and the number of male hunters were also significantly larger in successful compared with unsuccessful hunts. The Ngogo chimpanzees did not appear to hunt cooperatively, but reciprocal meat-sharing typically took place after kills. Hunts occurred throughout the year, though there was some seasonality as displayed by periodic hunting binges. The extremely high success rate and large number of kills made per successful hunt are the two most striking aspects of predation by the Ngogo chimpanzees. We compare currently available observations of chimpanzee hunting behavior across study sites and conclude that the large size of the Ngogo community contributes to their extraordinary hunting success. Demographic differences between groups are likely to contribute to other patterns of interpopulation variation in chimpanzee predation.

Lethal aggression in Pan is better explained by adaptive strategies than human impacts

Observations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) provide valuable comparative data for understanding the significance of conspecific killing. Two kinds of hypothesis have been proposed. Lethal violence is sometimes concluded to be the result of adaptive strategies, such that killers ultimately gain fitness benefits by increasing their access to resources such as food or mates. Alternatively, it could be a non-adaptive result of human impacts, such as habitat change or food provisioning. To discriminate between these hypotheses we compiled information from 18 chimpanzee communities and 4 bonobo communities studied over five decades. Our data include 152 killings (n = 58 observed, 41 inferred, and 53 suspected killings) by chimpanzees in 15 communities and one suspected killing by bonobos. We found that males were the most frequent attackers (92% of participants) and victims (73%); most killings (66%) involved intercommunity attacks; and attackers greatly outnumbered their victims (median 8:1 ratio). Variation in killing rates was unrelated to measures of human impacts. Our results are compatible with previously proposed adaptive explanations for killing by chimpanzees, whereas the human impact hypothesis is not supported.