Lethal intergroup aggression by chimpanzees in Kibale National Park, Uganda

Chimpanzees (Pan troglodytes) have hostile intergroup relations throughout most or all of their geographic range. Hostilities include aggressive encounters between members of neighboring communities during foraging and during patrols in which members of one community search for neighbors near territory boundaries. Attacks on neighbors involve coalitions of adult males, and are sometimes fatal. Targets include members of all age/sex classes, but the risk of lethal intergroup coalitionary aggression is highest for adult males and infants, and lowest for sexually swollen females. The best-supported adaptive explanation for such behavior is that fission-fusion sociality allows opportunities for low-cost attacks that, when successful, enhance the food supply for members of the attackers' community, improve survivorship, and increase female fertility. We add to the database on intergroup coalitionary aggression in chimpanzees by describing three fatal attacks on adult males, plus a fourth attack on an adult male and an attack on a juvenile that were almost certainly fatal. Observers saw four of these attacks and inferred the fifth from forensic and behavioral evidence. The attackers were males in two habituated, unprovisioned communities (Ngogo and Kanyawara) in Kibale National Park, Uganda. We also summarize data on other intercommunity attacks at Ngogo. Our observations are consistent with the "imbalance of power" hypothesis [Manson & Wrangham, Current Anthropology 32:369-390, 1991] and support the argument that lethal coalitionary intergroup aggression by male chimpanzees is part of an evolved behavioral strategy.     

New cases of inter-community infanticide by male chimpanzees at Ngogo,Kibale National Park,Uganda

Infanticide by males has been recorded in four chimpanzee populations, including that in Kibale National Park, Uganda. Some infanticidal attacks occur during inter-community aggression. The sexual selection hypothesis does not easily explain these attacks because they may not directly increase male mating opportunities. However, females in the attackers’ community may benefit by expanding their foraging ranges and thereby improving their reproductive success; thus infanticide may increase male reproductive success indirectly. We report two new cases of infanticide by male chimpanzees at Ngogo, Kibale National Park. Like two previous cases, these occurred during a boundary patrol and were almost certainly between-community infanticides. The patrolling males attacked despite the proximity of males from the victims’ presumed community. This probably explains why, unlike the earlier cases, they did not completely cannibalize their victims. Such attacks seem to be relatively common at Ngogo and infanticide may be an important source of infant mortality in neighboring communities. Our observations cannot resolve questions about the sexual selection hypothesis. However, they are consistent with the range expansion hypothesis: the infanticides occurred during a period of frequent encounters between communities associated with a mast fruiting event, and Ngogo community members greatly increased their use of areas near the attack site during another mast fruiting event one year later. Our observations contribute to growing evidence that lethal intergroup aggression is a common characteristic of wild chimpanzee populations.     

Female competition in chimpanzees

Female chimpanzees exhibit exceptionally slow rates of reproduction and raise their offspring without direct paternal care. Therefore, their reproductive success depends critically on long-term access to high-quality food resources over a long lifespan. Chimpanzee communities contain multiple adult males, multiple adult females and their offspring. Because males are philopatric and jointly defend the community range while most females transfer to new communities before breeding, adult females are typically surrounded by unrelated competitors. Communities are fission–fusion societies in which individuals spend time alone or in fluid subgroups, whose size depends mostly on the abundance and distribution of food. To varying extents in different populations, females avoid direct competition by foraging alone or in small groups in distinct, but overlapping core areas within the community range to which they show high fidelity. Although rates of aggression are low, females compete for space and access to food. High rank correlates with high reproductive success, and high-ranking females win direct contests for food and gain preferential access to resource-rich sites. Females are aggressive to immigrant females and even kill the newborn infants of community members. The intensity of such aggression correlates with population density. These patterns are compared to those in other species, including humans.     

Wounding aggression during the formation and maintenance of captive,multimale chimpanzee groups

Although the multimale community is the natural social organization of chimpanzees, both wild and captive adult males have killed other adult males and infants in intercommunity conflicts and intragroup aggression. Despite the potential for serious aggression, the formation of captive, multimale social groups is desirable for the efficient, long-term, humane housing of chimpanzees in socially and physically enriched environments and for the education of zoo visitors. The University of Texas Science Park (UTSP) has maintained multimale groups of chimpanzees for 14 years. In the UTSP outdoor corral housing, multimale/multifemale social groups of unrelated adult and adolescent chimpanzees (42 F, 46 M) were formed by a series of 397 individual introductions. Wounding aggression was minimal during introductions of females to males or other females and upon male-male introductions of formerly single-caged adolescent and young adult males having had long-term prior visual familiarity. Serious wounding occurred during male-male introductions when there were major discrepancies in the age and social experience of the subjects or when adult, socially experienced males were reintroduced to former group mates following lengthy separations. Male wounding in the eight established long-term groups of 5–11 adults (2–7 males) averaged 1.4 episodes per male-year of residence; 14% of male wounding episodes required surgical therapy. Adult wounding was significantly associated with the presence of one or more group females with maximally tumescent genital swellings. No male-perpetrated infanticides occurred. Not all multimale groupings are successful, but the majority of formerly laboratory-housed chimpanzees may live and reproduce safely in multimale groups. Experience with all-male groups at UTSP suggests that bachelor groups are also practical for long-term housing. © 1995 Wiley-Liss, Inc.     

Death of a wild chimpanzee community member: possible outcome of intense sexual competition

Our observations strongly support the view that a lethal gang attack occurred against a young adult male within a wild chimpanzee (Pan troglodytes schweinfurthii) community. This is the first report of such an occurrence. At least three adult male chimpanzees are believed to have been involved in the attack. This case is unusual because the attack was fatal, involved directed group aggression within a community, and was not linked to the overthrow of the alpha male. During the period before the attack, the percentage of cycling females in the community was very low (15 males:17 females, a maximum of two regularly cycling). This fact, coupled with the presence of one female in full genital tumescence, may have incited and escalated the violence of the attack. The lethal attack is interpreted as an act of intra-community male sexual competition resulting in the complete exclusion of one male from estrous females.     

Spontaneous heart disease in the adult chimpanzee (Pan troglodytes)

Background  A high incidence of heart disease, especially idiopathic cardiomyopathy (IC), is seen in chimpanzees ( Pan troglodytes ).
Methods  We reviewed clinical records and necropsy reports of 87 adult chimpanzees for possible causes of heart disease/IC. We examined age, sex, cause of death, weight, diet, environment, infectious diseases, experimental uses and clinical pathology.
Results  The overall prevalence of heart disease in chimpanzees was 67.81%; the prevalence of IC was 51.72%. The prevalence of IC was significantly higher in males (60.32%) than that in females (29.17%, P  = 0.009). The prevalence of other heart disease was higher in females (25%) than that in males (12.70%, P  = 0.165). Heart failure occurred in 47.13% of chimpanzees. Heart disease was the primary cause of death in 34.49% of chimpanzees; 29.88% died of unknown causes.
Conclusions  We found no evidence that diet, environment, viral agents, experimental use or disease exposure contributed to the deaths resulting from IC in chimpanzees.     

Impact of simian immunodeficiency virus infection on chimpanzee population dynamics

Like human immunodeficiency virus type 1 (HIV-1), simian immunodeficiency virus of chimpanzees (SIVcpz) can cause CD4+ T cell loss and premature death. Here, we used molecular surveillance tools and mathematical modeling to estimate the impact of SIVcpz infection on chimpanzee population dynamics. Habituated (Mitumba and Kasekela) and non-habituated (Kalande) chimpanzees were studied in Gombe National Park, Tanzania. Ape population sizes were determined from demographic records (Mitumba and Kasekela) or individual sightings and genotyping (Kalande), while SIVcpz prevalence rates were monitored using non-invasive methods. Between 2002-2009, the Mitumba and Kasekela communities experienced mean annual growth rates of 1.9% and 2.4%, respectively, while Kalande chimpanzees suffered a significant decline, with a mean growth rate of -6.5% to -7.4%, depending on population estimates. A rapid decline in Kalande was first noted in the 1990s and originally attributed to poaching and reduced food sources. However, between 2002-2009, we found a mean SIVcpz prevalence in Kalande of 46.1%, which was almost four times higher than the prevalence in Mitumba (12.7%) and Kasekela (12.1%). To explore whether SIVcpz contributed to the Kalande decline, we used empirically determined SIVcpz transmission probabilities as well as chimpanzee mortality, mating and migration data to model the effect of viral pathogenicity on chimpanzee population growth. Deterministic calculations indicated that a prevalence of greater than 3.4% would result in negative growth and eventual population extinction, even using conservative mortality estimates. However, stochastic models revealed that in representative populations, SIVcpz, and not its host species, frequently went extinct. High SIVcpz transmission probability and excess mortality reduced population persistence, while intercommunity migration often rescued infected communities, even when immigrating females had a chance of being SIVcpz infected. Together, these results suggest that the decline of the Kalande community was caused, at least in part, by high levels of SIVcpz infection. However, population extinction is not an inevitable consequence of SIVcpz infection, but depends on additional variables, such as migration, that promote survival. These findings are consistent with the uneven distribution of SIVcpz throughout central Africa and explain how chimpanzees in Gombe and elsewhere can be at equipoise with this pathogen.     

New Intercommunity Infanticides by the Chimpanzees of Ngogo,Kibale National Park,Uganda

Hostile intercommunity relations, including attacking and killing extra-community infants of both sexes have occurred at most wild chimpanzee sites. We describe three recent cases of intercommunity attacks on infants committed by members of the Ngogo chimpanzee community in Kibale National Park, Uganda. Two of the attacks resulted in confirmed infanticides while a third attack probably resulted in the infant's death. In common with previous accounts of chimpanzee infanticides, the attacks described here occurred during boundary patrols outside the Ngogo community's usual range, adult and adolescent males were the main participants, one infant was cannibalized after being killed, and the victims’ mothers did not accompany the attacking party back to the Ngogo range. However, the patrol parties during each infanticide were larger than before and included females from the Ngogo community. Our observations indirectly support both the range expansion and imbalance of power hypotheses, which address why and under which conditions chimpanzee intercommunity encounters lead to aggression. These cases of intercommunity infanticide add to the growing database of the phenomenon in wild chimpanzees.     

The development of affiliative and coercive reproductive tactics in male chimpanzees

Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.     

New Cases of Intergroup Violence Among Chimpanzees in Gombe National Park,Tanzania

Despite considerable attention to chimpanzee intergroup violence, the number of observed cases remains small. We report 4 cases of intergroup violence that occurred in Gombe National Park, Tanzania, between 1993 and 2002. We observed (3 cases) or inferred (1 case) males from the Kasekela community to attack members of their 2 neighboring communities: Mitumba and Kalande. In 1993, Kasekela males killed and ate a female infant from Mitumba. In 1998, Kasekela males captured 2 infants (sex unknown) from Kalande, one of which escaped and the other was killed and eaten. Also in 1998, Kasekela males attacked an adolescent male from Kalande. The victim was alive but severely injured by the end of the attack. The intensity and duration of the attack are comparable to other attacks that resulted in fatal injuries. In 2002, observers found the body of an adolescent male from Mitumba following an incursion by Kasekela males into the area. The injuries inflicted on the Mitumba male together with circumstantial evidence suggest that Kasekela males killed him. The attacks support the view that intergroup violence is a persistent feature of chimpanzee societies and that the primary benefit attackers gain from them is reduced competition for resources.     

Fatal Chimpanzee Attack in Loango National Park,Gabon

In some populations, chimpanzees engage in lethal aggression within and between social units. We report a fatal attack on an adult male chimpanzee at a new research site in Loango National Park, Gabon. We found a fresh corpse of an adult male chimpanzee only a few hundred meters from the research camp, after noting numerous vocalizations and chimpanzee movements the previous evening. Previous contacts with chimpanzees and fresh tracks in the area around the corpse suggest that 2 communities of chimpanzees range where the attack occurred and that members of the neighboring community killed the chimpanzee. To support the conclusion, we conducted genetic analysis for 13 Y-chromosome loci and 9 microsatellite loci of fecal samples from the dead individual, 5 possible attackers, and 2 members of the other community Though we cannot exclude the possibility of an intracommunity killing, the combined observational and genetic evidence suggest an intercommunity attack. The case study adds to the growing evidence that intercommunity killings are a rare but widespread phenomenon among chimpanzees and not an artifact of human provisioning or habituation.     

Intra‐community coalitionary lethal attack of an adult male southern muriqui (Brachyteles arachnoides)

We report on the first evidence of intra‐community coalitionary lethal aggression in muriquis (Brachyteles). The event occurred in southern muriquis (Brachyteles arachnoides) during a long‐term study (>15 years) of two social groups inhabiting mostly pristine Atlantic forest habitat in the Parque Estadual Carlos Botelho, southern São Paulo State, Brazil. The attack took place deep in the core area of the Group Caetê home range. Tense agonistic behaviors and vocalizations preceded the lethal coalitionary attack, and the tension increased over a 36–48 hr period. One adult female and two unidentified individuals also took part in a coalition led by six adult males. The members of the coalition collectively approached, embraced, immobilized and repeatedly bit the entire body of an adult male, resulting in severe bleeding injuries and the victim's death in less than 1 hr after the attack commenced. Combined ecological, behavioral and spatial data related to the event indicate that this was an intra‐community attack and suggest social tensions related to mating competition as the proximate trigger of the coalitionary killing. The attack resembled those reported for chimpanzees, with clear numeric superiority and a low risk of injury to aggressors, resulting in the death of a lone conspecific victim. This observation (n=1) is suggestive of a capacity for escalated aggression in muriquis and reinforces arguments for the potential adaptive significance of intra‐community aggression in male philopatric societies, as reported for spider monkeys and chimpanzees. These characteristics challenge the view of the muriquis as a peaceful primate and support the general hypothesis that imbalances of power contribute to intra‐specific killing in primates, such as chimpanzees and humans. Am. J. Primatol. 71:860–867, 2009. © 2009 Wiley‐Liss, Inc.     

Infanticide and cannibalism by male chimpanzees at Ngogo, Kibale National Park, Uganda

Researchers have documented infanticide by adult males in four wild chimpanzee populations. Males in three of these have killed infants from outside of their own communities, but most infanticides, including one from Kanyawara, in Kibale National Park, Uganda, took place within communities. Here we report two new cases of infanticide by male chimpanzees at a second Kibale site, Ngogo, where the recently habituated chimpanzee community is the largest yet known. Both infanticides happended during boundary patrols, which occur at a high frequency there. Patrolling males attacked solitary females who were unable to defend their infants successfully. The victims were almost certainly not members of the Ngogo community. Males cannibalized both infants and completely consumed their carcasses. These observations show that infanticide by males is widespread in the Kibale population and that between-community infanticide also happens there. We discuss our observations in the context of the sexual selection hypothesis and other proposed explanations for infanticide by male chimpanzees. The observations support the arguments that infanticide has been an important selective force in chimpanzee social evolution and that females with dependent infants can be at great risk near range boundaries, but why male chimpanzees kill infants is still uncertain.     

Comparative rates of violence in chimpanzees and humans

This paper tests the proposal that chimpanzees (Pan troglodytes) and humans have similar rates of death from intraspecific aggression, whereas chimpanzees have higher rates of non-lethal physical attack (Boehm 1999, Hierarchy in the forest: the evolution of egalitarian behavior. Harvard University Press). First, we assembled data on lethal aggression from long-term studies of nine communities of chimpanzees living in five populations. We calculated rates of death from intraspecific aggression both within and between communities. Variation among communities in mortality rates from aggression was high, and rates of death from intercommunity and intracommunity aggression were not correlated. Estimates for average rates of lethal violence for chimpanzees proved to be similar to average rates for subsistence societies of hunter–gatherers and farmers. Second, we compared rates of non-lethal physical aggression for two populations of chimpanzees and one population of recently settled hunter–gatherers. Chimpanzees had rates of aggression between two and three orders of magnitude higher than humans. These preliminary data support Boehms hypothesis.     

Female Mate Preferences Among Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park, Uganda

Studies of reproduction among chimpanzees traditionally have focused on the mating strategies of males. However, less is known about the mating strategies of female chimpanzees and whether they demonstrate mate choice. I investigated sexual behavior and female mate preference in the chimpanzees of the Kanyawara community. To estimate mate preferences, I analyzed female proceptivity and resistance rates of 6 estrous females toward a total of 13 males as well as male solicitation and aggression rates toward females. Males solicited some females more often than others for mating and preferred them throughout estrus, not only during the periovulatory period (POP), when conception was most likely. In contrast, though females had strong mate preferences in both non-POP and POP, their mate preferences were not consistent between the 2 phases. The shift in mate preferences is evidence of a promiscuous yet tactical mating strategy to confuse paternity. Further, females were more proceptive and generally less resistant toward eschewed males in non-POP and more proceptive and less resistant toward preferred males in POP. Hence, the results indicate that females attempted to mate selectively during the fertile phase. Kanyawara female chimpanzees appear to change their mating strategies and selectivity during estrus and thus may pursue a mixed reproductive strategy. The tactic may allow females to deceive males, indicating that promiscuity among chimpanzee females may be more strategic than previously thought.     

Rates of predation on mammals by gombe chimpanzees, 1972–1975

Rates of chimpanzee predation on mammals are calculated using data on 75 kills recorded during focal observation in Gombe National Park, Tanzania, from January 1972 to April 1975. The chimpanzees were members of two study communities (Kanyawara, or Northern, and Kahama, or Southern, community), and were observed as focal individuals for 14,583 hr by more than 30 researchers and field assistants working in pairs. The rate of predation by females was too low to allow reasonable estimates. For males, the mean rate of killing during the study period was 0.31 kills per male per 100 hr (N=17 males), or 4.65 kills per 100 hr in the two communities. In contrast to results from Mahale Mountains, there was no difference in predation rate between wet and dry seasons. However, predation rates varied over time, increasing by four times between the first three and last four seasons of the sample period. In an average year the 15 adult and subadult male chimpanzees are calculated to have killed 204 prey per year in an area of 16 km², varying between 99 and 420 prey per year in periods of low and high predation rate. Red colobus were the most frequent prey, followed by bushpig and bushbuck. Predation rates varied greatly on different prey species, and were not related to either the proportion of time spent within 200 m of male chimpanzees, or to their population densities. In relation to encounter rates and population density, baboons, blue monkeys, and redtail monkeys were killed at a fraction of the rate of red colobus monkeys, which suffered severe mortality from chimpanzee predation. Predation on bushpig and bushbuck also appears to have been high in relation to population density. The amount of food provided by predation is estimated to have averaged 600 kg per year for chimpanzees in the two communities (totalling 14–17 adult or subadult males, 18–20 adult of subadult females, and about 19 infants or juveniles). This suggests that adult males consumed around 25 kg of meat per year, although any average figure undoubtedly masks considerable individual variation. Present data suggest that chimpanzees in Gombe and Tai National Park, Ivory Coast, prey on mammals at rates higher than other populations.     

Why do male chimpanzees defend a group range?

Male chimpanzees, Pan troglodytes, cooperate to defend a community range within which resident females range in smaller core areas. There has been debate over exactly what males are defending, whether mates, territory or both. One hypothesis holds that males are defending mates, and that an increase in community range size will lead directly to the acquisition of more females. However, males frequently attack females as well as males at the edge of the community range. We examined 18 years of observational data on the Gombe chimpanzees to determine the behaviour of males during extragroup encounters, and the consequences of changes in community range size on the number of adult females and indirect measures of food availability. Males were always aggressive to males from other communities, and often attacked adult females, especially those that were not sexually receptive, were older, and/or had more than one offspring. The number of females did not increase with range size, but several measures suggested an increase in food availability with range size. These measures include more time spent in large foraging parties, higher encounter rates with resident females, more encounters with sexually receptive females and higher female reproductive rates. These findings suggest that males defend a feeding territory for their resident females and protect them from sexual harassment. Although a large range may eventually attract more females, this is not an immediate consequence of range expansion. Male number was not correlated with community range size.     

‘Impact hunters’ catalyse cooperative hunting in two wild chimpanzee communities

Even when hunting in groups is mutually beneficial, it is unclear how communal hunts are initiated. If it is costly to be the only hunter, individuals should be reluctant to hunt unless others already are. We used 70 years of data from three communities to examine how male chimpanzees ‘solve’ this apparent collective action problem. The ‘impact hunter’ hypothesis proposes that group hunts are sometimes catalysed by certain individuals that hunt more readily than others. In two communities (Kasekela and Kanyawara), we identified a total of five males that exhibited high hunt participation rates for their age, and whose presence at an encounter with red colobus monkeys increased group hunting probability. Critically, these impact hunters were observed to hunt first more often than expected by chance. We argue that by hunting first, these males dilute prey defences and create opportunities for previously reluctant participants. This by-product mutualism can explain variation in group hunting rates within and between social groups. Hunting rates declined after the death of impact hunter FG in Kasekela and after impact hunter MS stopped hunting frequently in Kanyawara. There were no impact hunters in the third, smaller community (Mitumba), where, unlike the others, hunting probability increased with the number of females present at an encounter with prey.     

Intergroup conflicts among chimpanzees in Taï National Park: lethal violence and the female perspective

Intercommunity aggression in chimpanzees and primitive warfare in humans possess striking similarities, such as the common occurrence of large male coalitions, systematic control of territory boundaries, and lethal attacks on isolated individuals from neighboring groups. However, an important apparent contrast is the absence of recurrent peaceful interactions between neighboring groups of chimpanzees. We observed a remarkable range of behavior in intergroup encounters among three habituated communities of chimpanzees in Taï National Park, Côte d'Ivoire. Lethal attacks are documented in these study groups for the first time, as well as year‐long exchanges of parous adult females and peaceful intergroup visits of mothers with infants. Demographic factors, including group size and number of adult males, are shown to affect the nature of intergroup interactions in ways not considered previously. A reconsideration of the difference in intergroup interactions between eastern and western chimpanzees is proposed including a more important consideration of the female's perspective. The inclusion of the new complexities in intergroup interactions in chimpanzees allows new parallels to be drawn with the evolution of primitive warfare in humans. Am. J. Primatol. 70:519–532, 2008. © 2008 Wiley‐Liss, Inc.     

Dominance, aggression and testosterone in wild chimpanzees: a test of the ‘challenge hypothesis’

The ‘challenge hypothesis’ posits that variation in male testosterone levels is more closely associated with aggression in reproductive contexts than it is with changes in reproductive physiology. Numerous bird studies support this idea, but few tests have been conducted with primates. We conducted behavioural observations and noninvasive hormone sampling of 11 male chimpanzees, Pan troglodytes schweinfurthii, in the Kanyawara study site, Kibale National Park, to test predictions of the challenge hypothesis. Results indicated that adult male chimpanzees showed significant testosterone increases during periods when parous females showed maximally tumescent sexual swellings. These periods were also marked by increased rates of male aggression. Male testosterone levels did not increase in the presence of maximally tumescent nulliparous females. Such females are less attractive to males: they are not mate-guarded, nor do rates of male aggression increase when they are swelling. Male chimpanzees copulate with parous and nulliparous females at similar rates, however, suggesting that testosterone increases in the presence of cycling parous females are associated with aggression rather than sexual behaviour. High-ranking chimpanzees were more aggressive than low-ranking males and produced higher levels of urinary testosterone. Thus, the predictions of the challenge hypothesis were generally upheld. This suggests that the hypothesis may have wider applicability among primates, including humans.