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Cooperation and Competition in Chimpanzees: Current Understanding and Future Challenges JOHN C. MITANI Two goals in the study of evolutionary anthropology are to determine the factors that make humans unique and to reconstruct the evolution of our behavior. As humans’ closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) have always been of special interest in this regard. Because of their close evolutionary relationship to us, these animals provide the requisite comparative data to evaluate claims made about human uniqueness. In addition, knowledge of the dif- ferences among chimpanzees, bonobos, and us furnishes important insights into the changes that occurred during human evolution. Given these circumstances, studies of chimpanzees and bonobos remain high priorities for research. The volatile political situation in the Democratic Republic of the Congo, home to bonobos, has made long-term study of their behavior difficult, if not impossible. In contrast, field research on chimpanzees, initiated by Jane Goodall 1 and Toshisada Nishida 2 nearly 50 years ago, continues to grow and thrive. While past and ongoing field work has added enormously to our understanding of the behavior of chimpanzees, 3–8 gaps in knowl- edge persist. In this paper, I summarize some of these gaps, giving special emphasis to male cooperation and female competition. Cooperation and competition gener- ate considerable theoretical interest and remain prominent issues in the study of evolutionary biology. Dar- win’s 9,10 twin theories of natural selec- tion and sexual selection furnish the basis for our current understanding of cooperation and competition in the bi- ological world. Cooperation, defined as behavior that increases the fitness of others, 11 poses a problem because it is not immediately clear why organisms might help others in the face of selec- tion operating to produce organic structures and behaviors ‘‘solely by and for the good of each.’’ 9 Why males cooperate poses an additional puzzle because these individuals typically compete to fertilize females, who are neither easily divided nor shared. As a result, extensive research has been devoted to attempting to explain the evolution of cooperation during the past 50 years. 11–20 After having been virtually ignored for 100 years after its publication in The Descent of Man and Selection in Relation to Sex, Darwin’s theory of sex- ual selection now serves as the founda- tion for an active and vibrant field of research. Sexual selection furnishes a compelling rationale for why males frequently compete. A resurgence of interest in this evolutionary process during the past 40 years has led to the publication of several important stud- ies regarding how males compete across the animal kingdom. 21 The focus on male-male competition has tended to obscure the fact that females in a wide variety of species often com- pete. Growing realization of the impor- tance of female competition, fueled in part by studies of primates, is begin- ning to alter this situation, leading to renewed attention to this process. 22 My goal in the following is to provide a road map for future research. This road map depends, in part, on under- standing what we already know. As a consequence, I highlight selected find- ings regarding male chimpanzee coop- eration and female competition. This is not intended to be an exhaustive review of the literature, but instead an admittedly personal view of the state of the art and field. Because our cur- rent understanding of wild chimpan- zee behavior derives from years of research by several individuals, it will be instructive to begin with a summary of the major long-term field studies of chimpanzee behavior. CHIMPANZEE FIELD STUDIES Much of our understanding of what it is to be a chimpanzee in the wild derives from the pioneering studies ini- tiated by Jane Goodall 23 at the Gombe National Park and Toshisada Nishida 2 at the Mahale Mountains National Park, both in Tanzania. Field work by Goodall and her colleagues and Nish- ida and his co-workers now into their 49 th and 44 th years, respectively, has been responsible for seminal discov- eries regarding chimpanzee tool use ARTICLES John C. Mitani is the James N. Spuhler Collegiate Professor of Anthropology at the University of Michigan. During the past 15 years, he has been engaged in a long-term study of the behavior of chimpanzees living in an unusually large community at Ngogo, Kibale National Park, Uganda. His research there focuses on male chimpanzee social behavior and cooperation. Over the past 30 years, he has conducted field work on all five of the living apes, including gibbons and orangutans in Indonesia, gorillas in Rwanda, bonobos in the Democratic Republic of Congo, and chimpanzees in Tanzania and Uganda. E-mail: mitani@ umich.edu) Key words: chimpanzee; Pan troglodytes; behavior V V C 2009 Wiley-Liss, Inc. DOI 10.1002/evan.20229 Published online in Wiley InterScience (www. interscience.wiley.com). Evolutionary Anthropology 18:215–227 (2009)

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Cooperation and Competition in Chimpanzees:Current Understanding and Future ChallengesJOHNC.MITANI

Two goals in the study of evolutionary anthropology are to determine the factorsthat make humans unique and to reconstruct the evolution of our behavior. Ashumans’ closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Panpaniscus) have always been of special interest in this regard. Because of their closeevolutionary relationship to us, these animals provide the requisite comparative datato evaluate claims made about human uniqueness. In addition, knowledge of the dif-ferences among chimpanzees, bonobos, and us furnishes important insights into thechanges that occurred during human evolution. Given these circumstances, studiesof chimpanzees and bonobos remain high priorities for research. The volatile politicalsituation in the Democratic Republic of the Congo, home to bonobos, has madelong-term study of their behavior difficult, if not impossible. In contrast, field researchon chimpanzees, initiated by Jane Goodall1 and Toshisada Nishida2 nearly 50 yearsago, continues to grow and thrive. While past and ongoing field work has addedenormously to our understanding of the behavior of chimpanzees,3–8 gaps in knowl-edge persist. In this paper, I summarize some of these gaps, giving special emphasisto male cooperation and female competition.

Cooperation and competition gener-ate considerable theoretical interestand remain prominent issues in thestudy of evolutionary biology. Dar-win’s9,10 twin theories of natural selec-tion and sexual selection furnish the

basis for our current understanding ofcooperation and competition in the bi-ological world. Cooperation, defined asbehavior that increases the fitness ofothers,11 poses a problem because it isnot immediately clear why organismsmight help others in the face of selec-tion operating to produce organicstructures and behaviors ‘‘solely byand for the good of each.’’9 Why malescooperate poses an additional puzzlebecause these individuals typicallycompete to fertilize females, who areneither easily divided nor shared. As aresult, extensive research has beendevoted to attempting to explain theevolution of cooperation during thepast 50 years.11–20

After having been virtually ignoredfor 100 years after its publication inThe Descent of Man and Selection inRelation to Sex, Darwin’s theory of sex-ual selection now serves as the founda-tion for an active and vibrant field ofresearch. Sexual selection furnishes acompelling rationale for why malesfrequently compete. A resurgence of

interest in this evolutionary processduring the past 40 years has led to thepublication of several important stud-ies regarding how males competeacross the animal kingdom.21 Thefocus on male-male competition hastended to obscure the fact that femalesin a wide variety of species often com-pete. Growing realization of the impor-tance of female competition, fueled inpart by studies of primates, is begin-ning to alter this situation, leading torenewed attention to this process.22

My goal in the following is to providea road map for future research. Thisroad map depends, in part, on under-standing what we already know. As aconsequence, I highlight selected find-ings regarding male chimpanzee coop-eration and female competition. Thisis not intended to be an exhaustivereview of the literature, but instead anadmittedly personal view of the stateof the art and field. Because our cur-rent understanding of wild chimpan-zee behavior derives from years ofresearch by several individuals, it willbe instructive to begin with a summaryof the major long-term field studies ofchimpanzee behavior.

CHIMPANZEE FIELD STUDIES

Much of our understanding of whatit is to be a chimpanzee in the wildderives from the pioneering studies ini-tiated by Jane Goodall23 at the GombeNational Park and Toshisada Nishida2

at the Mahale Mountains NationalPark, both in Tanzania. Field work byGoodall and her colleagues and Nish-ida and his co-workers now into their49th and 44th years, respectively, hasbeen responsible for seminal discov-eries regarding chimpanzee tool use

ARTICLES

John C. Mitani is the James N. SpuhlerCollegiate Professor of Anthropology at theUniversity of Michigan. During the past 15years, he has been engaged in a long-termstudy of the behavior of chimpanzees livingin an unusually large community at Ngogo,Kibale National Park, Uganda. His researchthere focuses on male chimpanzee socialbehavior and cooperation. Over the past30 years, he has conducted field work onall five of the living apes, including gibbonsand orangutans in Indonesia, gorillas inRwanda, bonobos in the DemocraticRepublic of Congo, and chimpanzees inTanzania and Uganda. E-mail: [email protected])

Key words: chimpanzee; Pan troglodytes; behavior

VVC 2009Wiley-Liss, Inc.DOI 10.1002/evan.20229Published online in Wiley InterScience (www.interscience.wiley.com).

Evolutionary Anthropology 18:215–227 (2009)

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and hunting,1 inter community vio-lence and aggression,24,25 social struc-ture and dispersal,2,26,27 culture,28 andmedicinal plant use.29 Vernon Reyn-olds30 initially began field work onchimpanzees in the Budongo ForestReserve, Uganda, at about the sametime as Goodall and Nishida, in theearly 1960s. Brief field studies by Yuki-maru Sugiyama31 and Akira Suzuki32

preceded a long hiatus in research atBudongo as political unrest in Ugandamade continuous work there impracti-cal. In 1992, Reynolds reinitiated fieldwork at Budongo,33 with research con-tinuing to this day.34

Following Adrian Kortlandt’s35 earlyfield work at Bossou, Guinea,Sugiyama36 began intermittent obser-vations there. Research at Bossou con-tinues now under the direction of Tet-suro Matsuzawa.37 Woodland habitatcharacterizes Gombe and Mahale,while chimpanzees at Bossou liveintermingled with humans. Recogniz-ing the need for studies of chimpan-zees in rainforests, Michael Ghiglieri38

initiated field work at Ngogo in theKibale National Park, Uganda. Mean-while, Christophe Boesch39 beganlong-term study in the Taı̈ NationalPark, Ivory Coast. Ghiglieri’s workspawned subsequent research on theKanyawara community of chimpan-zees in Kibale by Richard Wranghamand colleagues.40 Ghiglieri’s andWrangham’s efforts also led to my ownand David Watts’s study of the Ngogochimpanzees.41 Building on prior field

work conducted by Bill McGrew andcolleagues,42 Jill Pruetz43 has begunchimpanzee research anew in theregion surrounding Mt. Assirik in Sen-egal. This study of chimpanzees livingin a hot, dry, arid savanna comple-ments another recently initiated fieldstudy of chimpanzees in the forests ofthe Republic of Congo, led by CricketteSanz and DaveMorgan.44

In sum, previous and ongoing fieldresearch on chimpanzees has yieldedover 200 person years of observationsand resulted in an unprecedentedamount of data. These data lay thegroundwork for studies investigatingthe dual problems of male cooperationand female competition.

MALE CHIMPANZEECOOPERATION

Male chimpanzees are extremelygregarious2,3,40,45–47 and frequentlyengage in highly charged, noisyaggressive interactions. This ledearly observers to emphasize the rolethat male competition plays in chim-panzee life.48,49 High levels of malecompetition follow directly from thelow reproductive rates of femalechimpanzees, which give birth once,on average, every 5–6 years.3,5,6,50

Heavily biased male operational sexratios result, with the number ofreproductively active males dwarfingthe number of reproductively activefemales at any moment in time. This

sets the stage for intense male-malecompetition for mates and reproduc-tive opportunities.Male chimpanzees compete within

and between communities. Withincommunities, male chimpanzees strivefor status as they attempt to dominateothers, forming linear dominance hier-archies in the process.46,51–53 Recentresearch from several sites now indi-cates that males achieving high domi-nance rank obtain substantial fitnessbenefits, with alpha males siring up to30%–50% of all infants born duringtheir tenures at the top of hierar-chies.53–56 Male chimpanzees alsocompete with conspecifics from othercommunities as they defend their feed-ing grounds via group territorialbehavior.57

Despite their highly competitive na-ture, male chimpanzees also cooperatein several contexts to obtain direct andindirect fitness benefits.7,58 Coalitio-nary behavior, meat sharing, and terri-torial boundary patrolling providethree examples in this regard.

Coalitionary Behavior

Coalitions are a conspicuous andtheoretically interesting aspect of pri-mate behavior, taking place in speciesacross the Order.59 Coalitionary behav-ior involves two or more individualscooperating to direct aggression to-ward others (Fig. 1). In these situa-tions, one animal typically intervenesin an ongoing dispute between two

Figure 1. Male chimpanzee coalitionary behavior. A. The three males to the left have formed a coalition against the male on the right. B. Thetarget of aggression in A. Is driven off by the combined efforts of the three males who have formed a coalition. [Color figure can be viewed inthe online issue, which is available at www.interscience.wiley.com.]

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individuals. That primates form coali-tions so readily raises a puzzling evolu-tionary question.Why does a third partycome to the aid of another and put himor herself at risk in the process?Previous studies of male chimpan-

zees have emphasized the crucial rolecoalitions play in the acquisition ofdominance rank. Because high rankconfers fitness benefits,53–56 malescompete vigorously to achieve alphastatus. While large, strong males occa-sionally rise to the top, coalitionarysupport is frequently a more criticalvariable in that males typically obtainthe alpha position only if they receivehelp from others.60–65 Seminal studiesof chimpanzees in captivity by De-Waal61 and in the wild by Nishida62

document the complex coalitionarytactics male chimpanzees employ asthey cooperate to overthrow alphamales. In these situations, male chim-panzees form coalitions to improvetheir own status and are likely to benefitdirectly. Additional observations sug-gest that male chimpanzees recipro-cally exchange support and engage inmore complex interactions, tradingcoalitionary support for goods and serv-ices such as grooming and meat.66–68

Other studies indicate that alpha malescede matings to lower ranking males,who help them maintain their positionin the dominance hierarchy.62,69 All ofthese studies invoke reciprocity andcontinue to be debated, as the impor-tance of this process in animals otherthan humans is unclear.17,70 Inresearch on wild chimpanzees, it isextremely difficult to establish the con-tingent nature of exchanges betweenindividuals who live in uncontrolledconditions and who are not always to-gether due to the fission-fusion natureof their society. More work, perhaps incaptivity, where the behavior of oneindividual can be shown to depend onthe actions of another, will be necessaryto address this concern.71

The previous examples suggest thatmales receive direct fitness benefitsthrough coalitionary behavior. Inrecent work, my colleagues and I haveinvestigated whether male chimpan-zees derive indirect benefits by formingcoalitions with others. Here we com-bined genetic analyses designed todetermine who is related to whomwithlong-term behavioral observations to

ask whether genetic relationshipsaffect who does what with whom. Ourresults indicated that maternal halfsiblings form coalitions more oftenthan do unrelated or distantly relatedindividuals.58 In contrast, rates of coa-lition formation did not differ betweenpaternal half siblings and nonkin.Finally, several pairs of males sup-ported each other more often than pre-dicted by chance, and most of thesedyads were unrelated.58 Taken to-gether, these results suggest that malechimpanzees form coalitions primarilyfor selfish reasons, obtaining direct fit-ness benefits as they do so.

Prior research reveals how malechimpanzees use coalitions to improvetheir own fitness and those of theirclose relatives, thereby helping to

resolve the apparent paradox posed byindividuals who support others. Never-theless, several unanswered questionsremain regarding male chimpanzeecoalitionary behavior. Specifically, weknow remarkably little about the fre-quency, form, and long-term functionof coalitionary behavior. While it issometimes claimed that male chim-panzees form coalitions often,72,73

scant data exist to evaluate exactlyhow often they do compared withother primate species.74,75

Additional data regarding the natu-ral history of male chimpanzee coali-tionary behavior are sorely lacking.Coalitions are heterogeneous in form,involving a minimum of three individ-uals. In situations where two individu-als are involved in an aggressive inter-action and a third party intervenes, the

latter (‘‘supporter’’) helps one of thetwo contestants (‘‘recipient’’) targetingthe third individual (‘‘target’’). In ‘‘con-servative’’ coalitions,72 two high-rank-ing individuals cooperate to attack alower ranking animal (Fig. 2). Alterna-tively, a high-ranking individual canjoin forces with a low-ranking individ-ual in a ‘‘bridging’’ coalition to directaggression toward an animal rankingbetween them both (Fig. 2). A thirdpossibility involves ‘‘revolutionary’’coalitions in which two low-rankinganimals cooperate against a higherranking individual (Fig. 2).Different types of coalitions are

likely to have different ultimateeffects. A great deal has been writtenabout how male chimpanzees formrevolutionary coalitions as theyattempt to improve their own status,causing dramatic upheavals in thedominance hierarchy in the pro-cess.61–63 Less attention has beenpaid to conservative and bridgingcoalitions. The former reinforce thestatus quo, with two males benefitingby stabilizing and maintaining theirpositions in the dominance hierar-chy. Participants derive similar directfitness effects through bridging coali-tions. In one type of bridging coali-tion (top panel, Fig. 2), a low-rankingmale might support one high-rankingindividual against another high-rank-ing individual to gain leverageagainst the latter. In a second type ofbridging coalition (bottom panel, Fig.2), a high-ranking animal might sup-port the lower ranking individual of apair to reinforce his relative positionin the hierarchy.Revolutionary coalitions have re-

ceived considerable research attention,in part because of the significant effectthey have onmale dominance relationsand thus male fitness. This has led to ageneral impression that revolutionarycoalitions form quite frequently, butthis is unlikely to be the case as malechimpanzee dominance hierarchiesare often stable for long periods, withalphas remaining unchallenged as aresult. At Ngogo, two males main-tained their alpha status for more thanseven years, during which time theirposition at the top was only rarelythreatened in serious fashion. In sum,quantitative data are necessary to eval-uate how often different types of coali-

That primates formcoalitions so readily raisesa puzzling evolutionaryquestion. Why does athird party come to theaid of another and puthim or herself at riskin the process?

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tions actually occur and to assess theirconcomitant fitness effects.Several outstanding questions re-

main regarding the frequency, form,and function of short-term coalitions.However, the development and long-term maintenance of coalitions alsowarrant further study. My own anec-dotal observations suggest that malesmay not always help their youngermaternal brothers when there is a largedisparity in age, with strong coopera-tive bonds forming between them onlywhen both are adults and in a positionto obtain reproductive benefits by aid-ing each other. Additional observationsalso suggest that males may begin tosupport their younger brothers morevigorously as they age. In these situa-tions, males may increase their help toothers as their own reproductive valuedeclines. Additional long-term studywill be necessary to evaluate these pos-sibilities.Animals that consistently support

each other over long periods are saidto form an ‘‘alliance.’’76 More researchis needed to describe how short-termcoalitions between specific pairs ofmales develop into long-term alliances.What factors affect the development ofalliances and their long-term stability?Recent studies of female monkeys indi-

cate that individuals who form strongsocial bonds reproduce more than dofemales who develop only weakbonds.77,78 Because reproduction isthe currency of import in the eyes ofevolution, an important goal for futureresearch will be to document the long-term fitness consequences of malechimpanzee coalitionary behavior.Recent research indicates that malechimpanzees form long-lasting andenduring social bonds with others,79

but to what extent do these bonds,manifested by participation in coali-tions, affect male reproduction?Finally, we know little about the cogni-tive mechanisms and communicativeprocesses that underlie chimpanzeecoalitionary behavior. Field observa-tions and experiments previouslyemployed to investigate cognition andcommunication in monkeys will berequired to address these issues.80,81

Meat Sharing

The hunting behavior of chimpan-zees has been studied intensively atseveral study sites.82–90 The favoredprey of chimpanzees are red colobusmonkeys, which they hunt avidlywherever the two species live sympatri-cally. Chimpanzees also hunt other

vertebrate prey in habitats where redcolobus monkeys do not exist.43,91–93

Chimpanzees frequently share meatthat theyobtain inhunts (Fig. 3).66,84,94–96

At first glance, meat sharing is one ofthe most perplexing facets of chimpan-zee behavior. Meat, after all, is anextremely valuable resource, packedwith valuable micronutrients that arenot easily obtained elsewhere,41,97 mak-ing it highly prized by all individuals.Most chimpanzees, however, consumemeat infrequently because it is ext-remely hard to obtain. At Taı̈ andNgogo,chimpanzees engage in prolonged‘‘hunting patrols’’ during which chim-panzees travel in an apparently purpos-ive fashion across their territories insearch of red colobus prey.84,87 Huntingpatrols are energetically costly as patrol-lers rarely feed while they search formonkeys over periods averaging twohours. Patrols can sometimes last five tosix hours of a 12-hour day. Chimpanzeesmay hunt red colobus monkeys uponencounter, but hunts themselves arepotentially costly, as adult male colobusmonkeys typically mob and woundchimpanzee predators. Taken together,the inherent costs associated with hunt-ing make it puzzling why chimpanzeessharemeatwith others.Prior research has highlighted a

potential intersexual function of meatsharing. Building on a proposal ini-tially made by Geza Teleki,82 who con-ducted the first systematic study of thehunting behavior of wild chimpanzeesat Gombe, Craig Stanford and col-leagues94 hypothesized that malechimpanzees are motivated to hunt toobtain meat that they use to swap formatings. A similar hypothesis hasrecently been proposed to explain foodsharing between male and femalechimpanzees.98 Despite the provoca-tive nature of these hypotheses, severalobservations have been made that arenot consistent with them. Estrousfemales do not always obtain meatfrom their begging efforts and matingsdo not regularly occur when malesshare meat with females.66,95 Addi-tional data indicate that male chim-panzees do not always hunt red colo-bus monkeys upon encountering themand that the presence of estrousfemales actually inhibits huntingattempts by males.66,97 In situationswhere male chimpanzees pursue mon-

Figure 2. Types of coalitionary behavior. Solid arrows indicate directions of coalitionaryaggression toward third-party targets. Broken arrows showwho supports whom.

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keys instead of guarding estrousfemales, males are likely to suffer op-portunity costs in the form of lost mat-ings.97 Finally, sharing meat withfemales fails to improve male matingsuccess.66

While the preceding findings do notsupport the hypothesis that malechimpanzees share meat with femalesto improve their mating success, arecent study from the Taı̈ NationalPark suggests otherwise.96 Observa-tions made there indicate that malescopulated more frequently if theyshared meat with females than if theydid not. This relationship persists aftercontrolling several potential confound-ing variables, including male domi-nance rank, the amount of time malesand females spent together, and femaleage, gregariousness, and frequency ofbegging. The discrepancy betweenthese results and those derived fromother research may be due to two dif-ferent reasons, both of which requirefurther investigation. First, thereported differences may be attribut-able to differences in the length ofstudy. While the report from Taı̈ wasbased on data collected over 22months, previous research examinedthe relationship between male meatsharing and mating success overshorter times. Second, published dif-

ferences may reflect real variationbetween study sites. It is relevant tonote that the association between malemating success and meat sharing atTaı̈ suggests that females there rou-tinely exercise their choice in selectingmating partners. Current data indicatethat while females at Taı̈ may be ableto do so,99 additional observationsreveal that male coercion severelyrestricts the ability of females to dis-play their mating preferences else-where100 (personal observation).

An alternate hypothesis suggests apossible intrasexual function for meatsharing. This hypothesis takes its leadfrom field work conducted by Toshi-sada Nishida and colleagues101 atthe Mahale Mountains. There theyobserved a particularly clever alphamale, Ntologi, selectively share meatwith other males. Males who consis-tently obtained meat supported Nto-logi in aggressive disputes, therebyhelping him maintain his alpha statusfor an unprecedented period of 16years. From these observations, Nish-ida and co-workers formulated the‘‘male social bonding’’ hypothesis,66

which suggests that male chimpanzeesuse meat as a political tool to developand maintain valuable social bondswith others. My own observations arelargely consistent with this hypothesis,

as male chimpanzees at Ngogo sharemeat nonrandomly and reciprocallywith each other and exchange meat forcoalitionary support.66 More recentstudies at Gombe suggest that malechimpanzees there do not use meat asa social tool in a similar way.95,97 Thisclaim is difficult to evaluate as the criti-cal data needed to test this hypothesishave not been presented. Specifically,it remains to be determined whethermales at Gombe or at any other siteexchange meat for coalitionary sup-port. In sum, further study will be nec-essary to assess how generally we canapply the male social bonding hypoth-esis across chimpanzee communities.Recently, a third hypothesis has

been revived to explain the meat-shar-ing behavior of chimpanzees. Extend-ing an idea originally proposed byRichard Wrangham,102 Ian Gilby95 hasproposed that chimpanzees sharemeat to reduce the costs associatedwith possession. This ‘‘sharing underpressure’’ hypothesis begins with theobservation that hunts generate con-siderable frenzy. Because meat is ascarce and valuable resource, severalchimpanzees typically gather aroundindividuals who have captured prey,harassing them and attempting to grabbits of meat. This hypothesis proposesthat meat sharing represents a form of‘‘tolerated theft’’103 and that possessorsshare meat primarily to reduce thecosts of harassment imposed by beg-gars. Observations at Gombe supportthis hypothesis. Feeding rates by indi-viduals who possess meat decrease asa function of the number of beggars,the probability of sharing increaseswith the occurrence and duration ofharassment, and levels of harassmentdecline following sharing events.95 De-spite these findings, the hypothesis failsto explain why alpha males, who fre-quently possess meat and are not espe-cially vulnerable to harassment, readilyshare with others. In addition, the hy-pothesis does not account for voluntarytransfers that are frequently made byother chimpanzees. In sum, the shar-ing-under-pressure hypothesis goessome way to explain why chimpanzeesshare meat. It may, in fact, may bemore broadly applicable to the behaviorof chimpanzees at other study sites. Todate, however, the necessary data totest this hypothesis elsewhere have not

Figure 3. Male chimpanzee meat-sharing behavior. The male chimpanzee on the right tearsoff of a piece of meat, which he will later share with the male on the left. [Color figure can beviewed in the online issue, which is available at www.interscience.wiley.com.]

ARTICLES Wild Chimpanzee Behavior 219

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been collected. Consequently, as is thecase with the male social-bondinghypothesis, it is unclear to what extentthe sharing-under-pressure hypothesisapplies to the meat-sharing behaviordisplayed by chimpanzees in othercommunities. Additional work will berequired to address this issue.Ideally, future studies will continue

to consider the possibility that meatsharing occurs for different reasons, asthe male social bonding and sharingunder pressure hypotheses are notmutually exclusive. In this regard, an-ecdotal observations made at Ngogosuggest that meat may be relinquishedor stolen shortly after initial capture,but is treated with remarkable ‘‘respectfor ownership’’ thereafter, leading tovoluntary exchanges between individu-als. In addition, it will repay the effortto revisit how we define and operation-alize terms. For instance, Gilby95

defines chimpanzees who ‘‘harass’’individuals who possess meat as thosewho sit next to them, reach withouttouching them, hold the carcass of theprey, and touch the possessor’s mouth.Most of these behaviors do not accordwith what would commonly be consid-ered harassment. It will be important,therefore, to standardize definitions sothat they are operationally tractableand yield results that can be comparedin meaningful ways across studies.Because chimpanzees are well knownfor displaying intraspecific variation inbehavior,104,105 itwill also be importantto consider the possibility that thereported differences in meat sharingreflect real differences in the behaviorof chimpanzees across study sites. Insum, the meat sharing behavior ofchimpanzees continues to generatenew questions. Equally compellingquestions about male chimpanzeecooperation emerge from observationsof their territorial behavior.

Territorial Boundary Patrols

Perhaps the most dramatic way thatmale chimpanzees cooperate is in theirterritorial behavior. Chimpanzees aretypically hostile to members of othercommunities. Intercommunity aggres-sion occasionally leads to fatalities asmale chimpanzees make lethalcoalitionary attacks on their neighbors(Fig. 4).24,106–111 Adult male chimpan-

zees are typically targeted in suchattacks, with most fatalities involvingthem.7,112 However, infants also fre-quently fall victim,with the killers canni-balizing them in the process.7,112 Cur-rent evidence suggests that by killingconspecifics in other communities malechimpanzees achieve dominance overtheir neighbors and are thus able toexpand their territories at the latters’expense. Territorial expansion, in turn,leads to larger feeding territories andimproved reproduction by communityfemales.57 These observations leavethree questions unanswered. First,females are rarely recruited into newcommunities because secondary trans-

fer does not typically occur. Thus, whyare females fromother communities sel-dom targeted and killed? Second, whyare infants typically cannibalized? Alter-natively, why are adult chimpanzees leftunconsumed? To date, these questionsremain unresolved.

Attacks on chimpanzees belonging toother communities are frequently pre-ceded by territorial boundary patrols, abehavior that raises additional ques-tions about male cooperation (Fig. 5).Patrols typically involve males, whomove together in single file and directedfashion to the periphery of their terri-tory. When they arrive, their behaviorchanges dramatically. Patrollers fallcompletely silent. They visually scan theenvironment, sniff the ground, and

check signs, such as urine, feces, andfood, left behind by conspecifics. Occa-sionally, patrollers make deep incur-sions into the territories of their neigh-bors. AtNgogo, patrols include, on aver-age, about 13–18 individuals and occurabout once every 9–10 days.106,113,114

Patrollers make aural or visual contactwithmembers of adjacent communitiesin about 30%of these events.106

Patrols are costly. Individuals whoparticipate can, at least in theory, beattacked by members of other com-munities and injured or killed in theprocess. Patrollers also incur energeticand opportunity costs. Patrols atNgogo last an average of two hours,during which chimpanzees feed lessand travel more than they do duringother times.114 Whether the psycholog-ical stress and energetic costs associ-ated with patrols have a measurablephysiological effect on participantsremains to be determined. Tangiblecosts nevertheless exist, and patrollerscan offset these costs by obtaining sev-eral benefits through the joint defenseof territories. These benefits includeincreased access to food and improvedsafety. Because these benefits are likelyto be shared, males are predicted tocontribute regularly and participate inpatrols with equal frequency. Ourobservations nevertheless indicate thatthere is considerable heterogeneity inpatrol participation.106 While somemales patrol quite often, others partici-pate infrequently (Fig. 6). Data such asthese create a classic cooperationproblem. Specifically, why are somemales permitted to ‘‘free-ride’’ and torefrain from participating, thus reap-ing the communal benefits derivedfrom territorial patrols without payingany of the costs?Several possibilities exist, all of

which require further study. First, het-erogeneity in participation may reflectthe fact that the fitness benefits of pa-trolling are not equally distributedamong males. As a result, some malesmay be willing to pay greater coststhan others, with the former partici-pating more frequently than the latter.In this regard, previous observations atNgogo reveal that male patrollingeffort varies positively with matingsuccess.106 From this, it is tempting toconclude that males who mate fre-quently, and presumably have the

. . . the sharing-under-pressure hypothesis goessomeway to explain whychimpanzees sharemeat. It may, in fact, maybemore broadlyapplicable to thebehavior of chimpanzeesat other study sites. Todate, however, thenecessary data to test thishypothesis elsewherehave not been collected.

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most offspring in the group to protectnow and in the future, are motivated topatrol more than are males who mateless often. Ultimately, our ability toassess whether males accrue variablefitness benefits by patrolling willdepend on establishing a direct linkbetweenmale reproduction and patrol-ling frequency. Long-term records ofmales that do and don’t patrol, com-bined with paternity analyses usinggenetic markers, can be employed toinvestigate this possibility.Male chimpanzees may obtain other

direct benefits by participating inpatrols. Because patrols are costly interms of time and energy, and canpotentially lead to injury duringaggressive encounters with neighbors,they provide a forum for males toadvertise their ability and willingnessto take risks, and thus their quality aspotential long-term allies. To date, thehypothesis that patrolling represents aform of costly signaling115,116 hasreceived scant attention. A direct testof the hypothesis will require addi-tional observations regarding whethervariation in patrol participation affectsrates of received aggression and alli-ance formation.Male chimpanzees are philopat-

ric,26,27 and thus live with their geneticrelatives throughout their lives. Fromthis, a third possibility arises, which isthat males adjust their patrolling effortto obtain indirect fitness benefits.117

Specifically, this hypothesis predictsthat variation in the number of closekin with whom a male co-resides willaffect his tendency to patrol, withmales having many kin expected topatrol more often than do individualshaving fewer relatives to protect.Finally, fitness costs, as well as bene-

fits, might affect variation in patrolparticipation, leading to a fourth hy-pothesis, that males punish others whofail to patrol. Punishment, defined as‘‘retailiatory infliction of fitness reduc-tion,’’118 can prevent others fromengaging in harmful behaviors as wellas encourage them to perform benefi-cial behaviors. Compared with otherpotential explanations for cooperativebehavior, punishment has received rel-atively little attention in studies of ani-mal behavior. Observations of captivechimpanzees indicate that malesattack their long-term allies who fail to

Figure 4. Lethal coalitionary aggression. A. A group of male chimpanzees attack an adultmale from another community. The victim is at the bottom of the pile of attackers and hiddenfrom view. B. After 15 minutes, the victim is dead. C. About 40 minutes later, a young adultmale who participated in the attack leaps on the dead body of the victim. [Color figure canbe viewed in the online issue, which is available at www.interscience.wiley.com.]

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provide coalitionary support,61 butwhether groups of males punish otherswho do not participate in boundarypatrols remains an open question inneed of further study.

FEMALE CHIMPANZEECOMPETITION

Our knowledge of the behavior offemale chimpanzees lags behind stud-ies of male behavior and remains farfrom complete. There are several rea-sons for this, which are unrelated toany lack of interest or field effort onthe part of researchers. Put simply,female chimpanzees are very difficultto study. Female chimpanzees, specifi-cally those living in East Africa, are rel-atively asocial.119–122 Because of this,females rarely interact with conspe-cifics, so that social relationships bet-ween them have been difficult to docu-ment. In addition, females reproduceslowly3,5,6,50 and most disperse fromtheir natal groups,5,26,27 making theirsubsequent activities invisible tohuman observers. Given these circum-stances, it has taken an extraordinaryamount of time to obtain even themost basic information about thebehavior of female chimpanzees in thewild.Social relationships between females

represent one aspect of behavior thathas proven hard to unravel. In strikingcontrast to males, female chimpanzeesshow few overt signs of striving for sta-tus. This, combined with their compa-ratively low rates of interaction, makesit notoriously difficult to rank females.Dominance rank relationships bet-ween individuals can, on occasion, bedetermined, but typically only aftermany years of observation.123–128 As aresult, female chimpanzees are oftenportrayed as comparatively shy, secre-tive, and noncompetitive. Long-termstudies are beginning to transform thisdepiction of female chimpanzees,revealing a surprisingly competitiveside that has remained hidden untilnow.Female chimpanzees display ext-

remely slow life histories, character-ized by prolonged development,delayed reproduction, and low repro-ductive rates.3,5,6,50 These factors leadto the natural expectation that females

Figure 5. Territorial boundary patrol. Male chimpanzees patrol their territories by moving in sin-gle file, occasionally making deep incursions into neighboring territories. [Color figure can beviewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 6. Inter-individual variation in the tendency to patrol. Data fromWatts andMitani.106

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will compete, but for what? Here sex-ual selection theory provides criticalinsight. Female chimpanzees, likemost other mammals, invest more intheir offspring than domales. As a con-sequence, their reproduction is typi-cally limited by the ability to convertenvironmental energy directly into off-spring, with the result that femalescompete primarily for food.129

Because chimpanzees specialize infeeding on ripe fruit,130 they face a lim-ited and unpredictable food supplythat fluctuates in space and time. Thisforaging regime creates a special chal-lenge for females. Those living in EastAfrica appear to adapt by movingalone with their dependent offspringover relatively small core areas withinthe larger territory occupied by theentire community.121,122,126,131 Follow-ing dispersal, females settle into coreareas and remain faithful to them overtime. Through long-term site fidelityto core areas, females presumablybecome intimately familiar with thelocations of food in good times andbad. Recent observations now revealthat instead of competing directly forfood during face-to-face encounterswith conspecifics, female chimpanzeescompete for high-quality coreareas.125,126,128

The tropical habitats occupied bychimpanzees are heterogeneous and,as a consequence, female core areasvary in quality and size. Studies of EastAfrican chimpanzees indicate thathigh-ranking females reside in moreproductive core areas than do low-ranking individuals. Specifically, thecore areas of dominant females aresmaller and contain more preferredfoods than do those occupied by subor-dinates.126,128 Despite long-term site fi-delity, the core areas of individualfemales change in size over time as afunction of feeding competition. Dur-ing periods of fruit scarcity, competi-tion for food is accentuated, and atGombe, differences in the size of coreareas occupied by high- and low-rank-ing females grow larger.126 Observa-tions of interactions between immi-grant and resident females haveprovided further evidence of femalecompetition. When new femalesimmigrate into communities andattempt to establish core areas, theymeet sharp resistance from residents,

with rates of aggression increasingbetween them.128,132 While attemptingto settle, immigrant females increasetheir rates of association with maleswho, in turn, protect them fromattacks. In this way, immigrants areable reduce the levels of aggressionthey receive from resident females.127

Taken together, the preceding obser-vations suggest that female chimpan-zees compete for space, with high-ranking females excluding lower rank-ing females from high-quality habitats.This, in turn, has important conse-quences for female feeding behavior,condition, and reproduction. High-ranking females, who inhabit high-quality core areas, spend less time for-

aging and eat higher quality foods thando low-ranking females.125,133 Domi-nant females are also heavier and showless variation in weight across seasonsthan do subordinate females.134 More-over, the attendant feeding advantagesobtained by competition for space andfood influence female reproduction inimportant ways. At Gombe, high-rank-ing females live longer and haveshorter birth intervals than do low-ranking females.135 Dominant femalesalso give birth to more surviving off-spring and produce daughters thatreach sexual maturity earlier than dothose born to subordinate mothers.135

Similar observations have recentlybeen reported at Kanyawara, where

female chimpanzees who occupy coreareas with more preferred foods haveshorter birth intervals and higherinfant survivorship than do those liv-ing in poorer habitats.133

Recent studies are beginning toreveal that female chimpanzees com-pete with each other for space, food,and opportunities to reproduce.Female competition, for the most part,is indirect and manifest in subtle ways,differing dramatically from the loud,conspicuous, aggressive interactionsthat frequently take place betweenmale chimpanzees. Additional obser-vations indicate, however, that compe-tition between female chimpanzeescan escalate significantly under certaincircumstances. Competition betweenfemale chimpanzees is particularlyacute when new females immigrateinto communities. As they attempt tointegrate themselves into their newhomes and establish a core area, immi-grant females receive considerableaggression from resident females. AtGombe and the Budongo ForestReserve, resident females have nowbeen observed to form coalitions toattack and kill the infants of immigrantfemales.34,132 These attacks are partic-ularly extreme manifestations of com-petition between female chimpanzeesfor space and food.The research summarized here has

begun to paint an unexpectedly com-plex picture of female chimpanzeebehavior. But much remains to belearned. Specifically, what are thephysiological causes and consequencesof female competition? How do immi-grant females integrate themselvesinto their new communities? How doimmigrants select their core areas?What factors influence their decisions?How does female competition influencethe short- and long-term strategiesmothers use in raising their young?Studies of primates, which are long-lived and reproduce slowly, haveyielded scant data about infant growthand development. As a result, we con-tinue to lack information about howmaternal behavior influences patternsof chimpanzee development in the wild.Long-term behavioral observationscombined with endocrine analyses ofsamples noninvasively collected fromanimals in the wild will provide a wayto address these and other questions

Put simply, femalechimpanzees are verydifficult to study. Femalechimpanzees,specifically those living inEast Africa, are relativelyasocial. Because of this,females rarely interactwith conspecifics, so thatsocial relationshipsbetween them havebeen difficult todocument.

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about the behavior of female chimpan-zees. As studies continue to highlightintraspecific variation in chimpanzeebehavior,104,105 it will be important toexamine whether, how, and why pat-terns of female competition vary acrosspopulations. For example, it hasbecome increasingly clear that femalechimpanzees living in the Taı̈ NationalPark in West Africa are much moresocial than are individuals in EastAfrica.136 Collaborative work imple-menting standardized methods of datacollection and analysis is needed to vali-date these differences and to investigatetheir causal, developmental, and func-tional correlates.

IMPLICATIONS FOR HUMANBEHAVIOR AND EVOLUTION

Evolutionary anthropologists take akeen interest in studies of chimpanzeesand bonobos because they are ourclosest living relatives. As such, theyprovide valuable information to assesshow we as a species are unique and toreconstruct the evolution of humanbehavior. Differences that exist amongall three species highlight changes thathave occurred during the course ofhuman evolution and some of theselective factors that contributed toour extraordinary spread and domi-nance on earth. For example, theresearch reviewed here indicates thatmale chimpanzees cooperate in severalsituations, including coalitions, meatsharing, and territorial boundarypatrols. Observations indicate thatwhile maternal kinship affects whocooperates with whom, male chimpan-zees nonetheless cooperate quite oftenand readily with unrelated individuals.Despite these findings, cooperationbetween wild chimpanzees remainslimited in its extent and effects, asmales do not appear to cooperate withtheir paternal relatives58 and femalesdo not cooperate as often as males do.Also, cooperation typically is restrictedto pairs of individuals and it does notextend beyond members living withinthe same social group. In contrast,human cooperation involves extensivenetworks of individuals who assumespecialized roles to trade goods andservices both within and betweengroups. As a consequence, it is argu-ably true that cooperation, with kin

and nonkin alike, is a hallmark ofhumankind, setting us apart in a sig-nificant way from our closest living rel-atives.137

Other differences involving coopera-tion reviewed in this issue138 and else-where139 highlight an additional selec-tive factor that may have played a rolein the evolution of humans as a‘‘uniquely unique’’140 species. Recentresearch on female chimpanzee com-petition should not detract from thefact that female chimpanzees are car-ing mothers who are extraordinarilyattentive to and solicitous of theiryoung.3 Offspring care is nonethelessgenerally restricted to mothers. In thisrespect, chimpanzees differ sharplyfrom the cooperative breeding systems

displayed by Callitrichid primates andother animals.139 This observation hasled to the hypothesis that cooperativebreeding may have been a singularlyimportant trait leading to the evolutionof several unusual aspects of humanbehavior, life history, and cogni-tion.137–139

Similarities as well as differencescan be employed to reconstruct theevolution of human behavior. Behav-ioral similarities among chimpanzees,bonobos, and humans evolve as theresult of convergent evolution or com-mon descent. Homologous similaritiesdue to the latter process are of specialinterest for purposes of behavioralreconstruction.141 Homologies sharedamong chimpanzees, bonobos, andhumans are likely to have also beenshared by the common ancestor of allthree species. From this, it is reasona-

ble to assume that early humans pos-sessed these characteristics as well.Although this logic is unquestionableand easy to understand, it is not neces-sarily easy to apply. Some problems,not always entertained or acknowl-edged, hinder using information aboutchimpanzees to make inferences abouthuman behavioral evolution.One significant problem involves the

fact that bonobos are a sister taxon ofchimpanzees. Accordingly, data re-garding bonobos and chimpanzees arerequired to determine behaviors thatmay have been displayed by the lastcommon ancestor. Most attempts touse chimpanzees to reconstruct theevolution of our behavior fail toincorporate bonobos into theiranalyses.142–147 Why this is a problembecomes apparent when consideringthe potential significance of theextreme intergroup violence that chim-panzees display. Some have interpretedthis as supporting the claim that the ev-olutionary roots of human aggressionrun deep.148,149 Bonobos, however, aremuch less aggressive than chimpan-zees. Clearly, any argument that earlyhumans were extremely aggressive as aconsequence of shared ancestry wouldbe on much firmer ground if aggres-sion was practiced on a regular and fre-quent basis by all three species.In sum, information about the

behavior of chimpanzees continues toinform the study of human behaviorand evolution in important ways.Applying this information is some-times controversial150 and presentsproblems. In addition, a focus onchimpanzees should not take awayfrom the fact that behavioral observa-tions of other animals, primates andnonprimates alike, provide criticalcomparative data to understand thehuman condition. Nonetheless, asHuxley151 recognized more than 140years ago, their close evolutionary rela-tionship to us furnishes a strong theo-retical rationale for why chimpanzeesremain central to our understandinghuman evolution and behavior.

CONCLUDINGCOMMENTS

Nearly 50 years after their inception,studies of the behavior of wild chimpan-zees continue to generate widespreadattention and interest. Yet despite years

Recent studies arebeginning to reveal thatfemale chimpanzeescompete with each otherfor space, food, andopportunities toreproduce. Femalecompetition, for themostpart, is indirect andmanifest in subtle ways . . .

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of dedicated field work by several indi-viduals at sites across the African conti-nent, we still lack answers to fundamen-tal questions. The reason for this is sim-ple. Because of their extremely long lifespans and slow reproduction, chimpan-zees are slow to give up the secrets oftheir lives to human observers. Asshould be clear from the preceding,answering questions regarding malecooperation and female competitionwill require additional long-term study.But whether such study will be possibleremains unclear because chimpanzeesare critically endangered throughoutAfrica. Habitat destruction,152,153 athriving bushmeat trade,152,154 andrecurrent outbreaks of infectious dis-ease,152,155 threaten to drive chimpan-zees to extinction. Recent research indi-cates that populations of chimpanzeesin West Africa have suffered a precipi-tous decline during the past 20 years,156

while the famed Kasekela chimpanzeecommunity at Gombe in East Africacontinues to face an uncertain fate.157

Seven years ago, in an earlier review ofchimpanzee behavior for this journal, Iconcluded by noting the massive voidthat will be created if we fail to conservechimpanzees in the wild. Time haspassed and it is running out.

ACKNOWLEDGMENTS

This paper arose as part of a confer-ence organized by the L. S. B. LeakeyFoundation to honor two Leakey Prizerecipients, Jane Goodall and ToshisadaNishida, for their seminal fieldresearch investigating the behavior ofwild chimpanzees. I thank the Boardof Trustees, the Scientific ExecutiveCommittee, and the staff of the LeakeyFoundation for inviting me to partici-pate in this conference. John Fleaglesolicited this review, and I am espe-cially grateful for his patience duringthe time this paper was conceived,gestated, and finally written and re-vised. I also thank John for gentlycoaxing me to step out on a limb andwrite about the implications of chim-panzee behavior for the study ofhuman behavior and evolution. JohnFleagle, Kristen Hawkes, and threeanonymous reviewers furnished help-ful comments on the manuscript. Mypast and ongoing field work in Ugandahas been sponsored by the Makerere

University Biological Field Stations,the Uganda Wildlife Authority, and theUganda National Council for Scienceand Technology. My field research onchimpanzees has been generouslyfunded by grants from the U. S.National Science Foundation (SBR-9253590, BCS-0215622, IOB-0516644),L. S. B. Leakey Foundation, NationalGeographic Society, Wenner-GrenFoundation for AnthropologicalResearch, University of Michigan, andDetroit Zoological Institute.

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