Long-term reciprocation of grooming in wild West African chimpanzeesIntroductionMaterial and methodsBehavioural data collectionStatistical analysisModel specificationsTime frame of grooming reciprocationDetails of the within-bouts analysisDetails of the within-days analysisDetails of the dyadic long-term analysisDetails of the comparison between the analyses of different time framesResultsGeneral grooming patternsReciprocity and the time frame of grooming reciprocationDiscussionProximate mechanisms of long-term reciprocityThis research complied with the ethics guidelines of the Max Planck Society and supported by the Ivorian authorities (Ivory Coast Park Authorities and Ministry of Science and Research, Ivory Coast).Referencesdoi: 10.1098/rspb.2008.1324, 699-706276 2009 Proc. R. Soc. B Cristina M Gomes, Roger Mundry and Christophe Boesch chimpanzeesLong-term reciprocation of grooming in wild West African Referenceshttp://rspb.royalsocietypublishing.org/content/276/1657/699.full.html#ref-list-1 This article cites 47 articles, 8 of which can be accessed freeSubject collections (1154 articles)behaviour  Articles on similar topics can be found in the following collectionsEmail alerting service hereright-hand corner of the article or click Receive free email alerts when new articles cite this article - sign up in the box at the top http://rspb.royalsocietypublishing.org/subscriptions go to: Proc. R. Soc. BTo subscribe to This journal is © 2009 The Royal Society on April 2, 2010rspb.royalsocietypublishing.orgDownloaded fromLong-ter m reciprocation of grooming in wildWest African chimpanzeesCristina M. Gomes*, Roger Mundry and Christophe BoeschMax Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, GermanyHumans are well known for their ability to keep track of social debts over extended periods of time, and fortheir tendency to preferentially cooperate with closely bonded partners. Non-human primates have beenshown to cooperate with kin and non-kin, and reciprocate helpful acts. However, there is ongoing debateover whether they keep track of previous interactions and, if so, whether they can do it over extended periodsof time, or are constrained to finalize exchanges within a single encounter. In this study, we used 3000 hoursof all-day focal follows of wild chimpanzees (Pan troglodytes verus) to investigate whether both females andmales reciprocate grooming within a single interaction, throughout the day, or over longer periods of time.We found that grooming was reciprocated more symmetrically when measured on a long-term, rather thanon an immediate or short-term basis. Random giving, general allocation of grooming efforts, similaritiesamong individuals and kinship do not appear to explain these highly reciprocal exchanges. Previouslycollected consecutive focal follows of single individuals revealed that dyads groomed an average of onceevery 7 days. Our findings strongly suggest that chimpanzees, similar to humans, are able to keep track ofpast social interactions, at least for a one-week period, and balance services over repeated encounters.Keywords: grooming; reciprocity; chimpanzees; time frame; time lag; Pan troglodytes verus1. INTRODUCTIONReciprocity has been a major area of investigation due tothe theoretical dilemma that helping others represents, thecognitive implications it may have in terms of memory andrecognition and, therefore, its inevitable repercussions onthe evolution of human trading. The theory of reciprocalaltruism proposes that if giving is contingent uponreceiving and if individuals give more services (i.e. helpfulbehaviours) or resources to those from whom they receivethe most, performing helpful acts or giving resourcescan be an evolutionarily stable strategy (Trivers 1971;Axelrod & Hamilton 1981).The time lag between giving and receiving of services orresources is one of the crucial aspects of reciprocity. Whenstudying exchange behaviours, choosing an inappropriatetime frame for reciprocation could lead to findinginaccurate measures of the symmetry of reciprocation(i.e. the relationship between giving and receiving) or evento concluding erroneously on the absence of reciprocity(i.e. if the time frame chosen is too short and individualshave not yet reciprocated). Much controversy surroundsthis topic since researchers disagree on the length of thetime frame for reciprocation in primates. Some authorshave suggested that non-human primates’ cognitiveabilities enable them only to reciprocate acts immediatelyor on a short-term basis (Barrett & Henzi 2002; Stevens &Hauser 2004). Such is the case of female chacma baboons(Papio cynocephalus ursinus)andsamangomonkeys(Cercopithecus mitis erythrarchus), which reciprocatedgrooming short term (Barrett et al. 1999, 2002; Payneet al. 2003; Pazol & Cords 2005), and, as other vertebrates(Hart & Hart 1992; Connor 1995), were proposed totrade commodities immediately. Others have suggestedthat reciprocation takes place over a longer time frame(Manson et al. 2004; Schino et al. 2007). This wasobserved in female olive baboons (Papio anubis; Frank2007), bonnet macaques (Macaca radiata; Manson et al.2004), tufted (Schino et al. in press) and white-facedcapuchins (Cebus capucinus; Manson et al. 2004), whichreciprocated grooming long term and did not havebalanced grooming bouts (i.e. individuals did not giveand receive the same amount within a single interaction,thus the symmetry of the relationship between giving andreceiving was not close to 1). It is unknown, however,whether these differences are due to exploring only limitedtime frames for reciprocation which could lead toerroneous conclusions on the time lag between givingand receiving, or if they are due to real species differences.Grooming is an ideal behaviour for the investigation ofthe time frame of reciprocation since non-human primatestend to groom frequently (reviewed in Spruijt et al. 1992),which allows for it to be exchanged immediately or overlonger time frames. As it benefits the recipient at some costto the actor, it is proposed to function as a service that canbe provided to others (de Waal 1997). Some of these costsinclude decreased vigilance (Mooring & Hart 1995) andresting time (Dunbar & Sharman 1984; Dunbar 1992),and exposure to microparasite transmission ( Johnson et al.2004; Nunn & Altizer 2006). However, it is a profitablecommodity to exchange due to the benefits to therecipient. As grooming serves to remove