Experimental evidence that grooming and play are social currency in bonobos and chimpanzees

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?


While natural observations show apes use grooming and play as social currency, no experimental manipulations have been carried out to measure the effects of these behaviours on relationship formation in apes. While previous experiments have demonstrated apes quickly learn the identity of individuals who will provide food in a variety of cooperative and non-cooperative situations, no experiment has ever examined how grooming and play might shape the preferences of apes for different individuals. We gave a group bonobos (N=25) and chimpanzees (N=30) a choice between an unfamiliar human who had recently groomed or played with them and one who had not. Both species showed a preference for the unfamiliar human that had interacted with them over the one who did not. The effect was largely driven by the males of both species while interacting with females showed little effect on their preferences for unfamiliar humans. Subjects showed this preference even though they only had social interactions with one of the unfamiliar humans for a few minutes before each trial and their choices were not rewarded with food differentially. Our results support the long held idea that grooming and play act as a form of social currency in great apes (and likely many other species) that can rapidly shape social relationships, particularly between unfamiliar individuals.

Experimental evidence that grooming and play are social currency in bonobos and chimpanzees

in Behaviour



BoeschC.KohouG.NeneH.VigilantL. (2006). Male competition and paternity in wild chimpanzees of the Tai forest. — Am. J. Phys. Anthropol. 130: 103-115.

BrosnanS.F.SilkJ.B.HenrichJ.MarenoM.C.LambethS.P.SchapiroS.J. (2009). Chimpanzees (Pan troglodytes) do not develop contingent reciprocity in an experimental task. — Anim. Cogn. 12: 587-597.

de WaalF.B.M. (1982). Chimpanzee politics. — The Johns Hopkins University PressBaltimore, MD.

de WaalF.B.M. (1997). The chimpanzee’s service economy: food for grooming. — Evol. Hum. Behav. 18: 375-386.

FuruichiT. (1997). Agonistic interactions and matrifocal dominance rank of wild bonobos (Pan paniscus) at Wamba. — Int. J. Primatol. 18: 855-875.

GerloffU.HartungB.HohmannG.TautzD. (1999). Intracommunity relationship, dispersal pattern and paternity success in a wild living community of bonobos (Pan paniscus) determined from DNA analysis of faecal samples. — Proc. Roy. Soc. Lond. B: Biol. Sci. 266: 1189-1195.

GilbyI.C.WranghamR.W. (2008). Association patterns among wild chimpanzees (Pan troglodytes schweinfurthii) reflect sex differences in cooperation. — Behav. Ecol. Sociobiol. 62: 1831-1842.

GilbyI.C.BrentL.J.N.WroblewskiE.E.RudicellR.S.HahnB.H.GoodallJ.PuseyA.E. (2013). Fitness benefits of coalitionary aggression in male chimpanzees. — Behav. Ecol. Sociobiol. 67: 373-381.

GomesC.M.BoeschC. (2009). Wild chimpanzees exchange meat for sex on a long-term basis. — PLoS One 4: e5116.

GoodallJ. (1986). The chimpanzees of Gombe. — Belknap PressCambridge, MA.

HareB.KwetuendaS. (2010). Bonobos voluntarily share their own food with others. — Curr. Biol. 20: R230-R231.

HareB.MelisA.P.WoodsV.HastingsS.WranghamR.CarolinaN. (2007). Tolerance allows bonobos to outperform chimpanzees on a cooperative task. — Curr. Biol. 17: 619-623.

HerrmannE.HareB.CallJ.TomaselloM. (2010). Differences in the cognitive skills of bonobos and chimpanzees. — PLoS One 5: e12438.

HerrmannE.HareB.CissewskiJ.TomaselloM. (2011). A comparison of temperament in nonhuman apes and human infants. — Dev. Sci. 14: 1393-1405.

HerrmannE.KeuppS.HareB.VaishA.TomaselloM. (2013a). Direct and indirect reputation formation in nonhuman great apes and human children. — J. Comp. Psychol. 127: 32.

HerrmannE.KeuppS.HareB.VaishA.TomaselloM. (2013b). Direct and indirect reputation formation in nonhuman great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, Pongo pygmaeus) and human children (Homo sapiens). — J. Comp. Psychol. 127: 63-75.

HohmannG.GerloffU.TautzD.FruthB. (1999). Social bonds and genetic ties: kinship, association and affiliation in a community of bonobos (Pan paniscus). — Behaviour 136: 1219-1235.

HøjsgaardS.HalekohU.YanJ. (2006). The R package geepack for generalized estimating equations. — J. Stat. Softw. 15: 1-11.

IdaniG. (1991). Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba. — Folia Primatol. 57: 83-95.

KahlenbergS.M.Emery ThompsonM.MullerM.N.WranghamR.W. (2008). Immigration costs for female chimpanzees and male protection as an immigrant counterstrategy to intrasexual aggression. — Anim. Behav. 76: 1497-1509.

KanoT. (1992). The last ape: pygmy chimpanzee behavior and ecology. — Stanford University PressStanford, CA.

KanoT. (1996). Male rank order and copulation rate in a unit-group of bonobos at Wamba, Zaire. — In: Great ape societies ( McGrewT.MarchantW.NishidaL. eds). Cambridge University PressCambridge p.  135-143.

KoyamaN.F.CawsC.AureliF. (2006). Interchange of grooming and agonistic support in chimpanzees. — Int. J. Primatol. 27: 1293-1309.

LangergraberK.MitaniJ.VigilantL. (2009). Kinship and social bonds in female chimpanzees (Pan troglodytes). — Am. J. Primatol. 71: 840-851.

LehmannJ.BoeschC. (2009). Sociality of the dispersing sex: the nature of social bonds in West African female chimpanzees, Pan troglodytes. — Anim. Behav. 77: 377-387.

MacleanE.HareB. (2013). Spontaneous triadic engagement in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). — J. Comp. Psychol. 127: 245-255.

MelisA.P.HareB.TomaselloM. (2006). Chimpanzees recruit the best collaborators. — Science 311: 1297-1300.

MelisA.P.HareB.TomaselloM. (2008). Do chimpanzees reciprocate received favours?Anim. Behav. 76: 951-962.

MelisA.P.HareB.TomaselloM. (2009). Chimpanzees coordinate in a negotiation game. — Evol. Hum. Behav. 30: 381-392.

MitaniJ.C. (2006). Reciprocal exchange in chimpanzees and other primates. — In: Cooperation in primates and humans ( KappelerP.van SchaikC.P. eds). SpringerBerlin p.  107-119.

MitaniJ.C. (2009). Male chimpanzees form enduring and equitable social bonds. — Anim. Behav. 77: 633-640.

MitaniJ.C.WattsD.P. (2001). Why do chimpanzees hunt and share meat?Anim. Behav. 61: 915-924.

MullerM.N.MitaniJ.C. (2005). Conflict and cooperation in wild chimpanzees. — Adv. Stud. Behav. 35: 275-331.

NishidaT. (2012). Chimpanzees of the lakeshore. — Cambridge University PressCambridge.

NishidaT.HosakaK. (1996). Coalition strategies among adult male chimpanzees of the Mahale Mountains, Tanzania. — In: Great ape societies ( McGrewT.MarchantW.NishidaL. eds). Cambridge University PressCambridge p.  114-134.

NoëR.HammersteinP. (1995). Biological markets. — Trends Ecol. Evol. 10: 336-339.

PalagiE.PaoliT. (2007). Play in adult bonobos (Pan paniscus): modality and potential meaning. — Am. J. Phys. Anthropol. 134: 219-225.

PalagiE.CordoniG.TarliS.M.B. (2004). Immediate and delayed benefits of play behaviour: new evidence from chimpanzees (Pan troglodytes). — Ethology 962: 949-962.

ParishA.R. (1996). Female relationships in bonobos (Pan paniscus): evidence for bonding, cooperation, and female dominance in a male-philopatric species. — Hum. Nat. 7: 61-96.

PuseyA.E. (1980). Inbreeding avoidance in chimpanzees. — Anim. Behav. 28: 543-552.

PuseyA.E.Schroepfer-WalkerK. (2013). Female competition in chimpanzees. — Phil. Trans. Roy. Soc. Lond. 368: 20130077.

PuseyA.E.WilliamsJ.GoodallJ. (1997). The influence of dominance rank on the reproductive success of female chimpanzees. — Science 277: 828-831.

R Core Team (2014). R: a language and environment for statistical computing. — R Foundation for Statistical ComputingVienna.

RosatiA.G.HareB. (2012). Decision making across social contexts: competition increases preferences for risk in chimpanzees and bonobos. — Anim. Behav. 84: 869-879.

RussellY.I.CallJ.DunbarR.I.M. (2008). Image scoring in great apes. — Behav. Proc. 78: 108-111.

SchülkeO.OstnerJ. (2008). Male reproductive skew, paternal relatedness, and female social relationships. — Am. J. Primatol. 70: 695-698.

SilkJ.B.BeehnerJ.C.BergmanT.J.CrockfordC.EnghA.L.MoscoviceL.R.CheneyD.L. (2009). The benefits of social capital: close social bonds among female baboons enhance offspring survival. — Proc. Roy. Soc. Lond. B: Biol. Sci. 276: 3099-3104.

SilkJ.B.BeehnerJ.C.BergmanT.J.CrockfordC.EnghA.L.MoscoviceL.R.CheneyD.L. (2010). Strong and consistent social bonds enhance the longevity of female baboons. — Curr. Biol. 20: 1359-1361.

StevensJ.M.G.VervaeckeH.De VriesH.Van ElsackerL. (2006). Social structures in Pan paniscus: testing the female bonding hypothesis. — Primates 47: 210-217.

SubiaulF.VonkJ.Okamoto-BarthS.BarthJ. (2008). Do chimpanzees learn reputation by observation? Evidence from direct and indirect experience with generous and selfish strangers. — Anim. Cogn. 11: 611-623.

SurbeckM.MundryR.HohmannG. (2011). Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). — Proc. Roy. Soc. Lond. B: Biol. Sci. 278: 590-598.

TanJ.HareB. (2013). Bonobos share with strangers. — PLoS One 8: e51922.

WattsD.P. (2000). Grooming between male chimpanzees at Ngogo, Kibale National Park, Uganda. 1. Partner number and diversity and reciprocity. — Int. J. Primatol. 21: 189-210.

WattsD.P. (2002). Reciprocity and interchange in the social relationships of wild male chimpanzees. — Behaviour 139: 343-370.

WobberV.HareB. (2009). Testing the social dog hypothesis: are dogs also more skilled than chimpanzees in non-communicative social tasks?Behav. Proc. 81: 423-428.

WobberV.HareB. (2011). Psychological health of orphan bonobos and chimpanzees in African sanctuaries. — PLoS One 6: e17147.

WobberV.HareB.MabotoJ.LipsonS.WranghamR.EllisonP.T. (2010). Differential changes in steroid hormones before competition in bonobos and chimpanzees. — Proc. Natl. Acad. Sci. USA 107: 12457-12462.

WobberV.WranghamR.HareB. (2010). Bonobos exhibit delayed development of social behavior and cognition relative to chimpanzees. — Curr. Biol. 20: 226-230.

WroblewskiE.E.MurrayC.M.KeeleB.F.Schumacher-StankeyJ.C.HahnB.H.PuseyA.E. (2009). Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. — Anim. Behav. 77: 873-885.

YanJ. (2002). Geepack: yet another package for generalized estimating equations. — R News 2: 12-14.

YanJ.FineJ.P. (2004). Estimating equations for association structures. — Stat. Med. 23: 859-880.


  • View in gallery

    The y-axis represents the proportion of trials the experimenter who groomed the subject or ‘actor’ was chosen over an experimenter who did not in the baseline (light grey) and test conditions (dark grey) for both species separated by sex in the play condition. Error bars represent standard error.

  • View in gallery

    The y-axis represents the proportion of trials the experimenter who groomed the subject or ‘actor’ was chosen over an experimenter who did not in the baseline (light grey) and test conditions (dark grey) for both species separated by sex in the groom condition. Error bars represent standard error.

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 14 14 7
Full Text Views 6 6 6
PDF Downloads 3 3 3
EPUB Downloads 0 0 0