Supply and demand determine the market valueof food providers in wild vervet monkeysCe´cile Fruteaua,b, Bernhard Voelklb, Eric van Dammea,c, and Ronald Noe¨b,d,1aCentER for Economic Research, University of Tilburg, 5000 LE Tilburg, The Netherlands;bEthologie des Primates, De´ partement Ecologie, Physiologie etEthologie, Institut Pluridisciplinaire Hubert Curien, Centre National de la Recherche Scientifique Unite´ Mixte de Recherche 7178, 67087 Strasbourg Cedex 2,France;cTilburg Law and Economics Center, University of Tilburg, 5000 LE Tilburg, The Netherlands; anddApplied Behavioural Ecology Research Unit,School of Environmental Sciences, University of South Africa, Private Bag X6, Florida 1710, South AfricaEdited by Frans B. M. de Waal, Emory University, Atlanta, GA, and approved June 1, 2009 (received for review December 3, 2008)Animals neither negotiate verbally nor conclude binding contracts,but nevertheless regularly exchange goods and services withoutovert coercion and manage to arrive at agreements over exchangerates. Biological market theory predicts that such exchange ratesfluctuate according to the law of supply and demand. Previousstudies showed that primates pay more when commodities be-come scarcer: subordinates groomed dominants longer beforebeing tolerated at food sites in periods of shortage; femalesgroomed mothers longer before obtaining permission to handletheir infants when there were fewer newborns and malesgroomed fertile females longer before obtaining their compliancewhen fewer such females were present. We further substantiatedthese results by conducting a 2-step experiment in 2 groups offree-ranging vervet monkeys in the Loskop Dam Nature Reserve,South Africa. We first allowed a single low-ranking female torepeatedly provide food to her entire group by triggering theopening of a container and measured grooming bouts involvingthis female in the hour after she made the reward available. Wethen measured the shifts in grooming patterns after we added asecond food container that could be opened by another low-ranking female, the second provider. All 4 providers received moregrooming, relative to the amount of grooming they providedthemselves. As biological market theory predicts, the initial gain offirst providers was partially lost again after the introduction of asecond provider in both groups. We conclude that grooming wasfine-tuned to changes in the value of these females as socialpartners.biological markets 兩 cooperation 兩 economic behavior 兩primates 兩 reciprocityTrading in humans and cooperation in animals are part of ac ontinuum in which both human and nonhuman agentsusually have to take 3 crucial steps: ( i) choose a partner, (ii)deter mine how much to invest to obtain the desired commodi-ties, and (iii) prevent being short-changed by the chosen partner.While research in economics traditionally concentrates on fac-tors that determine the price of commodities, quantitativeaspects have gained much less attention in studies of nonhumanc ooperation (1). Over the past decades, c ooperation research hasfocused mainly on the question of partner control rather than onthe relative values of goods and services exchanged. By contrast,the biological market paradigm (2, 3) focuses on the link betweensteps i and ii and predicts that the law of supply and demandaf fects the exchange rates in nonhuman ‘‘trading’’ in a similarfashion as in human economic exchanges. Here we test thisprediction in 2 wild vervet monkey groups by measuring changesin grooming patterns after experimentally changing the numberof individuals that could provide food to their group.We envisage the exchange of commodities in primate groupsas trading on a market with exchange rates fluctuating from dayto day depending on supply and demand. Monkeys trading goodsand services have to agree on exchange rates to avoid overtc onflicts, but lack the option of negotiating verbally and c on-cluding binding c ontracts. Not all commodities exchangedamong nonhuman primates can be adapted in quantit y or qualityduring each interaction, but 1 service, grooming, can be adjustedeasily. Grooming can be exchanged against grooming itself, butalso against other goods or services, lending it currency-likecharacteristics. Commodities bought with grooming includetolerance at food sites (4–9), access to newborns (10, 11),c ompliance of females (12), and support in conflicts (13–15),although results on grooming–support exchanges have beenmixed (16–18). Monkeys do not necessarily track value fluctu-ations for each commodity on the market separately, however,but they may change their general attitude toward group mem-bers (19) in accordance with the accumulated value of thedif ferent commodities each one of them has on offer. Mecha-n istically the value attributed to a partner is likely to be ex pressedin physiological parameters such as titers of neurohormones andneurotransmitters implicated in trust and pair bonding (20–25).We created an artificial market in 2 groups of wild vervetmonkeys in the Loskop Dam Nature Reserve (South Af rica) andcaused sudden changes in the market value of a few animals insuch a way that these affected all other group members and couldeasily be perceived by them. After an initial phase in which wegathered baseline data on g rooming (phase 0), we allowed asingle low-ranking female in each study g roup to produce abonanza of food for herself and her group members by triggeringthe open ing of a cont ainer (Movie S1) in 16 trials spread overa period of 9 weeks (phase 1). These first 2 stages resemble astudy previously done in captivity with long-tailed macaques(26). In that ex periment, a single individual that could producea small food reward and share it with up to 2 other an imalsex perienced an increase in social status. We developed thisparadigm further to show the quantitative effects of a shift insupply on grooming patterns. This requires a manipulation eitherof the amount of reward per provider or of the number ofproviders. We opted for the latter approach because it is veryhard to control the amount of food each individual will obtainonce the provider made it available. In phase 2 of the ex perimentwe therefore introduced a second provider in each group,another low-ranking female with a second food container(Movie S2) that only she could open. The same amount of food(5 apples per trial sliced in small pieces) was now divided overthe 2 containers that were