Animal Behaviour 110 (2015) 51e60

Contents lists available at ScienceDirect

Animal Behaviour

journal homepage: www.elsevier.com/locate/anbehav

Essay Are primates out of the market?

* Alejandro Sanchez-Amaro a, , Federica Amici a, b a Max Planck Institute for Evolutionary Anthropology, Developmental and Comparative Psychology, Leipzig, Germany b Department of Developmental Psychology, University of Zurich, Switzerland article info Biological Market Theory (BMT) has provided an elegant framework to study how commodities are Article history: exchanged among individuals. In primates, BMT predicts that individuals exchange grooming with other Received 26 May 2015 commodities based on the law of supply and demand. However, BMT still suffers some theoretical and Initial acceptance 24 June 2015 methodological limitations. Our aim in this paper is to discuss some of these limitations, including the Final acceptance 9 September 2015 lack of consensus over the time frame in which exchanges take place, and over the commodities Available online 23 October 2015 involved, the cognitive challenges imposed by biological markets (BMs), and the heterogeneity of MS. number: 15-00451R methods used to test BMT across studies. In particular, we discuss (1) the importance of predetermining both the time frame over which exchanges take place and (2) the commodities that are exchanged in Keywords: primate BMs, (3) the cognitive skills that primates need to navigate in a BM, and (4) other methodo- biological market theory (BMT) logical issues arising when testing BMT. For each of these points, we propose an agenda with possible cognition solutions and we show how the issues raised also apply to BMs in species other than primates. exchange of commodities © grooming 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. primate biological market (PBM) social relationships

Biological market theory (BMT) was introduced by Noe€ and discuss these issues and pinpoint possible ways to better address Hammerstein (1994, 1995) to explain how commodities are them in the future. We mainly restrict our review to intraspecific exchanged among individuals. In biological markets (BMs), classes exchanges of commodities and, especially, to the primate biological of traders exchange commodities to their mutual benefit, whenever market (PBM). However, at the end of each section, we also assess commodities cannot be obtained by the use of force and are under how the problems raised also apply to BMs in species other than the exclusive control of one class (or only accessible from alterna- primates. In the following sections, we (1) introduce PBMs, (2) tive sources at high costs). Within the same class of traders, in- discuss the lack of a clear time frame over which commodities are dividuals compete with each other over access to partners, by exchanged, (3) review the commodities exchanged in PBMs, (4) providing more valuable commodities rather than engaging in discuss the cognitive challenges imposed by BMs, (5) question the aggressive behaviour. Therefore, individuals are chosen as partners use of heterogeneous methods to test PBMs and (6) draw general depending on the value of the commodities they offer, and the conclusions on our actual knowledge of PBMs. choice is made by comparing the offers of all potential partners, similarly to what happens in human markets. As a result, resources THE PRIMATE BIOLOGICAL MARKET with no a priori intrinsic value are exchanged according to the laws fi of supply and demand, explaining the formation of short and nite In most primates, grooming is frequently exchanged among relationships between different classes of individuals. group members. In female philopatric groups, grooming mainly So far, BMT has provided an elegant framework to study social occurs between females with a similar rank, although higher- fi relationships in areas that span from sexual selection, interspeci c ranking individuals usually receive more grooming than they give fi mutualism and intraspeci c cooperation. However, BMT still suffers (e.g. Dunbar, 1992; Schino, 2001; Seyfarth, 1980). To explain these from a series of theoretical and methodological problems that limit consistent findings, Seyfarth (1977) introduced a model assuming its applicability in some research areas. Our aim in this paper is to that (1) grooming is highly valuable for primates, (2) females are attracted to each other, but especially to higher-ranking individuals, who might provide valuable agonistic support, (3) time to engage in * Correspondence: A. Sanchez-Amaro, Department of Psychology, Max Planck grooming is limited, (4) females compete with each other to reach Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany. an optimal ratio between grooming received and grooming given, E-mail address: [email protected] (A. Sanchez-Amaro). and (5) higher-ranking individuals outcompete others when trying http://dx.doi.org/10.1016/j.anbehav.2015.09.020 0003-3472/© 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 52 A. Sanchez-Amaro, F. Amici / Animal Behaviour 110 (2015) 51e60 to access the same partner. When these assumptions are met, fe- for instance, predicted that primate exchanges depend on their males groom partners with a similar rank, and higher-ranking fe- current needs and the immediate availability of commodities. The males receive more grooming than they give (i.e. females ‘groom up reason for that is that most primates (with the possible exception of the hierarchy’), which is exactly what has been found in most great apes: Barrett & Henzi, 2006) would lack the cognitive skills to primates (e.g. Schino, 2001). keep track of the value of multiple commodities over long time According to some authors, however, agonistic support is not a frames (see section Cognitive challenges). Even grooming would be common event in primates, and grooming is unlikely to be traded for grooming within single bouts, and this should be a exchanged for such an uncertain future benefit(Barrett & Henzi, crucial mechanism to maintain grooming dyads over time (Barrett 2006; Henzi & Barrett, 1999, 2007). Therefore, when individuals & Henzi, 2002, 2006; Henzi, Lycett, & Weingrill, 1997). Several groom up the hierarchy, they might exchange grooming for rank- studies have provided evidence that grooming given and grooming related benefits other than agonistic support, such as tolerance received are time matched within bouts (e.g. Barrett et al., 2002, over food or other commodities that higher-ranking individuals 1999; Chancellor & Isbell, 2009; Payne, Lawes, & Henzi, 2003). monopolize and might trade for grooming (Barrett & Henzi, 2006). However, most of these studies only analysed bouts in which both Moreover, when competition is low and resources cannot be individuals provided grooming (e.g. Barrett et al., 2002, 1999; monopolized, dominance gradients are usually shallow and higher- Chancellor & Isbell, 2009; see Gumert, 2007a, for a similar ranking individuals have few commodities to trade for grooming; approach in grooming e sex exchanges). In this way, up to 82% of all therefore, grooming should be mainly exchanged for grooming in a grooming bouts are completely dismissed from analyses (e.g. reciprocal way (Barrett, Gaynor, & Henzi, 2002; Barrett, Henzi, Chancellor & Isbell, 2009). The risk of only analysing bouts that Weingrill, Lycett, & Hill, 1999; Henzi et al., 2003). Consequently, already hint to some form of reciprocation is that different con- some authors have advocated the need for a more dynamic theory, clusions might be reached (see Manson, Navarrete, Silk, & Perry, better able to catch the variety of benefits that may be traded for 2004). Moreover, if grooming is reciprocated within bouts, why grooming, and have pointed out that exchanges might be affected are there so many bouts in which only one individual grooms the by the level of competition in a group and by whether it is possible other? to monopolize resources. In this respect, BMT was the perfect Other authors have also observed that primates often fail to candidate to improve, although not fully replace, Seyfarth's (1977) reciprocate within bouts, and suggested that primates might ex- model. change goods over an intermediate time frame (e.g. Frank, 2007; The main advantage of applying BMT to primate exchanges is Manson et al., 2004; Schino, di Giuseppe, & Visalberghi, 2009; that it offers a richer and more dynamic tool to understand the Schino, Polizzi di Sorrentino, & Tiddi, 2007). In bonnet macaques, complexity of primate interactions, as compared to Seyfarth's Macaca radiata, for instance, immediately reciprocated bouts ac- model. First, BMT offers a more individual-based approach, in count for only 5e7% of the total grooming observed, so that which individuals behave differently depending on the commod- grooming is significantly unbalanced over longer time spans ities traded and the interacting partners (Barrett & Henzi, 2006). (Manson et al., 2004). In line with this, de Waal (1997) found evi- Therefore, rather than exerting their control over the partner in dence that grooming is exchanged for (passive) food tolerance dyadic interactions, individuals freely choose their partners among within a 2 h time frame. Similarly, Fruteau, Voelkl, Van Damme, and all group members in order to maximize profit(Noe€ & Noe€ (2009) found that food is exchanged for grooming within 1 h, Hammerstein, 1994). Second, BMT takes into account dynamic leading them to talk about ‘exchange rates fluctuating from day to changes in the group: supply and demand determine the bartering day’ (Fruteau et al., 2009, p. 12007). value of commodities, and the ‘value’ of each partner changes To our knowledge, few studies have specifically analysed the through time depending on the commodities it can trade (Noe€ & time frame over which primate exchanges occur. Importantly, Hammerstein, 1994). However, if circumstances do not vary, it be- these studies also included bouts in which exchanges were not comes impossible to test whether exchanges follow the law of immediately reciprocated. Frank and Silk (2009) found that supply and demand, since by definition both of these variables grooming in olive baboons, Papio anubis, was more evenly remain constant (Barrett & Henzi, 2006). Finally, BMT provides an balanced across multiple bouts, rather than within single bouts. appealing alternative to the central role played by agonistic support Interestingly, most grooming bouts were completely one-sided, in Seyfarth's (1977) model, which despite being a sort of BM on its and females did not groom up the hierarchy, suggesting that own (according to Henzi et al., 2003), failed to consider the wide grooming is not reciprocated in the short term, but also not range of commodities that primates might exchange for grooming exchanged for other commodities. Two other studies were not (Henzi & Barrett, 1999). explicitly framed in line with BMT, but also found that great apes exchange commodities over long time frames (grooming e TIME FRAME OF EXCHANGES grooming: Gomes et al., 2009;sexe meat: Gomes & Boesch, 2009). Gomes et al. (2009), for instance, found that grooming in One problem of BMT, however, is that we do not know the exact chimpanzee, Pan troglodytes, dyads is reciprocated over a period of time frame over which exchanges take place. Are commodities 15 months. Similarly, Gomes and Boesch (2009) found that female exchanged within minutes, hours or even months? Determining chimpanzees copulate more with males having shared meat with the real time frame of interaction is a crucial problem for all studies them over a period of 22 months, but not in the short term. At analysing exchanges among individuals, even when they are not least in great apes, therefore, exchanges would happen on a long- explicitly framed in a BMT (e.g. Gomes & Boesch, 2009; Gomes, term basis. Importantly, by extending the time frame over which Mundry, & Boesch, 2009; see Schino & Aureli, 2010). Although it exchanges take place, these findings would also reconcile BMT might be difficult to determine the time frame over which animals (assuming that exchange of commodities drives the formation of exchange commodities, and over which BMT should be tested short-term finite relationships) with the cumulating evidence of (Barrett et al., 2002, 1999), understanding this time frame appears a long-lasting social bonds in primates, which appear to be robust crucial preliminary step to test BMT, rather than ‘an important goal through time and crucial for individuals' fitness (e.g. Langergraber, for the future’ (Barrett & Henzi, 2006, p. 231). Mitani, & Vigilant, 2007; Lehmann & Boesch, 2009; Mitani, 2009; So far, most authors have assumed that primates exchange Seyfarth & Cheney, 2012; Silk, Alberts, & Altmann, 2003; Silk commodities on a very short-term basis. Barrett and Henzi (2006), et al., 2009, 2010). A. Sanchez-Amaro, F. Amici / Animal Behaviour 110 (2015) 51e60 53

Determining the real time frame over which exchanges take control) with a protocol similar to that used by Fruteau et al. (2009). place is clearly a hard task, especially in primates, the species of In their study, exchanges of grooming were regularly monitored which differ significantly in terms of ecology, demography and across three phases: (1) a baseline phase, in which no experimental social structure. First, different species may use different time manipulations were introduced; (2) the experimental phase, in frames, reflecting their ability to keep track of values and exchanges which one individual allowed group members access to food; (3) a over longer periods (see section Cognitive challenges). Second, subsequent phase, in which more individuals provided food access even dyads belonging to the same group and species might ex- to group members. Comparisons of grooming across phases change over different time frames. In chimpanzee dyads, for allowed the researchers to see whether food access was exchanged instance, providing grooming increases instances of food sharing in for grooming, and the time frame over which these exchanges took the following hours, but the effect is stronger for those dyads rarely place. By carefully keeping other commodities constant across grooming each other (de Waal, 1997; but see Colmenares, Zaragoza, phases (e.g. no infants are born, no females are in oestrus, no other & Hernandez-Lloreda, 2002; Leinfelder, De Vries, Deleu, & Nelissen, food sources are monopolized), one could use this approach to test 2001). This suggests that individuals with looser bonds (e.g. rarely whether and when individuals are groomed in exchange for food grooming each other) might show more contingency-based ex- access. Importantly, by varying the commodity monopolized by changes, while individuals with stronger bonds might reciprocate individuals (e.g. access to food, outdoor areas, oestrous females, over longer time frames, because their relationship quality allows mothers with infants), we could understand whether different them to better tolerate unbalanced exchanges and reciprocate over commodities are exchanged across different time frames. If we longer time frames (see Cheney & Seyfarth, 2012). Third, in- could determine an exact time frame for exchanges, we could dividuals might discount commodities provided over a long time question its biological significance (e.g. why would primates ex- frame: primates are known to prefer immediate over delayed re- change some goods within the very same bout, but others within wards (e.g. Stevens, Hallinan, & Hauser, 2005), so that grooming months?), the mechanisms allowing these exchanges (see section provided today might not be the same as grooming received Cognitive challenges) and the validity of using the same time frame tomorrow. How should researchers take this into account when across different conspecific populations. analysing data? Fourth, the amount of data collected might affect Determining the time frame of exchanges appears to be a key the time frame over which exchanges of commodities correlate. issue in studies of primates, but might be less crucial in other When observations of particular events are scarce, power is low species. In a series of studies by Bshary, for instance, cleaners and and reciprocity might be revealed over longer time frames (e.g. client fishes interacted according to BMT (Bshary, 2001; Bshary and Gomes & Boesch, 2009). Therefore, simply increasing the hours of Grutter, 2002; Bshary & Grutter, 2002; Bshary & Schaffer,€ 2002). daily observations might lead to very different results (see However, the time frame over which commodities were exchanged Campennì & Schino, 2014). If grooming is provided randomly, for was not a real issue, as interactions (once established via partner instance, rates of grooming given and received tend to balance over choice) always involved the contextual exchange of the same two long periods of observation, providing another explanation as to commodities. In contrast to primates, individuals in other species why exchanges of commodities balance over several months, and might simply lack the chance to engage in exchanges over longer casting doubt on the existence of PBMs with long-term time frames time frames, by not living in the same cohesive long-lasting social (e.g. Frank & Silk, 2009; Gomes & Boesch, 2009; Gomes et al., group in which exchanges may be reciprocated over long time 2009). frames. Probably, the same issues raised for primates will instead Overall, these considerations cast doubt on the existence of a concern BMs in other species living in cohesive long-lasting social general time frame of interaction over which primate exchanges groups, such as social carnivores or marine mammals. take place. Therefore, although BMT provides no guideline to solve this issue, it is evident that we need to make clear, justified, specific COMMODITIES EXCHANGED a priori predictions on the exact time frame of exchanges, which presumably varies according to the species, individuals and cur- Grooming is highly valuable for primates, serving multiple rencies involved. Even if it were feasible to predict that chimpan- functions: it might strengthen social bonds (Dunbar, 1984), cement zees exchange sex for meat in 22 months (Gomes & Boesch, 2009) coalitions (Seyfarth & Cheney, 1984), produce endorphins (Keverne, but grooming for food in 2 h (de Waal, 1997), which would be the Martensz, & Tuite, 1989), serve a hygienic function (Hutchins & biological significance of our prediction? In their brilliant review, Barash, 1976; Saunders & Hausfater, 1988; Tanaka & Takefushi, Gilby, Thompson, Ruane, and Wrangham (2010) noted how sur- 1993; Zamma, 2002), modulate immune system changes (see prising it is that meat sharing predicts long-term, but not short- Gust, Gordon, Brodie, & McClure, 1996) and reduce tension (Aureli, term mating frequency in Gomes and Boesch's (2009) study. Why Preston, & de Waal, 1999; Schino, Rosati, & Aureli, 1998). According should males give meat to oestrous females who will only recip- to BMT, grooming is thus both a valuable commodity and a currency rocate with mating within 22 months? Finally, consistency in the to exchange for other commodities (Barrett & Henzi, 2001; Barrett interpretation of results is needed. When analyses are limited to et al., 1999). However, the intrinsic costs and benefits of grooming immediately reciprocated exchanges (because exchanges would are still debated (see Kaburu & Newton-Fisher, 2015; Russell & happen in the short term), longer-term consequences should not be Phelps, 2013; Schino, Ventura, & Troisi, 2003), and its multiple inferred. If it is assumed that exchanges happen in the same bout, functions might make grooming ambiguous to interpret (see for instance, one should not conclude that grooming that is not Colmenares et al., 2002; Metz, Klump, & Friedl, 2007). For example, immediately reciprocated in a bout might be reciprocated over a grooming might have a different value across species (see Barrett & longer time frame (Chancellor & Isbell, 2009). Similarly, if grooming Henzi, 2006; Manson et al., 2004), and ‘not all instances of is predicted to be exchanged for sex in the same bout, there is no grooming need represent ‘market trading’’ (Barrett & Henzi, 2006, reason to infer that grooming might also secure more sexual op- p. 216), meaning that some grooming might not be traded for other portunities after the bout (Gumert, 2007a). commodities. However, the effect of these variables cannot be In the future, experimentally controlled studies should be easily predicted or quantified. Furthermore, according to BMT, implemented to improve our understanding of the time frame over grooming is largely exchanged for other commodities when hier- which exchanges take place. One possible approach could be to test archies are steep (and higher-ranking individuals manipulate captive populations (where confounding variables are easier to commodities), and is highly reciprocal when hierarchies are 54 A. Sanchez-Amaro, F. Amici / Animal Behaviour 110 (2015) 51e60 swallow (and commodities cannot be monopolized; Barrett et al., support (e.g. Carne et al., 2011; Koyama, Caws, & Aureli, 2006; 2002, 1999; Henzi et al., 2003). However, all individuals exchange Schino, 2007; Schino et al., 2007; but see Silk, Alberts, & grooming with each other and grooming is thus always partly Altmann, 2004; Stevens, Vervaecke et al., 2005), although this reciprocal, regardless of the dominance gradient (Barrett & Henzi, might require planning skills that most primates would lack 2006). For instance, grooming might be traded for grooming also (Barrett & Henzi, 2006; see section Cognitive challenges). Some when hierarchies are steep and conditions ‘stressful’ studies have also found a positive correlation between grooming (Balasubramaniam, Berman, Ogawa, & Li, 2011, p. 1269), or if ‘the provided and aggression received (e.g. Gumert & Ho, 2008; Port, sole benefits that grooming itself offers’ are enough (Henzi & Clough, & Kappeler, 2009; Schino, Ventura, & Troisi, 2005; Xia Barrett, 1999, p. 54). Consequently, the steepness of the hierarchy et al., 2012, 2013): some individuals might ‘extort’ grooming by provides only partially reliable indications of the commodities that the threat of force, and partners might groom them more to reduce individuals would exchange. aggression (e.g. Barrett & Henzi, 2006; Schino et al., 2005). How- If grooming can be traded for different commodities (e.g. ever, the risk lurking in this elegant explanation is that any result grooming, food, tolerance at feeding or drinking sites, access to can be a posteriori interpreted as evidence of BM: if A provides food infants, preferential mating, agonistic support), which percentage to B, B will groom A in exchange (e.g. Fruteau et al., 2009); but if A is of grooming given should we correlate with the amount of each aggressive to B, B will also groom A in exchange (e.g. Schino et al., commodity received, when testing BMT? Correlating grooming 2005). Moreover, how can we know how much of the grooming with more than one commodity is no solution: if grooming is a provided is paid in exchange for some commodity (e.g. agonistic currency paid in exchange for some commodity according to the support, tolerance) and how much serves an appeasement func- law of supply and demand, the same amount of grooming cannot be tion, being exchanged for a commodity that we cannot measure exchanged for more than one commodity (e.g. Carne, Wiper, & (e.g. lack of aggression)? In the end, given that PBM should be a free Semple, 2011). In turn, commodities might be exchanged with market in which individuals do not compete aggressively over re- each other. For instance, different studies have shown that sources (Noe€ & Hammerstein, 1994; but see Bshary, 2001; Clutton- grooming is traded for sex (e.g. Gumert, 2007a), sex for food (e.g. Brock & Parker, 1995), the mere possibility that some individuals Gomes & Boesch, 2009) and food for grooming (e.g. Fruteau et al., might be aggressive to ‘extort’ other commodities might be seen as 2009). How can we predict the complex ways in which all these a distortion of market forces and used to explain negative results commodities might be exchanged with each other? Note that the that otherwise would not fit BMT (e.g. Balasubramaniam et al., problem is not solved by analysing only those bouts in which two 2011; Gumert, 2007b; Kaburu & Newton-Fisher, 2015). Impor- commodities are exchanged: first, commodities might be tantly, these findings also cast doubt on the possibility of realisti- exchanged with each other also across bouts (see section Time cally considering primate groups as BMs: primates generally appear frame of exchanges); second, some grooming in a grooming bout to aggressively compete to access partners and resources (i.e. might not represent ‘market trading’; and third, even within the partner control), in contrast to the assumption of BMT, according to same bout individuals might exchange more than two which individuals would freely choose their partners depending on commodities. the commodities available on the market (e.g. Noe€ & Hammerstein, Another approach is to analyse how grooming is distributed 1994). among group members: if grooming is not exactly reciprocated, Furthermore, some studies have shown that primates recipro- and higher-ranking individuals receive more grooming than they cate grooming to a lesser extent when the hierarchy is steep, as give, it is assumed that grooming is traded in exchange for com- predicted by BMT, but have failed to provide evidence that modities that only higher-ranking individuals can provide (Barrett grooming is exchanged for other rank-related commodities (e.g. et al., 1999; Henzi et al., 2003). Meta-analyses, for instance, have Balasubramaniam et al., 2011; Stevens, Vervaecke et al., 2005). shown that primates often groom up the hierarchy, suggesting that Recently, Kaburu and Newton-Fisher (2015) failed to find evidence grooming is exchanged for rank-related benefits (Schino, 2001; that chimpanzees with a steeper hierarchy trade grooming for Schino & Aureli, 2008). However, this is not always the case, even agonistic support, while chimpanzees in more egalitarian groups when dominance hierarchies are steep and individuals should groom more reciprocally. Instead of concluding that grooming groom up the hierarchy (e.g. Balasubramaniam et al., 2011; reciprocity was not affected by hierarchy steepness and that their Colmenares et al., 2002; Leinfelder et al., 2001; Schino et al., study thus provides no evidence of a BM, they argued that 2003). Moreover, grooming up the hierarchy is per se no proof of ‘grooming is sufficiently valuable to male chimpanzees that they BM, as this explanation also fits Seyfarth's model. To prove BMT, will continue to trade for it when other services are available and one would also need to show that there is really an exchange taking for which they also trade’ (Kaburu & Newton-Fisher, 2015, p. 68). place, and that this exchange happens according to the laws of Moreover, they argued that by providing benefits to reproductive supply and demand, by, for instance, being stronger in groups with rivals, grooming should be given in a limited amount. Of course, it a steeper dominance hierarchy. What evidence do we have so far makes sense to consider grooming as a valuable commodity. The for exchanges of commodities following the laws of supply and question is whether we can find a priori a reason why grooming demand in primates? should be a highly valuable commodity in some chimpanzee groups, and thus always be reciprocally exchanged (Kaburu & Grooming for Tolerance, Agonistic Support, Aggression Newton-Fisher, 2015), but not in baboons (e.g. Barrett & Henzi, 2006), or whether we are once again running the risk of making Primates can trade grooming for increased tolerance over food our findings fit BMT with a posteriori interpretations. (e.g. Barrett et al., 2002; Carne et al., 2011; Richter, Mevis, Malaivijitnond, Schülke, & Ostner, 2009; Tiddi, Aureli, Polizzi di Grooming for Access to Infants Sorrentino, Janson, & Schino, 2011; Ventura, Majolo, Koyama, Hardie, & Schino, 2006; de Waal, 1997; but see Frank, 2007; It is also controversial whether primates trade grooming for Fruth & Hohmann, 2002; Kaburu & Newton-Fisher, 2015; Molesti access to infants. According to BMT, if infants are a valuable com- & Majolo, 2015; Stevens, Vervaecke, de Vries, & van Elsacker, 2005; modity, females should groom mothers to access their infants, and Surbeck & Hohmann, 2014; Vervaecke, De Vries, & Van Elsacker, should do that more when the number of infants decreases 2000; Watts, 2002). They may also trade grooming for agonistic (Fruteau, van de Waal, Van Damme, & Noe,€ 2011; Gumert, 2007b; A. Sanchez-Amaro, F. Amici / Animal Behaviour 110 (2015) 51e60 55

Henzi & Barrett, 2002; but see Fruteau et al., 2011, for reasons why however, raises several methodological issues, including the giving an infant is also good for mothers). In most studies, however, exclusion of all those grooming and mating instances that did not the amount of grooming provided to access infants did not fluc- happen in the same bout (see section Time frame of exchanges), the tuate depending on the law of supply and demand (Frank & Silk, use of a questionable proxy of female availability (see section 2009; Lazaro-Perea, de Fatima Arruda, & Snowdon, 2004; Payne Cognitive challenges), and the analysis of grooming given and et al., 2003; Slater, Schaffner, & Aureli, 2007; Tiddi, Aureli, & Schino, received as if they were two completely independent measures (see 2010). Interestingly, affiliative behaviours might be simply pro- section Methodological issues). Therefore, more evidence is needed vided to mothers as a signal of benign intent, having no market to claim that grooming is exchanged for sex according to BMT. value (Slater et al., 2007; Tiddi et al., 2010). This would also explain Overall, there is no convincing evidence for the existence of a why mothers need to be groomed longer when few infants are PBM in which individuals exchange meat or grooming for sex, or available (Tiddi et al., 2010), or when they are higher-ranking in- grooming for infant handling or social tolerance. There are several dividuals (Gumert, 2007b; Henzi & Barrett, 2002): more grooming reasons why researchers might have failed to consistently detect would be needed to calm down mothers (and access their infants) BMs for these commodities: exchanges might have involved other/ when infants are scarce and mothers might be more frequently multiple commodities, they might have happened in another time harassed, or when mothers are higher-ranking individuals and thus frame, or they might have simply not followed the law of supply potentially more dangerous to approach. and demand. In some cases, it is possible that other contingent effects altered the value of commodities (e.g. grooming might be Meat for Sex more valuable after a stressful event). In other cases, the changes in circumstances (required to detect BMs: Barrett & Henzi, 2006) Even more controversial is the existence of a BM in which males might have simply not been salient enough to trigger a change in trade meat with females in exchange for mating opportunities partners' value. In this respect, it is possible that only especially rare (Stanford, 1996). Few studies have provided evidence that male commodities are salient enough to alter long-term bonds, which chimpanzees are more likely to hunt when oestrous females are are based on the long-term reciprocal exchange of frequent com- available (Stanford, Wallis, Mpongo, & Goodall, 1994; but Gilby, modities (e.g. grooming). However, it is clear that the frequency of Eberly, Pintea, & Pusey, 2006; Gilby & Wrangham, 2008; Mitani commodities probably varies across species/populations and & Watts, 2001), and preferentially share meat with oestrous fe- through time, so that if grooming and tolerance may be generally males (Teleki, 1973; Watts & Mitani, 2002; but Gilby, 2006; Gilby considered a frequent commodity, for instance, frequency of infant et al., 2010). Similarly, some authors have shown that mating handling strongly depends on the species' reproductive rates increase after meat has been shared (Gomes & Boesch, 2009; characteristics. Stanford, 1998; but Gilby, 2006; Gilby et al., 2010; Mitani & Watts, In the future, more experimentally controlled studies are 2001; Watts & Mitani, 2002). However, positive evidence of a BM is needed to understand which commodities are exchanged accord- scant and has important limits. Theoretically, for instance, there is ing to BMT. Experimentally manipulating the frequency of certain no reason why female chimpanzees would need meat as an commodities (e.g. providing access to common versus rare food) incentive to overcome a reluctance to mate, given that promiscuous might provide insight as to whether commodities are exchanged mating might have several benefits (see Gilby et al., 2010). More- according to BMT only if their frequency falls below a certain over, female mate choice probably plays a very minor role in threshold. After predetermining the time frame of exchanges (see chimpanzees (Feldblum et al., 2014; Muller, Emery-Thompson, section Time frame of exchanges), experimental manipulations like Kahlenberg, & Wrangham, 2011), so that males could hardly in- those implemented by Fruteau et al. (2009) should assess BMs crease their reproductive success by exchanging meat for sex (see when individuals can only exchange two commodities (e.g. when Gilby et al., 2010). Methodologically, these studies are also prob- no infants are born, no females are in oestrus and no other food lematic, by using too broad a definition (of ‘oestrous’: Stanford sources can be monopolized). Once there are baseline results on the et al., 1994;of‘sharing’: Teleki, 1973) or failing to compare find- way two commodities are exchanged (e.g. grooming for food ac- ings with baseline controls (e.g. Stanford, 1998; Watts & Mitani, cess), some of the tested individuals should be provided with a 2002). Even Gomes and Boesch (2009) found no evidence of further commodity to trade (e.g. sex, when females go into oestrus), short-term exchanges of meat for sex, and no dyadic correlation to monitor how PBMs are affected by the availability of more between the amount of meat shared and the number of copula- commodities and how interactions vary when individuals are tions. While convincing evidence remains scant in the short term, it confronted with these changes. Importantly, experimental manip- is possible that sharing and mating are not causally linked in the ulations should be replicated in the same population regardless of long term, and males skilled at obtaining and sharing meat are the identity of the individuals involved, as well as across conspecific preferred sexual partners for reasons other than meat sharing (see populations and over time. Supply and demand being equal (e.g. Gilby et al., 2010). There is, therefore, still no conclusive evidence of number of individuals per food provided, number of oestrous fe- a BM in which males share meat in exchange for mating males per adult male), results should be consistent over time and opportunities. across individuals and populations, if exchanges really depend on the law of supply and demand. On the other hand, if primate ex- Grooming for Sex changes depend on the existence of social relationships resistant to contingent changes in resource availability, we would expect no Finally, some researchers have investigated whether grooming consistent patterns across individuals and populations, as well as is exchanged for sex. Some studies, for instance, have shown that temporal fluctuations independent of variations in supply and de- males groom oestrous females more frequently than anoestrous mand. Finally, a meta-analytical approach could be used to detect ones (e.g. Colmenares et al., 2002; Hemelrijk, VanLaere, & van patterns of similarities across studies and construct an intervening Hooff, 1992; Norscia, Antonacci, & Palagi, 2009; but Cooper & variable better capturing the network of causal connections among Bernstein, 2000). More relevantly for BMT, in Gumert's (2007a) dependent and independent variables in BMs (see Aureli & Whiten, study, male crab-eating macaques, Macaca fascicularis, groomed 2003). females in exchange for sex, and grooming duration was linked to Some of the concerns expressed for PBM do not apply to other the availability of females around the interaction. This last study, species, simply because these might have fewer commodities to 56 A. Sanchez-Amaro, F. Amici / Animal Behaviour 110 (2015) 51e60 trade. Cleaner fishes, for instance, can only offer removal of ecto- Alternatively, some authors have tried to reduce the cognitive parasites to their clients, while their clients can only offer food complexity of PBMs by assuming that all exchanges are based on transport to the cleaner's territory, resulting in an easier form of BM their current needs and the immediate availability of commodities (see Bshary, 2001). In contrast, testing BMT in cooperative breeders (Barrett & Henzi, 2002, 2006; Barrett et al., 1999). This assump- might imply similar challenges to primates. In meerkats, Suricata tion, however, is problematic. First, it limits the BM to a series of suricatta, for example, the majority of individuals do not reproduce, immediate exchanges, in which primates are blind to the past and but help female breeders to raise their offspring: according to BMT, the future (see Gilby, 2013). Second, it might mislead researchers the more helpers are available, the fewer the commodities helpers to only take into account behaviours that are immediately should receive from breeders in exchange for their help (e.g. exchanged in the very same bout, excluding relevant amounts of Kutsukake & Clutton-Brock, 2010). However, as in primates, com- data (see section Time frame of exchanges). Third, it disregards the modities traded can be multiple (e.g. infant protection, tolerance or fact that other researchers have found exchanges to happen over access to resources by helpers, in exchange for tolerance, lack of longer time frames (see e.g. Schino & Aureli, 2010; section Time aggression or access to resources by breeders), making predictions frame of exchanges), or with commodities such as agonistic sup- unclear and BMT harder to test. port that are not always immediately available (see section Commodities exchanged). Fourth, some authors have found that individuals groom in anticipation of future need, by for instance COGNITIVE CHALLENGES grooming in exchange for future tolerance at feeding sites (de Waal, 1997). Finally, this assumption does not drastically reduce In contrast to Seyfarth's (1977) model, partner choice plays a the cognitive challenges of PBMs, in that primates would still need crucial role in BMT (Noe€ & Hammerstein, 1994). Rather than a se- to be able to assess (although just in the immediate present) the ries of long-term dyadic interactions in which one subject exerts number of potential competitors and partners, and thus the rela- control over the other, BMT envisions primate relationships as a tive value of the different commodities to be exchanged. There- series of short-term polyadic interactions in which individuals fore, it is still unclear which level of cognitive complexity is continually choose the best available partners depending on the required for primates to trade in BMs, and whether all primates offer and demand. This approach poses several problems, in that possess these skills. evidence of long-term relationships in primates is abundant (e.g. In the future, research will need to better assess whether Langergraber et al., 2007; Lehmann & Boesch, 2009; Mitani, 2009; emotional book keeping can alone account for the complex ex- Seyfarth & Cheney, 2012; Silk et al., 2003, 2009, 2010), and it is no changes predicted by PBMs, involving multiple commodities and easy task to reconcile the coexistence of long-term social bonds and partners over long time frames. If primates navigate across poten- short-term fluctuations as predicted by BMT. Similarly, although tial partners and commodities by cognitively tracking previous social relationships are probably a combination of both dyadic exchanges with other partners, tracking and comparing the relative partner control and polyadic partner choice, BMT largely fails to value of the different commodities available and the number of take into account the interplay of both strategies. Another major potential competitors, they will need enhanced cognitive skills, for problem is that in order to select the best partner, individuals must instance in terms of memory and ability to quantify. If future not simply keep track of previous exchanges with every partner, but studies find convincing evidence of PBMs in primates that fail to also be able to track and compare the relative value of the different show these skills (as tested in the laboratory with ad hoc cognitive commodities available from each potential partner, and the number tasks), further support would be provided for the hypothesis that of potential competitors (although the effects of demand on the primates rely on emotional book keeping to navigate in BMs. exchange of commodities have not yet received similar attention to In other species, BMs are necessarily limited to a series of im- the effect of supply). mediate exchanges. In cleaner e client fish relationships, for In dyadic interactions, emotions might help primates keep track instance, exchanges of commodities happen in the short term, of resources and maintain cooperative exchanges through time, drastically reducing the cognitive complexity of such a BM. When without requiring complex cognitive skills (Brosnan & de Waal exchanges happen over a longer-term frame, as in the case of 2002; Schino & Aureli, 2009; de Waal, 2000). While emotional cooperative breeders, the same issues raised for primates apply: if book keeping might well work at the dyadic level, helping primates exchanges are not based on current needs and immediately avail- to keep (emotional) track of past relationships, it is harder to able commodities, emotional book keeping might provide a imagine that emotional book keeping might be a useful tool when cognitively less challenging tool to efficiently navigate in BMs. the value of different commodities, potential partners and com- petitors should be assessed and compared in the complex way of METHODOLOGICAL ISSUES PBMs. Gumert (2007a), for instance, explained how emotional book keeping would work in a BMT: grooming would alleviate stress/fear A much less theoretical problem is that most studies have used involved in social interactions, facilitating the trade of commod- very different methods to test BMT. This does not facilitate com- ities. Similarly, the other ‘parameters of the social market may parisons across studies, and raises questions on whether the trigger physiological states that modulate how motivated males appropriate methods are always used. In most studies, for instance, and females are to cooperate depending on the abundance of po- grooming is included as the main currency being exchanged. tential partners and competitors’ (Gumert, 2007a, p. 1666). However, different criteria are used to quantify grooming. In some Possibly, when competition over a resource is high, other in- studies, grooming is measured in terms of frequency of grooming dividuals may also feel the urge to compete over the same resource bouts (e.g. Stevens, Vervaecke et al., 2005), while in others in terms (maybe via emotional contagion), increasing the commodity of duration of grooming (e.g. Kaburu & Newton-Fisher, 2015). If offered in exchange (so that the value of commodities increases grooming is a currency exchanged for other commodities, however, when there are more competitors). Although this hypothesis de- it seems plausible that grooming duration should be a more reliable serves attention, operationalizing it is no easy task should different measure: why should primates prefer being groomed twice for a psychological states be triggered by the number of potential part- total of 2 min, for instance, rather than just once for 5 min? On the ners, by the ratio of potential partners per competitors, or by an contrary, the fact that the frequency of grooming bouts or the approximation of this ratio, as in Gumert (2007a)? categorical occurrence of grooming (rather than its duration) A. Sanchez-Amaro, F. Amici / Animal Behaviour 110 (2015) 51e60 57 sometimes predicts exchanges with other commodities might of two individuals grooming as long, but being often in proximity suggest that the function of grooming is to communicate benign without grooming. intent to partners and facilitate exchanges (see e.g. Tiddi et al., Finally, analyses of data also largely differ across studies. Some 2010), rather than to serve as a currency to be exchanged accord- studies, for example, include all instances in which specific be- ing to the law of supply and demand. haviours have been observed, while others only include behaviours Interestingly, there is not even consensus on the definition of a observed during reciprocal bouts (e.g. Barrett et al., 2002, 1999; grooming bout. While some studies consider grooming bouts to Chancellor & Isbell, 2009; Gumert, 2007a). As already discussed end when grooming is suspended for more than 10 s (e.g. Barrett (see section Time frame of exchanges), however, this might lead to et al., 1999; Henzi & Barrett, 2002; Tiddi et al., 2010), others the exclusion of very large portions of data (e.g. Chancellor & Isbell, consider grooming bouts to end after 20 s (Fruteau et al., 2009), 30 s 2009). Knowing at least how many data points have been excluded (e.g. Fruteau et al., 2011; Gumert, 2007a), 1 min (e.g. Chancellor & might be extremely informative about the strength of results, but Isbell, 2009; Manson et al., 2004), 2 min (e.g. Payne et al., 2003) this information is not always included (e.g. Gumert, 2007b). or even 5 min (e.g. Port et al., 2009). In other studies, no informa- Primate species differ strongly in their biology and socioecology. tion is provided on when grooming bouts are considered to end Therefore, a general agreement on the methodological approach to (e.g. Balasubramaniam et al., 2011; Koyama, Caws, & Aureli, 2012; be used is not always possible or desirable (e.g. in terms of obser- Norscia et al., 2009). Although practical issues linked to the visi- vational techniques chosen or length of grooming bouts). However, bility of primates and the socioecology of species might partly there is no reason why different approaches are used for the same explain methodological differences, such inconsistencies must species. Even across different taxa, the number of observation surely affect the analysis of data, especially if analyses only include hours should not be the casual result of practical contingencies, but exchanges happening in the same bout or use frequencies of have a strong ecological justification, as it might significantly affect grooming bouts as the dependent variable (but bouts are defined in the results of analyses. Similarly, regardless of the species tested, it always different ways). would be important to avoid excluding large parts of data sets, by Similarly, observations are often done using different tech- also including nonimmediately reciprocated bouts, and to refrain niques, spanning from focal sampling (e.g. Carne et al., 2011; Clarke, from a posteriori explanations, which might bias the interpretation Halliday, Barrett, & Henzi, 2010) to ad libitum sampling (e.g. of negative results according to BMT. Unless explicitly justified, Gumert, 2007b), combinations of ad libitum and focal sampling future studies should use duration instead of frequency of groom- (e.g. Fruteau et al., 2011), and combinations of scan and focal ing, while controlling grooming given for grooming received and sampling for shorter (e.g. Barrett et al., 1999; Henzi et al., 2003)or association time. longer observation sessions (e.g. Kaburu & Newton-Fisher, 2013). Similar considerations apply to species other than primates. Of course, the choice of observation techniques largely reflects Whenever possible, the use of similar methodological approaches socioecological aspects of the group and species studied, but as all facilitates comparisons and strengthens findings. The number of these studies aim to test the same hypothesis (e.g. whether pri- observation hours should be ecologically justified, data should not mates exchange commodities according to the law of supply and be excluded, and commodities should be quantified in a consistent demand), such a variety of approaches is partly unjustified. Another way, taking into account association time and the interdependence important aspect is the difference in the number or duration of of multiple commodities whenever needed. observations across studies. Some studies, for instance, provide no exact information on the number of observation hours that have Conclusion been implemented (e.g. Gumert, 2007b) or on the hours of grooming observed (e.g. Barrett et al., 1999). This is not as trivial as To date, BMT is still one of the most comprehensive theories it might seem, given that more observations provide more power to explaining the exchange of commodities among classes of in- the analyses, so that reciprocity might be detected over shorter dividuals. In a variety of research areas, it has proved a reliable tool time frames when observations are more frequent (see section to predict social interactions across conspecifics and members of Time frame of exchanges). different species (e.g. Barclay, 2013; Cowden & Peterson, 2009; Furthermore, grooming bout frequency/grooming duration can Schwartz & Hoeksema, 1998). Even in primates, the BTM has undergo different transformations before being analysed. Some often been used to explain the complex exchanges of commodities studies, for instance, have analysed the exchange of grooming given that characterize this taxon. The main strength of the PBM is its with other commodities, without controlling for grooming received complexity: multiple variables interact flexibly and predict ex- (e.g. Gumert, 2007a). This method, however, can be problematic, changes among individuals, largely reflecting the complexity of real because grooming given might fluctuate within dyads depending social interactions. In contrast to other theories, for instance, BMT on grooming received, and independently of other commodities recognizes the central role played by partner choice, introduces available in the BM. In other studies, therefore, grooming given and new resources that primates can exchange for grooming, ac- grooming received within each dyad are analysed as a ratio, which knowledges temporal variation in the value of commodities, and might be a more informative measure of the grooming relationship accepts the existence of high interindividual variability in the way between individuals (e.g. Fruteau et al., 2009; Payne et al., 2003; primates exchange commodities. Port et al., 2009). If it is true that grooming is always partly recip- Ironically, however, this complex, dynamic, individual-based rocal (e.g. Barrett & Henzi, 2006; Henzi & Barrett, 1999), exploring approach is also the main weakness of BMT: predictions are not the relation between grooming given and other commodities always straightforward and easy to test, and when results fail to received, while controlling for grooming received, might be the match them, several alternative explanations may be proposed a safest approach. However, grooming given and grooming received posteriori to still explain results in a BMT framework (e.g. aggres- have often been linked using complex indexes, whose rational is sion might have distorted market forces, grooming might not be not always evident (e.g. Barrett et al., 2002; Henzi et al., 2003; that valuable for a certain species, some instances of grooming Kaburu & Newton-Fisher, 2015). Similarly, grooming given should must have been exchanged for other commodities or in other time also be controlled for association time between subjects. If two frames, and so on). If individuals really balance costs and benefits of individuals spend little time together, but most of this time is spent commodities across partners and bouts (e.g. Schino et al., 2003), grooming, their relationship probably has a higher quality than that depending on the social characteristics of conspecifics (e.g. Gumert, 58 A. Sanchez-Amaro, F. Amici / Animal Behaviour 110 (2015) 51e60

2007b), on the relative value of the different commodities and on Barrett, L., & Henzi, S. P. (2006). Monkeys, markets and minds: biological markets the number of potential competitors (e.g. Carne et al., 2011), then and primate sociality. In P. M. Kappeler, & C. P. van Schaik (Eds.), Cooperation in primates and humans: Mechanisms and evolution (pp. 209e232). Berlin, Ger- complexity is so high and exchanges affected by so many variables, many: Springer. that predicting and testing them all might be simply impossible. Barrett, L., Henzi, S. P., Weingrill, T., Lycett, J. E., & Hill, R. A. (1999). Market forces How can we test whether an excess of meat in exchange for sex, for predict grooming reciprocity in female baboons. Proceedings of the Royal Society B: Biological Sciences, 266,665e670. http://dx.doi.org/10.1098/rspb.1999.0687. instance, has not been paid back (in a different time frame) by Becker, J. H. A., & Grutter, A. S. (2005). Client fish ectoparasite loads a cleaner shrimp asking for less grooming to handle infants? Perhaps not surpris- Urocaridella sp. c hunger levels affect cleaning behavior. Animal Behaviour, 70, ingly, the most convincing examples of BM to date are those 991e996. http://dx.doi.org/10.1016/j.anbehav.2005.01.004. Brosnan, S. F., & de Waal, F. B. (2002). A proximate perspective on reciprocal involving species other than primates, in which few commodities altruism. Human Nature, 13,129e152. http://dx.doi.org/10.1007/s12110-002- can be exchanged over a very short time frame (e.g. Becker & 1017-2. Grutter, 2005; Hellmann et al., 2015; Wyatt, Kiers, Gardner, & Bshary, R., & Grutter, A. S. (2002). Experimental evidence that partner choice is a driving force in the payoff distribution among cooperators or mutualists; the West, 2014). cleaner fish case. Ecology Letters, 5,130e136. http://dx.doi.org/10.1046/j.1461- Although we see no clear solution to the excessive complexity of 0248.2002.00295.x. PBMs, we have provided some possible solutions that might help Bshary, R. (2001). The cleaner fish market. In R. Noe,€ J. A. R. A. M. van Hooff, & address the main issues raised in this essay: the time frame over P. Hammerstein (Eds.), Economics in nature: Social dilemmas, mate choice and biological markets (pp. 146e172). Cambridge, U.K.: Cambridge University Press. which exchanges take place, the commodities exchanged in PBMs, Bshary, R., & Grutter, A. S. (2002). Asymmetric cheating opportunities and partner the cognitive challenges imposed by PBMs and consistency in the control in a cleaner fish mutualism. Animal Behaviour, 63,547e555. http:// methodological approach. Only after addressing these issues shall dx.doi.org/10.1006/anbe.2001.1937. Bshary, R., & Schaffer,€ D. (2002). Choosy reef fish select cleaner fish that provide we be able to understand whether primates can still be considered high-quality service. Animal Behaviour, 63, 558e564. http://dx.doi.org/10.1006/ ‘to be in the market’. Although the largest majority of studies have anbe.2001.1923. so far provided no convincing support to the existence of PBMs, Campennì, M., & Schino, G. (2014). Partner choice promotes cooperation: the two faces of testing with agent-based models. Journal of Theoretical Biology, 344, only more systematic studies addressing the theoretical and 49e55. http://dx.doi.org/10.1016/j.jtbi.2013.11.019. methodological issues reviewed here might provide us with reli- Carne, C., Wiper, S., & Semple, S. (2011). Reciprocation and interchange of grooming, able conclusions on the realistic applicability of BMT to primates. agonistic support, feeding tolerance, and aggression in semi-free-ranging Bar- bary macaques. American Journal of Primatology, 73,1127e1133. http:// Our hard task for the future is to transpose the complexity of real dx.doi.org/10.1002/ajp.20979. social interactions into a series of clear predictions which can be Chancellor, R. L., & Isbell, L. A. (2009). Female grooming markets in a population of easily tested and interpreted. To date, the complex interactions of gray-cheeked mangabeys (Lophocebus albigena). Behavioral Ecology, 20,79e86. fl http://dx.doi.org/10.1093/beheco/arn117. multiple factors might often allow an exaggerated exibility in the Cheney, D. L., & Seyfarth, R. M. (2012). The evolution of a cooperative social mind. In interpretation of results. Of course, all hypotheses might be true, J. Vonk, & T. Shackelford (Eds.), Oxford Handbook of Comparative Evolutionary but a theory that does not allow clear testable predictions has Psychology (pp. 507e528). Oxford, U.K.: Oxford University Press. probably lost much of its utility. Clarke, P. M. R., Halliday, J. E. B., Barrett, L., & Henzi, S. P. (2010). Chacma baboon mating markets: competitor suppression mediates the potential for intersexual exchange. Behavioral Ecology, 21, 1211e1220. http://dx.doi.org/10.1093/beheco/ arq125. Acknowledgments Clutton-Brock, T. H., & Parker, G. A. (1995). Punishment in animal societies. Nature, 373, 209e216. http://dx.doi.org/10.1038/373209a0. We thank Filippo Aureli and two anonymous referees for useful Colmenares, F., Zaragoza, F., & Hernandez-Lloreda, M. V. (2002). Grooming and coercion in one-male units of hamadryas baboons: market forces or relation- comments on the manuscript. We are also grateful to Josep Call, for ship constraints? Behaviour, 139, 1525e1553. http://dx.doi.org/10.1163/ allowing us to collect data for a related project on PBMs at the 15685390260514753. Wolfgang Koehler Primate Research Center in the Leipzig Zoo, Cooper, M. A., & Bernstein, I. S. (2000). Social grooming in Assamese macaques e Germany, and to Carla Sebastian-Enesco and Victor Bravo for (Macaca assamensis). American Journal of Primatology, 50,7785. http:// dx.doi.org/10.1002/(SICI)1098-2345. helping in data collection and inspiring discussions. Thanks also to Cowden, C. C., & Peterson, C. J. (2009). A multi-mutualist simulation: applying Barbara Tiddi for suggesting the title and sharing ideas. F.A. is also biological market models to diverse mycorrhizal communities. Ecological e grateful to Anna Albiach-Serrano and Trix Cacchione for always Modelling, 220, 1522 1533. http://dx.doi.org/10.1016/j.ecolmodel.2009.03.028. Dunbar, R. I. M. (1984). Reproductive decisions: An economic analysis of gelada baboon stimulating, critical, constructive thought. social strategies. Princeton, NJ: Princeton University Press. Dunbar, R. I. M. (1992). Neocortex size as a constraint on group size in primates. Journal of Human Evolution, 22, 469e493. http://dx.doi.org/10.1016/0047- References 2484(92)90081-J. Feldblum, J. T., Wroblewski, E. E., Rudicell, R. S., Hahn, B. H., Paiva, T., Cetinkaya- Aureli, F., Preston, S. D., & de Waal, F. (1999). Heart rate responses to social in- Rundel, M., et al. (2014). Sexually coercive male chimpanzees sire more teractions in free-moving rhesus macaques (Macaca mulatta): a pilot study. offspring. Current Biology, 24, 2855e2860. http://dx.doi.org/10.1016/ Journal of Comparative Psychology, 113, 59. http://dx.doi.org/10.1037/0735- j.cub.2014.10.039. 7036.113.1.59. Frank, R. E. (2007). The role of contingent reciprocity and market exchange in the lives Aureli, F., & Whiten, A. (2003). Emotions and behavioral flexibility. In D. Maestripieri of female olive baboons. PhD dissertation. Anthropology Department, UCLA. (Ed.), Primate psychology (pp. 289e323). Cambridge, MA: Harvard University Frank, R. E., & Silk, J. B. (2009). Impatient traders or contingent reciprocators? Ev- Press. idence for the extended time-course of grooming exchanges in baboons. Balasubramaniam, K. N., Berman, C. M., Ogawa, H., & Li, J. (2011). Using biological Behaviour, 146,1123e1135. http://dx.doi.org/10.1163/156853909X406455. € markets principles to examine patterns of grooming exchange in Macaca thi- Fruteau, C., van de Waal, E., Van Damme, E., & Noe, R. (2011). Infant access and betana. American Journal of Primatology, 73, 1269e1279. http://dx.doi.org/ handling in sooty mangabeys and vervet monkeys. Animal Behaviour, 81, 10.1002/ajp.20999. 153e161. http://dx.doi.org/10.1016/j.anbehav.2010.09.028. € Barclay, P. (2013). Strategies for cooperation in biological markets, especially for Fruteau, C., Voelkl, B., Van Damme, E., & Noe, R. (2009). Supply and demand humans. Evolution and Human Behavior, 34,164e175. http://dx.doi.org/10.1016/ determine the market value of food providers in wild vervet monkeys. Pro- j.evolhumbehav.2013.02.002. ceedings of the National Academy of Sciences, 106, 12007e12012. http:// Barrett, L., Gaynor, D., & Henzi, S. P. (2002). A dynamic interaction between dx.doi.org/10.1073/pnas.0812280106. aggression and grooming reciprocity among female chacma baboons. Animal Fruth, B., & Hohmann, G. (2002). How bonobos handle hunts and harvests: why Behaviour, 63, 1047e1053. http://dx.doi.org/10.1006/anbe.2002.3008. share food? In C. Boesch, G. Hohmann, & L. Marchant (Eds.), Behavioural di- Barrett, L., & Henzi, S. P. (2001). The utility of grooming in baboon troops. In R. Noe,€ versity in chimpanzees and bonobos (pp. 231e243). Cambridge, U.K.: Cambridge J. A. R. A. M. van Hooff, & P. Hammerstein (Eds.), Economics in nature: Social University Press. dilemmas, mate choice and biological markets (pp. 119e145). Cambridge, U.K.: Gilby, I. C. (2006). Meat sharing among the Gombe chimpanzees: harassment and Cambridge University Press. reciprocal exchange. Animal Behaviour, 71, 953e963. http://dx.doi.org/10.1016/ Barrett, L., & Henzi, S. P. (2002). Constraints on relationship formation among fe- j.anbehav.2005.09.009. male primates. Behaviour, 139, 263e289. http://dx.doi.org/10.1163/ Gilby, I. C. (2013). Cooperation among non-kin: reciprocity, markets and mutualism. 156853902760102672. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The A. Sanchez-Amaro, F. Amici / Animal Behaviour 110 (2015) 51e60 59

evolution of primate societies (pp. 514e530). Chicago, IL: The University of Lehmann, J., & Boesch, C. (2009). Sociality of the dispersing sex: the nature of social Chicago Press. bonds in West African female chimpanzees, Pan troglodytes. Animal Behaviour, Gilby, I. C., Eberly, L. E., Pintea, L., & Pusey, A. E. (2006). Ecological and social in- 77,377e387. http://dx.doi.org/10.1016/j.anbehav.2008.09.038. fluences on the hunting behaviour of wild chimpanzees, Pan troglodytes Leinfelder, I., De Vries, H., Deleu, R., & Nelissen, M. (2001). Rank and grooming schweinfurthii. Animal Behaviour, 72,169e180. http://dx.doi.org/10.1016/ reciprocity among females in a mixed-sex group of captive hamadryas baboons. j.anbehav.2006.01.013. American Journal of Primatology, 55,25e42. http://dx.doi.org/10.1002/ajp.1036. Gilby, I. C., Thompson, M. E., Ruane, J. D., & Wrangham, R. (2010). No evidence of Manson, J. H., Navarrete, C. D., Silk, J. B., & Perry, S. (2004). Time-matched grooming short-term exchange of meat for sex among chimpanzees. Journal of Human in female primates? New analyses from two species. Animal Behaviour, 67, Evolution, 59,44e53. http://dx.doi.org/10.1016/j.jhevol.2010.02.006. 493e500. http://dx.doi.org/10.1016/j.anbehav.2003.05.009. Gilby, I. C., & Wrangham, R. W. (2008). Association patterns among wild chim- Metz, M., Klump, G. M., & Friedl, T. W. (2007). Temporal changes in demand for and panzees (Pan troglodytes schweinfurthii)reflect sex differences in cooperation. supply of nests in red bishops (Euplectes orix): dynamics of a biological market. Behavioral Ecology and Sociobiology, 62, 1831e1842. http://dx.doi.org/10.1007/ Behavioral Ecology and Sociobiology, 61, 1369e1381. http://dx.doi.org/10.1007/ s00265-008-0612-6. s00265-007-0367-5. Gomes, C. M., & Boesch, C. (2009). Wild chimpanzees exchange meat for sex on a Mitani, J. C. (2009). Male chimpanzees form enduring and equitable social bonds. long-term basis. PLoS One, 4,e5116.http://dx.doi.org/10.1371/ Animal Behaviour, 77, 633e640. http://dx.doi.org/10.1016/j.anbehav.2008.11.021. journal.pone.0005116. Mitani, J. C., & Watts, D. P. (2001). Why do chimpanzees hunt and share meat? Gomes, C. M., Mundry, R., & Boesch, C. (2009). Long-term reciprocation of grooming Animal Behaviour, 61,915e924. http://dx.doi.org/10.1006/anbe.2000.1681. in wild West African chimpanzees. Proceedings of the Royal Society B: Biological Molesti, S., & Majolo, B. (2015). No short-term contingency between grooming and Sciences, 276, 699e706. http://dx.doi.org/10.1098/rspb.2008.1324. food tolerance in Barbary macaques (Macaca sylvanus). Ethology, 121,372e382. Gumert, M. D. (2007a). Payment for sex in a macaque mating market. Animal http://dx.doi.org/10.1111/eth.12346. Behaviour, 74, 1655e1667. http://dx.doi.org/10.1016/j.anbehav.2007.03.009. Muller, M. N., Emery-Thompson, M., Kahlenberg, S. M., & Wrangham, R. W. (2011). Gumert, M. D. (2007b). Grooming and infant handling interchange in Macaca fas- Sexual coercion by male chimpanzees shows that female choice may be more cicularis: the relationship between infant supply and grooming payment. In- apparent than real. Behavioral Ecology and Sociobiology, 65,921e933. http:// ternational Journal of Primatology, 28, 1059e1074. http://dx.doi.org/10.1007/ dx.doi.org/10.1007/s00265-010-1093-y. s10764-007-9202-0. Noe,€ R., & Hammerstein, P. (1994). Biological markets: supply and demand determine Gumert, M. D., & Ho, M. H. R. (2008). The trade balance of grooming and its coor- the effect of partner choice in cooperation, mutualism and mating. Behavioral dination of reciprocation and tolerance in Indonesian long-tailed macaques Ecology and Sociobiology, 35,1e11. http://dx.doi.org/10.1007/BF00167053. (Macaca fascicularis). Primates, 49,176e185. http://dx.doi.org/10.1007/s10329- Noe,€ R., & Hammerstein, P. (1995). Biological markets. Trends in Ecology & Evolution, 008-0089-y. 10, 336e339. http://dx.doi.org/10.1016/S0169-5347(00)89123-5. Gust, D. A., Gordon, T. P., Brodie, A. R., & McClure, H. M. (1996). Effect of companions Norscia, I., Antonacci, D., & Palagi, E. (2009). Mating first, mating more: biological in modulating stress associated with new group formation in juvenile rhesus market fluctuation in a wild prosimian. PLoS One, 4, e4679. http://dx.doi.org/ macaques. Physiology & Behavior, 59,941e945. http://dx.doi.org/10.1016/0031- 10.1371/journal.pone.0004679. 9384(95)02164-7. Payne, H. F., Lawes, M. J., & Henzi, S. P. (2003). Competition and the exchange of Hellmann, J. K., Reddon, A. R., Ligocki, I. Y., O'Connor, C. M., Garvy, K. A., Marsh- grooming among female samango monkeys (Cercopithecus mitis erythrarchus). Rollo, S. E., et al. (2015). Group response to social perturbation: impacts of Behaviour, 140, 453e471. http://dx.doi.org/10.1163/156853903322127931. isotocin and the social landscape. Animal Behaviour, 105,55e62. http:// Port, M., Clough, D., & Kappeler, P. M. (2009). Market effects offset the reciprocation dx.doi.org/10.1016/j.anbehav.2015.03.029. of grooming in free-ranging redfronted lemurs, Eulemur fulvus rufus. Animal Hemelrijk, C. K., Van Laere, G. J., & van Hooff, J. A. (1992). Sexual exchange re- Behaviour, 77,29e36. http://dx.doi.org/10.1016/j.anbehav.2008.08.032. lationships in captive chimpanzees? Behavioral Ecology and Sociobiology, 30, Richter, C., Mevis, L., Malaivijitnond, S., Schülke, O., & Ostner, J. (2009). Social re- 269e275. http://dx.doi.org/10.1007/BF00166712. lationships in free-ranging male Macaca arctoides. International Journal of Pri- Henzi, S. P., & Barrett, L. (1999). The value of grooming to female primates. Primates, matology, 30, 625e642. http://dx.doi.org/10.1007/s10764-009-9364-z. 40,47e59. http://dx.doi.org/10.1007/BF02557701. Russell, Y. I., & Phelps, S. (2013). How do you measure pleasure? A discussion about Henzi, S. P., & Barrett, L. (2002). Infants as a commodity in a baboon market. Animal intrinsic costs and benefits in primate allogrooming. Biology & Philosophy, 28, Behaviour, 63,915e921. http://dx.doi.org/10.1006/anbe.2001.1986. 1005e1020. http://dx.doi.org/10.1007/s10539-013-9372-4. Henzi, S. P., & Barrett, L. (2007). Coexistence in female-bonded primate groups. Saunders, C. D., & Hausfater, G. (1988). The functional significance of baboon Advances in the Study of Behavior, 37,43e81. http://dx.doi.org/10.1016/S0065- grooming behavior. Annals of the New York Academy of Sciences, 525, 430e432. 3454(07)37002-2. http://dx.doi.org/10.1111/j.1749-6632.1988.tb38635.x. Henzi, S. P., Barrett, L., Gaynor, D., Greeff, J., Weingrill, T., & Hill, R. A. (2003). Effect of Schino, G. (2001). Grooming, competition and social rank among female primates: a resource competition on the long-term allocation of grooming by female ba- meta-analysis. Animal Behaviour, 62, 265e271. http://dx.doi.org/10.1006/ boons: evaluating Seyfarth's model. Animal Behaviour, 66,931e938. http:// anbe.2001.1750. dx.doi.org/10.1006/anbe.2003.2244. Schino, G. (2007). Grooming and agonistic support: a meta-analysis of primate Henzi, S. P., Lycett, J. E., & Weingrill, T. (1997). Cohort size and the allocation of social reciprocal altruism. Behavioral Ecology, 18,115e120. http://dx.doi.org/10.1093/ effort by female mountain baboons. Animal Behaviour, 54, 1235e1243. http:// beheco/arl045. dx.doi.org/10.1006/anbe.1997.0520. Schino, G., & Aureli, F. (2008). Grooming reciprocation among female primates: a Hutchins, M., & Barash, D. P. (1976). Grooming in primates: implications for its meta-analysis. Biology Letters, 4,9e11. http://dx.doi.org/10.1098/rsbl.2007.0506. utilitarian function. Primates, 17,145e150. http://dx.doi.org/10.1007/ Schino, G., & Aureli, F. (2009). Reciprocal altruism in primates: partner choice, BF02382848. cognition, and emotions. Advances in the Study of Behavior, 39,45e69. http:// Kaburu, S. S., & Newton-Fisher, N. E. (2013). Social instability raises the stakes dx.doi.org/10.1016/S0065-3454(09)39002-6. during social grooming among wild male chimpanzees. Animal Behaviour, 86, Schino, G., & Aureli, F. (2010). Primate reciprocity and its cognitive requirements. 519e527. http://dx.doi.org/10.1016/j.anbehav.2013.06.003. Evolutionary Anthropology, 19,130e135. http://dx.doi.org/10.1002/evan.20270. Kaburu, S. S., & Newton-Fisher, N. E. (2015). Egalitarian despots: hierarchy steep- Schino, G., di Giuseppe, F., & Visalberghi, E. (2009). The time frame of partner choice ness, reciprocity and the grooming-trade model in wild chimpanzees, Pan in the grooming reciprocation of Cebus apella. Ethology, 115,70e76. http:// troglodytes. Animal Behaviour, 99,61e71. http://dx.doi.org/10.1016/ dx.doi.org/10.1111/j.1439-0310.2008.01581.x. j.anbehav.2014.10.018. Schino, G., Polizzi di Sorrentino, E. P., & Tiddi, B. (2007). Grooming and coalitions in Keverne, E. B., Martensz, N. D., & Tuite, B. (1989). Beta-endorphin concentrations in Japanese macaques (Macaca fuscata): partner choice and the time frame cerebrospinal fluid of monkeys are influenced by grooming relationships. Psy- reciprocation. Journal of Comparative Psychology, 121, 181. http://dx.doi.org/ choneuroendocrinology, 14,155e161. http://dx.doi.org/10.1016/0306-4530(89) 10.1037/0735-7036.121.2.181. 90065-6. Schino, G., Rosati, L., & Aureli, F. (1998). Intragroup variation in conciliatory ten- Koyama, N. F., Caws, C., & Aureli, F. (2006). Interchange of grooming and agonistic dencies in captive Japanese macaques. Behaviour, 135,897e912. http:// support in chimpanzees. International Journal of Primatology, 27, 1293e1309. dx.doi.org/10.1163/156853998792640314. http://dx.doi.org/10.1007/s10764-006-9074-8. Schino, G., Ventura, R., & Troisi, A. (2003). Grooming among female Japanese ma- Koyama, N. F., Caws, C., & Aureli, F. (2012). Supply and demand predict male caques: distinguishing between reciprocation and interchange. Behavioral grooming of swollen females in captive chimpanzees, Pan troglodytes. Animal Ecology, 14, 887e891. http://dx.doi.org/10.1093/beheco/arg070. Behaviour, 84,1419e1425. http://dx.doi.org/10.1016/j.anbehav.2012.09.007. Schino, G., Ventura, R., & Troisi, A. (2005). Grooming and aggression in captive Kutsukake, N., & Clutton-Brock, T. H. (2010). Grooming and the value of social re- Japanese macaques. Primates, 46, 207e209. http://dx.doi.org/10.1007/s10329- lationships in cooperatively breeding meerkats. Animal Behaviour, 79,271e279. 004-0124-6. http://dx.doi.org/10.1016/j.anbehav.2009.10.014. Schwartz, M. W., & Hoeksema, J. D. (1998). Specialization and resource trade: bio- Langergraber, K., Mitani, J., & Vigilant, L. (2007). The limited impact of kinship on logical markets as a model of mutualisms. Ecology, 79, 1029e1038. http:// cooperation in wild chimpanzees. Proceedings of the National Academy of Sci- dx.doi.org/10.1007/s10329-004-0124-6. ences of the United States of America, 104, 7786e7790. http://dx.doi.org/10.1073/ Seyfarth, R. M. (1977). A model of social grooming among adult female monkeys. pnas.0611449104. Journal of Theoretical Biology, 65,671e698. http://dx.doi.org/10.1016/0022- Lazaro-Perea, C., de Fatima Arruda, M., & Snowdon, C. T. (2004). Grooming as a 5193(77)90015-7. reward? Social function of grooming between females in cooperatively Seyfarth, R. M. (1980). The distribution of grooming and related behaviours among breeding marmosets. Animal Behaviour, 67,627e636. http://dx.doi.org/10.1016/ adult female vervet monkeys. Animal Behaviour, 28, 798e813. http://dx.doi.org/ j.anbehav.2003.06.004. 10.1016/S0003-3472(80)80140-0. 60 A. Sanchez-Amaro, F. Amici / Animal Behaviour 110 (2015) 51e60

Seyfarth, R. M., & Cheney, D. L. (1984). Grooming, alliances and reciprocal altruism Teleki, G. (1973). The predatory behavior of wild chimpanzees. Lewisburg, PA: Buck- in vervet monkeys. Nature, 308,541e543. http://dx.doi.org/10.1038/308541a0. nell University Press. Seyfarth, R. M., & Cheney, D. L. (2012). The evolutionary origins of friendship. Annual Tiddi, B., Aureli, F., Polizzi di Sorrentino, E. P., Janson, C. H., & Schino, G. (2011). Review of Psychology, 63,153e177. http://dx.doi.org/10.1146/annurev-psych- Grooming for tolerance? Two mechanisms of exchange in wild tufted capuchin 120710-100337. monkeys. Behavioral Ecology, 22, 663e669. http://dx.doi.org/10.1093/beheco/ Silk, J. B., Alberts, S. C., & Altmann, J. (2003). Social bonds of female baboons arr028. enhance infant survival. Science, 302, 1231e1234. http://dx.doi.org/10.1126/ Tiddi, B., Aureli, F., & Schino, G. (2010). Grooming for infant handling in tufted science.1088580. capuchin monkeys: a reappraisal of the primate infant market. Animal Behav- Silk, J. B., Alberts, S. C., & Altmann, J. (2004). Patterns of coalition formation by adult iour, 79,1115e1123. http://dx.doi.org/10.1016/j.anbehav.2010.02.008. female baboons in Amboseli, Kenya. Animal Behaviour, 67, 573e582. http:// Ventura, R., Majolo, B., Koyama, N. F., Hardie, S., & Schino, G. (2006). Reciprocation dx.doi.org/10.1016/j.anbehav.2003.07.001. and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., et al. support. American Journal of Primatology, 68,1138e1149. http://dx.doi.org/ (2009). The benefits of social capital: close social bonds among female baboons 10.1002/ajp.20314. enhance offspring survival. Proceedings of the Royal Society B: Biological Sciences, Vervaecke, H., De Vries, H., & Van Elsacker, L. (2000). Dominance and its behavioral 276, 3099e3104. http://dx.doi.org/10.1098/rspb.2009.0681. measures in a captive group of bonobos (Pan paniscus). International Journal of Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., et al. Primatology, 21,47e68. http://dx.doi.org/10.1023/A:1005471512788. (2010). Strong and consistend social bonds enhance the longevity of female ba- de Waal, F. B. (1997). The chimpanzee's service economy: food for grooming. Evo- boons. Current Biology, 20,1359e1361. http://dx.doi.org/10.1016/j.cub.2010.05.067. lution and Human Behavior, 18,375e386. http://dx.doi.org/10.1016/S1090- Slater, K. Y., Schaffner, C. M., & Aureli, F. (2007). Embraces for infant handling in 5138(97)00085-8. spider monkeys: evidence for a biological market? Animal Behaviour, 74, de Waal, F. B. (2000). Attitudinal reciprocity in food sharing among brown capuchin 455e461. http://dx.doi.org/10.1016/j.anbehav.2006.11.026. monkeys. Animal Behaviour, 60, 253e261. http://dx.doi.org/10.1006/ Stanford, C. B. (1996). The hunting ecology of wild chimpanzees: implications for anbe.2000.1471. the evolutionary ecology of Pliocene hominids. American Anthropologist, 98, Watts, D. P. (2002). Reciprocity and interchange in the social relationships of wild 96e113. http://dx.doi.org/10.1525/aa.1996.98.1.02a00090. male chimpanzees. Behaviour, 139, 343e370. http://dx.doi.org/10.1163/ Stanford, C. B. (1998). The social behavior of chimpanzees and bonobos: empirical 156853902760102708. evidence and shifting assumptions. Current Anthropology, 39, 399e420. http:// Watts, D. P., & Mitani, J. C. (2002). Hunting behavior of chimpanzees at Ngogo, dx.doi.org/10.1086/204757. Kibale national Park, Uganda. International Journal of Primatology, 23,1e28. Stanford, C. B., Wallis, J., Mpongo, E., & Goodall, J. (1994). Hunting decisions in wild http://dx.doi.org/10.1023/A:1013270606320. chimpanzees. Behaviour, 131,1e18. http://dx.doi.org/10.1163/156853994X00181. Wyatt, G. A., Kiers, E. T., Gardner, A., & West, S. A. (2014). A biological market Stevens, J. M. G., Vervaecke, H., de Vries, H., & van Elsacker, L. (2005). The influence analysis of the plant-mycorrhizal symbiosis. Evolution, 68, 2603e2618. http:// of the steepness of dominance hierarchies on reciprocity and interchange in dx.doi.org/10.1111/evo.12466. captive groups of bonobos (Pan paniscus). Behaviour, 142,941e960. Xia, D., Li, J., Garber, P. A., Sun, L., Zhu, Y., & Sun, B. (2012). Grooming reciprocity in Stevens, J. R., Hallinan, E. V., & Hauser, M. D. (2005). The ecology and evolution of female Tibetan macaques Macaca thibetana. American Journal of Primatology, 74, patience in two New World monkeys. Biology Letters, 1, 223e226. http:// 569e579. http://dx.doi.org/10.1002/ajp.21985. dx.doi.org/10.1098/rsbl.2004.0285. Xia, D. P., Li, J. H., Garber, P. A., Matheson, M. D., Sun, B. H., & Zhu, Y. (2013). Surbeck, M., & Hohmann, G. (2014). Social preferences influence the short-term Grooming reciprocity in male Tibetan macaques. American Journal of Primatol- exchange of social grooming among male bonobos. Animal Cognition,1e7. ogy, 75,1009e1020. http://dx.doi.org/10.1002/ajp.22165. http://dx.doi.org/10.1007/s10071-014-0826-0. Zamma, K. (2002). Grooming site preferences determined by lice infection among Tanaka, I., & Takefushi, H. (1993). Elimination of external parasites (lice) is the Japanese macaques in Arashiyama. Primates, 43,41e49. http://dx.doi.org/ primary function of grooming in free-ranging Japanese macaques. Anthropo- 10.1007/BF02629575. logical Science, 101,187e193. http://dx.doi.org/10.1537/ase.101.187.