Gintis Moral Sentiments and Material Interests The Foundations of Cooperation in Economic Life (MIT, 2005)

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capuchins rarely gave food to their partners directly (de Waal 1997b), even though they did little to protect their food from theft. Thus, capuchins may be strongly motivated to be near particular partners, and food transfers may be an inadvertent side effect of their sociability. The fact that the quality of social bonds influences food transfer rates suggest that the capuchins may not share in a strictly contingent manner (de Waal 1997b). De Waal (2000) conducted a second set of experiments in which two females housed in adjacent cages were given food at the same time, but the food items differed in their desirability. Females spent more time near the mesh partition when a monkey was in the adjacent cage than when it was empty, but they dropped less food near the partition when it was occupied by another monkey. Moreover, females tended to spend less time near the partition (and within their partner’s reach) when they had more desirable foods than their partners. Thus, females seem to be drawn to favored companions, but are also wary of losing desirable food items to them. Observed rates of food transfer are the product of a compromise between these competing motivations (de Waal 2000).

Using a different experimental paradigm, de Waal and Berger (2000) explored capuchins willingness to participate in cooperative tasks. As in the previous experiment, monkeys were held in adjacent cages separated by a wire mesh partition. Here, the monkeys had to pull a counterweighted bar to bring a tray holding a baited food bowl within reach. De Waal and Berger examined the monkeys’ participation in this task under three different conditions. In the solo condition, only one food bowl was baited and a single monkey was able to pull the bowl to within reach. In the cooperative condition, only one food bowl was baited, but it required joint action by both monkeys to pull the bowl within reach. In the mutualistic condition, both bowls were baited and it required joint action by both monkeys to pull the bowl within reach. Monkeys were equally successful in the solo and mutualistic conditions, pulling the food bowl forward approximately 85 percent of the time. Monkeys succeeded on the cooperative task only 40 percent of the time. However, when monkeys did succeed on the cooperative task, more food was transferred than in the successful solo trials. Moreover, a larger fraction of food transfers were tolerated (in sight and reach of the owner) than in solo trials.

De Waal and Berger (2000) argue that these experiments show that ‘‘capuchins cooperate even if it is obvious that only one of them, and which one, will be rewarded,’’ and that that capuchins ‘‘exchange labor

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for payment.’’ Yet given the small size of the cages, the capuchins marked affinity for their partners, and the messiness of their eating habits, both parties may be relatively certain that they will obtain food if they cooperate in pulling the bowl forward. Moreover, it is not clear that food transfers reflect an exchange of payment for labor. Even in solo trials, some food is transferred and the incremental effects of cooperation on food transfers and tolerance is relatively small. In solo trials seven to nine pieces of food are transferred on average and 58 percent of those transfers are tolerated by the owner. In cooperative trials, these numbers increase only slightly—nine to eleven pieces are taken and 65 percent of these transfers are tolerated.

Primatologists have recently begun to explore the psychological predispositions that underly exchanges in primate groups. One of the key assumptions of reciprocity is that animals must be able to evaluate the value of the commodities or services that are being exchanged. Brosnan and de Waal (2003) conducted an intriguing experiment to explore how monkeys assess ‘‘value.’’ In these experiments, capuchins were trained to exchange tokens for food rewards. When a monkey handed a token to the experimenter, it was given a piece of food. The experimenters then conducted a series of trials in which the subjects observed transfers involving other individuals. In some cases, monkeys saw others receive food without any exchange of tokens, and in some cases they saw other monkeys receive a higher quality food reward than they received themselves when they exchanged tokens for foods. Monkeys who observed others obtain rewards without exchange or obtain higher quality rewards than they received were significantly more likely to refuse the food rewards that they obtained themselves—sometimes flinging food back at the experimenters. Monkeys virtually never refused rewards unless they observed others who had gotten a better deal. The authors suggest that monkeys displayed an aversion to inequality, although this interpretation has been questioned (Henrich 2004). At the very least, the data suggest that monkeys have some ability to evaluate the value of commodities and react negatively when they perceive that an exchange is disadvantageous to themselves.

The psychology underlying exchange has also been explored in captive tamarins. Hauser et al. (2003) created an experimental paradigm in which one individual could pull a tool that would provide food for its partner but no food for itself. The researchers trained several tamarins to be ‘‘unconditional altruists’’ who always pulled and others to be

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‘‘unconditional defectors’’ who never pulled. They paired these trained animals with untrained animals to determine whether the untrained tamarins would adjust their behavior in a contingent way. Tamarins pulled more when paired with unconditional altruists than when paired with unconditional defectors, indicating that cooperation was contingent on the behavior of the partner. However, Stevens and Hauser (2004) emphasize that the tamarins cooperated only half the time and that cooperation with unconditional altruists declined over the course of the experiments. They conclude that tamarins do not ‘‘demonstrate robust reciprocity’’ and conclude that ‘‘cognitive limitations such as temporal discounting, numerical discrimination, and memory make reciprocity difficult for animals’’ including nonhuman primates.

2.6Evolutionary Mechanisms Underlying Reciprocity in Primates

Balanced exchanges between partners and interchange across currencies are often interpreted as evidence that monkeys practice reciprocal altruism. De Waal has questioned this interpretation, suggesting that balanced exchanges might simply arise from mutual tolerance or high rates of association between partners rather than from contingent exchanges that require careful record keeping (de Waal and Luttrell 1988; de Waal 1997b; de Waal 2000; de Waal and Berger 2000): ‘‘If members of a species were to direct aid preferentially to close associates, a reciprocal distribution would automatically result due to the symmetrical nature of association’’ (de Waal 2000). De Waal calls this ‘‘symmetry-based reciprocity’’ and suggests that proximity should be controlled in analyses of reciprocity (de Waal and Luttrell 1988).

There are both logical and empirical reasons to doubt that symmetry-based reciprocity accounts for the distribution of altruistic behavior in primate groups. Symmetry-based reciprocity implies that proximity can be treated as an independent variable that is not affected by the nature of interactions between individuals. It seems more likely that association patterns reflect the nature of affiliative relationships between individuals. Thus, animals preferentially associate with those that tolerate, groom, and help them; they do not preferentially tolerate, help, and groom those that they just happen to associate with. Second, it seems unlikely that symmetry-based reciprocity would be stable against invasion by cheaters. Those who accepted help from close associates but did not return it would be at a distinct advantage. In

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fact, there is no evidence for symmetry-based reciprocity in primate groups. Significant correlations between benefits given and received are maintained, even when proximity is controlled statistically (de Waal and Luttrell 1988). Moreover, several experimental studies demonstrate contingencies between benefits given and subsequently received (Seyfarth and Cheney 1984; Hemelrijk 1994; de Waal 1997a, 1997b, 2000).

De Waal’s (2000) observations of fluctuations in the rate of food transfer within dyads over the course of successive experiments led him to suggest that reciprocity may be based on a tendency to mirror the social predispositions of partners, responding positively to positive social overtures and negatively to negative social overtures: ‘‘If facilitated taking is mediated by such general social predispositions, this would mean that, rather than keeping track of exact amounts of given and received food, the monkeys follow a simple tolerance- breeds-tolerance scheme’’ (de Waal 2000, 260). Attitudinal reciprocity is assumed to be less cognitively demanding than ‘‘calculated reciprocity,’’ which relies on precise quantification of benefits given and received in different currencies.

Attitudinal reciprocity is analogous to strong reciprocity because both processes focus on the proximate motives that generate cooperation and assume that reciprocity could occur without concern for long-term consequences. However, it is not clear how evolution could sustain attitudinal reciprocity (or strong reciprocity) in primate groups. It seems likely that individuals who systematically returned somewhat less than they received would benefit at the expense of their partners. To avoid this, costs and benefits must be translated into affect, a process that may hide the calculus of reciprocal altruism, but does not eliminate it.

2.7Punishment

Strong reciprocity relies on the tendency to punish noncooperators. Among nonhuman primates there is considerable evidence of negative reciprocity. Thus, animals use aggression or other forms of costly sanctions to shape the behavior of group members (Clutton-Brock and Parker 1995a, 1995b) or to exact revenge (de Waal and Luttrell 1988; Silk 1992). But there is very little evidence that monkeys and apes use aggression or negative sanctions to shape the behavior of third parties or to punish deviation from social norms.

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Several researchers have reported episodes of aggressive behavior that could be interpreted as punishment. In the Mahale Mountains of Tanzania, a young adult male was brutally attacked by eight members of his own group (Nishida et al. 1995). The authors speculated that this young male may have been victimized because he did not conform to social rules—he did not defer to higher-ranking males and launched unprovoked attacks on adult females. The problem with these observations (and other anecdotal observations) is that they are based on a single event. In these cases, conspicuous aggressive responses to unusual types of behavior may be more salient than occasions in which unusual behaviors were ignored. Without systematic analyses of the consequences of aberrant behaviors, it is difficult to be certain that violations of social norms are consistently punished.

The only systematic evidence of third party punishment comes from an experimental study on rhesus macaques conducted by Hauser and Marler (1993a, 1993b, Hauser 1997). Rhesus macaques give characteristic calls when they discover food items (Hauser and Marler 1993a). Taking advantage of this situation, Hauser and Marler (1993b) conducted an experiment in which observers surreptitiously dropped handfuls of coconut or monkey chow and waited for monkeys to find it. When monkeys found the food, they sometimes called and sometimes remained silent. Calling had little effect on the likelihood of being detected after finding food, but calling significantly reduced the likelihood of being harassed after discovery by other group members. Monkeys who discovered food and subsequently called were less likely to be supplanted, chased, or attacked than monkeys who remained silent after they found food. In the published report, the authors did not control for the relative dominance of the original possessors and the discoverers, even though macaque females rarely initiate aggression toward more dominant animals. However, subsequent reanalyses of the data (Hauser personal communication) indicate that noncallers were more likely to be harassed when they were discovered by higherranking animals than callers were. Apparently, these rules apparently apply only to females. Males virtually never call when they find food and are rarely punished (Hauser and Marler 1993b; Hauser 1997).

These data provide intriguing evidence that rhesus macaques punish group members who violate social norms. However, the weight of this conclusion is limited by the fact that these results have not been replicated, and no other observers have reported similar findings in other groups or species.

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2.8Prospects for Finding Strong Reciprocity in Primate Groups

For primates, cooperation is bounded by kinship and reciprocity and involves pairs of animals who have long-term social bonds. Most primatologists have assumed that reciprocal altruism is ultimately responsible for reciprocity within dyads, an assumption that is bolstered by experimental evidence that cooperative behavior is contingent on the nature of previous interactions. However, de Waal (2000) has suggested that reciprocal exchanges in capuchins may be the product of attitudinal reciprocity—a tendency to mirror the predispositions of their partners. If he is right, then we have reason to believe that strong reciprocity is rooted in the behavior of nonhuman primates. However, it is also possible that the monkey’s initial attitude toward its partner reflects the quality of their social relationship, and this is based on a long series of cooperative exchanges over time.

Good evidence of punishment would provide support for the idea that strong reciprocity operates in primate groups. Presently, systematic evidence for punishment rests on a single experiment. These data are quite provocative, but their significance will not be established until these experiments are replicated and extended to other species.

To understand the role of strong reciprocity in primate groups, we need to know more about the proximate factors that motivate cooperative behavior. Strong reciprocity in humans seems rooted in a deep sense of fairness and concern for justice that is extended even toward strangers, but we have no systematic evidence that other animals have similar sensibilities. Even those who have argued most forcefully for the emergence of moral sentiments in monkeys and apes have drawn their evidence from the interactions of close associates with long-term social bonds, not interactions among strangers (de Waal 1996; Flack and de Waal 2000).

The idea of strong reciprocity emerged from carefully designed experimental studies on humans that revealed surprisingly high levels of altruism in one-shot interactions with strangers. It is hard to imagine obtaining comparable data on interactions among strangers in nonhuman primates. Most primates live in stable social groups where they restrict peaceful social interactions mainly to known group members. Close associations with strangers are fraught with tension, generating aggression and avoidance, not cooperation. Aversions to strangers extend to captive settings. It might be possible to adapt de Waal’s experimental studies of capuchins to assess cooperative

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behavior with anonymous partners, but it is not clear whether capuchins or other primates would tolerate this protocol.

In conclusion, the literature suggests that primates reserve cooperation mainly for kin and reciprocating partners, but punishment is apparently uncommon. While we know a lot about what nonhuman primates do, we know very little about what motivates them to do it. The patterning of cooperative interactions among nonrelatives could be the product of reciprocal altruism, but the same patterns could also arise from strong reciprocity. To identify the proximate mechanisms that generate cooperation in primate groups, we need to develop experimental procedures that allow us to assess the tendency to cooperate in one-shot interactions with strangers. The ability to interact peacefully in one-shot interactions with strangers may prove to be one of the most remarkable traits of our own species. We also need to know more about other primates’ propensity to punish violations of social norms. Work addressing these issues in nonhuman primates is needed to assess the evolutionary roots of strong reciprocity.

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