Original Article
Capuchin monkeys punish those who have more

https://doi.org/10.1016/j.evolhumbehav.2015.12.002Get rights and content

Abstract

Punishment of non-cooperators is important for the maintenance of large-scale cooperation in humans, but relatively little is known about the relationship between punishment and cooperation across phylogeny. The current study examined second-party punishment behavior in a nonhuman primate species known for its cooperative tendencies—the brown capuchin monkey (Cebus apella). We found that capuchins consistently punished a conspecific partner who gained possession of a food resource, regardless of whether the unequal distribution of this resource was intentional on the part of the partner. A non-social comparison confirmed that punishment behavior was not due to frustration, nor did punishment stem from increased emotional arousal. Instead, punishment behavior in capuchins appears to be decidedly social in nature, as monkeys only pursued punitive actions when such actions directly decreased the welfare of a recently endowed conspecific. This pattern of results is consistent with two features central to human cooperation: spite and inequity aversion, suggesting that the evolutionary origins of some human-like punitive tendencies may extend even deeper than previously thought.

Introduction

Cooperation is central to human societies, and the punishment of non-cooperators is thought to play a key role in both the emergence (Boyd, Gintis, Bowles, & Richerson, 2003) and maintenance of cooperation within social communities (Boyd, Gintis, & Bowles, 2010). While self-serving strategies quickly proliferate in the absence of punitive options (e.g., Boyd et al., 2003, Fehr and Gächter, 2002), the mere threat of punishment (Fehr and Gächter, 2002, Gintis et al., 2001) as well as negative gossip that may lead to punishment (Beersma and Van Kleef, 2011, Ellingsen and Johannesson, 2008, Piazza and Bering, 2008) is sufficient to deter selfish individuals from profiting at the expense of the group. Accordingly, many researchers have argued that punishment of non-cooperative individuals can uphold group cooperative norms by dissuading recidivist non-cooperators, while also signaling to others in the group that such violations will not be tolerated (Clutton-Brock & Parker, 1995).

Accordingly, research shows that human adults routinely engage in punitive actions, even when such actions are personally costly or are undertaken to benefit a group rather than the individual in the case of “altruistic” punishment (Fehr and Fischbacher, 2004, Fehr and Gächter, 2000, Fehr and Gächter, 2002, Gürerk et al., 2006). This raises important questions concerning why individuals would willingly bear the immediate burden of punishment for the long-term benefit of the group. More specifically, what psychological motivations lead individuals to engage in costly punitive actions? Importantly, both second-party punishment (when one has a self-interested stake) and third-party punishment (as an unaffected observer) depend on the actor having the urge to punish and may share common psychological roots (Buckholtz & Marois, 2012). A growing body of research suggests that people’s decisions to punish others are sensitive to a number of social and psychological factors. That is, human punishment is often selective: people are more likely to engage in costly punitive behaviors when certain psychological conditions are met.

First, people take into account the intentions of a transgressor when making judgments about blameworthiness (Nelson, 2002). Specifically, decision-makers tend to punish those perceived to have malintent more than those with good intentions, even when the negative outcomes are equated (Charness & Levine, 2003). The evaluation of intentions is particularly relevant in punishment of fairness violations, as several studies show that unfair outcomes are punished most harshly when they come about as the result of unfair intentions (Falk et al., 2008, Fehr and Schmidt, 1999, Rabin, 1993). Second, individual decisions to engage in punishment are driven by egocentric motivations. In fact, much of the punitive behavior in which humans engage is motivated by feelings of personal – not social – injustice. People punish others out of revenge (e.g. Bone and Raihani, 2015, Cota‐McKinley et al., 2001), spite (e.g. Abbink and Herrmann, 2011, Abbink and Sadrieh, 2009), or simply because of an aversion to having less than others (e.g. Johnson, Dawes, Fowler, McElreath, & Smirnov, 2009). Indeed, research suggests that an aversion to personally disadvantageous outcomes plays a large role in driving punishment in adults (Raihani & McAuliffe, 2012); this notion is supported by evidence that those engaging in punishment behavior often do so not to achieve equality, but to create inequality in their own favor (Houser & Xiao, 2010). Third, people are more likely to engage in punishment when they experience certain emotional states, such as anger or moral disgust. For example, individuals are more likely to punish others who make unfair offers when they feel anger in response to that person’s behavior (Pillutla and Murnighan, 1996, Xiao and Houser, 2005). Finally, people consider how their actions are likely to be perceived by other parties when making punishment decisions. In particular, people are more likely to engage in costly punishment of moral violations in the presence of a social audience than in anonymous situations (Kurzban, DeScioli, & O’Brien, 2007). In this way, punishment can potentially allow actors to reap positive social benefits associated with being seen as a cooperative individual in the eyes of fellow group members.

There is also increasing evidence that punishment behaviors – and this suite of psychological motivations underlying them – emerge fairly early in development. Indeed, even young children will punish others by avoiding social interactions with them, or redistributing resources away from them. For example, when given the option, toddlers systematically direct their own negative actions towards an antisocial individual over a prosocial one (Hamlin & Wynn, 2011). Around 3–4 years of age, children begin acting less prosocially toward people whom they’ve seen harm or intend to harm another individual (Kenward and Dahl, 2011, Vaish et al., 2010), and tattle on puppets whom they’ve witnessed committing moral violations (Vaish, Missana, & Tomasello, 2011). Finally, by the age of 5, children appear willing to take a personal cost to punish those who exhibit non-cooperative tendencies (McAuliffe et al., 2015, Robbins and Rochat, 2011).

More importantly, recent evidence suggests that young children’s resource distribution and punishment decisions appear sensitive to the same psychological motivations that underlie punishment decisions in adults. First, children pay attention to the intentions of actors when making punitive judgments, much like adults. Even 8-month-old infants distinguish between actors who cause bad outcomes because of bad intentions and those who bring about bad outcomes accidently (Hamlin, 2013), and children begin to incorporate information about other’s intentions into their naughtiness and punishability judgments between 4 and 8 years of age (Cushman, Sheketoff, Wharton, & Carey, 2013). Second, there is growing evidence that young children show spiteful preferences and are willing to take a cost to achieve resource distributions that personally benefit them (McAuliffe et al., 2014, Sheskin et al., 2014). Finally, by the age of 5, children are sensitive to the presence of a social audience when making decisions tied to norms of cooperation and fairness (Engelmann et al., 2012, Leimgruber et al., 2012, McAuliffe et al., 2013). These results have led some researchers to suggest that the presence of an audience and, relatedly, reputational concerns may influence many aspects of children’s cooperative decisions even early in life (Shaw, Li, & Olson, 2013).

Taken together, this work suggests that some of the psychological motivations underlying adult human punishment – factors like understanding the intentions of others, considerations regarding relative resource distributions, and reputational concerns – are in place very early in human development. Given this pattern of early emergence in humans, these types of responses likely depend at least in part on foundational social cognitive skills that are shared with other species, such as the ability to judge other’s intentions (Call et al., 2004, Phillips et al., 2009). However, while the psychological factors that promote punishment in our own species have been the focus of intense research, the evolutionary origins of the capacities supporting punishment are less well understood. In fact, many comparative studies of punishment in nonhumans typically define punishment as behaviors that impose an immediate cost on others to decrease the occurrence of an undesirable behavior (Clutton-Brock & Parker, 1995). Using this definition, examples of punishment behavior in non-human animals are relatively rare, even in primates (for one exception in fish, see Raihani, Thornton, & Bshary, 2012). Several species of non-human primates appear to engage in retributive behavior in reaction to harm to themselves or closely-affiliated others (Aureli et al., 1992, Crofoot and Wrangham, 2010, de Waal, 1982). However, these studies focus on whether such behaviors occur, and not the psychological motivations that underlie primates’ punitive behaviors.

One important exception is a set of studies examining punitive tendencies in chimpanzees (Jensen et al., 2007, Riedl et al., 2012). Jensen et al. (2007) investigated the circumstances under which chimpanzees would collapse a table to prevent a conspecific from accessing food. In fact, chimpanzees were more likely to collapse the table when their partner had initially stolen the resource, compared to when an experimenter had redistributed the resource—suggesting that the chimpanzees, like humans, were sensitive to the intentions of the actor. Interestingly, chimpanzees were not willing to punish when the same transgressions happened to a third party (Riedl et al., 2012). Overall, these results suggest that chimpanzees use punishment as a means of retaliation for direct personal harm, an explanation supported by evidence that behavioral signs of arousal correlated with increased punishment behavior (Jensen et al., 2007).

The results from Jensen and colleagues indicate that chimpanzees share some of psychological mechanisms underlying punishment in humans. However, chimpanzees are not the only primate species that can provide insights into the relationship between punishment and the evolution of cooperation. In fact, chimpanzees show important divergences from humans in some aspects of their social behavior. Although chimpanzees have relatively sophisticated perspective-taking abilities (Call & Tomasello, 2008) and are capable of recognizing cues of need in others (Melis and Tomasello, 2013, Melis et al., 2011, Warneken et al., 2007, Warneken and Tomasello, 2006), chimpanzees and humans differ in patterns of prosociality. For example, chimpanzees are often indifferent to opportunities to donate food to conspecifics at no personal cost (Jensen et al., 2006, Silk et al., 2005, Vonk et al., 2008, but see Horner, Carter, Suchak, & de Waal, 2011 for an exception) Consequently, studies of species that more consistently engage in cooperative and prosocial behaviors are critical for understanding the evolution of a human-like punishment psychology, and its relationship to cooperation more generally.

Here, we aimed to disentangle the importance of motivations underlying punishment behavior in a primate species known to engage in rich cooperative behaviors—the brown capuchin monkey (Cebus apella) (Brosnan, 2010, Hattori et al., 2005). Capuchin monkeys more consistently exhibit other-regarding tendencies in donation tasks than chimpanzees (de Waal and Suchak, 2010, de Waal et al., 2008, Lakshminarayanan and Santos, 2008, Takimoto et al., 2010, although see Drayton & Santos, 2014 for an exception), and are sensitive to social disparity in outcomes (Brosnan, 2011, Brosnan et al., 2006). There is also evidence that capuchin monkeys avoid non-reciprocators when making affiliative decisions (Anderson, Takimoto, Kuroshima, & Fujita, 2013) and cease participation in a joint-pulling task when it is likely that the cooperative partner will monopolize the reward (de Waal & Davis, 2003, see also Brosnan et al., 2006). Taken together with evidence that capuchins modify their social behavior when visually and audibly isolated from conspecifics (de Waal et al., 2008, Pollick et al., 2005), this set of findings suggests that capuchin monkeys are a strong phylogenetic model of the human-like relationship between punishment and cooperation.

Using a method modeled after that used with chimpanzees (Jensen et al., 2007), we assessed the importance of the factors that influence human punishment on the monkeys’ punishment decisions. In particular, we examined how monkeys responded to inequality of reward outcomes (i.e., having less of a reward than another monkey), the intentionality of the benefactor (i.e., having a resource deliberately stolen), the importance of emotional arousal as indexed by scratching (a common measure of stress or arousal in primates; Maestripieri et al., 1992, Polizzi di Sorrentino et al., 2012), and the presence of an audience proximate to the social interaction. Here we focused on second-party punishment, given that there is currently no evidence for robust third-party punishment in nonhumans. Importantly, such second-party punishment behaviors have been suggested to represent the evolutionary roots of human punishment behaviors (Buckholtz & Marois, 2012). Overall, this approached allowed us to disentangle which psychological motivators of human punishment behaviors are shared with capuchins by modeling which of these factors best predicted the capuchins’ likelihood of punishing a conspecific.

Section snippets

Participants

We tested 6 brown capuchin monkeys (Cebus apella) ranging in age from 6 to 17 years (3 males [AH, FL, NN], 3 females [HG, JM, MD]; Mage = 166.8 months, SD = 52.41). All monkeys were familiar with one another prior to testing, as they were socially housed as part of a nine-member group that comprised the Yale Comparative Cognition Laboratory. This indoor enclosure was equipped with natural branches and toys, and had access to water and food ad libitum. An additional monkey who was the lowest ranking

Results

Overall, monkeys collapsed the table on 25.7% ± 3.7 (Mean ± SE) of trials in the Partner Feeding condition, 20.1% ± 3.4 of trials in the Outcome Disparity condition, 26.4% ± 3.7 of trials after Theft, but only 9.0% ± 2.4 of trials in the Loss condition (Fig. 3a). To analyze pulling behavior, we first built a basic model including subject as random factor (random subject intercepts); trial number as a covariate to assess learning effects within sessions; and each individual’s pretest pulling frequency (in

Discussion

To goal of this study was to investigate the roots of human-like punitive behaviors in another highly cooperative primate species. Our findings indicate that our capuchin monkeys were most likely to pursue punitive measures when confronted with a conspecific possessing relatively more of a food resource, regardless of how this situation arose. Importantly, punishment was not the result of mere frustration over an inaccessible resource, as monkeys were significantly less likely to collapse the

Supplementary Materials

following are the Supplementary data to this article.

Supplementary materials.

Acknowledgments

We thank Janelle Gagnon, Jenny Friedman, and Linda Chang for their help with data collection.

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