Cross-societal variation in norm enforcement systems.

Across human societies, people are sometimes willing to punish norm violators. Such punishment can take the form of revenge from victims, seemingly altruistic intervention from third parties, or legitimized sanctioning from institutional representatives. Although prior work has documented cross-cultural regularities in norm enforcement, substantial variation exists in the prevalence and forms of punishment across societies. Such cross-societal variation may arise from universal psychological mechanisms responding to different socio-ecological conditions, or from cultural evolutionary processes, resulting in different norm enforcement systems. To date, empirical evidence from comparative studies across diverse societies has remained disconnected, owing to a lack of interdisciplinary integration and a prevalent tendency of empirical studies to focus on different underpinnings of variation in norm enforcement. To provide a more complete view of the shared and unique aspects of punishment across societies, we review prior research in anthropology, economics and psychology, and take a first step towards integrating the plethora of socio-ecological and cultural factors proposed to explain cross-societal variation in norm enforcement. We conclude by discussing how future cross-societal research can use diverse methodologies to illuminate key questions on the domain-specificity of punishment, the diversity of tactics supporting social norms, and their role in processes of norm change. This article is part of the theme issue 'Social norm change: drivers and consequences'.

State-dependent risky choices in primates: Variation in energy budget does not affect tufted capuchin monkeys' (Sapajus spp.) risky choices.

Economic models predict that rational decision makers' choices between a constant, "safe" option and a variable, "risky" option leading, on average, to the same payoff, should be random. However, a wealth of research has revealed that, when faced with risky decisions, both human and nonhuman animals deviate from economic rationality. According to the risk-sensitivity theory, individuals should prefer a safe option when they are in a positive energy state and a risky option when they are in a negative energy state. The abundance/risk hypothesis proposes that individuals should prefer risky options when diet quality exceeds their nutritional requirements. We tested how energy budget affects decision making under risk by presenting 22 capuchins belonging to two colonies (IT: N = 12, US: N = 10) with a risky choice task. Capuchins had to choose between a constant option (always four food items) and a variable option (one or seven food items with a 50% probability) in two conditions. In the Low-energy condition capuchins were tested before their main meal, whereas in the High-energy condition they were tested following a high-caloric meal. In neither colony did we find a significant difference between conditions, suggesting that the energy budget did not affect risk preferences. However, we found differences between colonies in their general response to risky choices: US capuchins were more risk-prone after selecting a safe option than a risky option and after selecting a bad (one food item) than a good (seven food items) risky option, whereas this did not hold true in IT capuchins. Furthermore, in the IT colony, males were more risk-prone under the High-energy condition compared to the Low-energy condition. Subtle differences in individual characteristics, management conditions, or stochastic founder effects may be implied, with relevant consequences for the outcomes of research on risky decision-making across laboratories.

The Evolution of Cognitive Control in Lemurs.

Cognitive control, or executive function, is a key feature of human cognition, allowing individuals to plan, acquire new information, or adopt new strategies when the circumstances change. Yet it is unclear which factors promote the evolution of more sophisticated executive-function abilities such as those possessed by humans. Examining cognitive control in nonhuman primates, our closest relatives, can help to identify these evolutionary processes. Here, we developed a novel battery to experimentally measure multiple aspects of cognitive control in primates: temporal discounting, motor inhibition, short-term memory, reversal learning, novelty responses, and persistence. We tested lemur species with targeted, independent variation in both ecological and social features (ruffed lemurs, Coquerel's sifakas, ring-tailed lemurs, and mongoose lemurs; N = 39) and found that ecological rather than social characteristics best predicted patterns of cognitive control across these species. This highlights the importance of integrating cognitive data with species' natural history to understand the origins of complex cognition.

Are capuchin monkeys (Sapajus spp.) sensitive to lost opportunities? The role of opportunity costs in intertemporal choice.

Principles of economics predict that the costs associated with obtaining rewards can influence choice. When individuals face choices between a smaller, immediate option and a larger, later option, they often experience opportunity costs associated with waiting for delayed rewards because they must forego the opportunity to make other choices. We evaluated how reducing opportunity costs affects delay tolerance in capuchin monkeys. After choosing the larger option, in the High cost condition, subjects had to wait for the delay to expire, whereas in the Low cost different and Low cost same conditions, they could perform a new choice during the delay. To control for the effect of intake rate on choices, the Low cost same condition had the same intake rate ratio as the High cost condition. We found that capuchins attended both to intake rates and to opportunity costs. They chose the larger option more often in the Low cost different and Low cost same conditions than in the High cost condition, and more often in the Low cost different condition than in the Low cost same condition. Understanding how non-human primates represent and use costs in making decisions not only helps to develop theoretical frameworks to explain their choices but also addresses similarities with and differences from human decision-making. These outcomes provide insights into the origins of human economic behaviour. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Variation in primate decision-making under uncertainty and the roots of human economic behaviour.

Uncertainty is a ubiquitous component of human economic behaviour, yet people can vary in their preferences for risk across populations, individuals and different points in time. As uncertainty also characterizes many aspects of animal decision-making, comparative research can help evaluate different potential mechanisms that generate this variation, including the role of biological differences or maturational change versus cultural learning, as well as identify human-unique components of economic decision-making. Here, we examine decision-making under risk across non-human primates, our closest relatives. We first review theoretical approaches and current methods for understanding decision-making in animals. We then assess the current evidence for variation in animal preferences between species and populations, between individuals based on personality, sex and age, and finally, between different contexts and individual states. We then use these primate data to evaluate the processes that can shape human decision-making strategies and identify the primate foundations of human economic behaviour. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Contextual factors modulate risk preferences in adult humans.

Humans have generally been considered risk averse for gains. Yet, growing evidence shows that risk preferences may change across reward currencies and depend on the type of tasks used to measure them. Here, we examined how context affects human risk preferences to shed light on the psychological mechanisms underlying human decision-making under risk. Participants were presented with a descriptive risky choice task involving repeated choices between real options and they were provided with trial-by-trial feedback. We manipulated the type of reward and, for the first time, the format of the choice stimuli. Options were either 2D computer-based images or concrete 3D objects, and participants received food or money as reward. First, we found that participants were more risk-seeking for food compared to money, suggesting that people treat money differently from consumable rewards. Second, we found that people were more risk-seeking when they made choices between concrete 3D objects than between 2D computer-based images. Our results strengthened the evidence that human choice patterns may change depending on the context and, for the first time, showed that the format of the choice stimuli does affect risk preferences, an important consideration for future research.

Rhesus macaques use probabilities to predict future events.

Humans can use an intuitive sense of statistics to make predictions about uncertain future events, a cognitive skill that underpins logical and mathematical reasoning. Recent research shows that some of these abilities for statistical inferences can emerge in preverbal infants and non-human primates such as apes and capuchins. An important question is therefore whether animals share the full complement of intuitive reasoning abilities demonstrated by humans, as well as what evolutionary contexts promote the emergence of such skills. Here, we examined whether free-ranging rhesus macaques (Macaca mulatta) can use probability information to infer the most likely outcome of a random lottery, in the first test of whether primates can make such inferences in the absence of direct prior experience. We developed a novel expectancy-violation looking time task, adapted from prior studies of infants, in order to assess the monkeys' expectations. In Study 1, we confirmed that monkeys (n = 20) looked similarly at different sampled items if they had no prior knowledge about the population they were drawn from. In Study 2, monkeys (n = 80) saw a dynamic 'lottery' machine containing a mix of two types of fruit outcomes, and then saw either the more common fruit (expected trial) or the relatively rare fruit (unexpected trial) fall from the machine. We found that monkeys looked longer when they witnessed the unexpected outcome. In Study 3, we confirmed that this effect depended on the causal relationship between the sample and the population, not visual mismatch: monkeys (n = 80) looked equally at both outcomes if the experimenter pulled the sampled item from her pocket. These results reveal that rhesus monkeys spontaneously use information about probability to reason about likely outcomes, and show how comparative studies of nonhumans can disentangle the evolutionary history of logical reasoning capacities.

Ecological rationality: Convergent decision-making in apes and capuchins.

Humans and other animals appear to defy many principles of economic 'rationality' when making decisions. Here, we use an ecological rationality framework to examine patterns of decision-making across species to illuminate the origins of these strategies. We argue that examples of convergent evolution-the independent emergence of similar traits in species facing similar environments-can provide a crucial test for evolutionary theories of decision-making. We first review theoretical work from evolutionary biology proposing that many economically-puzzling patterns of decision-making may be biologically adaptive when considering the environment in which they are made. We then focus on convergence in ecology, behavior, and cognition of apes and capuchin monkeys as an example of how to apply this ecological framework across species. We review evidence that wild chimpanzees and capuchins, despite being distantly related, both exploit ecological niches characterized by costly extractive foraging and risky hunting behaviors. We then synthesize empirical studies comparing these species' decision preferences. In fact, both capuchins and chimpanzees exhibit high tolerance for delays in inter-temporal choice tasks, as well as a preference for risky outcomes when making decisions under uncertainty. Moreover, these species exhibit convergent psychological mechanisms for choices, including emotional responses to decision outcomes and sensitivity to social context. Finally, we argue that identifying the evolutionary pressures driving the emergence of specific decision strategies can shed light into the adaptive nature of human economic preferences.

Evolutionary origins of money categorization and exchange: an experimental investigation in tufted capuchin monkeys (Sapajus spp.).

Money is a cultural artefact with a central role in human society. Here, we investigated whether some features of money may be traced back to the exchange habits of nonhuman animals, capitalizing on their ability to flexibly use tokens in different domains. In Experiment 1, we evaluated whether capuchins can recognize token validity. Six subjects were required to exchange with the experimenter valid/familiar tokens, valid/unfamiliar tokens, invalid tokens, and no-value items. They first exchanged a similar number of valid/familiar and valid/unfamiliar tokens, followed by exchanges of invalid tokens and no-value items. Thus, as humans, capuchins readily recognized token validity, regardless of familiarity. In Experiment 2, we further evaluated the flexibility of the token-food association by assessing whether capuchins could engage in reverse food-token exchanges. Subjects spontaneously performed chains of exchanges, in which a food item was exchanged for a token, and then the token was exchanged for another food. However, performance was better as the advantage gained from the exchange increased. Overall, capuchins recognized token validity and successfully engaged in chains of reverse and direct exchanges. This suggests that-although nonhuman animals are far from having fully-fledged monetary systems-for capuchins tokens share at least some features with human money.

When is it worth waiting for? Food quantity, but not food quality, affects delay tolerance in tufted capuchin monkeys.

When faced with choices between smaller sooner options and larger later options (i.e. intertemporal choices), both humans and non-human animals discount future rewards. Apparently, only humans consistently show the magnitude effect, according to which larger options are discounted over time at a lower rate than smaller options. Most of the studies carried out in non-human animals led instead to negative results. Here, we tested ten tufted capuchin monkeys (Sapajus spp.) in a delay choice task to evaluate whether they show a magnitude effect when choosing between different quantities of the same food or when the options are represented by high- and low-preferred foods in different conditions. Whereas food quality did not play a role, we provided the first evidence of an effect of the reward amount on temporal preferences in a non-human primate species, a result with potential implications for the validity of comparative studies on the evolution of delay tolerance. In contrast with human results, but as shown in other animal species, capuchins' choice of the larger later option decreased as the amount of the smaller sooner option increased. Capuchins based their temporal preferences on the quantity of the smaller sooner option, rather than on that of the larger later option, probably because in the wild they virtually never have to choose between the above two options at the same time, but they more often encounter them consecutively. Thus, paying attention to the sooner option and deciding on the basis of its features may be an adaptive strategy rather than an irrational response.

Do tufted capuchin monkeys play the odds? Flexible risk preferences in Sapajus spp.

As humans, several non-human animal species avoid risk, defined as "variability in rate of gain". However, non-human primate studies revealed a more complicated picture, with different species ranging from risk aversion to risk proneness. Within an ecological rationality framework, a species' feeding ecology should influence its risk preferences, as it has been shown in bonobos and chimpanzees. Although the feeding ecology hypothesis is promising, it has not been yet verified in species other than apes. Here, we aimed to assess whether this hypothesis holds true in tufted capuchin monkeys (Sapajus spp.). Ten capuchins were presented with choices between a "safe" option and a "risky" option in three conditions differing for the probability of receiving the larger reward when selecting the risky option. Similarly to chimpanzees, capuchins were risk prone. However, capuchins' behaviour was not the result of a bias towards the choice of the risky option, since-when facing options with different probabilities of obtaining the larger outcome-they were able to flexibly modify their preferences. Capuchins' decision-making under risk mirrors their risk-prone behaviour in the wild, where they often rely on unpredictable and/or hazardous food sources, thus satisfying the feeding ecology hypothesis.

Nonhuman gamblers: lessons from rodents, primates, and robots.

The search for neuronal and psychological underpinnings of pathological gambling in humans would benefit from investigating related phenomena also outside of our species. In this paper, we present a survey of studies in three widely different populations of agents, namely rodents, non-human primates, and robots. Each of these populations offers valuable and complementary insights on the topic, as the literature demonstrates. In addition, we highlight the deep and complex connections between relevant results across these different areas of research (i.e., cognitive and computational neuroscience, neuroethology, cognitive primatology, neuropsychiatry, evolutionary robotics), to make the case for a greater degree of methodological integration in future studies on pathological gambling.

Waiting by mistake: symbolic representation of rewards modulates intertemporal choice in capuchin monkeys, preschool children and adult humans.

In the Delay choice task subjects choose between a smaller immediate option and a larger delayed option. This paradigm, also known as intertemporal choice task, is frequently used to assess delay tolerance, interpreting a preference for the larger delayed option as willingness to wait. However, in the Delay choice task subjects face a dilemma between two preferred responses: "go for more" (i.e., selecting the larger, but delayed, option) vs. "go for sooner" (i.e., selecting the immediate, but smaller, option). When the options consist of visible food amounts, at least some of the choices of the larger delayed option might be due to a failure to inhibit a prepotent response towards the larger option rather than to a sustained delay tolerance. To disentangle this issue, we tested 10 capuchin monkeys, 101 preschool children, and 88 adult humans in a Delay choice task with food, low-symbolic tokens (objects that can be exchanged with food and have a one-to-one correspondence with food items), and high-symbolic tokens (objects that can be exchanged with food and have a one-to-many correspondence with food items). This allows evaluating how different methods of representing rewards modulate the relative contribution of the "go for more" and "go for sooner" responses. Consistently with the idea that choices for the delayed option are sometimes due to a failure at inhibiting the prepotent response for the larger quantity, we expected high-symbolic tokens to decrease the salience of the larger option, thus reducing "go for more" responses. In fact, previous findings have shown that inhibiting prepotent responses for quantity is easier when the problem is framed in a symbolic context. Overall, opting for the larger delayed option in the visible-food version of the Delay choice task seems to partially result from an impulsive preference for quantity, rather than from a sustained delay tolerance. In capuchins and children high-symbolic stimuli decreased the individual's preference for the larger reward by distancing from its appetitive features. Conversely, the sophisticated symbolic skills of adult humans prevented the distancing effect of high-symbolic stimuli in this population, although this result may be due to methodological differences between adult humans and the other two populations under study. Our data extend the knowledge concerning the influence of symbols on both human and non-human primate behavior and add a new element to the interpretation of the Delay choice task. Since high-symbolic stimuli decrease the individual's preference for the larger reward by eliminating those choices due to prepotent responses towards the larger quantity, they allow to better discriminate responses based on genuine delay aversion. Thus, these findings invite greater caution in interpreting the results obtained with the visible-food version of the Delay choice task, which may overestimate delay tolerance.

How capuchin monkeys (Cebus apella) behaviorally cope with increasing delay in a self-control task.

Displacement activities are behavior patterns apparently irrelevant to the situation in which they are performed that facilitate transitions between behavioral states. Scratching is one of the most commonly described displacement activities in primates and is related to frustration and anxiety. In chimpanzees scratching during cognitive tasks increases with task difficulty. We analyzed behavioral data obtained from video clips on nine capuchin monkeys tested in a delay choice task, a potentially stressful self-control task where subjects choose between a small immediate and a large delayed option. Scratching, response latency, and motor impulsivity scored during the delay decreased across sessions, as capuchins became indifferent between options, whereas the bias for choosing the option placed on one side of the apparatus increased. Capuchins might have found the delay choice task less stressful over time because they shifted from slower discriminatory responses in the earlier sessions to more 'automatic', faster responses in the later sessions. However, it cannot be excluded that they habituated over time to the contingencies of the task. In contrast with previous data on chimpanzees, handedness in scratching behavior or preferential scratching on one side of the body did not emerge, but further studies are needed to corroborate this finding.

Delay choice versus delay maintenance: different measures of delayed gratification in capuchin monkeys (Cebus apella).

Delaying gratification involves 2 components: (1) delay choice (selecting a delayed reward over an immediate one) and (2) delay maintenance (sustaining the decision to delay gratification even if the immediate reward is available during the delay). Two tasks most commonly have explored these components in primates: the intertemporal choice task and the accumulation task. It is unclear whether these tasks provide equivalent measures of delay of gratification. Here, we compared the performance on the intertemporal choice task and the accumulation task of capuchin monkeys (Cebus apella) belonging to 2 study populations. We found only limited evidence of a significant correlation in performance. Consequently, in contrast to what is often assumed, our data provide only partial support for the hypothesis that these tasks provide equivalent measures of delay of gratification.