No evidence of attentional bias toward threatening conspecific and allospecific faces in capuchin monkeys (Sapajus [Cebus] apella) using a dot-probe task.

The ability to quickly perceive and interpret threatening facial expressions from others is critical for successfully maintaining group cohesion in social nonhuman primate species. Rapid detection of threatening or negative stimuli in the environment compared to neutral stimuli, referred to as an attentional bias toward threat, is adaptive in that faster threat detection can lead to greater survival outcomes. However, the evolutionary roots of attentional bias formation toward social threat are not well understood. The present study investigated attentional biases toward social threat and the factors associated with them, including underlying hormonal mechanisms, in socially housed capuchin monkeys. Attentional biases were assessed using a dot-probe task that measured capuchins' latency to respond to a target using a joystick after viewing threatening or neutral conspecific or allospecific faces or nonface stimuli. In our first study, we examined how age, dominance status, sex, and cortisol level related to attentional biases. In our second study, we examined how manipulated oxytocin (OT) influenced attentional biases. Capuchin monkeys did not show attentional biases toward threatening faces or objects, but they showed attentional avoidance of scrambled familiar conspecific face stimuli. Cortisol and social rank were associated with attentional bias toward threat in the capuchin monkeys that participated in this study, which suggests that stress and dominance relate to attentional bias toward social threat. Manipulated OT increased attentional avoidance of scrambled familiar and unfamiliar face images, but not unscrambled faces or objects. Overall, we did not find compelling evidence of attentional biases toward social threat in capuchin monkeys. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

The Joint Simon task is not joint for capuchin monkeys.

Human cooperation can be facilitated by the ability to create a mental representation of one's own actions, as well as the actions of a partner, known as action co-representation. Even though other species also cooperate extensively, it is still unclear whether they have similar capacities. The Joint Simon task is a two-player task developed to investigate this action co-representation. We tested brown capuchin monkeys (Sapajus [Cebus] apella), a highly cooperative species, on a computerized Joint Simon task and found that, in line with previous research, the capuchins' performance was compatible with co-representation. However, a deeper exploration of the monkeys' responses showed that they, and potentially monkeys in previous studies, did not understand the control conditions, which precludes the interpretation of the results as a social phenomenon. Indeed, further testing to investigate alternative explanations demonstrated that our results were due to low-level cues, rather than action co-representation. This suggests that the Joint Simon task, at least in its current form, cannot determine whether non-human species co-represent their partner's role in joint tasks.

Capuchin monkeys' (Sapajus [Cebus] apella) categorization of photos of unknown male conspecifics suggests attention to fWHR and a dominance bias.

The ability to quickly perceive others' rank minimizes costs by helping individuals behave appropriately when interacting with strangers. Indeed, humans and at least some other species can quickly determine strangers' rank or dominance based only on physical features without observing others' interactions or behavior. Nonhuman primates can determine strangers' ranks by observing their interactions, and some evidence suggests that at least some cues to dominance, such as facial width-to-height ratio (fWHR), are also present in other primates. However, it is unknown whether they can determine strangers' rank simply by looking at their faces, rather than observing their interactions. If so, this would suggest selective pressure across the primates on both cues to dominance and the ability to detect those cues accurately. To address this, we examined the ability of male and female tufted capuchin monkeys (Sapajus [Cebus] apella) to categorize images of the faces of unknown conspecifics (Sapajus from different colonies) and humans (computer-generated and real) as dominant or nondominant based only on still images. Capuchins' categorization of unknown conspecific faces was consistent with fWHR, a cue to dominance, although there was a strong tendency to categorize strangers as dominant, particularly for males. This was true despite the continued correct categorization of known individuals. In addition, capuchins did not categorize human strangers in accordance with external pre-ratings of dominance by independent human raters, despite the availability of the same cue, fWHR. We consider these results in the context of capuchin socio-ecology and what they mean for the evolution of rapid decision-making in social contexts.

Some dogs can find the payoff-dominant outcome in the Assurance game.

Studies on coordination often present animals with the choice of either cooperating or remaining inactive; however, in nature, animals may also choose to act alone. This can be modeled with the Assurance game, an economic game that has recently been used to explore decision-making in primates. We investigated whether dyads of pet dogs coordinate in the Assurance game. Pairs were presented with two alternatives: they could individually solve an apparatus baited with a low-value reward (Hare) or they could coordinate to solve a cooperative apparatus baited with a high-value reward for each dog (Stag). All individuals matched their partner's choices, but after controlling for side bias, only four out of eleven dyads consistently coordinated on the payoff-dominant strategy (Stag-Stag). Thus, some dogs are capable of finding coordinated outcomes, as do primates, at least when their partner's actions are visible and coordination results in the biggest payoff for both individuals.

In search of animal normativity: a framework for studying social norms in non-human animals.

Social norms - rules governing which behaviours are deemed appropriate or inappropriate within a given community - are typically taken to be uniquely human. Recently, this position has been challenged by a number of philosophers, cognitive scientists, and ethologists, who have suggested that social norms may also be found in certain non-human animal communities. Such claims have elicited considerable scepticism from norm cognition researchers, who doubt that any non-human animals possess the psychological capacities necessary for normative cognition. However, there is little agreement among these researchers about what these psychological prerequisites are. This makes empirical study of animal social norms difficult, since it is not clear what we are looking for and thus what should count as behavioural evidence for the presence (or absence) of social norms in animals. To break this impasse, we offer an approach that moves beyond contested psychological criteria for social norms. This approach is inspired by the animal culture research program, which has made a similar shift away from heavily psychological definitions of 'culture' to become organised around a cluster of more empirically tractable concepts of culture. Here, we propose an analogous set of constructs built around the core notion of a normative regularity, which we define as a socially maintained pattern of behavioural conformity within a community. We suggest methods for studying potential normative regularities in wild and captive primates. We also discuss the broader scientific and philosophical implications of this research program with respect to questions of human uniqueness, animal welfare and conservation.

Evaluation of decision-making behavior under uncertainty in capuchin monkeys (Sapajus apella) and humans (Homo sapiens) using a modified Balloon Analogue Risk Task.

Many animals, including humans, must make decisions when outcomes involve risk and/or ambiguity. To explore the evolutionary roots of decision making when outcomes are unknown, we modified the Balloon Analogue Risk Task (BART) for use with tufted capuchin monkeys (Sapajus [Cebus] apella), creating the Primate Analogue Risk Task (PART). Using both the BART and the PART, we first compared human performance across the two tasks using analogous parameters. Humans' performance on the two tasks was positively correlated. Next, we tested capuchin monkeys' performance on the PART to assess their decision-making strategies in the context of ambiguity. Secondarily, although it was not the main goal of the study, this allowed us to look at species differences between capuchins' and humans' performance. Finally, we investigated the influence of prior experience on human and capuchin decision-making behavior. Neither capuchins nor humans behaved differently following an unsuccessful trial compared to a successful trial. We found individual differences in capuchin monkeys' choice behavior, though as a whole they demonstrated a pattern of reward maximization over time. Finally, as a species, capuchins had lower PART risk scores than humans. This paradigm presents a useful way to assess behavior in a context with uncertain outcomes using a comparative approach. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Humans' (Homo sapiens), capuchin monkeys' (Sapajus [Cebus] apella), and rhesus macaques' (Macaca mulatta) size judgments shift when stimuli change in frequency.

When making decisions, humans often strive to uphold objective, absolute standards, such as about what is small versus large, blue versus purple, or unfair versus fair, suggesting that our judgments should not be swayed by extraneous factors such as the sequence or frequency of events to be judged. Yet in previous research, when some items (e.g., threatening faces) became less frequent, humans responded by expanding their concept (of "threatening") to include more ambiguous stimuli. We assessed the origins of this perceptual frequency bias by testing 25 capuchins, seven rhesus monkeys, and 102 humans on a computer task in which they had to classify one circle at a time (pulled from a continuum of 50 circle sizes) as either small or large. Small and large circles initially appeared with equal probability but over time small circles either became less frequent, more frequent, or did not change in frequency. All three species showed changes in judgment, but contrary to predictions, they contracted, rather than expanded, their size judgments of the less frequent category. In other words, when small circles became rare, participants were more likely to judge ambiguous circles sizes as large (and vice versa). This may have been due to the immediate explicit feedback, as has recently been found in humans, and we consider possible mechanisms driving our participants' responses. These results suggest that humans' difficulties in maintaining absolute standards are shared with other animals. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Sex differences in white matter tracts of capuchin monkey brains.

Nonhuman primates exhibit sexual dimorphism in behavior, suggesting that there could be underlying differences in brain organization and function. Understanding this neuroanatomical variation is critical for enhancing our understanding of the evolution of sex differences in the human brain. Tufted capuchin monkeys (Sapajus [Cebus] apella) represent a phylogenetically diverse taxa of neotropical primates that converge on several behavioral characteristics with humans relevant to social organization, making them an important point of comparison for studying the evolution of sex differences in primates. While anatomical sex differences in gray matter have previously been found in capuchin monkeys, the current study investigates sex differences in white matter tracts. We carried out tract-based spatial statistical analysis on fractional anisotropy images of tufted capuchin monkeys (15 female, 5 male). We found that females showed significantly higher fractional anisotropy than males in regions of frontal-parietal white matter in the right cerebral hemisphere. Paralleling earlier findings in gray matter, male and female fractional anisotropy values in these regions were nonoverlapping. This complements prior work pointing toward capuchin sex differences in limbic circuitry and higher-order visual regions. We propose that these sex differences are related to the distinct socioecological niches occupied by male and female capuchins. Capuchin neuroanatomical sex differences appear to be more pronounced than in humans, which we suggest may relate to human adaptations for prolonged neurodevelopmental trajectories and increased plasticity.

Under pressure: the interaction between high-stakes contexts and individual differences in decision-making in humans and non-human species.

Observed behavior can be the result of complex cognitive processes that are influenced by environmental factors, physiological process, and situational features. Pressure, a feature of a situation in which an individual's outcome is impacted by his or her own ability to perform, has been traditionally treated as a human-specific phenomenon and only recently have pressure-related deficits been considered in relation to other species. However, there are strong similarities in biological and cognitive systems among mammals (and beyond), and high-pressure situations are at least theoretically common in the wild. We hypothesize that other species are sensitive to pressure and that we can learn about the evolutionary trajectory of pressure responses by manipulating pressure experimentally in these other species. Recent literature indicates that, as in humans, pressure influences responses in non-human primates, with either deficits in ability to perform ("choking") or an ability to thrive when the stakes are high. Here, we synthesize the work to date on performance under pressure in humans and how hormones might be related to individual differences in responses. Then, we discuss why we would expect to see similar effects of pressure in non-humans and highlight the existing evidence for how other species respond. We argue that evidence suggests that other species respond to high-pressure contexts in similar ways as humans, and that responses to pressure are a critical missing piece of our understanding of cognition in human and non-human animals. Understanding pressure's effects could provide insight into individual variation in decision-making in comparative cognition and the evolution of human decision-making.

Comparative economics: how studying other primates helps us better understand the evolution of our own economic decision making.

The origins of evolutionary games are rooted in both economics and animal behaviour, but economics has, until recently, focused primarily on humans. Although historically, specific games were used in targeted circumstances with non-human species (i.e. the Prisoner's Dilemma), experimental economics has been increasingly recognized as a valuable method for directly comparing both the outcomes of economic decisions and their underlying mechanisms across species, particularly in comparison with humans, thanks to the structured procedures that allow for them to be instantiated across a variety of animals. So far, results in non-human primates suggest that even when outcomes are shared, underlying proximate mechanisms can vary substantially. Intriguingly, in some contexts non-human primates more easily find a Nash equilibrium than do humans, possibly owing to their greater willingness to explore the parameter space, but humans excel at more complex outcomes, such as alternating between two Nash equilibria, even when deprived of language or instruction, suggesting potential mechanisms that humans have evolved to allow us to solve complex social problems. We consider what these results suggest about the evolution of economic decision-making and suggest future directions, in particular the need to expand taxonomic diversity, to expand this promising approach. This article is part of the theme issue 'Half a century of evolutionary games: a synthesis of theory, application and future directions'.

Oxytocin increases during fur-rubbing regardless of level of social contact in tufted capuchin monkeys.

Social interactions induce oxytocin release in many social species, suggesting that oxytocin is a critical part of social bonding among individuals. However, oxytocin also increases as a result of physical contact and stimulation, making it unclear which features of affiliative behaviors (for instance, social interaction or physical contact with a conspecific) drive the oxytocin increase observed after engaging in these behaviors. We attempted to tease this apart by studying the differential effect of social interaction, visual coordination with a conspecific, and physical stimulation during the fur-rubbing behavior of tufted capuchin monkeys (Sapajus [Cebus] apella), which often involves social contact with groupmates but is in some cases performed alone. We induced fur-rubbing by providing onions under three conditions: when capuchins had physical access to their social group and fur-rubbed in contact with groupmates (social condition), when capuchins were separated from their social group but could still see them fur-rub (visual coordination), and when capuchins were physically and visually separated from their groupmates (physical stimulation only). We assessed urinary oxytocin in these three conditions and compared them to a control condition in which apples were provided and no fur-rubbing was observed. Capuchins fur-rubbed for less time when they could not see their groupmates, but fur-rubbing increased urinary oxytocin above the control condition in all three fur-rubbing conditions equally, suggesting that the physical stimulation derived from fur-rubbing was the most important driver of oxytocin increase. These results support a model in which physical stimulation is an important factor in the relationship between oxytocin and at least some behaviors, suggesting that oxytocin increase alone is not necessarily indicative of a social influence on behavior. Future work is needed to determine the contexts in which social factors do impact oxytocin, and whether the downstream behaviors are the same for socially and nonsocially induced oxytocin release.

Dogs take into account the actions of a human partner in a cooperative task.

Humans stand out for their capacity to flexibly cooperate, possibly because they understand their partners' role. Researchers have explored if such understanding is unique to humans by assessing whether non-human species wait to manipulate a cooperative apparatus until a delayed partner arrives. If animals do wait, then it is assumed that they recognize the need for a partner. However, success in these tasks may be the result of social facilitation, while failure may be due to poor inhibitory control. Moreover, this approach does not test if animals take their partners' actions into account. Here we trained dogs to press a button simultaneously with their human partner. Afterwards, we tested them in several conditions to disentangle which elements of their partner's behaviour they take into account. Dogs waited to press the button until the delayed partner arrived, the button was available to the partner and the partner acted (pressed the button). We found no relationship between inhibitory control and success. We conclude that dogs are not merely reacting to the presence of their human partners, but are also taking their actions into account when coordinating with them.

Oxytocin and social gaze during a dominance categorization task in tufted capuchin monkeys.

Visual attention to facial features is an important way that group-living primate species gain knowledge about others. However, where this attention is focused on the face is influenced by contextual and social features, and emerging evidence in Pan species suggests that oxytocin, a hormone involved in forming and maintaining affiliative bonds among members of the same group, influences social attention as measured by eye gaze. Specifically, bonobos tend to focus on conspecifics' eyes when viewing two-dimensional images, whereas chimpanzees focus more on the edges of the face. Moreover, exogenous oxytocin, which was hypothesized to increase eye contact in both species, instead enhanced this existing difference. We follow up on this to (1) determine the degree to which this Pan pattern generalizes across highly social, cooperative non-ape primates and (2) explore the impact of exogenously administered vs. endogenously released oxytocin in impacting this behavior. To do so, we tracked gaze direction on a computerized social categorization task using conspecific faces in tufted capuchin monkeys (Sapajus [Cebus] apella) after (1) exogenously administering intranasal oxytocin using a nebulizer or (2) inducing an endogenous increase in oxytocin using fur-rubbing, previously validated to increase oxytocin in capuchins. Overall, we did not find a general tendency in the capuchins to look toward the eyes or mouth, but we found that oxytocin was related to looking behavior toward these regions, albeit not in a straightforward way. Considering frequency of looking per trial, monkeys were more likely to look at the eye region in the fur-rubbing condition as compared to either the saline or exogenous oxytocin conditions. However, in terms of duration of looking during trials in which they did look at the eye region, monkeys spent significantly less time looking at the eyes in both oxytocin conditions as compared to the saline condition. These results suggest that oxytocin did not necessarily enhance eye looking in capuchins, which is consistent with the results from Pan species, and that endogenous and exogenous oxytocin may behave differently in their effect on how social attention is allocated.

Validating Urinary Neopterin as a Biomarker of Immune Response in Captive and Wild Capuchin Monkeys.

Non-invasive health monitoring is advantageous for wild and captive primate populations because it reduces the need for traditional invasive techniques (i.e., anesthetization) that can be stressful and potentially harmful for individuals. The biomarker neopterin is an emerging tool in primatology to measure immune activation and immunosenescence, however, most neopterin studies have focused on catarrhine species with little comparative work examining neopterin and health in platyrrhines. To address this gap, we validated a commercially available enzyme-linked immunosorbent assay (ELISA) to measure urinary neopterin in two types of capuchin monkeys, a wild population of white-faced capuchins (Cebus imitator) and a socially housed captive colony of tufted capuchins (Sapajus apella). We analytically validated methods for measuring urinary neopterin in two capuchin populations and demonstrated that two commonly-used methods to control for urine concentration-creatinine and specific gravity (SG)-produced highly concordant results. We also biologically validated these methods by examining variation in neopterin levels based on environment (captive and wild) and age, and changes in levels associated with immune-response. We found that neopterin increased after immune perturbation (rabies vaccine booster), varied by environmental condition, and mirrored expected trends in immune system ontogeny. Our results improve understanding of the innate immune system in platyrrhine species and suggest neopterin may be useful for non-invasive health monitoring in both captive and wild primates.

Signatures of adaptive evolution in platyrrhine primate genomes.

The platyrrhine family Cebidae (capuchin and squirrel monkeys) exhibit among the largest primate encephalization quotients. Each cebid lineage is also characterized by notable lineage-specific traits, with capuchins showing striking similarities to Hominidae such as high sensorimotor intelligence with tool use, advanced cognitive abilities, and behavioral flexibility. Here, we take a comparative genomics approach, performing genome-wide tests for positive selection across five cebid branches, to gain insight into major periods of cebid adaptive evolution. We uncover candidate targets of selection across cebid evolutionary history that may underlie the emergence of lineage-specific traits. Our analyses highlight shifting and sustained selective pressures on genes related to brain development, longevity, reproduction, and morphology, including evidence for cumulative and diversifying neurobiological adaptations across cebid evolution. In addition to generating a high-quality reference genome assembly for robust capuchins, our results lend to a better understanding of the adaptive diversification of this distinctive primate clade.

Nudges for Judges: An Experiment on the Effect of Making Sentencing Costs Explicit.

Judges are typically tasked to consider sentencing benefits but not costs. Previous research finds that both laypeople and prosecutors discount the costs of incarceration when forming sentencing attitudes, raising important questions about whether professional judges show the same bias during sentencing. To test this, we used a vignette-based experiment in which Minnesota state judges (N = 87) reviewed a case summary about an aggravated robbery and imposed a hypothetical sentence. Using random assignment, half the participants received additional information about plausible negative consequences of incarceration. As predicted, our results revealed a mitigating effect of cost exposure on prison sentence term lengths. Critically, these findings support the conclusion that policies that increase transparency in sentencing costs could reduce sentence lengths, which has important economic and social ramifications.

Endogenous cortisol correlates with performance under pressure on a working memory task in capuchin monkeys.

Humans often experience striking performance deficits when their outcomes are determined by their own performance, colloquially referred to as "choking under pressure." Physiological stress responses that have been linked to both choking and thriving are well-conserved in primates, but it is unknown whether other primates experience similar effects of pressure. Understanding whether this occurs and, if so, its physiological correlates, will help clarify the evolution and proximate causes of choking in humans. To address this, we trained capuchin monkeys on a computer game that had clearly denoted high- and low-pressure trials, then tested them on trials with the same signals of high pressure, but no difference in task difficulty. Monkeys significantly varied in whether they performed worse or better on high-pressure testing trials and performance improved as monkeys gained experience with performing under pressure. Baseline levels of cortisol were significantly negatively related to performance on high-pressure trials as compared to low-pressure trials. Taken together, this indicates that less experience with pressure may interact with long-term stress to produce choking behavior in early sessions of a task. Our results suggest that performance deficits (or improvements) under pressure are not solely due to human specific factors but are rooted in evolutionarily conserved biological factors.

Correctional "Free Lunch"? Cost Neglect Increases Punishment in Prosecutors.

Prosecutors can influence judges' sentencing decisions by the sentencing recommendations they make-but prosecutors are insulated from the costs of those sentences, which critics have described as a correctional "free lunch." In a nationally distributed survey experiment, we show that when a sample of (n=178) professional prosecutors were insulated from sentencing cost information, their prison sentence recommendations were nearly one-third lengthier than sentences rendered following exposure to direct cost information. Exposure to a fiscally equivalent benefit of incarceration did not impact sentencing recommendations, as predicted. This pattern suggests that prosecutors implicitly value incorporating sentencing costs but selectively neglect them unless they are made explicit. These findings highlight a likely but previously unrecognized contributor to mass incarceration and identify a potential way to remediate it.

Modelling collective decision-making: Insights into collective anti-predator behaviors from an agent-based approach.

Collective decision-making is a widespread phenomenon across organisms. Studying how animal societies make group decisions to the mutual benefit of group members, while avoiding exploitation by cheaters, can provide unique insights into the underlying cognitive mechanisms. As a step toward dissecting the proximate mechanisms that underpin collective decision-making across animals, we developed an agent-based model of antipredatory alarm signaling and mobbing during predator-prey encounters. Such collective behaviors occur in response to physical threats in many distantly related species with vastly different cognitive abilities, making it a broadly important model behavior. We systematically assessed under which quantitative contexts potential prey benefit from three basic strategies: predator detection, signaling about the predator (e.g., alarm calling), and retreating from vs. approaching the predator. Collective signaling increased survival rates over individual predator detection in several scenarios. Signaling sometimes led to fewer prey detecting the predator but this effect disappeared when prey animals that had seen the predator both signaled and approached it, as in mobbing. Critically, our results highlight that collective decision-making in response to a threat can emerge from simple rules without needing a central leader or needing to be under conscious control.