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.

Available and unavailable decoys in capuchin monkeys (Sapajus spp.) decision-making.

Decision-making has been observed to be systematically affected by decoys, i.e., options that should be irrelevant, either because unavailable or because manifestly inferior to other alternatives, and yet shift preferences towards their target. Decoy effects have been extensively studied both in humans and in several other species; however, evidence in non-human primates remains scant and inconclusive. To address this gap, this study investigates how choices in capuchin monkeys (Sapajus spp.) are affected by different types of decoys: asymmetrically dominated decoys, i.e., available and unavailable options that are inferior to only one of the other alternatives, and phantom decoys, i.e., unavailable options that are superior to another available alternative. After controlling for the subjective strength of initial preferences and the distance of each decoy from its target in attribute space, results demonstrate a systematic shift in capuchins' preference towards the target of both asymmetrically dominated decoys (whether they are available or not) and phantom decoys, regardless of what options is being targeted by such decoys. This provides the most comprehensive evidence to date of decoy effects in non-human primates, with important theoretical and methodological implications for future comparative studies on context effects in decision-making.

Context-effect bias in capuchin monkeys (Sapajus spp.): exploring decoy influences in a value-based food choice task.

Decision making is known to be liable to several context effects. In particular, adding a seemingly irrelevant alternative (decoy) to a set of options can modify preferences: typically, by increasing choices towards whatever option clearly dominates the decoy (attraction effect), but occasionally also decreasing its appeal and generating a shift in the opposite direction (repulsion effect). Both types of decoy effects violate rational choice theory axioms and suggest dynamic processes of preference-formation, in which the value of each alternative is not determined a priori, but it is instead constructed by comparing options during the decision process. These effects are well documented, both in humans and in other species: e.g., amoebas, ants, honeybees, frogs, birds, cats, dogs. However, evidence of decoy effects in non-human primates remains surprisingly mixed. This study investigates decoy effects in capuchin monkeys (Sapajus spp.), manipulating time pressure across different conditions, to test whether such effects require time-consuming comparative processes among available alternatives. Whereas the time-dependent nature of decoy effects is a robust finding in the human literature, this is its first investigation in non-human animals. Our results show that capuchins exhibit an attraction effect with decoys targeting their preferred food, and that this effect disappears under time pressure; moreover, we observe preliminary evidence of a repulsion effect when decoys target instead the less-preferred food, possibly due to the larger distance between decoy and target in the attribute space. Taken together, these results provide valuable insight on the evolutionary roots of comparative decision making.

Observation of Masturbation After Visual Sexual Stimuli From Conspecifics in a Captive Male Bearded Capuchin (Sapajus libidinosus).

Masturbation is part of the natural behavioral repertoire of primates, with visual sexual stimuli known to trigger this behavior. Here, we report masturbation events triggered by visual sexual stimulus (VSS) in the South American primate Sapajus libidinosus. We observed a multi-male multi-female captive colony of 17 bearded capuchins between January and October 2014. Over this period, we registered 11 copulation events, 68 attempt copulations, and five masturbation events. The same low-ranking male (named Fu) performed all masturbation events. Fu directly looked at other individuals engaged in sexual displays while he masturbated in three events. The masturbation events associated with VSS lasted up to 2 min and 40 s. Our observations show that VSS can trigger masturbation in capuchin monkeys. The low hierarchy rank of the male, and the consequent lack of mating opportunities in the multi-male multi-female recently formed group in captivity, may have prompted the masturbation events.

Moving.

Examples of realized scientific careers can provide ideas and inspiration for others aiming to pursue such careers. Here I recount in brief the story of my long career in primatology (1973 to the present), focusing on one enduring theme in my research: the nature and genesis of goal-directed action (evident in movement). The story begins in graduate school, passes through developing my own laboratory, on to pursuing a spectrum of studies with mentees and collaborators, developing a theoretical explanatory framework for goal-directed action that I think holds promise for the field as a whole, and ends with an exciting field project that seems a suitable finale to my career. I mention the value to me, the field, and society of participation in scientific societies, including the American Society of Primatologists, throughout my career.

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.

A robust tool kit: First report of tool use in captive crested capuchin monkeys (Sapajus robustus).

Primate tool use is of great interest but has been reported only in a limited number of species. Here we report tool use in crested capuchin monkeys (Sapajus robustus), an almost completely unstudied robust capuchin species. Crested capuchins and their sister species, the yellow-breasted capuchin, diverged from a common ancestor over 2 million years ago, so this study fills a significant gap in understanding of tool use capacity and variation within the robust capuchin monkey radiation. Our study group was a captive population of seven individuals at the Santa Ana Zoo in California. The monkeys were given no prior training, and they were provided with a variety of enrichment items, including materials that could be used as tools as well as hard-to-access resources, for open-ended interactions. In 54 observation hours, monkeys performed eleven tool use actions: digging, hammering, probing, raking, sponging, striking, sweeping, throwing, waving, wedging, and wiping. We observed tool modification, serial tool use, and social learning opportunities, including monkeys' direct observation of tool use and tolerated scrounging of foods obtained through tool use. We also observed significant individual skew in tool use frequency, with one individual using tools daily, and two individuals never using tools during the study. While crested capuchins have never been reported to use tools in the wild, our findings provide evidence for the species' capacity and propensity for tool use, highlighting the urgent need for research on this understudied, endangered primate. By providing detailed data on clearly identified S. robustus individuals, this study marks an effort to counteract the overgeneralization in the captive literature in referring to any robust capuchins of unknown provenance or ancestry as Cebus apella, a practice that obfuscates potential differences among species in tool use performance and repertoire in one of the only species-rich tool-using genera in the world.

Diet, activity patterns, and home range use in forest and cultivated areas for one wild group of endangered crested capuchin monkeys (Sapajus robustus) in Reserva Natural Vale, Espírito Santo, Brazil.

Robust capuchin monkeys (Sapajus spp.) are distributed widely in the Neotropics and may be able to survive in modified landscapes because of their omnivorous, opportunistic diet. The poorly known and endangered crested capuchin monkey (Sapajus robustus) is endemic to the Atlantic Forest in Bahia, Minas Gerais and Espírito Santo states, Brazil. We collected data on diet and home range for a crested capuchin group with access to forest and cultivated areas. We hypothesized that with access to cultivated exotic fruit, capuchins would use cultivated areas more for feeding during the season of fruit scarcity in the surrounding forest and have a small home range size because of higher fruit availability. Both the forest and the cultivated areas peaked in fruit availability in the wet season, with a low proportion of trees producing fruit in the dry season; cultivated areas had a higher proportion of trees in fruit compared to the forest throughout the study. While monkeys consumed exotic fruits like jackfruit and oil palm, we recorded more samples of them eating forest fruits than exotic fruits in all but 1 month, and they consumed a more diverse array of forest fruits (56 species) but only six exotic species. Home range size was relatively small compared with other studies: 120.5 ha across the year (wet season 102 ha, dry season 111.5 ha). Natural and human-intensified fruit sources in a protected area without hunting may have allowed monkeys to maintain a smaller home range size. The group composition changed during the study; this also likely influenced home range use. Studies focused on robust capuchin groups that utilize agricultural or cultivated foods may underestimate home range needs for groups without access to human-intensified food sources. Studying crested capuchin ecology in additional locations will be important for establishing a sound species conservation program.

What happened? Do preschool children and capuchin monkeys spontaneously use visual traces to locate a reward?

The ability to infer unseen causes from evidence is argued to emerge early in development and to be uniquely human. We explored whether preschoolers and capuchin monkeys could locate a reward based on the physical traces left following a hidden event. Preschoolers and capuchin monkeys were presented with two cups covered with foil. Behind a barrier, an experimenter (E) punctured the foil coverings one at a time, revealing the cups with one cover broken after the first event and both covers broken after the second. One event involved hiding a reward, the other event was performed with a stick (order counterbalanced). Preschoolers and, with additional experience, monkeys could connect the traces to the objects used in the puncturing events to find the reward. Reversing the order of events perturbed the performance of 3-year olds and capuchins, while 4-year-old children performed above chance when the order of events was reversed from the first trial. Capuchins performed significantly better on the ripped foil task than they did on an arbitrary test in which the covers were not ripped but rather replaced with a differently patterned cover. We conclude that by 4 years of age children spontaneously reason backwards from evidence to deduce its cause.

Initial experimental experience of triple-knockout pig red blood cells as potential sources for transfusion in alloimmunized patients with sickle cell disease.

BACKGROUND: Blood transfusion remains important in the treatment of patients with sickle cell disease (SCD). However, alloimmunization after blood transfusion is associated with patient morbidity and mortality. Triple-knockout (TKO) pigs (i.e., pigs in which the three known xenoantigens to which humans have anti-pig antibodies have been deleted) may be an alternative source of RBCs for these patients because many humans have no preformed antibodies to TKO pig RBCs (pRBCs). METHODS AND MATERIALS: In an in vitro study, plasma from alloimmunized (n = 12) or non-alloimmunized (n = 12) SCD patients was used to determine IgM/IgG binding to, and CDC of, TKO pRBCs. In an in vivo study, after an estimated 25% of blood volume was withdrawn from two capuchin monkeys, CFSE-labeled TKO pRBCs were transfused. Loss of TKO pRBCs was monitored by flow cytometry, and 7 weeks later, 25% of blood was withdrawn, and CFSE-labeled monkey RBCs were transfused. RESULTS: The in vitro study demonstrated that plasma from neither alloimmunized nor non-alloimmunized SCD patients bound IgM/IgG to, or induced CDC of, TKO pRBCs. In the in vivo study, survival of TKO pRBCs in the two capuchin monkeys was of 5 and 7 days, respectively, whereas after allotransfusion, survival was >28 days. CONCLUSIONS: In conclusion, (1) in the present limited study, no antibodies were detected that cross-reacted with TKO pRBCs, and (2) TKO pigs may possibly be an alternate source of RBCs in an emergency if no human RBCs are available.

Do capuchin monkeys (Sapajus apella) use exploration to form intuitions about physical properties?

Humans' flexible innovation relies on our capacity to accurately predict objects' behaviour. These predictions may originate from a "physics-engine" in the brain which simulates our environment. To explore the evolutionary origins of intuitive physics, we investigate whether capuchin monkeys' object exploration supports learning. Two capuchin groups experienced exploration sessions involving multiple copies of two objects, one object was easily opened (functional), the other was not (non-functional). We used two within-subject conditions (enrichment-then-test, and test-only) with two object sets per group. Monkeys then underwent individual test sessions where the objects contained rewards, and they choose one to attempt to open. The monkeys spontaneously explored, performing actions which yielded functional information. At test, both groups chose functional objects above chance. While high performance of the test-only group precluded us from establishing learning during exploration, this study reveals the promise of harnessing primates' natural exploratory tendencies to understand how they see the world.

Anticipating future actions: Motor planning improves with age in wild bearded capuchin monkeys (Sapajus libidinosus).

Self-directed object manipulation tasks illuminate development of motor planning. Grasping strategies that lead to good object control to perform the following action(s) reveal second-order motor planning. Motor planning for efficient grips develops slowly in children. Age-related differences in other primates have been poorly investigated. Here, we investigated anticipatory motor planning of infant, juvenile and adult wild capuchin monkeys grasping a horizontally positioned stick baited to the left or right side (a version of the elevated spoon task). We recorded the grasps capuchins used to bring the baited end of the stick to the mouth. The percentage of efficient radial grips positively correlated with age and adults used efficient grips significantly more frequently than infants. Adult wild capuchins' use of radial grips was higher than that reported for adult captive capuchins in similar tasks, suggesting that experience throughout life may influence motor anticipation. Self-directed object manipulation tasks will be useful to compare this aspect of cognition across primates. A video abstract of this article can be viewed at https://youtu.be/a1Zbr_AQkb8.

The role of hunting on Sapajus xanthosternos' landscape of fear in the Atlantic Forest, Brazil.

Habitats with spatial variation in food availability, predation risk, and hunting pressure allow us to study how animals resolve the trade-off between food searching and predator avoidance. We investigated the influence of food availability, predation risk, and the perceived predation risk on habitat use by a primate living under high hunting pressure, the yellow-breasted capuchin monkeys, Sapajus xanthosternos, at Una Biological Reserve (ReBio Una). We hypothesized that the hunting pressure occurring in the capuchins' home range would favor predator avoidance to the detriment of searching for food. We characterized a set of covariates related to resource availability (fruit and invertebrate biomasses, feeding on dispersed and clumped food items, sleeping sites), perceived predation risk (alarm calls given to terrestrial and aerial predators, silent group movement, and vigilance behavior), and actual predation risk (evidence of hunting) and estimated their effects on how one group of capuchin monkeys uses its habitat. The group divides its time among three major forest types within their home range: agroforest, mature, and secondary. Our results suggest that the actual and perceived risk of hunting by humans, as well as the perceived predation risk by both terrestrial and aerial predators, were significant determinants of capuchin monkeys' space use. Yellow-breasted capuchin monkeys' space use was negatively related to the risk of hunting by humans (actual evidence and silent behavior), the perceived risk of predation by both aerial and terrestrial predators, and the presence of sleeping sites. Capuchin monkeys' use of space was not related to the biomass of fruits in the habitat, and the biomass of invertebrates had a very low positive effect. We confirmed our prediction that in a habitat with high hunting pressure, the risk of predation, both perceived and actual, had a more significant impact on how yellow-breasted capuchins used space than did food availability.

Optional tool use: The case of wild bearded capuchins (Sapajus libidinosus) cracking cashew nuts by biting or by using percussors.

Tool use in humans can be optional, that is, the same person can use different tools or no tool to achieve a given goal. Strategies to reach the same goal may differ across individuals and cultures and at the intra-individual level. This is the first experimental study at the intra-individual level on the optional use of a tool in wild nonhuman primates. We investigated optional tool use by wild bearded capuchins (Sapajus libidinosus) of Fazenda Boa Vista (FBV; Piauí, Brazil). These monkeys habitually succeed in cracking open the mesocarp of dry cashew nuts (Anacardium spp.) by pounding them with stones and/or by biting. We assessed whether availability of a stone and resistance of the nut affected capuchins' choice to pound or to bite the nuts and their rates of success. Sixteen capuchins (1-16 years) received small and large dry cashew nuts by an anvil together with a stone (Stone condition) or without a stone (No-Stone condition). In the Stone conditions, subjects used it to crack the nut in 89.1% (large nuts) and 90.1% (small nut) of the trials. Nut size significantly affected the number of strikes used to open it. Availability of the stone significantly increased the average percent of success. In the No-Stone conditions, monkeys searched for and used other percussors to crack the nuts in 54% of trials. In all conditions, age affects percentage of success and number of strikes to reach success. We argue that exclusive use of stones in other sites may be due to the higher abundance of stones at these sites compared with FBV. Since capuchins opened cashews with a tool 1-2 years earlier than they succeed at cracking more resistant palm nuts, we suggest that success at opening cashew nuts with percussors may support the monkeys' persistent efforts to crack palm nuts.

Efficacy of ATG and Rituximab in capuchin monkeys (a New World monkey)-An in vitro study relevant to xenotransplantation.

While Old World monkeys, for example, baboons, have antibodies against triple-knockout (TKO) pig cells, thus complicating pig organ transplantation studies, capuchin monkeys (a New World monkey) do not, thus more closely mimicking humans in respect to the response to TKO pig cells. Whether drugs such as anti-thymocyte globulin (ATG) and Rituximab are effective in capuchin monkeys remains uncertain. We measured the binding and cytotoxicity of ATG and Rituximab to human (n = 7), baboon (n = 7), and capuchin monkey (n = 5) peripheral blood mononuclear cells (PBMCs), T cells or B cells by flow cytometry.The effect in vitro of ATG in depleting PBMCs in capuchin monkeys and baboons was significantly less than in humans, but the depletion in capuchin monkeys was not significantly different from that in baboons. In contrast, the effect in vitro of Rituximab in depleting B cells in capuchin monkeys was very limited, and significantly less than in humans and baboons.Although capuchin monkeys mimic the human antibody response to TKO pig cells more closely than baboons, Rituximab had a minimal effect in capuchin monkeys in vitro. This observation may limit the value of New World Monkeys as recipients of pig organs, tissues, or cells in experimental studies of xenotransplantation or, indeed, in allotransplantation.

Outcome expectancy and suboptimal risky choice in nonhuman primates.

Animals will favor a risky option when a stimulus signaling reward bridges the choice and the outcome. The present experiments investigated signal-induced risky choices and reward-outcome expectations in rhesus and capuchin monkeys. Risky choice was assessed by preference for a large-probabilistic reward over a modest-certain reward. Outcome expectancy was assessed by providing a truncation-response to shorten the delay period. In Experiment 1 both species generally favored the risky option compared to a safe option when the outcomes were signaled and generally shortened the delays except when a signaled-loss stimulus was presented. The use of the delay-truncation response suggested that the monkeys were sensitive to the information conveyed by the stimulus. Experiments 2 and 3 were designed to investigate whether the delay-truncation response used by capuchin monkeys was strategically used reflecting explicit decision-making versus a conditioned response to reward stimuli. A perceptual judgment task was included and the selective use of the delay-truncation response on unsignaled correct trials may suggest the involvement of metacognitive processes. The capuchin monkeys generally truncated the delays except under conditions where reward would not be expected (risky-loss or incorrect-judgment). When the outcomes were unsignaled during the delay some capuchin monkeys were less likely to truncate the delay following an incorrect task response. Overall, the monkeys: (1) made more risky choices when the outcomes were signaled - consistent with gambling-like behavior. (2) selectively truncated the unsignaled delays when rewards could be anticipated (even when metacognitive-like awareness guided anticipation) - suggesting that delay truncation responses reflect explicit outcome expectancy.

Linear numerosity illusions in capuchin monkeys (Sapajus apella), rhesus macaques (Macaca mulatta), and humans (Homo sapiens).

Numerosity illusions emerge when the stimuli in one set are overestimated or underestimated relative to the number (or quantity) of stimuli in another set. In the case of multi-item arrays, individual items that form a better Gestalt are more readily grouped, leading to overestimation by human adults and children. As an example, the Solitaire illusion emerges when dots forming a central cluster (cross-pattern) are overestimated relative to the same number of dots on the periphery of the array. Although this illusion is robustly experienced by human adults, previous studies have produced weaker illusory results for young children, chimpanzees, rhesus macaques, capuchin monkeys, and guppies. In the current study, we presented nonhuman primates with other linear arrangements of stimuli from Frith and Frith's (Percept Psychoph 11:409-410, 1972) original paper with human participants that included the Solitaire illusion. Capuchin monkeys, rhesus macaques, and human adults learned to quantify black and white dots that were presented within intermingled arrays, responding on the basis of the more numerous dot colors. Humans perceived the various illusions similar to the original findings of Frith and Frith (1972), validating the current comparative design; however, there was no evidence of illusory susceptibility in either species of monkey. These results are considered in light of illusion susceptibility among primates as well as considering the role of numerical discrimination abilities and perceptual processing mode on illusion emergence.

Ultrasonographic appearance and measurement of abdominal structures in healthy Capuchin monkeys (Sapajus spp.).

BACKGROUND: Previous ultrasonographic studies of Sapajus apella to determine the normal anatomy and physiology are incomplete. The aim of this study was to determine normal ultrasonographic appearance and measurements of all abdominal organs and structures of interest. METHODS: Twelve adult monkeys were recruited considered healthy on the basis of history, physical examination, and general blood work. To avoid additional anesthesia, the ultrasonographic examinations were performed during routine screening, annually scheduled by the Unit of Cognitive Primatology & Primate Center, CNR-Rome, where the animals were housed. Ultrasound data were processed offline by two experienced ultrasonographers. RESULTS: Topography, morphology and echostructure were described for almost all organs and descriptive statistics were provided. CONCLUSION: To the author's knowledge, this is the most complete ultrasonographic study in Capuchin monkeys.

Exploring the Jastrow Illusion in Humans ( Homo sapiens), Rhesus Monkeys ( Macaca mulatta), and Capuchin Monkeys ( Sapajus apella).

In the Jastrow size illusion, two vertically stacked but offset stimuli of identical size are misperceived such that the bottom stimulus is overestimated relative to the top stimulus due to their spatial layout. In this study, we explored whether nonhuman primates perceive this geometric illusion in the same manner as humans. Human adults, rhesus macaques, and capuchin monkeys were presented with a computerized size discrimination task including Jastrow illusion probe trials. Consistent with previous results, humans perceived the illusory stimuli, validating the current experimental approach. Adults selected the bottom figure as larger in illusion trials with identical shapes, and performance was facilitated in trials with a true size difference when the larger figure was positioned at bottom. Monkeys performed very well in trials with a true size difference including difficult discriminations (5% difference in stimuli size), but they did not show evidence of the Jastrow illusion. They were indifferent between top and bottom stimuli in the illusory arrangement, showing no evidence of a human-like (or reversed) bias. These results are considered in light of differences in perceptual processing across primates and in comparison to previous comparative studies of the Jastrow and other size illusions.

Irrational choice behavior in human and nonhuman primates.

Choice behavior in humans has motivated a large body of research with a focus on whether decisions can be considered to be rational. In general, humans prefer having choice, as do a number of other species that have been tested, even though having increased choice does not necessarily yield a positive outcome. Humans have been found to choose an option more often only because the opportunity to select it was diminishing, an example of a deviation from economic rationality. Here we extend this paradigm to nonhuman primates in an effort to understand the mechanisms underlying this finding. In this study, we presented two groups of laboratory monkeys, capuchins (Cebus apella) and rhesus macaques (Macaca mulatta), as well as human subjects, with a computerized task in which subjects were presented with two differently colored icons. When the subject selected an icon, differing numbers of food pellets were dispensed (or points were assigned), making each icon correspond to a certain level of risk (one icon yielded 1 or 4 pellets/points and the other yielded 2 or 3). Initially, both options remained constantly available and we established choice preference scores for each subject. Then, we assessed preference patterns once the options were not continuously available. Specifically, choosing one icon would cause the other to shrink in size on the screen and eventually disappear if never selected. Selecting it would restore it to its full size. As predicted, humans shifted their risk preferences in the diminishing options phase, choosing to click on both icons more equally in order to keep both options available. At the group level, capuchin monkeys showed this pattern as well, but there was a great deal of individual variability in both capuchins and macaques. The present work suggests that there is some degree of continuity between human and nonhuman primates in the desire to have choice simply for the sake of having choice.