Erratum: The shape of lipsmacking: socio-emotional regulation in bearded capuchin monkeys (Sapajus libidinosus) - CORRIGENDUM.

[This corrects the article DOI: 10.1017/ehs.2023.10.].

Towards an Integrated Concept of Personality in Human and Nonhuman Animals.

Every individual has an idiosyncratic way of feeling, thinking and behaving, which is relatively stable across time and situations. Usually known as Personality, today this phenomenon is recognized in many species, including arthropods, fish, avian or mammals. From an evolutionary perspective, research has shown that personality differences are manifest in distinctive forms of dealing with selective pressures, with consequences for fitness. Despite these facts, the study of personality in animals other than humans is relatively new. Only two decades ago, consistent behavioral individual differences were considered 'noise' around an optimal strategy for behavioral ecologists. Also, psychologists were not interested in animal personality as a consequence of the fear of anthropomorphization and the erroneous belief that humans are unique in nature. Fortunately, this misconception seems already overcome but there are still conceptual issues preventing a unified concept of personality. Throughout this review, we first explore the etymological origins of personality and other terminological issues. We further revise the historical course of the study of personality in humans and other animals, from the perspectives of Psychology and Behavioral Ecology, on the basis of the most used approach, the trait theory. We present the study of nonhuman primates as a paradigmatic example in between both frameworks. Finally, we discuss about the necessity of a unified science of personality.

News and Perspectives: Words matter in primatology.

Postings on social media on Twitter (now X), BioAnthropology News (Facebook), and other venues, as well as recent publications in prominent journals, show that primatologists, ecologists, and other researchers are questioning the terms "Old World" and "New World" due to their colonial implications and history. The terms are offensive if they result in erasing Indigenous voices and history, ignoring the fact that Indigenous peoples were in the Americas long before European colonization. Language use is not without context, but alternative terminology is not always obvious and available. In this perspective, we share opinions expressed by an international group of primatologists who considered questions about the use of these terms, whether primatologists should adjust language use, and how to move forward. The diversity of opinions provides insight into how conventional terms used in primatological research and conservation may impact our effectiveness in these domains.

The shape of lipsmacking: socio-emotional regulation in bearded capuchin monkeys (Sapajus libidinosus).

Capuchin monkeys have rich social relationships and from very young ages they participate in complex interactions with members of their group. Lipsmacking behaviour, which involves at least two individuals in socially mediated interactions, may tell about processes that maintain, accentuate or attenuate emotional exchanges in monkeys. Lipsmacking is a facial expression associated with the establishment and maintenance of affiliative interactions, following under the 'emotional regulation' umbrella, which accounts for the ability to manage behavioural responses. We investigated behaviours related to the emitter and to the receiver (infant) of lipsmacking to answer the question of how lipsmacking occurs. In capuchin monkeys, lipsmacking has been previously understood solely as a face-to-face interaction. Our data show that emitters are engaged with infants, looking longer towards their face and seeking eye contact during the display. However, receivers spend most of the time looking away from the emitter and stay in no contact for nearly half of the time. From naturalistic observations of wild infant capuchin monkeys from Brazil we found that lipsmacking is not restricted to mutual gaze, meaning there are other mechanisms in place than previously known. Our results open paths to new insights about the evolution of socio-emotional displays in primates.

Ontogenesis of sociability of wild immature capuchin monkeys (Sapajus libidinosus): Sex more than personality explains interindividual variation.

Sociability is a fundamental trait that social animals need to survive and reproduce in societies. Sociability predicts how an individual can consistently interact with its conspecifics across time and situations. By studying capuchin monkeys (Sapajus libidinosus), a neotropical primate with complex social behavior and high cognitive capacity, our research aims to analyze the development of the social axis of personality of immature individuals, from birth to the third year of life. We studied wild monkeys belonging to a group with infants, juveniles, and adults of both sexes that inhabits northeastern Brazil. We analyzed the behavior of 12 immature capuchins (6 males and 6 females) in 94 h of videos recorded weekly from birth until 36 months, through daily focal sampling. We verified whether there was intraindividual consistency throughout development by fitting regression models for the effect of age on initiating affiliative social behaviors, controlling for monkey identity and sex. Our results indicate that the individuals of this study exhibit high variation in the initiation of behaviors at the beginning of infancy; there was low repeatability and high intra-individual variation during the first 3 years of life of these individuals, indicating that the social personality is not consolidated in this period. Immature females were more sociable than immature males. Therefore, differences in sociability in early life of bearded capuchin monkeys are best explained by sex rather than personality. We suggest that the high initial behavioral variation in the social axis of personality allows for plasticity influenced by the environment throughout development. The high sociability of females in infancy may be related to female philopatry and their high sociability in adulthood.

Homosexual Courtship in Young Wild Capuchin Monkeys: A Case Study.

In primates, many species exhibit same-sex sexual behaviors (SSB), defined as "genital contact or genital manipulation between same-sex individuals." Several sociosexual functions have been proposed, including proceptivity enhancement, receptivity reduction, dominance assertion, practice for heterosexual copulation, tension regulation, reconciliation, and alliance formation. Capuchin monkeys are known for their rich and flexible sexual behavioral repertoire and elaborated courtships. At present, the few reports of SSB in capuchin monkeys (genera Sapajus and Cebus) focused on mounting. Here, we describe the case observed in a population of wild yellow-breasted capuchin monkeys (Sapajus xanthosternos) in which two young males, aged 5-6 years and 19 months, performed a 15-min uninterrupted sequence of courtship behaviors and mounting. Comparing with a previously established ethogram of 20 behaviors typical for heterosexual behavior of tufted capuchins, we show that these males performed 16 of them. Thus, SSBs are already present in the repertoire of young individuals and the practice may serve to create or strengthen bonds. Although same-sex mounting and genital inspection are common in capuchins' play and other social interactions, the almost entire array of courtship behaviors has never been observed in youngsters. Additionally, this example supports the notion that primate (homo)sexual behavior is not limited to genitalia and copulation, since the observed courtship included diverse behaviors different from genital contact. Thus, we propose a broader definition of sexual behavior.

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.

Stone tools improve diet quality in wild monkeys.

Tool use is a fundamental feature of human evolution. Stone tools are in the archaeological record from 3.4 Ma, even before Homo,1 and the use of stone tools probably predated the split between hominins and panins.2 Using tools (hereafter, tooling cf Fragaszy and Mangalam3) is hypothesized to have improved hominins' foraging efficiency or access to high-quality foods.4-7 This hypothesis is supported if feeding with tools positively contributes to diet quality in extant non-human primates or if foraging efficiency is increased by tooling. However, the contribution of tooling to non-human primates' foraging success has never been investigated through a direct analysis of nutritional ecology.8,9 We used multi-dimensional nutritional geometry to analyze energy and macronutrients (nonstructural carbohydrates, lipids, and protein) in the diets of wild capuchin monkeys (Sapajus libidinous) that routinely crack palm nuts with stone hammers.10,11 We show that eating nuts obtained through tooling helps monkeys to achieve more consistent dietary intakes. Tooling increased the net energy gain by 50% and decreased the proportion of fiber ingested by 7%. Tooling also increased the daily non-protein energy intake. By contrast, protein intake remained constant across foraging days, suggesting a pattern of macronutrient regulation called protein prioritization, which is also found in contemporary humans.8,9 In addition, tooling reduced dispersion in the ratio of protein to non-protein energy, suggesting a role in macronutrient balancing. Our findings suggest that tooling prior to tool making could have substantially increased the nutritional security of ancestral hominins, sowing the seeds for cultural development.5,7 VIDEO ABSTRACT.

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.

Black capuchin monkeys dynamically adjust group spread throughout the day.

Variation in group spread can affect communication between individuals, synchrony of activity and collective decision-making. Most studies have measured this variation in large time scales, but the variables that influence group spread change as the social unit ranges over different areas throughout the day. Thus, our aim was to analyze the diurnal variation in group spread of a group of black capuchin monkeys (Sapajus nigritus) inhabiting an area within the southeastern Brazilian Atlantic Forest, the Carlos Botelho State Park. We measured group spread as the distance between the coordinates of the location of the two most distant group members every 5 min during entire days. Using time series analysis, we found that the group spread varied within short periods of time (15 min) throughout the day, revolving around the average group spread distance of 36 m. Group members tended to decrease the interindividual distance over time when they were more than 36 m apart, and to increase the distance when they were at a distance of less than 36 m. In addition, group spread was higher when monkeys were eating fruit than during other activities. We conclude that the variation in group spread may reflect competition for discrete food resources and that increasing cohesion several times throughout the day can be a way of resuming social contact between individuals.

Female emancipation in a male dominant, sexually dimorphic primate under natural conditions.

In most group-living animals, a dominance hierarchy reduces the costs of competition for limited resources. Dominance ranks may reflect prior attributes, such as body size, related to fighting ability or reflect the history of self-reinforcing effects of winning and losing a conflict (the winner-loser effect), or both. As to prior attributes, in sexually dimorphic species, where males are larger than females, males are assumed to be dominant over females. As to the winner-loser effect, the computational model DomWorld has shown that despite the female's lower initial fighting ability, females achieve some degree of dominance of females over males. In the model, this degree of female dominance increases with the proportion of males in a group. This increase was supposed to emerge from the higher fraction of fights of males among themselves. These correlations were confirmed in despotic macaques, vervet monkeys, and in humans. Here, we first investigate this hypothesis in DomWorld and next in long-term data of 9,300 observation hours on six wild groups of robust capuchin monkeys (Sapajus libidinosus; S. nigritus, and S. xanthosternos) in three Brazilian sites. We test whether both the proportion of males and degree of female dominance over males are indeed associated with a higher relative frequency of aggression among males and a higher relative frequency of aggression of females to males. We confirm these correlations in DomWorld. Next, we confirm in empirical data of capuchin monkeys that with the proportion of males in the group there is indeed an increase in female dominance over males, and in the relative frequency of both male-male aggression and aggression of females to males and that the female dominance index is significantly positively associated with male male aggression. Our results reveal that adult sex ratio influences the power relation between the sexes beyond predictions from socioecological models.

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.

Revisiting the fourth dimension of tool use: how objects become tools for capuchin monkeys.

Culture allows humans to adapt to a diversity of contexts. Participatory experience in technical activities and activity with artefacts provide the basis for learning traditional technical skills. Some populations of non-human animals use tools. The ways in which artefacts influence the development of a traditional skill in non-human species can provide insight into essential supports for technical traditions in humans and shared learning processes across species. In wild bearded capuchins, nut cracking leaves edible pieces of nuts, nut shells and stones used as hammers at anvil sites. We addressed how mastery of cracking nuts by young monkeys is associated with interactions with these objects. We studied monkeys' reuse of nuts, hammers and anvils and the outcome of attempts to crack nuts, and from these data derived their behavioural variability and proficiency in nut cracking. Behavioural variability was the most robust predictor of whether a monkey collects pieces of nuts cracked by others or reuses stones and nuts, and was a stronger predictor of proficiency than age. Young monkeys were increasingly likely to reuse the stone used by another after the other monkey had left the anvil as they increasingly focused their behaviour on actions relevant to cracking nuts.

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.

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.

Ingestive behaviors in bearded capuchins (Sapajus libidinosus).

The biomechanical and adaptive significance of variation in craniodental and mandibular morphology in fossil hominins is not always clear, at least in part because of a poor understanding of how different feeding behaviors impact feeding system design (form-function relationships). While laboratory studies suggest that ingestive behaviors produce variable loading, stress, and strain regimes in the cranium and mandible, understanding the relative importance of these behaviors for feeding system design requires data on their use in wild populations. Here we assess the frequencies and durations of manual, ingestive, and masticatory behaviors from more than 1400 observations of feeding behaviors video-recorded in a wild population of bearded capuchins (Sapajus libidinosus) at Fazenda Boa Vista in Piauí, Brazil. Our results suggest that ingestive behaviors in wild Sapajus libidinosus were used for a range of food material properties and typically performed using the anterior dentition. Coupled with previous laboratory work indicating that ingestive behaviors are associated with higher mandibular strain magnitudes than mastication, these results suggest that ingestive behaviors may play an important role in craniodental and mandibular design in capuchins and may be reflected in robust adaptations in fossil hominins.

Isotopic and elemental corroborates for wild bearded capuchin (Sapajus libidinosus) omnivorous dietary adaptation at Fazenda Boa Vista, Brazil.

RATIONALE: This study analyzes variability in the diets of wild bearded capuchin monkeys, Sapajus libidinosus, by analyzing stable carbon (δ13 C) and nitrogen (δ15 N) isotope ratios and elemental concentrations (%C and %N) of fecal samples and food items. Developing isotopic and elemental correlates for diets of habituated subjects is a necessary step towards applying similar methods to interpret diets of unhabituated or cryptic subjects. METHODS: Fecal samples from wild capuchins and their foods were collected at Fazenda Boa Vista, Brazil. Fecal samples from laboratory-housed Sapajus spp. and their foods were analyzed to establish diet-feces offsets for δ13 C, δ15 N, %C, and %N. Samples were dried, powdered, and measured for isotopic and elemental values. A Bayesian mixing model commutes isotopic and elemental data from wild capuchins into likely proportions of different food categories. RESULTS: The captive study shows small diet-feces spaces for Sapajus spp. of -0.8 ± 0.7‰ for δ13 C, -0.2 ± 0.4‰ for δ15 N, -6.1 ± 1.7% for %C, and -1.0 ± 0.6% for %N. The wild study shows omnivorous diets based on C3 , C4 , and CAM plants, and fauna. Subject diets are highly varied within and between days. Fecal data show age-related differences in diet and crop-raiding. There is no consistent isotopic or elemental difference between mothers and infants. CONCLUSIONS: Fecal stable isotope and elemental evidence employed in a Bayesian mixing model reflects the highly varied diets of capuchin monkeys in an isotopically heterogeneous environment. The isotopic and elemental variability reported here will aid similar diet reconstructions among unhabituated subjects in the future, but precludes tracking weaning isotopically among capuchins in this environment.

Adult and juvenile bearded capuchin monkeys handle stone hammers differently during nut-cracking.

Wild bearded capuchin monkeys (Sapajus libidinosus) habitually use stone hammers to crack open palm nuts and seeds on anvils. This activity requires strength, balance, and precise movement of a large stone with respect to the item placed on an anvil. We explored how well young monkeys cope with these challenges by examining their behavior and the behavior of adults while they cracked palm nuts using a stone. Using video records, we compared actions of six juvenile (2-5 years) and six adult (7+ years) wild monkeys during their first 20 strikes with one unfamiliar ellipsoid, quartzite stone (540 g), and the outcomes of these strikes. Compared with adults, juveniles cracked fewer nuts, performed a more diverse set of exploratory actions, and less frequently placed one or both hands on top of the stone on the downward motion. Adults and juveniles displayed similar low frequencies of striking with a slanted trajectory, missing the nut, and losing control over the nut or stone after striking. These findings indicate that young monkeys control the trajectory of a stone adequately but that is not sufficient to crack nuts as effectively as adults do. Compared with juveniles, adults more quickly perceive how to grip the stone efficiently, and they are able to adjust their grip dynamically during the strike. Young monkeys develop expertise in the latter aspects of cracking nuts over the course of several years of regular practice, indicating that perceptual learning about these aspects of percussion occurs slowly. Juvenile and adult humans learning to use stones to crack nuts also master these features of cracking nuts very slowly.

Assessing the personality structure of wild capuchin monkeys (Sapajus xanthosternos) using trait rating and behavioral coding.

The study of personality in nonhuman primates has increased substantially, but most studies so far have been conducted with captive animals. In addition, few studies investigated the personality of Neotropical (Platyrrhini) monkeys. If we aim at investigating the ecological and social significance of personality in nonhuman primates, conducting studies of wild populations and covering a wide range of taxa is essential. In this study, we analyzed the personality structure of a wild group of Neotropical monkeys, the yellow-breasted capuchin (Sapajus xanthosternos). We adopted two widespread methods: trait rating, using the Hominoid Personality Questionnaire, and behavioral coding, analyzing 13 behaviors and 3 derived variables. We described 3 traits with trait rating, labeled Openness-Neuroticism, Assertiveness, and Attentiveness-Sociability. We also described 3 traits with behavioral coding, labeled Prosociality, Aggressiveness, and Reactivity to Humans. Comparing both methods we found not only broad convergences between the structures obtained (e.g., both showed prosocial and aggressive traits) but also some differences (e.g., Openness-Neuroticism was not clearly defined with behavioral coding), concluding that combining both methods provided complementary findings. Some socioecological variables seem to influence the expression of personality in captive versus wild living monkeys. For example, in our study, assertive individuals were more vigilant, whereas in the studies in captivity, neurotic individuals were more vigilant. These questions highlight the need for more research in wild conditions and enlarging the number of species and populations studied. (PsycInfo Database Record (c) 2020 APA, all rights reserved).