A new approach to geostatistical synthesis of historical records reveals capuchin spatial responses to climate and demographic change.

Recent proliferation of GPS technology has transformed animal movement research. Yet, time-series data from this recent technology rarely span beyond a decade, constraining longitudinal research. Long-term field sites hold valuable historic animal location records, including hand-drawn maps and semantic descriptions. Here, we introduce a generalised workflow for converting such records into reliable location data to estimate home ranges, using 30 years of sleep-site data from 11 white-faced capuchin (Cebus imitator) groups in Costa Rica. Our findings illustrate that historic sleep locations can reliably recover home range size and geometry. We showcase the opportunity our approach presents to resolve open questions that can only be addressed with very long-term data, examining how home ranges are affected by climate cycles and demographic change. We urge researchers to translate historical records into usable movement data before this knowledge is lost; it is essential to understanding how animals are responding to our changing world.

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.

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.

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.

Sagittal suture strain in capuchin monkeys (Sapajus and Cebus) during feeding.

OBJECTIVES: Morphological variation in cranial sutures is used to infer aspects of primate feeding behavior, including diet, but strain regimes across sutures are not well documented. Our aim is to test hypotheses about sagittal suture morphology, strain regime, feeding behavior, and muscle activity relationships in robust Sapajus and gracile Cebus capuchin primates. MATERIALS AND METHODS: Morphometrics of sinuosity in three regions of the sagittal suture were compared among museum specimens of Sapajus and Cebus, as well as in robust and gracile lab specimens. In vivo strains and bilateral electromyographic (EMG) activity were recorded from these regions in the temporalis muscles of capuchin primates while they fed on mechanically-varying foods. RESULTS: Sapajus and the anterior suture region exhibited greater sinuosity than Cebus and posterior regions. In vivo data reveal minor differences in strain regime between robust and gracile phenotypes but show higher strain magnitudes in the middle suture region and higher tensile strains anteriorly. After gage location, feeding behavior has the most consistent and strongest impact on strain regime in the sagittal suture. Strain in the anterior suture has a high tension to compression ratio compared to the posterior region, especially during forceful biting in the robust Sapajus-like individual. DISCUSSION: Sagittal suture complexity in robust capuchins likely reflects feeding behaviors associated with mechanically challenging foods. Sutural strain regimes in other anthropoid primates may also be affected by activity in feeding muscles.

Experimental evidence of parasite-induced behavioural alterations modulated by food availability in wild capuchin monkeys.

In disease dynamics, host behaviour can both determine the quantity of parasites a host is exposed to, and be a consequence of infection. Observational and experimental studies in non-human primates have consistently found that parasitic infections result in less movement and reduced foraging, which was interpreted as an adaptive response of the host to counter infection. Variation in host nutritional condition may add complexity to the infection-behaviour relationship, and its influence may shed light on its significance. To experimentally evaluate how host activity and social relationships are affected by the interaction of parasitism and nutrition, during two years we manipulated food availability by provisioning bananas, and helminth infections by applying antiparasitic drugs, in two groups of wild black capuchin monkeys (Sapajus nigritus) in Iguazú National Park, Argentina. We collected faecal samples to determine the intensity of helminthic infections, as well as data on behaviour and social proximity. Individuals with unmanipulated helminth burdens foraged less than dewormed individuals only when food provisioning was low. Resting time was increased when capuchins were highly provisioned, but it did not vary according to the antiparasitic treatment. Proximity associations to other group members were not affected by the antiparasitic treatment. This is the first experimental evidence of a modulating effect of food availability on the influence of helminth infection on activity in wild primates. The findings are more consistent with an impact on host behaviour due to the debilitating effect caused by parasites than with an adaptive response to help fight infections.

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.

Wild robust capuchin monkey interactions with sympatric primates.

Examining interactions among sympatric primate species can provide interesting information about competition, cooperation, and avoidance between those species. Those interactions can be neutral, positive, or negative for the species involved. Capuchin monkeys are medium-sized primates that can encounter both larger and smaller primates in their varied habitats. Gracile capuchins (Cebus) are reported to present different types of interactions with other primates. Interactions with howler monkeys frequently include physical aggression, while interactions with spider monkeys are mostly threats and chases. Moreover, interaction types are not consistent across populations. Among robust capuchins (Sapajus spp.), however, no reports have been published. Here we describe and classify encounters of Sapajus libidinosus and S. nigritus with Alouatta caraya, A. guariba, Brachyteles arachnoides, and Callithrix jacchus in three sites in the environments of Cerrado, Caatinga (savannah-like), and Atlantic forest, and compare the interaction patterns among sites and different group sizes. The latter is a factor that can influence the outcome, and we expected capuchins in larger groups to be more aggressive toward other primates. Our results of 8421 h of total contact with the capuchin groups show that, indeed, capuchins in sites with larger groups presented aggressive interactions with higher frequency. However, the other species' body size also seems important as smaller primates apparently avoided capuchins, and interactions with the larger muriquis were mostly neutral for the capuchin. Capuchins showed neutral or aggressive behaviors toward howler monkeys, with differences between the rainforest and savannah groups. We found that robust capuchins can present aggressive interactions even to primates larger than themselves and that aggressive behavior was the most common response in populations living in larger groups and drier environments.

Social monkeys learn more slowly: Social network centrality and age are positively related to learning errors by capuchin monkeys (Cebus [Sapajus] apella).

The cognitive demand on animals to learn, maintain, and remember the complexities of social relationships is theoretically higher for individuals who live more complex social lives. Previous research has suggested that both across and within species, the cognitive ability to flexibly learn and manipulate information may increase with increased social complexity. In this study, we determined the relationship between social complexity and cognitive performance on 2 related tests of general learning: associative learning and reversal learning. Subjects were 16 members of a socially housed group of brown capuchin monkeys (Cebus [Sapajus] apella). A general learning score was extracted from a principal component analysis on learning rate across 5 repetitions of each of the 2 tasks. The complexity of each monkey's social life was characterised by their centrality in the grooming social network of the group. Generalised learning scores were predicted by age and network centrality, but in contrast to predictions, older monkeys and monkeys that were more central to the network made more errors. Future studies focusing on specific cognitive abilities that are theoretically linked to species-specific fitness and behavioural outcomes, rather than broad cognitive categories like learning, will be essential for clarifying the relationship between cognition and social complexity. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Wild Blonde Capuchins (Sapajus flavius) Perform Anointing Behaviour Using Toxic Secretions of a Millipede (Spirobolida: Rhinocricidae).

Defensive secretions of millipedes are remarkable for containing toxic quinones known to efficiently repell hematophagous arthropods. Here we show that Endangered blonde capuchin monkeys make use of such secretions. We (i) describe the anointing behavior performed by the monkeys (ii) identify the millipede species used in the process (iii) describe the volatile chemical composition of its secretion. The blonde capuchin monkeys selectively searched for millipedes hidden under the ground. We observed three bouts of anointing behavior, performed by 13 individuals of all age classes (from adults to independent infants), both solitarily (1 event) and socially (10 events). The only millipede species used by the monkeys is an undescribed species of the genus Poecilocricus (Spirobolida, Rhinocricidae). The volatile chemical composition of the secretions was predominantly comprised of a mixture of benzoquinones and hydroquinones. The social nature of the behavior and time of the observations (mosquito season), suggest that social bonding and mosquito avoidance is linked to the anointing behavior of the monkeys.

Increased terrestriality in a Neotropical primate living on islands with reduced predation risk.

An arboreal lifestyle is thought to be central to primate origins, and most extant primate species still live in the trees. Nonetheless, terrestrial locomotion is a widespread adaptation that has arisen repeatedly within the primate lineage. The absence of terrestriality among the New World monkeys (Platyrrhini) is thus notable and raises questions about the ecological pressures that constrain the expansion of platyrrhines into terrestrial niches. Here, we report the results of a natural experiment, comparing patterns of terrestrial behavior in white-faced capuchin monkeys (Cebus capucinus imitator) living on two islands off the Pacific coast of Panama that lack mammalian predators (island sites) with the behavior of capuchins at three sites in central Panama with more intact predator communities (mainland sites). Surveys with camera traps revealed increased terrestriality in island vs. mainland sites. Capuchin detection rates were higher, the range of party sizes observed was larger, and individuals engaged in a wider range of terrestrial behaviors on the islands lacking mammalian predators. Furthermore, females carrying infants were frequently photographed on the ground at the island sites, but never at the mainland sites. These findings support the long-standing hypothesis that predators constrain the exploitation of terrestrial niches by primates. These results are also consistent with the hypothesis that arboreal locomotion imposes costs that primates will avoid by walking on the ground when predation risk is low.

Differential responses of non-human primates to seasonal temperature fluctuations.

Non-human primates (NHPs) can adapt to conditions outside of their natural habitat and climatic ranges but this can be influenced by inherent evolutionary traits or plasticity of species that evolved in diverse environmental conditions. In this study, we investigated how five species of NHPs that have natural distributions across a range of climatic conditions responded to seasonal temperature changes in a captive environment. The activity levels of NHPs were affected by temperature changes over the season, where activity levels were generally reduced at the lower and higher temperature ranges. Species that are naturally found within narrower and warmer climatic ranges, compared to those found in colder environments with wider fluctuations in temperature, showed more marked changes in activity levels in response to temperature changes. In lower temperature conditions, three out of five species showed significantly lower activity levels; whereas in higher temperature conditions, the activity levels of all species did not significantly decrease. The frequency of thermoregulation behaviours was higher, and use of artificial thermoregulatory sources lower, for species that did not substantially adjust their activity levels in different temperature conditions. Our results suggest that NHPs largely retained the evolutionary traits related to thermoregulation, according to the different ambient conditions they evolved in and may have low behavioural plasticity in adapting to conditions outside of their natural ranges. These results provide insights for improving conservation and captive management and may have implications for understanding NHP resilience to the increasing impact of global climate change.

Touch improves visual discrimination of object features in capuchin monkeys (Sapajus spp.).

Primates perceive many object features through vision and touch. To date, little is known on how the synergy of these two sensory modalities contributes to enhance object recognition. Here, we investigated in capuchin monkeys (N = 12) whether manipulating objects and retaining tactile information enhanced visual recognition of geometrical object properties on different scales. Capuchins were trained to visually select the rewarded one of two objects differing in size, shape (larger-scale) or surface structure (smaller-scale). Objects were explored in two experimental conditions: the Sight condition prevented capuchins from touching the chosen object; the Sight and Touch condition allowed them to touch the selected object. Our results indicated that tactile information increased the capuchins' learning speed for visual discrimination of object features. Moreover, the capuchins' learning speed was higher in both size and shape discrimination compared to surface discrimination regardless of the availability of tactile input. Overall, our data demonstrated that the acquisition of tactile information about object features was advantageous for the capuchins and allowed them to achieve high levels of visual accuracy faster. This suggests that information from touch potentiated object recognition in the visual modality.

Non-invasive estimation of the costs of feeding competition in a neotropical primate.

A key goal in behavioral ecology is to investigate the factors influencing the access to food resources and energetic condition of females, which are strong predictors of their reproductive success. We aimed to investigate how ecological factors, social factors, and reproductive state are associated with energetic condition in a wild neotropical primate using non-invasive measures. We first assessed and compared urinary C-peptide levels (uCP), the presence of urinary ketones (uKet), and behaviorally assessed energy balance (bEB) in female white-faced capuchin monkeys (Cebus imitator) living in Santa Rosa, Costa Rica. Then, we assessed how these measures were associated with feeding competition, dominance rank, and reproductive state. As predicted, uCP and bEB were positively associated with each other, and bEB was negatively associated with uKet. However, we did not find a relationship between uCP and uKet. Females showed lower uCP and bEB values during periods of intense feeding competition, but this relationship was not dependent on dominance rank. Furthermore, rank was not directly associated with uCP and bEB. Urinary ketones, on the other hand, were only produced in the most adverse conditions: by low-ranking, lactating females during periods of intense feeding competition. Behavioral strategies are assumed to maximize reproductive success and not energetic condition per se, which might explain why rank was not generally associated with energetic condition in our study population. This highlights the importance of considering potential differences between reproductive success and proxies of reproductive success, such as energetic condition or food intake, when investigating predictions of socioecological models.

An anthropological analysis about primatology - Reports of a particular human-animal relationship with Capuchin monkeys.

This ethnography is about a particular human-animal relationship based on primatological research on groups of wild robust capuchin monkeys living in Parque Estadual Carlos Botelho (Brazil), one of the largest preserved areas of Atlantic Tropical Forest in the world. It emphasizes the complex situations that highlight the difficulty of making this research. This space integrates administrative, scientific and local interests, producing a unique cartography. We reflect on the scientific research considering the relations among primatologist, field assistant and other animals and comparing it with the hunt. "Hunt" is a model inspired in techniques and in some aspects of recreational hunt to expand the comprehension of a complex routine defined to obtain behavior data.

A competitive drive? Same-sex attentional preferences in capuchins.

In primates, faces provide information about several characteristics of social significance, including age, physical health, and biological sex. However, despite a growing literature on face processing and visual attention in a number of primate species, preferences for same- or opposite-sex faces have not yet been examined. In the current study, we explore the role of conspecific sex on visual attention in two groups of capuchin monkeys. Subjects were shown a series of image pairs on a Tobii Pro TX300 eye tracker, each depicting an unfamiliar male and an unfamiliar female face. Given the behavioral evidence of mate choice in both sexes, we hypothesized that capuchins would preferentially attend to images of unfamiliar conspecifics of the opposite sex. Our alternative hypothesis was that capuchins would preferentially attend to same-sex individuals to assess potential competitors. Our results provide support for our alternative hypothesis. When comparing attention to each stimuli type across sexes, females spent significantly larger percentages of time than males looking at female photos, whereas males spent significantly larger percentages of time than females looking at male photos. Within each sex, females looked for significantly larger percentages of time to female versus male images. Males also looked for larger percentages of time to same-sex images, though not significantly. To our knowledge, these data are the first to demonstrate significant sex-biased attentional preferences in adult primates of any species, and suggest that, for capuchins, potential competitors garner more attention than potential mates. In addition, our findings have implications for studies of visual attention and face processing across the primate order, and suggest that researchers need to control for these demographic factors in their experimental designs.

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.

Competition during sugarcane crop raiding by blond capuchin monkeys (Sapajus flavius).

Shifting to fallback food (FBF) consumption and crop raiding are behavioral adjustments that support primates' ability to endure in human-altered habitats. Nutritional models predict that the consumption of preferred foods leads to increased competition, while consumption of staple fallback foods results in decreased competition. We analyzed the competitive regime faced by individuals in a group of 133 blond capuchin monkeys (Sapajus flavius), an endangered species that inhabits a 270-ha fragment of Atlantic forest in northeast Brazil. During the study year, quantitative analyses show that fruits were a preferred food, while sugarcane was used as a staple FBF. As predicted by primate fallback foraging models, the consumption of sugarcane helped the group to survive in this fragment by providing these animals with half of the food they consumed throughout the year. Contrary to predictions, group dispersion increased with greater fruit abundance, while direct competition peaked during the consumption of sugarcane. We suggest that, although it is abundant and scattered in the area, the long handling time required to process sugarcane before consumption facilitates the direct competition. Overall, the pattern found indicates that consumption of a staple FBF does not directly translate into decreased competition and increased stability of social groups in forest fragments.

Hand preferences and differences in extractive foraging in seven capuchin monkey species.

Tool use and extractive foraging could be drivers for right hand use preference. The robust capuchins, Sapajus, are more specialized for destructive and extractive foraging than the gracile capuchins, Cebus. Thus, we predicted them to show right-hand preference and higher rates of extractive foraging when compared to the gracile capuchins. We hypothesized that capuchins that evolved in dry habitats are predisposed to show higher rates of extractive foraging and right-hand preference. We employed the tube task (152 individuals) and an extractive foraging task (212 individuals) in seven species of capuchins in captive settings. Data on hand preference and extractive foraging were collected using focal and scan sampling, respectively. Contrary to our hypothesis, S. libidinosus showed significant left hand preference, while S. robustus and S. flavius showed a right hand preference. The species S. xanthosternos, S. flavius, and S. robustus engaged in extractive foraging significantly more often than S. apella, S. libidinosus, and Cebus albifrons. As expected, the gracile capuchins showed significant higher left-hand bias when compared to the robust capuchins. The findings from this study is the first indication of left-hand population level laterality in S. libidinosus, a species that evolved in an environment selecting for increased tool use. Although tool use has been associated with population level right handedness, or a strong trend to use the right hand, our results suggest the link between tool use and right-hand preference is simplistic, at least in Sapajus. The ultimate explanation for the differences in hand preference across species might be due to differences in use of key food resources. We suggest that capuchin monkeys from the Atlantic forest evolved under a stronger selective pressure for high reliance on bimanual feeding and extractive foraging, which requires more sequential actions and planning, than those species from the Amazonia forest and Caatinga/Cerrado dry forest.