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.

Sex differences in white matter tracts of capuchin monkey brains.

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

A New Assessment of Robust Capuchin Monkey (Sapajus) Evolutionary History Using Genome-Wide SNP Marker Data and a Bayesian Approach to Species Delimitation.

Robust capuchin monkeys, Sapajus genus, are among the most phenotypically diverse and widespread groups of primates in South America, with one of the most confusing and often shifting taxonomies. We used a ddRADseq approach to generate genome-wide SNP markers for 171 individuals from all putative extant species of Sapajus to access their evolutionary history. Using maximum likelihood, multispecies coalescent phylogenetic inference, and a Bayes Factor method to test for alternative hypotheses of species delimitation, we inferred the phylogenetic history of the Sapajus radiation, evaluating the number of discrete species supported. Our results support the recognition of three species from the Atlantic Forest south of the São Francisco River, with these species being the first splits in the robust capuchin radiation. Our results were congruent in recovering the Pantanal and Amazonian Sapajus as structured into three monophyletic clades, though new morphological assessments are necessary, as the Amazonian clades do not agree with previous morphology-based taxonomic distributions. Phylogenetic reconstructions for Sapajus occurring in the Cerrado, Caatinga, and northeastern Atlantic Forest were less congruent with morphology-based phylogenetic reconstructions, as the bearded capuchin was recovered as a paraphyletic clade, with samples from the Caatinga biome being either a monophyletic clade or nested with the blond capuchin monkey.

Time budget and foraging strategies of two provisioned groups of tufted capuchin monkeys, Sapajus libidinosus, in a small, seasonal urban forest fragment.

Studies of urban monkeys provide important insights into the behavioral flexibility of primate species. We studied two provisioned groups of capuchin monkeys that inhabit a small forest fragment in the city of Goiânia, Brazil. One of the groups was dominant and had priority of access to both native and provisioned resources. Anthropic resources were available in two relatively small areas within this forest, but varied in their quality. We hypothesized that intergroup dominance and the seasonality of native resources would have different impacts on the foraging strategies and use of space by the two study groups. Data on the location of the members of the two groups, their behavior, and consumption of different food items were collected during five dry season and five rainy season months. The members of the dominant group spent more time in the provisioned area where anthropic food was less costly to obtain and consumed more provisioned fruit and vegetables than the members of the subordinate group. The differences between groups were exacerbated during the dry season, when sources of native fruit were less abundant. The results of the present study illustrate how capuchins may respond to the variation in proximate factors, such as intergroup dominance and seasonality. These factors were determinants to the variation in the diet and the use of space observed between the two study groups.

Is economic risk proneness in young children (Homo sapiens) driven by exploratory behavior? A comparison with capuchin monkeys (Sapajus apella).

Economic risk proneness is displayed by human children and some nonhuman primate species. To explore the role of attraction toward the unknown and the unexpected in economic choices, 2.5-year-old children and capuchin monkeys were presented in Experiment 1 with a gambling task in which participants had to choose between 2 options, a secure option and a risky option characterized by an unexpected event. In contrast to capuchins, toddlers showed a strong preference for the risky option over the safe option. In Experiment 2, toddlers maintained their risky choices despite the increased salience of the safe option. In contrast to toddlers, capuchins preferentially chose the safe option in this second experiment. We argue that capuchins' risk aversion reflects an exploitation strategy of known and safe options. In human children, the attractiveness of uncertain reward appears to be linked to their novelty seeking. We argue that toddlers' risk proneness in the gain domain reflects an exploratory search strategy. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Dominance and social interaction patterns in brown capuchin monkey (Cebus [Sapajus] apella) social networks.

Strong, stable social bonds in primates are characterized by high levels of social affiliation, low levels of aggression, minimal stress, and affiliative reciprocity within the dyad. In relatively well-studied catarrhine monkeys, these bonds tend to form most frequently between kin, animals close in age, and animals close in rank. This results in patterns of affiliation in which kin, similarly aged animals, and like-ranked animals tend to affiliate and patterns of aggression and submission where animals tend to aggress more toward nonkin and closely ranked animals, and submit more toward distantly ranked animals. However, literature on how affiliative and agonistic relationships are organized in platyrrhine primate species like brown capuchin monkeys is limited and conflicting. In this study, we used social network analyses to characterize how age, sex, maternal kinship, and dominance rank relate to the patterns of submissive, aggressive, contact, and grooming interactions in a group of captive brown capuchin monkeys. Like catarrhine monkeys, brown capuchin monkeys showed a steep linear dominance hierarchy, tended to affiliate with kin, similarly aged animals, and like-ranked animals, and tended to aggress more toward nonkin. However, our monkeys showed a pattern of affiliation and grooming down the hierarchy that is inconsistent with grooming up the hierarchy patterns often seen in catarrhine monkey groups, suggesting that brown capuchins do not compete for access to higher ranking social partners. Higher ranking monkeys were most central to the aggression network, and lower ranking monkeys were most central to the submission network. Mid-ranking monkeys were the most central to the contact network, suggesting that they may play an important role in the affiliative cohesion of the group. These results inform our understanding of brown capuchin social behavior specifically, and of how demographic factors relate to social organization in platyrrhine primates generally.

Are demographic correlates of white-faced capuchin monkey (Cebus capucinus) "Gargle and Twargle" vocalization rates consistent with the infanticide risk assessment hypothesis?

Zahavi's "Bond Testing Hypothesis" states that irritating stimuli are used to elicit honest information from social partners regarding their attitudes towards the relationship. Two elements of the Cebus capucinus vocal repertoire, the "gargle" and "twargle," have been hypothesized to serve such a bond-testing function. The greatest threat to C. capucinus infant survival, and to adult female reproductive success, is infanticide perpetrated by alpha males. Thus, we predicted that infants (<8 months), pregnant females and females with infants would gargle/twargle at higher rates than the rest of the population, directing these vocalizations primarily to the alpha male. Over 16 years, researchers collected data via focal follows in 11 habituated groups of wild capuchins in Lomas Barbudal, Costa Rica. We found some support for our hypothesis. Infants and females with infants (<8 months) vocalized at higher rates than the rest of the population. Pregnant females did not vocalize at relatively high rates. Infants (age 8-23 months) were the only target group that vocalized more when the alpha male was not their father. Monkeys gargled and twargled most frequently towards the alpha male, who is both the perpetrator of infanticide and the most effective protector against potentially infanticidal males.

Costs of male infanticide for female capuchins: When does an adaptive male reproductive strategy become costly for females and detrimental to population viability?

OBJECTIVES: Infanticide in white-faced capuchins (Cebus capucinus imitator) typically occurs in association with alpha male replacements (AMRs). Although infanticide is likely adaptive for males, it imposes costs on females that are difficult to quantify without long-term demographic data. Here we investigate effects of AMRs and infanticide on female reproductive success and how these costs affect capuchin groups. We investigate (1) effects of AMR frequency on the production of surviving infants; (2) energetic and (3) temporal "opportunity costs" of infant loss; and (4) how AMR frequency impacts capuchin group sizes. MATERIALS AND METHODS: We censused six groups (7-33 years/group, 74 adult females). We modeled surviving infant production in relation to AMR. We estimated a female's energy requirements for lost infants and the temporal cost relative to the median reproductive window. We simulated how varying AMR rates would affect future capuchin group sizes. RESULTS: Females exposed to more frequent AMR tended to produce fewer surviving offspring. We estimate the average lost infant requires approximately 33% additional energy intake for its mother and represents 10% of the average reproductive opportunity window available to females. Simulated populations remain viable at the observed rate of AMR occurrence but decrease in size at even slightly higher rates. DISCUSSION: While infanticide is adaptive for males, for females it affects lifetime reproductive success and imposes energetic and opportunity costs. Although capuchin populations have evolved with AMRs and infanticide, small increases in AMR frequency may lead to population decline/extinction. Infanticide likely plays a large role in population maintenance for capuchins.

Assessment of genetic variability in captive capuchin monkeys (Primates: Cebidae).

Capuchin monkeys (genera Cebus and Sapajus) show a wide range distribution, from Honduras to Argentina. The aim of this work was to evaluate the genetic and phenotypic variability of captive specimens putatively belonging to S. cay (SCY) and S. nigritus (SNI) at their southernmost distribution limit. Forty-four individuals held in five captive centers from Argentina were analyzed based on external morphology, karyology and DNA sequences of mitochondrial control region (mtDNA-CR). Three morphotypes associated with their probable geographical origin in SCY and a single morphotype in SNI were found. For SCY we could associate each morphotype with the most frequent karyotype. SNI showed a single phenotype and a homogenous karyotype. Heterochromatin showed geographical patterns within species. A 515-bp mtDNA-CR fragment was sequenced, defining fourteen haplotypes at 59 polymorphic sites. A network constructed with our 14 haplotypes and other 77 from S. apella, S. macrocephalus, S. cay and S. nigritus from bibliography revealed some phylogeographic signals. Our SCY and SNI samples rendered four groups that differed in multiple mutational steps, with SCY being more similar to S. apella than to S. macrocephalus. Also, we identified two genetic divergent SCY groups: samples from NOA and from NEA with high mitochondrial diversity. Our results highlight the relevance of using complementary genetic tools throughout the distribution ranges of SCY and SNI for a better assessment of their diversity.

Studying animal innovation at the individual level: A ratings-based assessment in capuchin monkeys (Sapajus [Cebus] sp.).

Large-scale studies of individual differences in innovative behavior among nonhuman animals are rare because of logistical difficulties associated with obtaining observational data on a large number of innovative individuals across multiple locations. Here, we take a different approach, using observer ratings to study individual differences in innovative behavior in 127 brown capuchin monkeys (Sapajus [Cebus] sp.) from 15 social groups and 7 facilities. Capuchins were reliably rated by 1 to 7 raters (mean 3.2 ± 1.6 raters/monkey) on a 7-point Likert scale for levels of innovative behavior, task motivation, sociality, and dominance. In a subsample, we demonstrate these ratings are valid: Rated innovation predicted performance on a learning task, rated motivation predicted participation in the task, rated dominance predicted social rank based on win/loss aggressive outcomes, and rated sociality predicted the time that monkeys spent in proximity to others. Across all 127 capuchins, individuals that were rated as being more innovative were significantly younger, more social, and more motivated to engage in tasks. Age, sociality, and task motivation all had independent effects on innovativeness, whereas sex, dominance, and group size were nonsignificant. Our findings are consistent with long-term behavioral observations of innovation in wild white-faced capuchins. Observer ratings may, therefore, be a valid tool for studies of animal innovation. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Capuchin and rhesus monkeys show sunk cost effects in a psychomotor task.

Human decision-making is often swayed by irrecoverable investments even though it should only be based on future-and not past-costs and benefits. Although this sunk cost effect is widely documented and can lead to devastating losses, the underlying psychological mechanisms are unclear. To tease apart possible explanations through a comparative approach, we assessed capuchin and rhesus monkeys' susceptibility to sunk costs in a psychomotor task. Monkeys needed to track a moving target with a joystick-controlled cursor for variable durations. They could stop at any time, ending the trial without reward. To minimize the work required for a reward, monkeys should have always persisted for at least 1 s, but should have abandoned the trial if that did not yield a reward. Capuchin monkeys and especially rhesus macaques persisted to trial completion even when it was suboptimal, and were more likely to complete the trial the longer they had already tracked the target. These effects were less pronounced, although still present, when the change in expected tracking duration was signalled visually. These results show that sunk cost effects can arise in the absence of human-unique factors and may emerge, in part, because persisting can resolve uncertainty.

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.

Social inhibition and behavioural flexibility when the context changes: a comparison across six primate species.

The ability to inhibit previously employed strategies and flexibly adjust behavioural responses to external conditions may be critical for individual survival. However, it is unclear which factors predict their distribution across species. Here, we investigated social inhibition and behavioural flexibility in six primate species (chimpanzees, bonobos, orangutans, gorillas, capuchin monkeys and spider monkeys) differing in terms of phylogenetic relatedness, foraging ecology and social organization. Depending on the social context, individuals could maximize their food intake by inhibiting the selection of a larger food reward in one condition (i.e. inhibition), but not in others, which required them to flexibly switching strategies across conditions (i.e. behavioural flexibility). Overall, our study revealed inter-specific differences in social inhibition and behavioural flexibility, which partially reflected differences in fission-fusion dynamics. In particular, orangutans and chimpanzees showed the highest level of inhibitory skills, while gorillas and capuchin monkeys showed the lowest one. In terms of behavioural flexibility, orangutans and spider monkeys were the best performers, while bonobos and capuchin monkeys were the worst ones. These results contribute to our understanding that inhibition and behavioural flexibility may be linked in more complex ways than usually thought, although both abilities play a crucial role in efficient problem solving.

Total energy expenditure in captive capuchins (Sapajus apella).

Primates have markedly lower total energy expenditure (TEE; kcal/day) than other placental mammals, expending approximately 50% less energy for their mass than non-primate eutherians. However, little is known regarding interspecific variation of energy expenditure within platyrrhine primates. We investigated TEE in captive tufted capuchins (Sapajus apella, n = 8, ages 7-36), a frugivorous platyrrhine, to compare TEE with other placental mammals and primates. We tested the hypothesis that large-brained capuchins would exhibit greater TEE than other platyrrhines that are less encephalized. We used the doubly labeled water (DLW) method to measure TEE over 7-11 days, during which physical activity data were recorded via focal observation. TEE was strongly correlated with fat free mass, but sex, age, and rates of walking and climbing were not correlated with variation in TEE in multivariate analyses controlling for fat free mass. We found evidence that daily physical activity was negatively correlated with body fat percentage. Capuchin TEE was similar (P = 0.67) to other, less encephalized platyrrhines (Callithrix and Alouatta) and 54% lower than other placental mammals, in analyses controlling for body mass. These results suggest that brain size and physical activity do not necessarily influence variation in daily energy expenditure across primate species.

Individual participation in intergroup contests is mediated by numerical assessment strategies in black howler and tufted capuchin monkeys.

Asymmetries in resource-holding potential between opposing groups frequently determine outcomes of intergroup contests. Since both numerical superiority and high intergroup dominance rank may confer competitive advantages, group members should benefit from assessing the relative strength of rivals prior to engaging in defensive displays. However, differences in individual assessment may emerge when cost-benefit trade-offs differ among group members. We examine the influence of numerical superiority and intergroup dominance relationships on individual participation in intergroup encounters in black howler monkeys (Alouatta pigra) and tufted capuchin monkeys (Sapajus nigritus). Black howlers responded with longer vocal displays during encounters with neighbours with an equal number of resident males, while tufted capuchins increased their participation with increasing relative male group size. Within each species, males and females responded similarly to varying numerical odds, suggesting that despite pay-off asymmetries between males and females, both sexes were similarly influenced by numerical asymmetries in deciding to participate in collective group defence. Whereas the outcome of contests among tufted capuchins was determined by relative male group size, reflected in a pronounced intergroup dominance hierarchy, the absence of dominance relationships among black howler groups may have provoked prolonged vocal displays in order to assess rival groups with matching competitive abilities.

Behavioural Repertoires and Time Budgets of Semi-Free-Ranging and Captive Groups of Wedge-Capped Capuchin Monkeys, Cebus olivaceus, in Zoo Exhibits in Venezuela.

The behavioural repertoires and time budgets of 2 captive groups and 1 semi-free-ranging group of Cebus olivaceus were determined with the aim to assess the impact of the zoo environment on behaviour. The repertoires were qualitatively similar between groups and to those reported for wild troops, but the captive groups showed self-directed and stereotyped behaviours not reported in the wild. The differences in repertoires between groups were easily associated with the opportunity to interact directly with the visitors, with particularities of the enclosure and with the severity of confinement. Overall, females spent more time foraging than males in the 2 captive groups, and adults rested and watched more than subadults in all the groups. Time budgets were dominated by foraging, resting, movement and affiliative interactions, but their relative importance varied between groups, with foraging being especially prominent in the most confined group. The time budgets also varied qualitatively from those reported for wild troops. We conclude the species is behaviourally able to adjust to captivity, but the slight differences along the continuum from wild to semi-free to captive are suggestive of mild stress or social tension probably due to unstimulating environmental conditions, high visitor pressure and deviations from typical sex-age group composition.

Do primates see the solitaire illusion differently? A comparative assessment of humans (Homo sapiens), chimpanzees (Pan troglodytes), rhesus monkeys (Macaca mulatta), and capuchin monkeys (Cebus apella).

An important question in comparative psychology is whether human and nonhuman animals share similar principles of perceptual organization. Despite much empirical research, no firm conclusion has been drawn. The Solitaire illusion is a numerosity illusion in humans that occurs when one misperceives the relative number of 2 types of items presented in intermingled sets. To date, no study has investigated whether nonhuman animals perceive the Solitaire illusion as humans do. Here, we compared the perception of the Solitaire illusion in human and nonhuman primates in 3 experiments. We first observed (Experiment 1) the spontaneous behavior of chimpanzees when presented with 2 arrays composed of a different number of preferred and nonpreferred food items. In probe trials, preferred items were presented in the Solitaire pattern in 2 different spatial arrangements (either clustered centrally or distributed on the perimeter). Chimpanzees did not show any misperception of quantity in the Solitaire pattern. Next, humans, chimpanzees, rhesus monkeys, and capuchin monkeys underwent the same testing of relative quantity judgments in a computerized task that also presented the Solitaire illusion (Experiments 2 and 3). Unlike humans, chimpanzees did not appear to perceive the illusion, in agreement with Experiment 1. The performance of rhesus monkeys and capuchin monkeys was also different from that of humans, but was slightly more indicative of a potential Solitaire illusion. On the whole, our results suggest a potential discontinuity in the visual mechanisms underlying the Solitaire illusion between human and nonhuman primates.

Activity budget, diet, and habitat use in the critically endangered Ka'apor capuchin monkey (Cebus kaapori) in Pará State, Brazil: a preliminary comparison to other capuchin monkeys.

The Ka'apor capuchin, Cebus kaapori, is perhaps the most endangered primate of the Brazilian Amazon. Endemic to a region with extreme intensification of habitat-degrading activities, it survives in remnant populations in a completely fragmented landscape. Before now, the only data available were isolated observations of feeding, locality records, and information on population densities and group size obtained during census. Here we present the first data on the activity budget, diet, and daily path length of the species, and compare our preliminary results with those for other capuchin monkeys. A group of nine Ka'apor capuchins was monitored over a period of four months during the dry season in the Goianésia do Pará municipality, Pará, Brazil. We used instantaneous scan sampling (n = 4,647 scans) to construct an activity budget for the monkeys, and we identified the plants in their diet to species level (n = 41 plant taxa), allowing us to compare dietary overlap with other gracile capuchin species, as well as with the robust capuchin (Sapajus spp.), a potential competitor present throughout the range of the Ka'apor capuchin. Like other species of gracile capuchins, C. kaapori was highly frugivorous, with the vast majority of the feeding records of arils and fruit pulp (74%), supplemented by arthropods (13%) and seeds (10%), although diet composition was highly variable across months. The group used a total area of 62.4 ha during the study period, and average daily path length was 2,173 m (±400 m), with the entire home range utilized in every month of the study. We found significant overlap in the diet of the Ka'apor capuchin and Sapajus, highlighting the urgency to increase knowledge of the ecological needs of C. kaapori and understand synergistic effects of sympatry with competitive species, increasing forest fragmentation, and widespread human impact on C. kaapori sustainability.

The cost of defeat: Capuchin groups travel further, faster and later after losing conflicts with neighbors.

Although competition between social groups is central to hypotheses about the evolution of human social organization, competitive interactions among group-mates are thought to play a more dominant role in shaping the behavior and ecology of other primate species. However, few studies have directly tested the impact of intergroup conflicts in non-human primates. What is the cost of defeat? To address this question, the movements of six neighboring white-faced capuchin (Cebus capucinus) social groups living on Barro Colorado Island, Panama were tracked simultaneously using an Automated Radio Telemetry System (ARTS), for a period of six months. Groups moved 13% (441 m) further on days they lost interactions compared with days they won interactions. To cover these larger distances, they traveled faster, stopped less frequently, and remained active later in the evening. Defeat also caused groups to alter their patterns of space use. Losing groups had straighter travel paths than winning groups, larger net displacements and were more likely to change their sleeping site. These results demonstrate that losing groups pay increased travel costs and suggest that they forage in low-quality areas. They provide some of the first direct evidence that intergroup conflicts have important energetic consequences for members of competitively unsuccessful primate social groups. A better understanding of how intergroup competition impacts patterns of individual fitness is thus needed to clarify the role that this group-level process plays in shaping the evolution of human- and non-human primate behavior.