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Understanding diet selectivity is a longstanding goal in primate ecology. Deciphering when and why primates consume different resources can provide insights into their nutritional ecology as well as adaptations to food scarcity. Plant pith, the spongy interior of plant stems, is occasionally eaten by primates, but the context is poorly understood. We examine the ecological, mechanical, chemical, and nutritional basis of plant pith selection by a wild, frugivorous-omnivorous primate (Cebus imitator). We test the hypothesis that pith is a fallback food, that is, consumed when fruit is less abundant, and test for differences between plant species from which pith is eaten versus avoided. We collected 3.5 years of capuchin pith consumption data to document dietary species and analyzed "pith patch visits" in relation to fruit availability, visits to fruit patches, and climatic seasonality. We analyzed dietary and non-dietary species for relative pith quantity, mechanical hardness, odor composition, and macronutrient concentrations. Capuchins ate pith from 11 of  ~300 plant species common in the dry forest, most commonly Bursera simaruba. We find that pith consumption is not directly related to fruit availability or fruit foraging but occurs most frequently (84% of patch visits) during the months of seasonal transition. Relative to common non-dietary species, dietary pith species have relatively higher pith quantity, have softer outer branches and pith, and contain more terpenoids, a class of bioactive compounds notable for their widespread medicinal properties. Our results suggest that greater pith quantity, lower hardness, and a more complex, terpenoid-rich odor profile contribute to species selectivity; further, as pith is likely to be consistently available throughout the year, the seasonality of pith foraging may point to zoopharmacognosy, as seasonal transitions typically introduce new parasites or pathogens. Our study furthers our understanding of how climatic seasonality impacts primate behavior and sheds new light on food choice by an omnivorous primate., (© 2023 The Authors. American Journal of Primatology published by Wiley Periodicals LLC.)

Capuchins are platyrrhines (monkeys found in the Americas) within the Cebidae family. For most of their taxonomic history, the two main morphological types of capuchins, gracile (untufted) and robust (tufted), were assigned to a single genus, Cebus . Further, all tufted capuchins were assigned to a single species, Cebus apella , despite broad geographic ranges spanning Central and northern South America. In 2012, tufted capuchins were assigned to their genus, Sapajus , with eight currently recognized species and five Cebus species, although these numbers are still under debate. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. However, Alu elements have rarely been used to study capuchins. Recent genome-level assemblies for capuchins ( Cebus imitator ; [Cebus_imitator_1.0] and Sapajus apella [GSC_monkey_1.0]) facilitated large scale ascertainment of young lineage-specific Alu insertions. Reported here are 1607 capuchin specific and 678 Sapajus specific Alu insertions along with candidate oligonucleotides for locus-specific PCR assays for many elements. PCR analyses identified 104 genus level and 51 species level Alu insertion polymorphisms. The Alu datasets reported in this study provide a valuable resource that will assist in the classification of archival samples lacking phenotypic data and for the study of capuchin phylogenetic relationships.

The major histocompatibility complex (MHC) is an important gene complex contributing to adaptive immunity. Studies of platyrrhine MHC have focused on identifying experimental models of immune system function in the equivalent Human Leukocyte Antigen (HLA). These genes have thus been explored primarily in captive platyrrhine individuals from research colonies. However, investigations of standing MHC variation and evolution in wild populations are essential to understanding its role in immunity, sociality and ecology. Capuchins are a promising model group exhibiting the greatest habitat diversity, widest diet breadth and arguably the most social complexity among platyrrhines, together likely resulting in varied immunological challenges. We use high-throughput sequencing to characterize polymorphism in four Class II DR and DQ exons for the first time in seven capuchin species. We find evidence for at least three copies for DQ genes and at least five for DRB, with possible additional unrecovered diversity. Our data also reveal common genotypes that are inherited across our most widely sampled population, Cebus imitator in Sector Santa Rosa, Costa Rica. Notably, phylogenetic analyses reveal that platyrrhine DQA sequences form a monophyletic group to the exclusion of all Catarrhini sequences examined. This result is inconsistent with the trans-species hypothesis for MHC evolution across infraorders in Primates and provides further evidence for the independent origin of current MHC genetic diversity in Platyrrhini. Identical allele sharing across cebid species, and more rarely genera, however, does underscore the complexity of MHC gene evolution and the need for more comprehensive assessments of allelic diversity and genome structure., Competing Interests: The authors have declared that no competing interests exist.

Ecological flexibility, extended lifespans, and large brains have long intrigued evolutionary biologists, and comparative genomics offers an efficient and effective tool for generating new insights into the evolution of such traits. Studies of capuchin monkeys are particularly well situated to shed light on the selective pressures and genetic underpinnings of local adaptation to diverse habitats, longevity, and brain development. Distributed widely across Central and South America, they are inventive and extractive foragers, known for their sensorimotor intelligence. Capuchins have among the largest relative brain size of any monkey and a lifespan that exceeds 50 y, despite their small (3 to 5 kg) body size. We assemble and annotate a de novo reference genome for Cebus imitator Through high-depth sequencing of DNA derived from blood, various tissues, and feces via fluorescence-activated cell sorting (fecalFACS) to isolate monkey epithelial cells, we compared genomes of capuchin populations from tropical dry forests and lowland rainforests and identified population divergence in genes involved in water balance, kidney function, and metabolism. Through a comparative genomics approach spanning a wide diversity of mammals, we identified genes under positive selection associated with longevity and brain development. Additionally, we provide a technological advancement in the use of noninvasive genomics for studies of free-ranging mammals. Our intra- and interspecific comparative study of capuchin genomics provides insights into processes underlying local adaptation to diverse and physiologically challenging environments, as well as the molecular basis of brain evolution and longevity., Competing Interests: The authors declare no competing interest., (Copyright © 2021 the Author(s). Published by PNAS.)

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., Competing Interests: Declaration of competing interest None., (Copyright © 2019 Elsevier Inc. All rights reserved.)

The horizontal transmission of pathogenic and beneficial microbes has implications for health and development of socially living animals. Social group is repeatedly implicated as an important predictor of gut microbiome structure among primates, with individuals in neighboring social groups exhibiting distinct microbiomes. Here we examine whether group membership is a predictor of gut microbiome structure and diversity across three groups of white-faced capuchins (Cebus capucinus imitator) inhabiting a seasonal Costa Rican forest. We collected 62 fecal samples from 18 adult females during four sampling bouts. Sampling bouts spanned the dry-to-wet-to-dry seasonal transitions. To investigate gut microbial composition, we sequenced the V4 region of the 16S rRNA gene. We used the DADA2 pipeline to assign amplicon sequence variants and the RDP database to classify taxa. Our findings are: 1) gut microbiomes of capuchins clustered by social group in the late dry season, but this pattern was less evident in other sampling bouts; 2) social group was a significant variable in a PERMANOVA test of beta diversity, but it accounted for less variation than season; 3) social group was not an important predictor of abundance for the ten most abundant microbial taxa in capuchins; 4) when examining log2-fold abundances of microbes between social groups, there were significant differences in some pairwise comparisons. While this is suggestive of group-wide differences, individual variation may have a strong impact and should be assessed in future studies. Overall, we found a minor impact of social group membership on the gut microbiota of wild white-faced capuchins. Future research including home range overlap and resource use, as well as fine-scale investigation of individual variation, will further elucidate patterns of socially structured microbes., (© 2019 Wiley Periodicals, Inc.)

Research on the gut microbiota of free-ranging mammals is offering new insights into dietary ecology. However, for free-ranging primates, little information is available for how microbiomes are influenced by ecological variation through time. Primates inhabiting seasonal tropical dry forests undergo seasonally specific decreases in food abundance and water availability, which have been linked to adverse health effects. Throughout the course of a seasonal transition in 2014, we collected fecal samples from three social groups of free-ranging white-faced capuchin monkeys (Cebus capucinus imitator) in Sector Santa Rosa, Área de Conservación Guanacaste, Costa Rica. 16S rRNA sequencing data reveal that unlike other primates, the white-faced capuchin monkey gut is dominated by Bifidobacterium and Streptococcus. Linear mixed effects models indicate that abundances of these genera are associated with fluctuating availability and consumption of fruit and arthropods, whereas beta diversity clusters by rainfall season. Whole shotgun metagenomics revealed that the capuchin gut is dominated by carbohydrate-binding modules associated with digestion of plant polysaccharides and chitin, matching seasonal dietary patterns. We conclude that rainfall and diet are associated with the diversity, composition, and function of the capuchin gut microbiome. Additionally, microbial fluctuations are likely contributing to nutrient uptake and the health of wild primate populations.

Objectives: The physical condition of females depends on access to resources, which vary over space and time. Assessing variation in physical condition can help identify factors affecting reproductive success, but noninvasive measurement is difficult in wild animals. Creatinine concentration relative to the specific gravity (i.e., density) of urine has promise for noninvasively quantifying the relative muscle mass (RMM) of wild primates. We verified the relationship between these urinary parameters for wild white-faced capuchin monkeys, and assessed temporal changes in the RMM of females across groups and between periods of high and low resource abundance., Materials and Methods: We collected urine from 25 adult females in three groups across varying seasons at Sector Santa Rosa, Costa Rica. We measured the specific gravity and creatinine concentration of 692 samples and the effect of specific gravity on creatinine concentration. We used the residuals of this relationship to measure effects of group and season using mixed-effects models., Results: Specific gravity significantly predicted creatinine concentration. Season, group membership and the interaction between these variables were significant predictors of residual creatinine variation. Specifically, RMM was higher during months with high fruit energy density, lower in one social group, and less variable among females in the smallest group., Discussion: Our findings suggest that specific gravity and creatinine may be used as urinary parameters to make inferences about the RMM of capuchins. Using this technique, we infer that females experienced changes in muscle mass according to variation in resource energy availability and social group variation., (© 2017 Wiley Periodicals, Inc.)

Objectives: Our goal is to investigate flower foraging by capuchin monkeys, a behavior rarely studied in wild primates. We ask what drives seasonal variation in florivory rates: flower quality and abundance or fluctuations in fruit and invertebrate abundances. We explore how capuchins affect the reproductive success of flower food species by quantifying the potential pollination rate., Materials and Methods: We followed capuchin groups from dawn to dusk and recorded all flower foraging bouts. Flower food nutritional composition was compared to fruit and invertebrate foods. We recorded overall flower, fruit, and invertebrate abundances and compared the rate of flower foraging to these. We estimated the likelihood of pollination from the proportion of flower patch visits to each plant species that satisfied minimum behavioral requirements., Results: Flower eating was highly seasonal, and was significantly negatively related to overall fruit and invertebrate abundance but not flower abundance. Although smaller than most fruits, flowers were nutritionally comparable to fruit foods by dry mass and contained higher average concentrations of protein. Capuchins are likely pollinators for Luehea speciosa; most foraging visits to this species occurred in a manner that makes outcrossing or geitonogamous pollination likely., Discussion: Flowers are an important seasonal resource for capuchins. Flowers likely act as fallback foods during periods of reduced fruit and invertebrate abundance, and may exert evolutionary pressure disproportionate to their consumption. Capuchin florivory likely affects the reproductive success of some plants, potentially shaping forest structure. Our study illustrates the value of assessing the importance of rare foods in the primate diet., (© 2016 Wiley Periodicals, Inc.)

Objective: Circannual variation in reproduction is pervasive in birds and mammals. In primates, breeding seasonality is variable, with seasonal birth peaks occurring even in year-round breeders. Environmental seasonality is reportedly an important contributor to the observed variation in reproductive seasonality. Given that food availability is the primary factor constraining female reproduction, predictions concerning responsiveness to environmental seasonality focus on females, with studies of males focusing primarily on social factors. We examined the influence of both environmental and social factors on male fecal testosterone (fT) and glucocorticoids (fGC) in moderately seasonally breeding white-faced capuchin monkeys (Cebus capucinus) in Costa Rica., Methods: Over 17 months, we collected 993 fecal samples from 14 males in three groups. We used LMM to simultaneously examine the relative effects of photoperiod, fruit biomass, rainfall, temperature, female reproductive status (i.e., number of periovulatory periods, POPs), and male age and dominance rank on monthly fT and fGC levels., Results: Male age and rank had large effects on fT and fGC. Additionally, some hormone variation was explained by environmental factors: photoperiod in the previous month (i.e., lagged photoperiod) was the best environmental predictor of monthly fT levels, whereas fGC levels were best explained by lagged photoperiod, fruit biomass, and rainfall. POPs predicted monthly fT and fGC, but this effect was reduced when all variables were considered simultaneously, possibly because lagged photoperiod and POP were highly correlated., Conclusions: Males may use photoperiod as a cue predicting circannual trends in the temporal distribution of fertile females, while also fine-tuning short-term hormone increases to the actual presence of ovulatory females, which may occur at any time during the year., (© 2016 Wiley Periodicals, Inc.)

Objectives: Fallback foods (FBFs) are hypothesized to shape the ecology, morphology, and behavior of primates, including hominins. Identifying FBFs is therefore critical for revealing past and present foraging adaptations. Recent research suggests invertebrates act as seasonal FBFs for many primate species and human populations. Yet, studies measuring the consumption of invertebrates relative to ecological variation are widely lacking. We address this gap by examining food abundance and entomophagy by primates in a seasonal forest., Materials and Methods: We study foraging behavior of white-faced capuchins (Cebus capucinus)-a species renowned for its intelligence and propensity for extractive foraging-along with the abundance of invertebrates, dietary ripe fruits, pith, and bromeliads. Consumption events and processing time are recorded during focal animal samples. We determine abundance of vegetative foods through phenological and density records. Invertebrates are collected in malaise, pan, and terrestrial traps; caterpillar abundance is inferred from frass traps., Results: Invertebrates are abundant throughout the year and capuchins consume invertebrates-including caterpillars-frequently when fruit is abundant. However, capuchins spend significantly more time processing protected invertebrates when fruit and caterpillars are low in abundance., Discussion: Invertebrate foraging patterns are not uniform. Caterpillar consumption is consistent with a preferred strategy, whereas capuchins appear to fallback on invertebrates requiring high handling time. Capuchins are convergent with hominins in possessing large brains and high levels of sensorimotor intelligence, thus our research has broad implications for primate evolution, including factors shaping cognitive innovations, brain size, and the role of entomophagy in the human diet., (© 2015 Wiley Periodicals, Inc.)

The parallel evolution of increased sensorimotor intelligence in humans and capuchins has been linked to the cognitive and manual demands of seasonal extractive faunivory. This hypothesis is attractive on theoretical grounds, but it has eluded widespread acceptance due to lack of empirical data. For instance, the effects of seasonality on the extractive foraging behaviors of capuchins are largely unknown. Here we report foraging observations on four groups of wild capuchins (Cebus capucinus) inhabiting a seasonally dry tropical forest. We also measured intra-annual variation in temperature, rainfall, and food abundance. We found that the exploitation of embedded or mechanically protected invertebrates was concentrated during periods of fruit scarcity. Such a pattern suggests that embedded insects are best characterized as a fallback food for capuchins. We discuss the implications of seasonal extractive faunivory for the evolution of sensorimotor intelligence (SMI) in capuchins and hominins and suggest that the suite of features associated with SMI, including increased manual dexterity, tool use, and innovative problem solving are cognitive adaptations among frugivores that fall back seasonally on extractable foods. The selective pressures acting on SMI are predicted to be strongest among primates living in the most seasonal environments. This model is proffered to explain the differences in tool use between capuchin lineages, and SMI as an adaptation to extractive foraging is suggested to play an important role in hominin evolution., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

Efficient detection and selection of reddish fruits against green foliage has long been thought to be a major selective pressure favoring the evolution of primate trichromatic color vision. This has recently been questioned by studies of free-ranging primates that fail to show predicted differences in foraging efficiency between dichromats and trichromats. In the present study, we use a unique approach to evaluate the adaptive significance of trichromacy for fruit detection by undertaking a functional substitution model. The color vision phenotypes of neotropical monkeys are simulated for human observers, who use a touch-sensitive computer interface to search for monkey food items in digital images taken under natural conditions. We find an advantage to trichromatic phenotypes - especially the variant with the most spectrally separated visual pigments - for red, yellow and greenish fruits, but not for dark (purple or black) fruits. These results indicate that trichromat advantage is task-specific, and that shape, size and achromatic contrast variation between ripe and unripe fruits cannot completely mitigate the advantage of color vision. Similarities in fruit foraging performance between primates with different phenotypes in the wild likely reflect the behavioral flexibility of dichromats in overcoming a chromatic disadvantage., (Copyright © 2013 Elsevier Ltd. All rights reserved.)