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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.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the ‘invariant rate of ageing’ hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed., The ‘invariant rate of ageing’ hypothesis suggests that the rate of ageing tends to be constant within species. Here, Colchero et al. find support for the hypothesis across primates, including humans, suggesting biological constraints on the rate of ageing.

On 5 February 2021, we observed the first instance of female-committed infanticide followed by cannibalism in a long-studied ( 35 years) population of wild white-faced capuchins (Cebus imitator) in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. The events leading up to and including the infanticide and cannibalism were observed and documented ad libitum, with segments digitally recorded, and a post-mortem necropsy performed. Here we detail our observations and evaluate the events within the framework of leading adaptive explanations. The infanticide may have been proximately motivated by resource competition or group instability. The circumstances of the observed infanticide provided support for the resource competition, adoption avoidance, and social status hypotheses of infanticide, but not for the exploitation hypothesis, as neither the perpetrator nor her kin consumed the deceased infant. The subsequent cannibalism was performed by juveniles who observed the infanticide and may have been stimulated by social facilitation and their prior experience of meat consumption as omnivores. To our knowledge, cannibalism has been documented only once before in C. imitator, in an adjacent study group, with the two cases sharing key similarities in the context of occurrence and manner of consumption. These observations add to our growing knowledge of the evolutionary significance of infanticide and its importance as a reproductive strategy in nonhuman primates.

Animals born with physical impairments may particularly require behavioural flexibility and innovation to survive and carry out social activities, such as grooming. Studies on free-ranging Japanese macaques on Awaji Island, Japan, have shown that individuals with congenital limb malformations exhibited compensatory behaviours while grooming, such as increased mouth and elbow use for removing ectoparasites. The aim of this study is to explore disabled and nondisabled grooming techniques to determine whether and to what extent disabled monkeys develop novel grooming techniques, and if there is disability-associated variation in grooming efficiency. We hypothesized that modified grooming techniques used by disabled monkeys fulfilled the social and relaxing functions of grooming, however, that grooming by manually impaired individuals may still carry a hygienic cost to the recipients. Grooming behavioural data were collected by video in 2007 on 27 adult females (11 with CLMs). With a detailed grooming-related ethogram, we transcribed 216 2-minute continuous grooming video samples. We analyzed the data using generalized linear mixed effects models in R. We found that monkeys with manual impairment were less efficient groomers, as measured by removal and movement efficiency during grooming. However, there were no significant differences associated with the number of grooming movements per sample among the focal animals. Additionally, with a behavioural sequential analysis, we isolated 8 distinct grooming techniques and 3 novel disability-specific movements. Our results indicate that innovation and modification of movement types does not entirely compensate for manual disability, and that manual impairment carries a cost to the hygienic function of grooming. However, for the grooming recipient, the experience of being groomed by a disabled or nondisabled groomer is likely similar, and through movement compensation, disabled monkeys are able to engage in the social aspect of grooming without incurring any disability-associated costs.

Most mammals live in social groups in which members form differentiated social relationships. Individuals may vary in their degree of sociality, and this variation can be associated with differential fitness. In some species, for example, female sociality has a positive effect on infant survival. However, investigations of such cases are still rare, and no previous study has considered how male infanticide might constrain effects of female sociality on infant survival. Infanticide is part of the male reproductive strategy in many mammals, and it has the potential to override, or even reverse, effects of female reproductive strategies, including sociality. Therefore, we investigated the relationships between female sociality, offspring survival, and infanticide risk in wild white-faced capuchin monkeys using long-term data from Santa Rosa, Costa Rica. Female capuchins formed differentiated bonds, and bond strength was predicted by kin relationship, rank difference, and the presence of female infants. Most females formed stable bonds with their top social partners, although bond stability varied considerably. Offspring of highly social females, who were often high-ranking females, exhibited higher survivorship during stable periods compared with offspring of less social females. However, offspring of highly social females were more likely to die or disappear during periods of alpha male replacements, probably because new alpha males are central to the group, and therefore more likely to target the infants of highly social, central females. This study shows that female sociality in mammals can have negative fitness consequences that are imposed by male behavior.

Primates have long been used as indicator species for assessing overall ecosystem health. However, area-wide census methods are time consuming, costly, and not always feasible under many field conditions. Therefore, it is important to establish whether monitoring a subset of a population accurately reflects demographic changes occurring in the population at large. Over the past 35 years, we have conducted 15 area-wide censuses in Sector Santa Rosa, Costa Rica. These efforts have revealed important trends in population growth patterns of capuchin monkeys following the protection and subsequent regeneration of native forests. During this same period, we have also intensively studied a subset of the capuchin groups. Comparing these two datasets, we investigate whether the population structures of the closely monitored groups are reliable indicators of area-wide demographic patterns. We compare the overall group size and the individual age/sex class compositions of study groups and nonstudy groups (i.e., those contacted during area-wide censuses only). Our study groups contained more individuals overall with a larger proportion of infants, and there were indications that the proportion of adult and subadult males was lower. These differences can be ascribed either to sampling errors or real differences attributable to human presence and/or better habitat quality for the study groups. No other sex/age classes differed, and major demographic changes were simultaneously evident in both study and nonstudy groups. This study suggests that the Santa Rosa capuchin population is similarly impacted by large-scale ecological patterns observable within our study groups.

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.

OBJECTIVES Invertebrates are important foods for many primates and provide valuable nutrients often unavailable from plant sources. We examine the diet of white-faced capuchins (Cebus capucinus imitator) to determine: (a) timing and types of invertebrate food consumption; (b) whether invertebrate consumption varies with availability of plant foods; and (c) how invertebrates contribute to energy and protein intake of females during different reproductive states. MATERIALS AND METHODS We analyze 2 years of behavioral data from 25 adult female capuchins to determine which invertebrates are eaten. We describe annual and monthly invertebrate consumption patterns, and, employing circular statistics, analyze seasonal consumption of the four most important invertebrate groups eaten. We apply logistic regression analyses to tree density and fruit energy data to determine whether capuchin invertebrate foraging is related to fruit energy availability of their most commonly consumed fruits. We evaluate the nutritional contribution of invertebrates to energetic and protein requirements of females over time and across reproductive stages. RESULTS Capuchins consumed invertebrates from 21 identifiable groups, but their diet was dominated by four orders: Lepidoptera, Orthoptera, Hemiptera, and Hymenoptera. All four orders were consumed in a significantly seasonal pattern, and reduced fruit energy availability was a significant predictor of increased invertebrate foraging. Capuchin females often required invertebrate energy intake to meet their overall monthly energetic needs, particularly while they were lactating, even though they appear to exceed their protein requirements every month. DISCUSSION These results indicate that invertebrate consumption is critical for capuchin energetic needs, particularly during periods of reduced fruit availability and lactation.

Documenting primate life history characteristics is important because it provides information about traits that affect the timing and rate of reproduction in these long-lived species. This study describes the hormonal correlates of female reproductive events and quantifies for the first time key life history variables for Colobus vellerosus, using hormonal and observational data. This study also biologically validates that the reproductive events determined in the hormone profiles correspond to observed reproductive events for each female. We collected behavioural data on 18 females in our four study groups during 12 months (May 2012-2013) at the Boabeng-Fiema Monkey Sanctuary, using 10-min continuous focal and ad libitum sampling. We concurrently collected faecal samples (n = 1866) every 2-3 days from these 18 females (prepubescent n = 2, cycling n = 2, lactating n = 12, pregnant, n = 7, and post-reproductive n = 1) and extracted oestrogen (E2) and progesterone (P) metabolites in the field using solid-phase extraction cartridges. We created a hormone profile for each female by analyzing 1586 of our samples for E2 using radio-immuno assays, and P using enzyme-immunoassays at the Wisconsin National Primate Research Center. Mean ovarian cycle length was 24 days ± 1 (n = 2 cycles). Mean gestation length was 23 weeks (range = 21-25 weeks, n = 2 complete pregnancies). For females whose infants survived to nutritional independence, the mean inter-birth interval (IBI) was significantly longer than for females whose infants died prior to reaching nutritional independence (Mann-Whitney U Test; U = 14.5, p = 0.006; IBI surviving infants: 17.75 months, range = 8-20.75 months, n = 11 vs. IBI infant death: 11.89 months, range = 8-18.5 months, n = 9). The values for most life history traits reported in this study are similar to those documented in other similarly sized colobine species. Some values are on the lower end of the range for similarly sized colobines; C. vellerosus shows a cycle of 24 days and gestation length of 5.75 months vs. a range of 24-29 days for cycle length and 5.25-7.5 months for gestation length in other colobines. This may be due to C. vellerosus' smaller body size, or their limited access to higher quality food resources.

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. Am J Phys Anthropol 159:671–682, 2016. © 2016 Wiley Periodicals, Inc.

Many plants use colour to attract pollinators, which often possess colour vision systems well-suited for detecting flowers. Yet, to isolate the role of colour is difficult, as flowers also produce other cues. The study of florivory by Neotropical primates possessing polymorphic colour vision provides an opportunity to investigate the importance of colour directly. Here we determine whether differences in colour vision within a mixed population of wild dichromatic and trichromatic white-faced capuchins (Cebus capucinus imitator) affect flower foraging behaviours. We collected reflectance data for flower foods and modelled their chromatic properties to capuchin colour vision phenotypes. We collected behavioural data over 22 months spanning four years, determined the colour vision phenotype of each monkey based on amino acid variation of the L/M opsin gene from fecal DNA, and compared foraging behaviours of dichromats and trichromats. Most flowers were more conspicuous to trichromats, and trichromats foraged in small flower patches significantly more often. These data demonstrate a difference in wild primate foraging patterns based on colour vision differences, supporting the hypothesis that trichromacy enhances detection of small, ephemeral resources. This advantage, which may also extend to other foods, likely contributes to the maintenance of colour vision polymorphism in Neotropical monkeys.

Debates about the likelihood of conspecific care for disabled individuals in ancestral hominins rely on evidence from extant primates, yet little is known about social treatment (positive, neutral or negative) of physically disabled individuals in nonhuman primates. A group of free-ranging Japanese macaques ( Macaca fuscata ) at the Awajishima Monkey Center (AMC) in Japan presents a unique opportunity to investigate the relationships between physical impairment and social behavior, in the context of congenital limb malformation in adult nonhuman primates. We collected behavioral data on 23 focal animals, taking 30-minute continuous time samples on disabled and nondisabled adult female Japanese macaques during three consecutive birth seasons (May–August 2005, 2006, and 2007). Disabled females were less social overall compared with nondisabled controls, a pattern that was evident from a variety of measures. Disabled females rested significantly more and socialized significantly less compared with controls, had fewer adult female affiliates, fewer adult female grooming partners, and spent less time engaged in grooming with adult females. Some measures suggested that the social differences were the result of behavioral flexibility on the part of disabled females compensating for their disabilities with lower levels of social involvement and more rest. Disabled females were as successful at groom solicitations as were nondisabled females and the ratio of disabled and nondisabled affiliates was similar among focal animals; there was no strong preference related to the disability status of affiliates. Disabled females were also bitten and chased less frequently. Overall, there was little evidence either for conspecific care or for social selection against disability. In general, there was a socially neutral response to disability, and while neutral social context allows for the possibility of care behaviors, our findings emphasize the self-reliant abilities of these disabled primates and suggest caution when inferring conspecific care for even very disabled ancestral humans.

Much attention has been paid to hormonal variation in relation to male dominance status and reproductive seasonality, but we know relatively little about how hormones vary across life history stages. Here we examine fecal testosterone (fT), dihydrotestosterone (fDHT), and glucocorticoid (fGC) profiles across male life history stages in wild white-faced capuchins (Cebus capucinus). Study subjects included 37 males residing in three habituated social groups in the Área de Conservacíon Guanacaste, Costa Rica. Male life history stages included infant (0 to

The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden, and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging. The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.

Women rarely give birth after ∼45 y of age, and they experience the cessation of reproductive cycles, menopause, at ∼50 y of age after a fertility decline lasting almost two decades. Such reproductive senescence in mid-lifespan is an evolutionary puzzle of enduring interest because it should be inherently disadvantageous. Furthermore, comparative data on reproductive senescence from other primates, or indeed other mammals, remains relatively rare. Here we carried out a unique detailed comparative study of reproductive senescence in seven species of nonhuman primates in natural populations, using long-term, individual-based data, and compared them to a population of humans experiencing natural fertility and mortality. In four of seven primate species we found that reproductive senescence occurred before death only in a small minority of individuals. In three primate species we found evidence of reproductive senescence that accelerated throughout adulthood; however, its initial rate was much lower than mortality, so that relatively few individuals experienced reproductive senescence before death. In contrast, the human population showed the predicted and well-known pattern in which reproductive senescence occurred before death for many women and its rate accelerated throughout adulthood. These results provide strong support for the hypothesis that reproductive senescence in midlife, although apparent in natural-fertility, natural-mortality populations of humans, is generally absent in other primates living in such populations.

Neotropical primate parasitology has been dominated by studies of howler monkeys (Alouatta spp.), whereas the literature on the parasites of other platyrrhines is relatively sparse. We analysed the faeces of white-faced capuchins (Cebus capucinus) in a Costa Rican tropical dry forest and recovered 8 parasite taxa (Filariopsis barretoi, Giardia duodenalis, Strongyloides sp., Prosthenorchis sp., a spirurid nematode, a subulurid nematode, a strongylid nematode and a cestode). F. barretoi and Strongyloides sp. were the most prevalent parasites and were recovered from 84 and 76% of the sampled individuals, respectively. Individual capuchins were infected with an average of 1.89 parasite species. Capuchins host a diverse suite of parasites belonging to several taxonomic groups (Nematoda, Cestoda, Acanthocephala, Protozoa) and including species with direct and indirect life cycles. Many capuchin parasites are transmitted through the consumption of invertebrate intermediate hosts making diet a critical component of capuchin-parasite ecology. This study represents the most intensive parasitological survey of wild capuchin monkeys to date.

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.

We provide male and female census count data, age-specific survivorship, and female age-specific fertility estimates for populations of seven wild primates that have been continuously monitored for at least 29 years: sifaka (Propithecus verreauxi) in Madagascar; muriqui (Brachyteles hypoxanthus) in Brazil; capuchin (Cebus capucinus) in Costa Rica; baboon (Papio cynocephalus) and blue monkey (Cercopithecus mitis) in Kenya; chimpanzee (Pan troglodytes) in Tanzania; and gorilla (Gorilla beringei) in Rwanda. Using one-year age-class intervals, we computed point estimates of age-specific survival for both sexes. In all species, our survival estimates for the dispersing sex are affected by heavy censoring. We also calculated reproductive value, life expectancy, and mortality hazards for females. We used bootstrapping to place confidence intervals on life-table summary metrics (R0, the net reproductive rate; λ, the population growth rate; and G, the generation time). These data have high potential for reuse; they derive from continuous population monitoring of long-lived organisms and will be invaluable for addressing questions about comparative demography, primate conservation and human evolution.

Human senescence patterns—late onset of mortality increase, slow mortality acceleration, and exceptional longevity—are often described as unique in the animal world. Using an individual-based data set from longitudinal studies of wild populations of seven primate species, we show that contrary to assumptions of human uniqueness, human senescence falls within the primate continuum of aging; the tendency for males to have shorter life spans and higher age-specific mortality than females throughout much of adulthood is a common feature in many, but not all, primates; and the aging profiles of primate species do not reflect phylogenetic position. These findings suggest that mortality patterns in primates are shaped by local selective forces rather than phylogenetic history.

Early investigations into variable repro- ductive success in nonhuman primates tended to focus on the benefits conferred by high dominance rank. How- ever, the effect of high rank on individual reproductive success has been found to vary both intra- and interspe- cifically, requiring researchers to expand their investiga- tions to include additional factors. Here we examine the age and rank of the mother, sex of the infant, group size, number of close kin, replacement of group males, and resource availability as possible predictors of female reproductive success in white-faced capuchins (Cebus capucinus) in the Santa Rosa sector of the Area de Con- servacion Guanacaste, Costa Rica. We examine the length of interbirth intervals (IBI) and infant survivor- ship as measures of individual reproductive success for the 31 adult females that resided in our three study groups between 1986 and 2007. The greatest predictor of IBI length was whether or not the first infant in the interval survived (number of matrilineal kin and resource availability were also significant predictors); while infant survivorship was most significantly pre- dicted by the occurrence of a turnover in group males in the year following the birth of an infant (infant sex was also a significant factor). Based on these findings, we conclude that male and female reproductive strategies are at odds in this species, with male strategies strongly influencing female reproductive success. Am J Phys

In many social mammals and birds, soft vocalizations are habitually produced during dispersed moving and foraging, the function being to maintain contact and regulate spacing between group members. In some species, much louder calls are given sporadically by specific individuals when they become separated from the group, or ‘lost’. The function of these calls has seldom been specifically tested, particularly among social primates, but is often assumed to involve regaining contact with the group based on a combination of individually distinctive calls and antiphonal responses to them from within the group. To test these assumptions, we conducted research on two groups of white-faced capuchins (Cebus capucinus) in Costa Rica. We analyzed 82 bouts of ‘lost’ calls given by 13 different adult individuals when separated from the group and the antiphonal responses they elicited. Lost calls were individually distinctive and were answered in 35% of calling episodes. Answers were selective: dominant males and females were answered more than were subordinate callers of either sex. As a result, dominant callers relocated and returned to the group more quickly than did subordinate callers. We discuss the potential proximate motivations for, and ultimate benefits of, such selective answering of dominant group members. Am. J. Primatol. 69:829–835, 2007. © 2007 Wiley-Liss, Inc.

Evidence for paternal kin recognition and paternally biased behaviors is mixed among primates. We investigate whether infant handling behaviors exhibit paternal kin biases in wild white-faced capuchins monkeys (Cebus capucinus) by comparing interactions between infants and genetic sires, potential sires, siblings (full sibling, maternal, and paternal half-siblings) and unrelated handlers. We used a linear mixed model approach to analyze data collected on 21 focal infants from six groups in Sector Santa Rosa, Costa Rica. Our analyses suggest that the best predictor of adult and subadult male interactions with an infant is the male's dominance status, not his paternity status. We found that maternal siblings but not paternal siblings handled infants more than did unrelated individuals. We conclude that maternal but not paternal kinship influence patterns of infant handling in white-faced capuchins, regardless of whether or not they can recognize paternal kin. Am. J. Primatol. 78:659-668, 2016. © 2016 Wiley Periodicals, Inc.

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug-of-war) or by how easily females can be monopolized (priority-of-access). These models have rarely been investigated in species with exceptionally long male tenures, such as white-faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white-faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession model's assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha male's probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well-established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.

Network optimality has been described in genes, proteins and human communicative networks. In the latter, optimality leads to the efficient transmission of information with a minimum number of connections. Whilst studies show that differences in centrality exist in animal networks with central individuals having higher fitness, network efficiency has never been studied in animal groups. Here we studied 78 groups of primates (24 species).We found that group size and neocortex ratio were correlated with network efficiency. Centralisation (whether several individuals are central in the group) and modularity (how a group is clustered) had opposing effects on network efficiency, showing that tolerant species have more efficient networks. Such network properties affecting individual fitness could be shaped by natural selection. Our results are in accordance with the social brain and cultural intelligence hypotheses, which suggest that the importance of network efficiency and information flow through social learning relates to cognitive abilities., SCOPUS: ar.j, info:eu-repo/semantics/published

In many primate species, conspicuous behavioral and/or morphological changes are indicators of the fertile phase of the female cycle. However, several primate species, such as the white-faced capuchin, lack these cues. This is referred to as "concealed ovulation," and is argued to be a reproductive strategy that confuses paternity and lowers the risk of infanticide. We studied 10 adult female white-faced capuchins in Santa Rosa National Park, Costa Rica, from January to June 2002. We determined their ovarian cycling patterns by analyzing fecal ovarian hormones, and compared simultaneously collected behavioral data to determine which, if any, cues females use to signal their fertile phases. We found that four females cycled during the study period but ceased to cycle without becoming pregnant. We considered several explanations for the lack of conception during our study, including reproductive seasonality. We found that female C. capucinus showed only small increases in rates of affiliative/proceptive behaviors directed toward adult males during their periovulatory phases. The best indicator of cycle phase was a significant increase in male affiliative behaviors (e.g., following and grooming bouts) and sexual behaviors (e.g., copulations and courtship displays) directed toward females during the periovulatory phase compared to the nonovulatory phase. Our finding that females exhibit little proceptive behavior, but that copulations and male courtship are nonetheless concentrated in periovulatory phases suggests that even though females do not provide behavioral and morphological cues to ovulation, males are still able to detect it. Infanticide occurs with some frequency in these monkeys, and there is evidence for postconceptive mating as a female strategy to lower risk of infanticide via paternity confusion. However, despite this occurrence of nonconceptive mating and the absence of female cues to ovulation, truly concealed ovulation does not appear to be characteristic of this study population of white-faced capuchins.

Observed patterns of variability in the food-processing behavior of white-faced capuchins (Cebus capucinus) across populations may reflect foraging traditions. However, there has been relatively little attention given to intrapopulation variability in food processing among groups and age/sex classes, making recent cross-population comparisons difficult to interpret. In this paper, we provide data on patterns of object use in foraging that we observed at Santa Rosa National Park, Costa Rica, for comparison with published data from a neighboring research site, Palo Verde National Park. We also describe the techniques used to process two food items consumed by Cebus capucinus at Santa Rosa, and discuss the factors that may underlie observed variability. We conducted a 6-month study on two groups of capuchins in 2001, and collected data on general activity and feeding patterns, rates and forms of object use, and distinctive processing techniques employed for two specific foods (Sloanea terniflora and Luehea candida). Rates of object-use behavior at Santa Rosa were considerably higher than those reported for Palo Verde and showed significant variation between groups and age/sex classes, as did patterns of Sloanea and Luehea processing. Observed differences in feeding rates between groups may reflect food availability or relative profitability, whereas variation between age/sex classes seems to reflect differences in the physical capabilities, foraging strategies, and the relative experience of mature and immature animals. Further research is needed to identify how a social context may influence the acquisition of food-processing techniques in juveniles and the development of foraging traditions in social groups.

The relationship of the ovarian cycle phase to same-sex mounting activity in adult female Japanese macaques (Macaca fuscata) was studied during the 1997/1998 mating season. Fecal samples were collected from eight female subjects two to three times per week and analyzed by enzyme immunoassay for fecal hormone levels. Hormone profiles of estrone (E1) and pregnanediol (PdG) were used to separate ovarian cycles into three phases: follicular, periovulatory, and luteal. Patterns of same-sex and heterosexual mounting behavior in the females were analyzed for phase variation during conceptive cycles. Same-sex mounting among female Japanese macaques occurred most frequently during the follicular and periovulatory phases of the cycle, and not at all during the luteal phase, paralleling the pattern found in heterosexual mounting behavior. These findings suggest a link between hormonal fluctuations and patterns of sexual mounting, regardless of whether the partner is of the same or opposite sex.

We conducted behavioral observations simultaneously with fecal sample collection on eight nonlactating females 2-3 times per week, October 1997-March 1998, to examine the relationship between ovarian hormones and the sexual behavior of female Japanese macaques (Macaca fuscata) during the mating season. We analyzed samples by enzyme immunoassay for fecal hormone levels. Hormone profiles of estrone-glucuronide (E1) and pregnanediol-glucuronide (PdG) were used to separate ovarian cycles into three phases (follicular, periovulatory, and luteal). Hormonal profiles indicate average cycle lengths of 27.6 +/- 4.2 days (+/- SD; n = 26). Average lengths of the luteal and follicular phases were 12.3 +/- 3.8 days (+/- SD) and 8.3 +/- 3.4 days (+/- SD), respectively. We observed female Japanese macaques engaging in sexual activity throughout the ovarian cycle, with the highest rates occurring during the follicular and periovulatory phases as compared to the luteal phase. The attractivity of female Japanese macaques increased significantly during the follicular and periovulatory phases of the ovarian cycle, when E1 levels are peaking and PdG levels drop to baseline. In addition, females displayed a significant increase in proceptive behavior during the follicular and periovulatory phases. Grooming bouts, as well as proximity between female and male macaques, also increased significantly during the follicular and periovulatory phases. We conclude that fluctuating levels of ovarian hormones in different phases of the cycle are significantly associated with variable rates of copulatory and pericopulatory behaviors in these Japanese macaque females.

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.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.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.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.

The leading explanatory model for the widespread occurrence of color vision polymorphism in Neotropical primates is the heterozygote superiority hypothesis, which postulates that trichromatic individuals have a fitness advantage over other phenotypes because redgreen chromatic discrimination is useful for foraging, social signaling, or predator detection. Alternative explanatory models predict that dichromatic and trichromatic phenotypes are each suited to distinct tasks. To conclusively evaluate these models, one must determine whether proposed visual advantages translate into differential fitness of trichromatic and dichromatic individuals. We tested whether color vision phenotype is a significant predictor of female fitness in a population of wild capuchins, using longterm 26 years survival and fertility data. We found no advantage to trichromats over dichromats for three fitness measures fertility rates, offspring survival and maternal survival. This finding suggests that a selective mechanism other than heterozygote advantage is operating to maintain the color vision polymorphism. We propose that attention be directed to field testing the alternative mechanisms of balancing selection proposed to explain opsin polymorphism nichedivergence, frequencydependence and mutual benefit of association. This is the first indepth, longterm study examining the effects of color vision variation on survival and reproductive success in a naturallyoccurring population of primates.

Examining seasonal mortality patterns can yield insights into the drivers of mortality and thus potential selection pressures acting on individuals in different environments. We compiled adult and juvenile mortality data from nine wild non-human primate taxa to investigate the role of seasonality in patterns of mortality and address the following questions: Is mortality highly seasonal across species? Does greater environmental seasonality lead to more seasonal mortality patterns? If mortality is seasonal, is it higher during wet seasons or during periods of food scarcity? and Do folivores show less seasonal mortality than frugivores? We found seasonal mortality patterns in five of nine taxa, and mortality was more often tied to wet seasons than food-scarce periods, a relationship that may be driven by disease. Controlling for phylogeny, we found a positive relationship between the degree of environmental seasonality and mortality, with folivores exhibiting more seasonal mortality than frugivores. These results suggest that mortality patterns are influenced both by diet and degree of environmental seasonality. Applied to a wider array of taxa, analyses of seasonal mortality patterns may aid understanding of life-history evolution and selection pressures acting across a broad spectrum of environments and spatial and temporal scales.

Dominance style, the level of tolerance displayed by dominant individuals toward subordinate ones, is exhibited along a continuum from despotic to relaxed. It is a useful concept to describe the nature of dominance relationships in macaque species and it bridges among multiple features of dominance hierarchies, aggression, kinship and conflict resolution. Capuchins share many behavioral similarities with Old World monkeys and like macaques, may exhibit a suite of covarying characteristics related to dominance. Here, we provide an assessment of dominance style by examining measures of aggression and kin bias in 22 adult female white-faced capuchin monkeys (Cebus capucinus) in three social groups at Santa Rosa Sector, Costa Rica. We found that bidirectionality of aggression was low (mean = 6.9% ± SE 1.6). However, there were few significant correlations between kin relatedness and social behavior (approaching, grooming, proximity, and co-feeding), even though the intensity of kin bias in grooming was moderate and higher in the larger group. We conclude that patterns of aggression and kin-biased behavior in our study animals are dissimilar to the patterns of covariation observed in macaque species. While unidirectional aggression suggests a despotic dominance style, the moderate expression of kin bias suggests an intermediate to relaxed classification when compared with results from an analysis of 19 macaque species. Additional studies of capuchin species and behaviors associated with dominance style (i.e., conciliatory tendencies) would help to create a comparative framework for the genus Cebus, and allow for more detailed cross-species comparison of dominance relationships across all primates.

Little is known about consequences of disability in nonhuman primates, yet individuals with disabilities can reveal much about behavioral flexibility, innovation, and the capabilities of a species. The Macaca fuscata population surrounding the Awajishima Monkey Center has experienced high rates of congenital limb malformation for at least 40 years, creating a unique opportunity to examine consequences of physical impairment in situ, in a relatively large sample of free-ranging adult monkeys. Here we present behavioral data on 11 disabled adult females and 12 nondisabled controls from 279 hours of randomly ordered 30-minute focal animal follows collected during May-August in 2005, 2006, and 2007. We quantified numerous statistically significant disability-related behavioral differences among females. Disabled females spent less time begging for peanuts from tourists, and employed a behavioral variant of such peanut begging; they had a lower frequency of hand use in grooming and compensated with increased direct use of the mouth or a two-arm pinch technique; and they had a higher frequency of self-scratching, and more use of feet in self-scratching. Self-scratching against substrates was almost exclusively a disability associated behavior. Two females used habitual bipedalism. These differences not withstanding, disabled females behaved similarly to controls in many respects: overall reliance on provisioned and wild foods, time spent feeding, and feeding efficiency did not differ among females, and there was no time difference in behavior performed arboreally or terrestrially. Disabled adult females were able to compensate behaviorally to perform social and life-sustaining activities, modifying existing behaviors to suit their individual physical situations and, occasionally, inventing new ways of doing things.

White-faced capuchin males disperse from their natal group at around 4.5 years of age, but there is much variation in dispersal timing: our youngest confirmed disperser was 19 months and the oldest 11 years old. In this study, we investigate possible factors influencing dispersal decisions in this species. Between 1983 and 2010, 64 males were born into three study groups in Santa Rosa National Park, Area de Conservación Guanacaste, and Costa Rica. As of August 2010, 21 died or were presumed dead (14 months), 13 remained natal residents, and 30 were presumed dispersers. We used backward logistic regression to identify proximate factors that predict the occurrence of male natal dispersal. The occurrence of a takeover (significant positive association) and group size (nonsignificant negative association) were included in the model. Male age, number of maternal brothers, and number of adult males were not significant predictors of natal dispersal. The resultant model correctly classified 97% of dispersed and 89% of resident natal males, for an overall success rate of 95%. The occurrence of a group takeover was the strongest predictor of male dispersal, with natal males being 18.7 times more likely to disperse in the context of a group takeover than during peaceful times. A linear regression model showed that the tenure length of a male's probable father influences the age of natal dispersal, explaining 15% of the observed variation in age. However, when our oldest disperser was removed (an outlier) this effect disappeared. Collectively, these results indicate that group instability, as evidenced by the occurrence of a takeover, shorter tenure length of a natal male's father, and smaller group size, triggers natal dispersal in this species while the converse leads to a delay. These data add to our growing evidence of the enormous impact that takeovers have on the behavioral ecology of this species.

Assessing glucocorticoid levels in free-ranging nonhuman primates provides a means to determine the social and environmental stress load for individuals. We investigated the effect of four proximate variables--reproductive state, season, male rank stability, and dominance rank--on the level of fecal glucocorticoids (cortisol metabolites) in eight adult female white-faced capuchin monkeys in Costa Rica. Reproductive state, season, and male rank stability significantly affected fecal glucocorticoids while female dominance rank did not. Cortisol levels were significantly higher in pregnant females as compared with lactating or other reproductive states. Cortisol levels were higher among females during the dry season compared with the wet season, suggesting a metabolic adaptation to maintain homeostasis in drier, hotter conditions. Although unfamiliar males present a greater infanticidal threat than do familiar ones, we found that females experienced higher glucocorticoid levels during male rank instability events, regardless of whether the alpha male role was taken over by a familiar or an unfamiliar male. Our findings provide important benchmark and comparative data for future studies on the variables that affect glucocorticoid levels in this species and other mammals.

Many factors have been hypothesized to affect the size and adult sex ratios of primate groups and these, in turn, have been argued to influence birth rates. Using park-wide census data collected on a population of capuchins over a 25-year period, we examined whether group size and adult sex ratio affect the per capita repro- ductive success of male and female white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. We found that the reproductive success of females (measured as the observed minus the expected ratio of immatures to adult females in the group) decreased with increasing group size, whereas that of males was independ- ent of group size. The proportion of adult males residing in groups had significant, yet contrasting effects on males and females. Male reproductive success was negatively associ- ated with the proportion of males residing in groups whereas female reproductive success increased with the proportion of males. The latter finding supports the inter- sexual conflict hypothesis, which suggests that a conflict of interest occurs between males and females over adult sex ratios. The effects of group size and composition on the reproductive success of capuchins, a male-dispersed omniv- orous species, are similar to those reported for howlers, a bisexually-dispersed folivorous species. One common factor between these taxa is that groups with low ratios of males to females are at greater risk of takeovers and resultant in- fanticide. Our results suggest that regardless of dietary preference and dispersal pattern, the threat of infanticide can constrain primate group size and composition. Am J Phys Anthropol 144:317-326, 2011. V C 2010 Wiley-Liss, Inc.

A total of 54 free-ranging monkeys were captured and marked in Santa Rosa National Park, Costa Rica, during May 1985, and an additional 17 were captured during March 1986. The animals were darted using a blowpipe or a CO2 gun. The drugs used were Ketaset®, Sernylan® and Telazol®. Ketaset was effective for Cebus capucinus but unsuccessful for Alouatta palliata and Ateles geoffroyi. Sernylan was successful for A. geoffroyi and A. palliata but is no longer commercially available. Telazol proved to be an excellent alternative capture drug for both A. palliata and A. geoffroyi.

A long-term study of two groups of white-faced capuchins (Cebus capucinus) in Santa Rosa National Park in Costa Rica provides evidence of unusually high levels of vertebrate predation compared to those reported in other field studies of Cebus. The hunting techniques for different prey types are described, and several questions concerning vertebrate predation in primates are addressed. Why is there variation between individuals and between groups in the rate of predation? Why do males hunt more than females? Previous hypotheses to explain hunting in Old World primates are applied to this Neotropical example. Finally, I argue that successful vertebrate predation can readily arise in species like Cebus, which are characterized by opportunistic foraging patterns, manipulative and cognitive skills and well-developed techniques for locating and subduing invertebrate prey.

Interpopulation variability in patterns of food processing, similar to what is described as "traditional" or "cultural" variation in chimpanzees (Pan troglodytes) and orangutans (Pongo pygmaeus), was identified in white-faced capuchins (Cebus capucinus). However, recent comparisons of food processing in capuchins were conducted only at the population level, with relatively little attention given to variability among groups, age/sex classes, or individuals. This paper examines variability in the processing of specific food types within the context of various social networks (i.e., patterns of association, rank, and kinship) among free-ranging Cebus capucinus at Santa Rosa National Park in Costa Rica. We collected data on two groups of white-faced capuchins in 2001, identifying rates of "food interest" for each individual, as well as forms of processing for specific food types. Juveniles exhibited the most interest in the food-processing behavior of other group members, and food interest was directed most frequently toward adult females. We identified distinctive processing techniques for several food items (Luehea candida pods, Sloanea terniflora fruits, and caterpillars) that facilitated comparisons among individuals within groups. Food-processing techniques for Sloanea fruit and caterpillars appeared to vary independently of the social networks examined in this study. However, we found evidence that variation in Luehea candida processing is to some degree linked to both patterns of association and social rank. The potential influence of these variables on observed food processing patterns warrants further scrutiny.

The feeding patterns of three neighboring groups of Cebus capucinus were documented over a 3-year period in Santa Rosa National Park, Costa Rica. We describe the diets of the three groups and examine whether dietary differences between groups could be attributed to environmental differences in food abundances, to differences in the profitability of what was available or to learned local traditions. Diets were variable among groups; group A primarily ate fruit (81.2% of feeding time) and spent little time eating insects (16.9%), while group C was more heavily reliant on insects (44.3%) and ate less fruit (53.0%). Group B had a diet that was somewhat intermediate (69.8% fruit, 29.0% insects). By measuring the densities of all major plant foods, we were able to determine that many of the dietary differences between groups could not be attributed to simple measures of food abundance, but we could not distinguish between the food profitability hypothesis and local tradition hypothesis.

The Arashiyama West troop of Macaca fuscata consists of 150 monkeys transported from Kyoto, Japan, in February 1972 to their present location near Laredo, Texas. At this site the animals range over 108 acres and during the study period were only minimally provisioned and disturbed. In the report of a 3-year study of consort partner selection it was suggested that yearlong social bonds within the troop appeared to be distinct from consort bonds formed during mating season. Like Sade, we consider grooming to be a good measure of yearround affinitive bonding in macaques. This study compares the pairs formed for consorting with those formed for yearlong grooming activities, by the 94 individuals who formed consort relationships during the mating season of 1973--1974. It was found that yearlong grooming involved pairs of monkeys which were significantly different from those for consorting. Grooming was relatively frequent between related monkeys, while consort partners were seldom related. In addition, yearlong grooming patterns were not disrupted during mating season. These results suggest that consort and grooming activities are behavioral expressions of two important social networks, involving mutually exclusive social bonds.

Lifetime reproductive success, measured by the number of offspring surviving to age five, varied from 0 to 10 in a group of 33 provisioned female Japanese macaques. Of the three contributors to reproductive success, the number of reproductive years, fecundity per year and survivorship of offspring to reproductive age, the first accounted for two-thirds of the variation. Fecundity per year and survivorship were negatively correlated, indicating reproductive costs of reducing interbirth interval. No other demographic measure used, nor the behavioral measure ‘dominance rank’, significantly correlated with lifetime reproductive success or its components. Age-specific changes in fecundity and infant survival were not found for this sample, neither could cessation of reproduction, even in very old females, be demonstrated.