Search

Understanding variation in social grouping patterns among animal taxa is an enduring goal of ethologists, who seek to evaluate the selective pressures shaping the evolution of sociality. Cohesive association with conspecifics increases intragroup feeding competition and may impose constraints on group size. Furthermore, in sexually dimorphic species, males and females may have different nutritional requirements, which can lead to suboptimal foraging in mixed-sex groups. How do animals living in permanent social groups mitigate these foraging costs? Niche differentiation is often hypothesized as a mechanism, but rigorous and detailed tests of the extent and context of differences in diet and habitat use, key tenets of this hypothesis, are rare. We investigated the potential for niche differentiation in foraging activity budget and environment use in a population of wild white-faced capuchin monkeys, Cebus imitator, in northwestern Costa Rica. Using a robust data set of 15 879 foraging scan samples collected from four groups over 13 months, we found that smaller individuals – e.g. juveniles and females – forage more often on smaller branches. We additionally found clear evidence of predator-sensitive foraging wherein the smallest individuals spent less time on the ground during invertebrate foraging. Importantly, niche differentiation was far more evident overall during invertebrate foraging, likely due to spatial constraints and environmental homogeneity imposed by fruit patches. In summary, we found considerable variation in habitat use across age and sex classes, likely attributable to differences in size and relative predation risk. These variables likely reduce intraspecific feeding competition by promoting differential diet and habitat use. Our results also provide insight into the limits of niche differentiation as a strategy for competition reduction and may shed light on the evolution of fission–fusion dynamics in highly frugivorous species.

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.

The polymorphic color vision system present in most North, Central, and South American monkeys is a textbook case of balancing selection, yet the mechanism behind it remains poorly understood. Previous work has established task-specific foraging advantages to different color vision phenotypes: dichromats (red-green colorblind) are more efficient foraging for invertebrates, while trichromats (color “normal” relative to humans) are more efficient foraging for “reddish” ripe fruit, suggesting that niche differentiation may underlie the maintenance of color vision variation. We explore a prediction of the niche differentiation hypothesis by asking whether dichromatic and trichromatic capuchin monkeys (Cebus imitator) diverge in their foraging activity budget, specifically testing whether dichromats forage more frequently for invertebrates and trichromats forage more frequently for “reddish” ripe fruit. To assess this, we analyze a large data set of behavioral scan samples (n = 21 984) from 48 wild adult female capuchins of known color vision genotype, dominance rank, and reproductive status, together with models of food conspicuity. We find no significant differences between dichromats and trichromats in the frequency of scans spent foraging for different food types but do find that nursing females forage less overall than cycling females. Our results suggest that the potential for color-vision-based niche differentiation in foraging time may be curtailed by the energetic requirements of reproduction, behavioral synchrony caused by group living, and/or individual preferences. While niche differentiation in activity budgets by color vision type is not apparent, fine-scale niche differentiation may be occurring. This research enhances our understanding of the evolutionary processes maintaining sensory polymorphisms.

Most primates produce one offspring at a time but can overlap investment in consecutive offspring (stacked investment) depending on ecological and/or social conditions. “Direct stacked investment” occurs when a female conceives and gestates a new offspring while a previous infant is still suckling. We investigate direct stacked investment in Colobus vellerosus by determining if there is a period of overlap between nipple contact with a female’s first infant and gestation of her subsequent infant. We then investigate the effect of male group-membership and stability on stacked investment to test the hypothesis that stacking investment is a female strategy to avoid infanticide. We collected scan data to record when an infant was in nipple contact from 16 females in four groups of C. vellerosus, from May 2012 to May 2013 at Boabeng-Fiema Monkey Sanctuary in Ghana. We studied three group types, stable multimale, multifemale; unstable multimale, multifemale; and stable unimale, multifemale. Eight of our study females directly stacked investment. The frequency of direct stacked investment varied significantly among the group types. Stacked investment was due to earlier conception rather than delayed weaning, with females in stable multimale groups conceiving a subsequent infant earlier than those in unstable multimale groups. The timing of conception did not differ between stable unimale groups and either unstable or stable multimale groups. There was no difference in time to last nipple contact among group types. These results do not support the predictions of the infanticide avoidance hypothesis, but a larger sample size would help to test the hypothesis more comprehensively. Delayed conception by females in unstable groups may be infanticide avoidance, however, if it allows time for females to spread paternity certainty among males. Alternatively, females in unstable groups may be under stress or experience reduced feeding time due to frequent male–male agonistic interactions, both of which can suppress female ovulation. This study contributes to a growing body of research that explores flexibility in infant investment strategies, particularly in relation to external factors such as male group membership and stability.

This article summarizes my perspective on vital lessons that I have learned over my 45 years as a practicing anthropologist. To avoid repeating previously published biographical details of my life, I have only briefly described the facts and stages of my career here. Instead I have focused on a personal account of what I have learned from the events and experiences of my career and have attempted to distill them into underlying premises that have guided my academic vocation. I call them “nine truths I live by.”

Cannibalism has been observed in a variety of animal taxa; however, it is relatively uncommon in primates. Thus, we rely heavily on case reports of this behavior to advance our understanding of the contexts under which it occurs. Here, we report the first observation of cannibalism in a group of wild white‐faced capuchin monkeys (Cebus imitator). The subject was a dead infant, estimated to be 10 days old, and the probable victim of infanticide. Consumption of the corpse was initiated by a 2‐year‐old male (second cousin of the infant), though it was eventually taken over and monopolized by the group's alpha female (grandaunt of the infant). Although most group members expressed interest in the corpse (sniffing, touching, and threatening it), no others made an attempt to consume it. Given that this is the only observation of cannibalism recorded in over 37 years of study on this population, we consider it to be a rare behavior in this species. This detailed record contributes new data, which, when combined with other reports within and across species and contexts, enables the evaluation of adaptive explanations of cannibalism., We report the first case of cannibalism observed in a group of wild white‐faced capuchin monkeys. The subject was a dead infant, estimated to be 10 days old. A 2‐year‐old male initiated the consumption of the corpse, though consumption was eventually taken over and monopolized by the alpha female.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

On 5 February 2021, we observed the frst 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 pro- vided 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 signifcance of infanticide and its importance as a reproductive strategy in nonhuman primates. El 5 de febrero de 2021, observamos el primer caso de infanticidio de hembras seguido de canibalismo en una población de capuchinos de cara blanca (Cebus imitator) en el Sector Santa Rosa del Área de Conservación Guanacaste, Costa Rica. Se observaron y documentaron ad libitum los eventos que condujeron al infanticidio y al canibalismo documentados ad libitum, con segmentos grabados digitalmente, y una necropsia post-mortem realizada. Aquí detallamos nuestras observaciones y evaluamos los acontecimientos en el marco de las principales explicaciones adaptativas. El infanticidio puede haber sido motivado por la competencia por los recursos o la inestabilidad del grupo. Las circunstancias del infanticidio observado apoyan las hipótesis de la competencia por los recursos, la evitación de la adopción y el estatus social del infanticidio, pero no la hipótesis de la explotación, ya que ninguno de los autores del infanticidio se ha visto afectado de explotación, ya que ni la autora ni sus parientes consumieron al bebé fallecido. El canibalismo posterior fue realizado por los jóvenes que observaron el infanticidio y puede haber sido estimulado por la facilitación social y su experiencia previa de consumo de carne como omnívoros. Hasta donde sabemos, el canibalismo sólo se ha documentado una vez antes en C. imitator, en un grupo de estudio adyacente, con los dos casos compartiendo similitudes clave en el contexto de ocurrencia y la forma de consumo. Estas observaciones se suman a nuestro creciente conocimiento del significado evolutivo del infanticidio y su importancia como estrategia reproductiva en primates no humanos. Universidad Nacional, Costa Rica Escuela de Medicina Veterinaria

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.

Is it possible to slow the rate of aging, or do biological constraints limit its plasticity? We test this ‘invariant rate of aging’ hypothesis with an unprecedented 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 aging 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 aging, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of aging hypothesis, implying biological constraints on how much the human rate of aging can be slowed.

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the lifespan. Here we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediatelyprecedingmaternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.

Extreme climate events can have important consequences for the dynamics of natural populations, and severe droughts are predicted to become more common and intense due to climate change. We analysed infant mortality in relation to drought in two primate species (white-faced capuchins, Cebus capucinus imitator, and Geoffroy's spider monkeys, Ateles geoffroyi ) in a tropical dry forest in northwestern Costa Rica. Our survival analyses combine several rare and valuable long-term datasets, including long-term primate life-history, landscape-scale fruit abundance, food-tree mortality, and climate conditions. Infant capuchins showed a threshold mortality response to drought, with exceptionally high mortality during a period of intense drought, but not during periods of moderate water shortage. By contrast, spider monkey females stopped reproducing during severe drought, and the mortality of infant spider monkeys peaked later during a period of low fruit abundance and high food-tree mortality linked to the drought. These divergent patterns implicate differing physiology, behaviour or associated factors in shaping species-specific drought responses. Our findings link predictions about the Earth's changing climate to environmental influences on primate mortality risk and thereby improve our understanding of how the increasing severity and frequency of droughts will affect the dynamics and conservation of wild primates.

With expanding anthropogenic disturbances to forests around the world, forest restoration is increasingly important for bird conservation. Restoration monitoring is critical for understanding how birds respond to forest regeneration and for assessing the effectiveness of restoration efforts. Using bioacoustic monitoring, we recorded bird communities during both dry and wet seasons at 62 sites along a chronosequence of tropical dry forests in the Área de Conservación Guanacaste in Costa Rica. Tropical dry forests rank among the globe's most imperiled ecosystems, adding special urgency to their restoration and accompanying restoration monitoring. We found that bird species diversity, richness, and abundance increase with measures of forest maturity. Our results show that bird communities in regenerating areas become more similar to those of undisturbed areas as forests mature. This suggests that bird communities are recovering to predisturbed conditions in regenerating sites, and that maturing tropical dry forests are home to an increasingly diverse and abundant community of birds. We conducted an additional assessment, by sampling 30 locations using point-counts that were originally surveyed 23 years ago. We found that species richness and abundance were similar across this 23-year interval, although bird community composition changed because several forest-specialist species were only detected in the later period. Our research reveals that the regenerating tropical dry forests of northwestern Costa Rica have recovered species richness and abundance levels and are currently undergoing a succession in community composition toward that of a primary tropical dry forest. Our study shows bird communities recovering in a nearly century-old chronosequence of regenerating forests.

Earth's rapidly changing climate creates a growing need to understand how demographic processes in natural populations are affected by climate variability, particularly among organisms threatened by extinction. Long-term, large-scale, and cross-taxon studies of vital rate variation in relation to climate variability can be particularly valuable because they can reveal environmental drivers that affect multiple species over extensive regions. Few such data exist for animals with slow life histories, particularly in the tropics, where climate variation over large-scale space is asynchronous. As our closest relatives, nonhuman primates are especially valuable as a resource to understand the roles of climate variability and climate change in human evolutionary history. Here, we provide the first comprehensive investigation of vital rate variation in relation to climate variability among wild primates. We ask whether primates are sensitive to global changes that are universal (e.g., higher temperature, large-scale climate oscillations) or whether they are more sensitive to global change effects that are local (e.g., more rain in some places), which would complicate predictions of how primates in general will respond to climate change. To address these questions, we use a database of long-term life-history data for natural populations of seven primate species that have been studied for 29-52 years to investigate associations between vital rate variation, local climate variability, and global climate oscillations. Associations between vital rates and climate variability varied among species and depended on the time windows considered, highlighting the importance of temporal scale in detection of such effects. We found strong climate signals in the fertility rates of three species. However, survival, which has a greater impact on population growth, was little affected by climate variability. Thus, we found evidence for demographic buffering of life histories, but also evidence of mechanisms by which climate change could affect the fates of wild primates.

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.

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.

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.

In many mammalian species, philopatric females reside with female kin with whom they form long-lasting cooperative bonds, whereas dispersing males rarely form strong bonds with other males. However, males may have the opportunity to disperse and form long-lasting bonds with paternal male kin in species with high male reproductive skew and parallel male dispersal. We used 54 group-years with demographic and genetic data to investigate how male dispersal and reproductive patterns affected the distribution of male kin in the Santa Rosa white-faced capuchins (Cebus capucinus imitator). During 41 of 54 group-years, there was a high degree of reproductive monopolization by either the alpha or a subordinate male. Natal males often co-resided with paternal brothers of similar age. The likelihood of parallel dispersal from the natal group increased with age similarity and paternal sibship. Some males may possibly gain inclusive fitness benefits by engaging in parallel dispersal and forming long-term cooperative bonds with other males. However, only one of three groups displayed a positive association between male-male relatedness and time spent co-resident in the breeding group. Inbreeding avoidance between alpha males and their daughters also gives subordinate males an opportunity to gain direct fitness benefits and may provide a strong incentive for cooperation among males that are not close kin. These findings suggest that cooperation between related and unrelated males likely evolved due to different reasons. Subordinate males related to the alpha male may gain inclusive fitness benefits, while only unrelated subordinate males gained reproductive opportunities and direct fitness benefits from cooperating.

Popular and scientific interest in menopause in humans has led to an increased interest in the extent of post-fertile life in other animals, particularly in long-lived social species such as other primates and cetaceans. Information on maximum lifespan achieved and age at last birth are available from long-term observations of known individuals from 11 primate species in the wild. Comparable information from wild cetaceans are more difficult to obtain; however there are relevant fisheries data, as well as a small number of long-term individual-based studies. Using post-reproductive representation (PrR) as a population measure of post-fertile lifespan that allows comparisons across populations and species, this review confirms that among primates, only humans have a maximum lifespan significantly longer than 50 years, and only human female life history includes a significant post-fertile stage of life. We conclude that although a prolonged post-fertile stage of life is very rare in mammals, it does occur in some exceptionally long-lived taxa, such as humans and resident killer and short-finned pilot whales. Thus menopause evolved independently at least three times in mammals, and the reasons for its evolution may differ in different lineages.

A keystone individual is defined as an individual that has a disproportionate impact on group dynamics relative to its representation in the population. Here we use over 30 years of behavioural, physiological, paternity, and demographic data collected on the Santa Rosa, Costa Rica, capuchin population to address the question of whether or not alpha male white-faced capuchins (Cebus capucinus imitator) are keystone individuals. Within groups of white-faced capuchins, the alpha male is easily distinguished from other adult males. He is usually of prime age (10–15 years) and often the largest male due to his pronounced secondary sexual characteristics. He is the most central adult male and the recipient of the highest rates of grooming. He is also the most active participant during encounters with predators and extragroup individuals. Using naturally occurring dispersal events, we assess the impact of the removal of an alpha versus subordinate adult male on group dynamics, specifically infant mortality. We found that infant mortality following the removal of an alpha male was more than double the rate observed following the removal of a subordinate adult male. The removal of an alpha male has additional consequences for group success, individual life histories, and population conservation that extend far beyond the immediate aftermath of an alpha male replacement. Based on these findings, we conclude that alpha male white-faced capuchins are keystone individuals, and future research should focus on identifying the factors that enable some males to attain alpha status while others live out their lives as subordinates.

Seasonal variation in food availability and nutritional intake can ultimately affect female reproductive success. Although many primate studies have looked at foraging behaviour as a measure of diet, nutritional ecology and associated physiological consequences are a relatively new area of research. We present data on variation in the dietary profiles, foraging behaviour, and nutritional intake of female white-faced capuchins (Cebus capucinus imitator) in response to temporal variation in food abundance within the home ranges of three groups in the Area de Conservacion Guanacaste, Sector Santa Rosa, Costa Rica. We estimated nutritional requirements based on published laboratory research and nutritional standards to determine whether females meet requirements in the face of seasonal variation in food abundance. Our results show that fruit contributed most to overall energy gain despite females devoting a greater proportion of foraging time to invertebrates; thus time spent foraging does not accurately reflect energy intake. On a dry matter basis, fruits provided the most important source of water-soluble carbohydrates, whereas high proportions of protein intake came from invertebrates, particularly when fruit availability was low. However, the greater weight of fruit items compared to invertebrates on a dry matter basis likely contributed to females’ ability to consume macronutrients at higher rates while foraging on fruit due to higher mass intake per unit time. Requirement estimates and observed intake revealed that there are times during low-fruit seasons in which females do not appear to meet their minimum nutritional requirements, warranting further investigation into the physiological consequences of this shortfall.

The spatial distribution of adult trees is typically not expected to reflect the spatial patterns of primary seed dispersal, due to many factors influencing post-dispersal modification of the seed shadow, such as seed predation, secondary seed dispersal and density-dependent survival. Here, we test the hypothesis that spatial distributions of primary seed shadows and adult trees are concordant by analysing the spatial distributions of adultGenipa americanatrees and the seed shadow produced by its key primary disperser, the capuchin monkey (Cebus capucinus) in a tropical dry forest in Costa Rica. We mapped the dispersal ofG. americanaseeds by the capuchins during focal animal follows (mean = 463 min,n= 50) of all adults in one free-ranging group over two early wet seasons (May–July, 2005 and 2006). We mapped the locations of allG. americanatrees within a 60-ha plot that lay within the home range of the capuchin group. We conducted multiple spatial point pattern analyses comparing degrees of clustering of capuchin defecations andG. americanatrees. We found that adult tree distributions and primary dispersal patterns are similarly aggregated at multiple spatial scales, despite the modification of the primary dispersal patterns and long dispersal distances.

Tropical dry forests are among the world’s most imperiled biomes, and most long-lived and large-bodied animals that inhabit tropical dry forests persist in small, fragmented populations. Long-term monitoring is necessary for understanding the extent to which such populations can cope with changing climate conditions and recover after the elimination of human disturbances. We investigated how conservation measures, local rainfall patterns, and large-scale climate oscillations have affected the population dynamics of white-faced capuchins (Cebus capucinus) in a Costa Rican tropical dry forest over a 42-year period after the elimination of most human disturbances. The population’s rapid initial growth and later stabilization suggests that it was below the habitat’s carrying capacity at the time of the conservation area’s establishment. Management practices, such as aggressive fire suppression, may have played an important role in promoting this growth. Rainfall patterns were strongly coupled with phases and intensity conditions of the El Nino Southern Oscillation. The population experienced two distinct growth phases after the conservation area’s establishment, a period of rapid growth through the 1980s and 1990s and a subsequent period of stability from about 2000 to the present. El Nino-like conditions in the three years preceding a census year were associated with declines in reproductive output and/or offspring mortality during the rapid growth phase. The sensitivity of this ecosystem to global climatic phenomena suggests that some animals will be negatively affected if drought years become more common as the global climate warms.

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. Am J Phys Anthropol, 2015. © 2015 Wiley Periodicals, Inc.

Allonursing is a highly cooperative behaviour that may have important fitness consequences for the infant while the benefits to the allomother are less clear. To investigate the function of this behaviour, we compared patterns of allonursing and nursing exhibited by white-faced capuchin monkeys (Cebus capucinus). We used a linear mixed model approach to analyse data collected on 21 infants from six social groups in Sector Santa Rosa, Costa Rica. Infants nursed at higher rates and for longer durations from their mothers than from allonurses. They also allonursed at higher rates from lactating and non-lactating parous females than from nulliparous females and at higher rates from maternally related female allonurses than other females. We found no observed effect of adult female rank or infant sex. We conclude that infant white-faced capuchins engage in allonursing as a means to acquire additional milk, and that participating allonurses may benefit from increased inclusive fitness.

Intraspecific color vision variation is prevalent among nearly all diurnal monkeys in the neotropics and is seemingly a textbook case of balancing selection acting to maintain genetic polymorphism. Clear foraging advantages to monkeys with trichromatic vision over those with dichromatic "red-green colorblind" vision have been observed in captive studies; however, evidence of trichromatic advantage during close-range foraging has been surprisingly scarce in field studies, perhaps as a result of small sample sizes and strong impacts of environmental or individual variation on foraging performance. To robustly test the effects of color vision type on foraging efficiency in the wild, we conducted an extensive study of dichromatic and trichromatic white-faced capuchin monkeys (Cebus capucinus imitator), controlling for plant-level and monkey-level variables that may affect fruit intake rates. Over the course of 14 months, we collected behavioral data from 72 monkeys in Sector Santa Rosa, Costa Rica. We analyzed 19,043 fruit feeding events within 1,602 foraging bouts across 27 plant species. We find that plant species, color conspicuity category, and monkey age class significantly impact intake rates, while sex does not. When plant species and age are controlled for, we observe that trichromats have higher intake rates than dichromats for plant species with conspicuously colored fruits. This study provides clear evidence of trichromatic advantage in close-range fruit feeding in wild monkeys. Taken together with previous reports of dichromatic advantage for finding cryptic foods, our results illuminate an important aspect of balancing selection maintaining primate opsin polymorphism.

Sex-biased dispersal can reduce kin cooperation and kin competition in the dispersed sex. However, this may not be the case when group-living animals engage in parallel dispersal, which occurs when an individual transfers between groups together with other animals or immigrates alone into a group that contains familiar animals. Despite this potential effect on kin cooperation and competition, few studies have thoroughly investigated how parallel dispersal affects the kin composition of groups. To further our understanding of this topic, we investigated the effect of parallel dispersal on access to coresident kin in male white-faced capuchins, Cebus capucinus. Between 2006 and 2013, we collected demographic and genetic data from two to five groups in Sector Santa Rosa, Costa Rica. We genotyped 41 females and 39 males at 14 short tandem repeat loci, and we calculated their estimated relatedness values. The majority of males dispersed in parallel, and parallel dispersing males were more closely related to one another than were other males. Parallel immigrant males and natal females resided with a similar number of same-sex kin. Single immigrant males in multimale groups rarely resided with male kin, and they resided with fewer same-sex kin than did parallel immigrant males and natal females. Because parallel dispersal offers an opportunity for males to form long-lasting cooperative relationships with familiar kin, this dispersal pattern should be taken into account in future models of the evolution of social structure.

The factors that drive within-species variation in animal space use remain poorly understood. A growing body of evidence suggests that both home range attributes and biological interpretations of the home range may depend fundamentally on the scale of analysis. We utilize a multiscale mixed effects modelling framework to examine how seasonal fluctuations in climate, food resource abundance and group mass affect variance in home range area and the maturity stage of forest used by a group-living Neotropical primate, the white-faced capuchin, Cebus capucinus. Using an 8-year data set representing over 20 000 contact hours, we estimated home ranges for seven social groups at four nested temporal scales and three nested spatial scales using a movement-based kernel method. Group mass was consistently the most important predictor of home range size in our models, and its effects were relatively insensitive to spatial or temporal scale. Mean daily maximum temperature was an influential factor in shaping monthly range area and composition, with hotter weather favouring smaller home range size and increased use of mature evergreen forest. Greater fruit availability was also associated with smaller monthly range area. The effects of temperature and fruit availability were both scale dependent: the impact of both variables was greatest on the core zone. The different study groups showed marked variation in the habitat composition of their home ranges, but in all groups, higher-use zones consisted of older, more evergreen forest. Our study illustrates the complex ecological processes that affect movement behaviour in a Neotropical primate across a range of spatial and temporal scales, highlighting the importance of group mass, climatic seasonality, landscape heterogeneity and dietary shifts in shaping the home range.

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.

Although predation has likely played a central role in the evolution of primate socioecology, we currently lack a thorough understanding of how fine-scale variation in perceived predation risk affects primates’ short-term space use patterns and predator avoidance strategies. We examined the spatial and ecological characteristics of predator encounters, as well as behavioral responses to perceived predation risk, in 5 groups of wild white-faced capuchins (Cebus capucinus) in Costa Rica over a 1.5-year period. Alarm-calling bouts directed at birds were more likely to originate in high forest strata, whereas alarm-calling bouts at snakes and terrestrial quadrupeds were more likely to originate near the ground. Relative risk maps based on the locations of predator encounters revealed that high-risk areas for birds and for all guilds combined consisted of more mature forest, whereas low-risk areas for these predators consisted of relatively younger forest. The animals were most vigilant near the ground, which may reflect greater perceived exposure to snakes and terrestrial predators in lower vertical levels. Incorporating the combined risk function into a predictive model of vigilance behavior improved prediction relative to null models of uniform risk or habitat-specific risk. Our results suggest that capuchin monkeys in this study system perceive reduced predation risk in the high and middle forest layers, and they adjust their vigilance behavior to small-scale spatial variation in perceived risk.

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.

Parasite infections in wildlife are influenced by many factors including host demography, behavior and physiology, climate, habitat characteristics, and parasite biology and ecology. White-faced capuchins (Cebus capucinus) host a suite of gastrointestinal and pulmonary parasites, yet the mechanisms affecting host susceptibility and parasite transmissibility have not been examined in this host species. We used the information-theoretic approach (Akaike's information criterion) and traditional null-hypothesis testing to determine which host characteristics, behaviors, or environmental factors affected the presence of two prevalent capuchin parasites (Filariopsis barretoi and Strongyloides sp.) as well as parasite species richness in four groups of wild capuchins from September 2007 to January 2008 and January to August 2009. Older capuchins were more likely to be infected with Filariopsis barretoi and had higher parasite species richness. Age-biased nematode infections may stem from age differences in capuchin behavior and physiology while high species richness likely results from long- term exposure to numerous parasite species. Infections with Strongyloides sp. were more likely to occur in the dry season when capuchins often descend to the forest floor to drink from terrestrial water sources, potentially increasing their risk of infection from soil-borne larvae. Capuchin behaviors were poor predictors of parasitism, as were female rank, host sex, home range size, and habitat quality. Many of our results were atypical for primate parasitology, suggesting that host-parasite interactions, and subsequently infection risk, may differ in highly seasonal habitats such as tropical dry forests where these monkeys occur.