Female reproductive aging in seven primate species: Patterns and consequences.

Age-related changes in fertility have increasingly been documented in wild animal populations: In many species the youngest and oldest reproducers are disadvantaged relative to prime adults. How do these effects evolve, and what explains their diversity across species? Tackling this question requires detailed data on patterns of age-related reproductive performance in multiple animal species. Here, we compare patterns and consequences of age-related changes in female reproductive performance in seven primate populations that have been subjects of long-term continuous study for 29 to 57 y. We document evidence of age effects on fertility and on offspring performance in most, but not all, of these primate species. Specifically, females of six species showed longer interbirth intervals in the oldest age classes, youngest age classes, or both, and the oldest females also showed relatively fewer completed interbirth intervals. In addition, five species showed markedly lower survival among offspring born to the oldest mothers, and two species showed reduced survival for offspring born to both the youngest and the oldest mothers. In contrast, we found mixed evidence that maternal age affects the age at which daughters first reproduce: Only in muriquis and to some extent in chimpanzees, the only two species with female-biased dispersal, did relatively young mothers produce daughters that tended to have earlier first reproduction. Our findings demonstrate shared patterns as well as contrasts in age-related changes in female fertility across species of nonhuman primates and highlight species-specific behavior and life-history patterns as possible explanations for species-level differences.

Factors influencing terrestriality in primates of the Americas and Madagascar.

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.

Maternal death and offspring fitness in multiple wild primates.

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 life span. 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 immediately preceding maternal 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.

Mothers of disabled infants had higher cortisol levels in a free-ranging group of Japanese macaques (Macaca fuscata).

Glucocorticoids (GCs) are hormones released in response to stressors and can provide insight into an organism's physiological well-being. Experiencing chronic challenges to homeostasis is associated with significant deviations from baseline fecal GCs (fGCs) in many species, providing a noninvasive biomarker for assessing stress. In the group of free-ranging Japanese macaques (Macaca fuscata) at the Awajishima Monkey Center in Japan, ~17% have congenital limb malformations. We collected 646 fecal samples from 27 females over three consecutive birth seasons (May-August) and analyzed them using enzyme immunoassay to extract fGCs. We explored the relationship between fGC levels and individual (physical impairment and reproductive status), social (dominance rank and availability of kin for social support), and ecological variables (exposure to potential predators, rainfall, and wild fruit availability). A disabled infant was associated significantly with higher fGC in the mother; however, physical impairment in adult females was not significantly related to fGC levels. Females with higher dominance rank had significantly lower fGC levels than lower ranking females. Other factors did not relate significantly to fGC. These results suggest that providing care that meets the support needs of disabled infants poses a physiological challenge for mothers and suggests that physically impaired adults are able to effectively compensate for their disabilities with behavioral plasticity. Once an individual with congenital limb malformations survives infancy through their mother's care, physical impairment does not appear to influence fGC values, while social variables like dominance rank significantly influenced cortisol values in free-ranging female Japanese macaques.

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

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

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

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

Trichromacy increases fruit intake rates of wild capuchins (Cebus capucinus imitator).

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.

Female sociality and sexual conflict shape offspring survival in a Neotropical primate.

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.

The nutritional importance of invertebrates to female Cebus capucinus imitator in a highly seasonal tropical dry forest.

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.

Group versus population level demographics: An analysis of comparability using long term data on wild white-faced capuchin monkeys (Cebus capucinus imitator).

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.

The emergence of longevous populations.

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.

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator).

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.

Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species.

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.

Using urinary parameters to estimate seasonal variation in the physical condition of female white-faced capuchin monkeys (Cebus capucinus imitator).

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.

Infant mortality in white-faced capuchins: The impact of alpha male replacements.

Infanticide is common in the context of alpha male replacements (AMR), particularly in groups where alpha males experience high reproductive skew and the infants are unlikely to be related to a new alpha male. We examined the relationship between the rate of infant mortality, infant age, and the occurrence and type of AMR in white-faced capuchin monkeys (Cebus capucinus imitator) of the Santa Rosa population in Sector Santa Rosa, Área de Conservación Guanacaste. Specifically, we investigated how the source of the new alpha male (coresident or extragroup) and relative aggression level during AMRs influenced infant mortality in this species. Between 1986 and 2015, we recorded 221 births in five study groups. Infants present at the time of an AMR, or born within 5.5 months following an AMR (i.e., conceived prior to AMR), experienced significantly higher mortality than those born during periods of group stability. Infant age was a significant predictor of infant survival, with the probability of surviving increasing by 0.4% for each additional day older an infant was at the time of the AMR. Infant mortality rates did not differ between AMRs by coresident males and extragroup males, possibly because the degree of relatedness between infants and new alphas did not significantly differ between coresident and extragroup AMRs. Infant mortality rates did not differ significantly between aggressive AMRs and more peaceful AMRs. Our results are consistent with predictions derived from the sexual selection hypothesis (SSH) of infanticide and suggest that future studies examine the role of testosterone as an underlying proximate mechanism for the aggression leading to this behavior. We argue that the sexual selection and generalized aggression hypotheses (GAH) of infanticide are best considered as different levels of analysis rather than competing hypotheses.

Seasonal importance of flowers to Costa Rican capuchins (Cebus capucinus imitator): Implications for plant and primate.

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

Male endocrine response to seasonally varying environmental and social factors in a neotropical primate, Cebus capucinus.

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.

Paternal kin recognition and infant care in white-faced capuchins (Cebus capucinus).

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 aging patterns in primates reveal that humans are distinct.

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.

Quantifying seasonal fallback on invertebrates, pith, and bromeliad leaves by white-faced capuchin monkeys (Cebus capucinus) in a tropical dry forest.

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.