Variability in food-processing behavior among white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica

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

Growth of Mantled Howler Groups in a Regenerating Costa Rican Dry Forest

We examined population dynamics in mantled howlers (Alouatta palliata palliata) in a regenerating tropical dry forest in Santa Rosa National Park (SRNP), Costa Rica. The population has grown at a rate of about 7% per annum during the past decade. The growth in numbers from 342 in 1984 to 554 in 1992 reflects an increase in the number of groups (from 25 to 34) and a slight increase in their average size (from 13.6 to 16.3). Population density has increased from 4.9 to 7.9 individuals per km ². Santa Rosa's population density and group compositions are similar to those at several other mantled howler sites, but densities of mantled howlers are much higher at two other well-studied sites: La Pacifica and Barro Colorado Island (BCI). We relate the low density of howlers at Santa Rosa to local historical and ecological factors. Howler populations at high and low densities differ in average group size and sex ratio. At high population densities, groups are larger and include more adult females. The number of male howlers per group appears to be more strictly limited and less variable than the number of females is. However, there is greater variation in male group membership at Santa Rosa than at La Pacifica or BCI, and at Santa Rosa there are more generating forests available into which males and females can disperse and form new groups. We present case studies describing two ways in which new howler groups are formed, and we suggest that, compared to females and compared to males at high density sites, males are relatively advantaged in the uncrowded habitats at Santa Rosa and other low density sites.     

Two girls for every boy: The effects of group size and composition on the reproductive success of male and female white-faced capuchins

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

Spatial Patterns of Seed Dispersal by White-Faced Capuchins in Costa Rica: Evaluating Distant-Dependent Seed Mortality

Spatial patterns of seed dispersal are the focus of numerous theoretical examinations of endozoochory. Here, we examine the spatial pattern of seed dispersal by white-faced capuchin monkeys Cebus capucinus in Santa Rosa National Park, Costa Rica, and the neighborhood characteristics and distance variables most closely associated with seed survival and germination, and seedling survival and growth in various locations. Overall, distance to the nearest fruiting conspecific tree has the most positive, consistent effect on growth and survival variables, which supports a variation of the Janzen–Connell seed escape hypothesis.     

Dominance style of female white‐faced capuchins

Dominance style, the level of tolerance displayed by dominant individuals toward subordinate ones, is exhibited along a continuum from despotic to relaxed. It is a useful concept to describe the nature of dominance relationships in macaque species and it bridges among multiple features of dominance hierarchies, aggression, kinship and conflict resolution. Capuchins share many behavioral similarities with Old World monkeys and like macaques, may exhibit a suite of covarying characteristics related to dominance. Here, we provide an assessment of dominance style by examining measures of aggression and kin bias in 22 adult female white‐faced capuchin monkeys (Cebus capucinus) in three social groups at Santa Rosa Sector, Costa Rica. We found that bidirectionality of aggression was low (mean = 6.9% ± SE 1.6). However, there were few significant correlations between kin relatedness and social behavior (approaching, grooming, proximity, and co‐feeding), even though the intensity of kin bias in grooming was moderate and higher in the larger group. We conclude that patterns of aggression and kin‐biased behavior in our study animals are dissimilar to the patterns of covariation observed in macaque species. While unidirectional aggression suggests a despotic dominance style, the moderate expression of kin bias suggests an intermediate to relaxed classification when compared with results from an analysis of 19 macaque species. Additional studies of capuchin species and behaviors associated with dominance style (i.e., conciliatory tendencies) would help to create a comparative framework for the genus Cebus, and allow for more detailed cross‐species comparison of dominance relationships across all primates. Am J Phys Anthropol 150:591–601, 2013. © 2013 Wiley Periodicals, Inc.     

Drought Impacts Survivorship and Reproductive Strategies of an Epiphyllous Leafy Liverwort in Central Amazonia

Understanding how changing precipitation patterns impact the population dynamics of Amazonian plants is necessary for predicting their long‐term survival. Most terrestrial plants are characterized by life cycles intractably slow for evaluating such demographic consequences. Due to the demands of surviving on an ephemeral substrate such as a leaf surface, epiphyllous (leaf‐inhabiting) bryophytes have some of the fastest generation times for terrestrial plants. Considering these advantages, we investigated the demographic consequences of seasonality in precipitation during one‐year of the epiphyllous bryophyte Radula flaccida Gott. (Radulaceae) in a central Amazonian rain forest. In a 1‐ha sized study area, 154 epiphyll colonies from 18 phorophytes of the understory shrub Naucleopsis ulei (Warb.) Ducke (Moraceae) were marked and colony growth, extinction, recolonization, as well as rates of sexual and asexual expression were measured in nine demographic censuses. The probability of survivorship decreased in the dry season due to the synergistic effects of both increased leaf fall (e.g., loss of occupied patches) and colony mortality on persisting leaves. Asexual expression also declined significantly during the driest months; however, sexual expression, as measured by sporophyte density, was not related to seasonality. Logistic regression probabilities also indicate a minimum threshold colony size for optimal sporophyte expression. Lower survivorship and colony growth in the dry season along with reduced sporophyte production in smaller colonies implies that both demographic stability as well as population structure of Amazonian epiphyll species may be compromised whether climate models projecting prolonged droughts for the region are accurate.     

Begging and transfer of coati meat by white-faced capuchin monkeys,Cebus capucinus

White-faced capuchin monkeys were frequently observed to raid the nests and predate the pups of coatis at two study sites (Santa Rosa National Park and Lomas Barbudal Biological Reserve) in northwestern Costa Rica. Adult monkeys of both sexes were the primary participants in nest-raiding. At Santa Rosa, the original captor of the pup tended to eat the entire carcass, whereas at Lomas Barbudal, the monkeys rapidly became satiated and allowed another monkey to have the carcass. At Lomas Barbudal, there was a tendency for adult females to share preferentially with their own offspring, but only if the offspring were less than 1 year old. Dominance rank of the owner of the carcass relative to the rank of the beggar did not significantly affect the probability of willingly transferring meat to the beggar. In one of two years, carcass theft was more likely to occur when the thief was higher ranking than the carcass owner.     

Male dispersal patterns in white-faced capuchins, Cebus capucinus: Part 1: patterns and causes of natal emigration

This is the first of two papers examining male dispersal patterns in white-faced capuchins. Our study was based on behavioural and demographic data collected on multiple groups of white-faced capuchins in Santa Rosa National Park, Costa Rica since 1985. Here we examine the patterns and proximate causation of male natal dispersal. Natal dispersal in white-faced capuchins occurred at a median age of 4.5 years, with no males remaining in the natal group past 8 years. Initial departure from the natal group appeared to be in response to an attraction to extragroup males and dispersing groupmates. Rates of parallel dispersal (dispersal with co-resident males and/or into groups containing familiar males) were very high for natal males (71-82%), and this pattern of dispersal may have evolved to increase inclusive fitness benefits in male-dispersed species. Additionally, this pattern of dispersal probably increases survivorship among dispersing males who are not yet physically mature, as is common in white-faced capuchins.     

A comparison of sex ratio,birth periods and calf survival among Serengeti wildebeest sub‐populations,Tanzania

Although adaptation and environmental conditions can easily predict demographic variation in most savannah ungulates, no study on demographic consequences arising from natural and anthropogenic factors among Serengeti wildebeest (Connochaetes taurinus) sub‐populations in Tanzania has been carried out. Here, I report estimates of annual sex ratio, calf and yearling survival rate and birth seasonality between resident and migratory sub‐populations to explore demographic patterns arising from the different age and sex structure. The results indicate significantly higher female‐biased sex ratios in the resident and almost even sex ratios among individual migrants. The calf recruitment estimated as mother: offspring ratios indicate a more synchronous birth in the migrant than the resident sub‐population. Also, birth seasonality in the migratory sub‐population coincided with seasonal variability of rainfall and the timing of the birth peak was more variable in the migrants than the resident sub‐population. The migratory sub‐population had a higher annual proportional mean calf survival estimate (0.84) than that of the residents (0.44) probably due to higher mortality resulting from predation in the western corridor. However, the proportion of yearling survival estimates was much lower (0.31) in the migrants and relatively higher (0.39) in the residents. Different demographic outcomes resulting from environment, predation, movements and ecological factors including resource competition have conservation implications for the two sub‐populations.     

Neotropical Primates in a Regenerating Costa Rican Dry Forest: A Comparison of Howler and Capuchin Population Patterns

Few data exist on how primate populations return to regenerating tropical forests. We compare the ways that two populations of neotropical monkeys, Alouatta palliata and Cebus capucinus, expanded over a 28-year period after the establishment of Santa Rosa National Park on reclaimed ranchlands in Costa Rica. We found that both howler and capuchin populations increased substantially in size subsequent to protection, but the howler population grew faster. This is likely due to their faster-paced life-history pattern than that of capuchins. The howler population increased mainly via the establishment of many new groups, whereas the capuchins expanded mainly by increasing the size of existing groups. We related this finding to the fact that capuchins are limited largely by their need to drink from water holes during the dry seasons whereas howlers are limited principally by their preference for larger-sized trees that occur in older forests. Proportions of adult male capuchins increased significantly during our study, likely due to skewed sex ratio at birth or male-biased immigration into the protected park or both factors. Our main finding is that, in as short a time period as 28 years, we can substantially enhance the size of monkey populations by allowing the regeneration of tropical forest. Furthermore, we provide a preliminary interpretation of how extrinsic factors—deforestation, hunting, crop-spraying, destruction of the watershed—and intrinsic variables, e.g., pace of reproduction; diet, differentially affect not only each species' vulnerability to extinction but also its capacity to recover when human disturbances are minimized.     

Color-vision polymorphism in wild capuchins (Cebus capucinus) and spider monkeys (Ateles geoffroyi) in Costa Rica

New World monkeys are unique in exhibiting a color-vision polymorphism due to an allelic variation of the red-green visual pigment gene. This makes these monkeys excellent subjects for studying the adaptive evolution of the visual system from both molecular and ecological viewpoints. However, the allele frequencies of the pigments within a natural population have not been well investigated. As a first step toward understanding the relationship between vision and behavior, we conducted color-vision typing by analyzing fecal DNA from two wild groups of white-faced capuchin monkeys (Cebus capucinus) and one group of black-handed spider monkeys (Ateles geoffroyi) inhabiting Santa Rosa National Park of Costa Rica. All color-typed monkeys were individually identified. In C. capucinus and A. geoffroyi we found three and two pigment types, respectively, and the spectral mechanism that created one of the two Ateles pigments was found to be novel. In one Cebus group and the Ateles group, all alleles were present, whereas in the other Cebus group only two alleles were found, with one allele predominating. This was likely due to the effect of close inbreeding, indicating that wild populations can exhibit a variety of allele compositions. This result also suggests that the color-vision polymorphism can be easily distorted by natural factors, such as inbreeding, skewing the population structure.     

Demographic consequences of habitat loss and crowding in large carnivores: A natural experiment

Habitat loss is one of largest threats to the persistence of large carnivore populations. However, because most large carnivores are long‐lived, cryptic and wide‐ranging, few studies examine the demographic consequences of habitat loss, and the resultant crowding that ensues, on these species. We used long‐term data to examine the demographic responses of an African lion (Panthera leo) population to flooding‐induced habitat loss in a seasonal wetland, the Okavango Delta, during a transition from low to high annual flooding patterns. We found that intraspecific competition reduced cub survival and that this effect was exacerbated by habitat loss and consequent crowding. The proportion of cubs recorded in the population also declined as crowding increased, and both the survival of cubs and proportion of cubs recorded declined as prey abundance decreased. Apparent sub‐adult survival declined with increasing pride size, but this likely reflects emigration rather than mortality. Adult survival remained relatively constant throughout the study period, a population response which is important in buffering populations against short‐term fluctuations in ecological conditions. As many large carnivore populations face future habitat loss, it is important that we understand the demographic consequences of habitat loss in order to better mitigate its effects in the future.     

The elephant population of Samburu and Buffalo Springs National Reserves, Kenya

A 21‐month individual identification project on the Samburu and Buffalo Springs National Reserves' elephant population was conducted between November 1997 and July 1999. The free ranging population, of at least 767 elephants, which relied heavily on areas outside the reserves, was individually identified. The numbers of elephants observed per day fluctuated but were greater during dry periods then wet. However, the sizes of aggregations were greater during wet periods. Preliminary investigation suggested that the population could be divided into two groups, which were designated resident and non‐resident family units. The groups comprised approximately equal numbers of cows and calves, but temporally had different reserve use patterns and calving peaks. The daily numbers of males and musth males were correlated with numbers of females. The reserves appeared to be a focal area for calving, indicating that the study area was of reproductive importance to the population. Demographic data indicated a female biased population sex ratio, with over twice the number of mature females to males. The observed sex skew was greatest for older age classes, and the density of musth bulls in the study area was low. The population was affected by poaching. Continued monitoring will assist conservation efforts by alerting authorities of major demographic or range use changes.     

Sex differences in diet and foraging behavior in white-faced capuchins (Cebus capucinus)

I examined sex differences in diet and foraging behavior in two groups of white-faced capuchin monkeys (Cebus capucinus)in a tropical dry forest at Santa Rosa National Park, Costa Rica. I tested three hypotheses: sex differences in diet and foraging behavior are best explained by (1) sexual dimorphism, (2) the energy demands of pregnancy and lactation for females;and (3) avoidance of competition between the sexes. Sexual dimorphism offered the best explanation of sex differences in the diet and foraging behavior of C. capucinus,accurately predicting that males do more strenuous foraging activity, make less use of small foraging supports, and spend more time on or near the ground. Females spent more time foraging than males did but probably obtained a lower protein yield per unit foraging time. Females exploited more small and embedded invertebrates, while males ate more large invertebrates and vertebrate prey. Pregnant and lactating females spent more time resting and less time foraging than other females did, increasing their foraging return by focusing on foods requiring little handling. There was little evidence of competition avoidance between the sexes.     

The rise and fall of local populations of ortolan buntings Emberiza hortulana: importance of movements of adult males

Changes in population size of local populations of birds have usually been interpreted in relation to adult return rate and recruitment of young individuals after natal dispersal. Little is known about the importance of redistribution of adult individuals through breeding dispersal. The small Norwegian population of ortolan buntings Emberiza hortulana has a patchy distribution with about 30 long‐term local populations. During a period of general population decline (29% decrease over 7 years), the population trends of local populations (measured as number of males recorded) were highly variable, with some even increasing four‐fold. Comparisons of demographic parameters showed that adult immigration rate (i.e. dispersal of adult males) explained both yearly changes in male population size and population trends over the whole study period better than adult return rate or adult emigration rate, or a measure of recruitment of young males. Adult immigration rates and recruitment rates were correlated, suggesting that both young and adult males find the same places attractive. In the study area, adult sex ratio was strongly male‐biased, and immigration rate was higher when local sex ratio was less skewed. In addition, less skewed sex ratio was related to higher adult return rate and lower emigration rate. We found no relationships between measures of breeding success and population change. We suggest that conspecific attraction may explain the observed patterns. Some local populations may act as hot‐spots attracting adult males from other populations. Thus, local population changes need not reflect overall population growth rate, but may be a consequence of redistribution of adult birds.     

Evaluating social influences on food-processing behavior in white-faced capuchins (Cebus capucinus)

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

A demographic model for sex ratio evolution and the effects of sex‐biased offspring costs

The evolution of the primary sex ratio, the proportion of male births in an individual's offspring production strategy, is a frequency‐dependent process that selects against the more common sex. Because reproduction is shaped by the entire life cycle, sex ratio theory would benefit from explicitly two‐sex models that include some form of life cycle structure. We present a demographic approach to sex ratio evolution that combines adaptive dynamics with nonlinear matrix population models. We also determine the evolutionary and convergence stability of singular strategies using matrix calculus. These methods allow the incorporation of any population structure, including multiple sexes and stages, into evolutionary projections. Using this framework, we compare how four different interpretations of sex‐biased offspring costs affect sex ratio evolution. We find that demographic differences affect evolutionary outcomes and that, contrary to prior belief, sex‐biased mortality after parental investment can bias the primary sex ratio (but not the corresponding reproductive value ratio). These results differ qualitatively from the widely held conclusions of previous models that neglect demographic structure.     

Sex Allocation in a Colobine Monkey

In polygynous, sexual dimorphic species with higher variance in male reproductive success compared with females, females are expected to invest more heavily in sons than daughters within the constraints imposed by their physical condition (Science 1973; 179:90). Mothers in good condition, usually those of high rank, should produce more sons than females in poor condition or of low rank. We investigated sex allocation and sex‐biased maternal investment in a population of wild Hanuman langurs using rank and group size as approximations of female physical condition. Our results show that reproductive costs of sons were higher with both significantly longer interbirth intervals following male births and longer lactational periods for sons. Not in all groups did analyses of rank‐dependent sex allocation reveal the expected pattern of high‐ranking mothers producing more sons. However, sex ratio was significantly influenced by group size, with females from larger groups, i.e., in worse physical condition, producing a daughter‐biased sex ratio. In fact, only females of population‐wide superior physical condition can be expected to produce sons, because in Hanuman langurs males disperse and compete population‐wide. Thus, our results support the Trivers–Willard model and may explain the mixed evidence accruing from studies of single groups. We present a graphical model of how group size and dominance‐related differences in energy gain may influence sex allocation under different competitive regimes relative to overall resource availability. Tests of adaptive sex allocation models should consider whether reproductive competition of the preferred sex takes place primarily within a group or within the population.     

Social structure of Atlantic spotted dolphins,Stenella frontalis,following environmental disturbance and demographic changes

Extreme environmental events and demographic changes can have variable effects on the social structure of animal populations. This study compared the social structure of a community of Atlantic spotted dolphins in the Bahamas before and after two hurricanes. Approximately 36% of the individuals were lost, with no subsequent increase in immigration. The majority of the social structure characteristics were consistent with results from a long‐term study covering the previous 12 yr, including community structure with definitive social clusters, sex preferences and overall association patterns. However some changes occurred, though still constrained within sex preferences. Posthurricane there was a decrease in social differentiation and increased cohesion within clusters and across age class. Males retained or made new first order alliances, however, only one second order alliance was evident, revealing a simplified alliance structure. Juvenile individuals made alliance level associations, unprecedented from long‐term analysis. Although other studies have shown stark restructuring, this study showed that less drastic changes within overall social structure stability can occur. Persistence and evolutionary changes in populations through environmental and/or demographic perturbations may depend on the social structure of a population or community. Understanding the processes involved in social development is paramount for conservation of diverse populations.     

Frequency‐dependent selection acting on the widely fluctuating sex ratio of the aphid Prociphilus oriens

Frequency‐dependent selection is a fundamental principle of adaptive sex ratio evolution in all sex ratio theories but has rarely been detected in the wild. Through long‐term censuses, we confirmed large fluctuations in the population sex ratio of the aphid Prociphilus oriens and detected frequency‐dependent selection acting on these fluctuations. Fluctuations in the population sex ratio were partly attributable to climatic factors during the growing season. Climatic factors likely affected the growth conditions of host plants, which in turn led to yearly fluctuations in maternal conditions and sex ratios. In the process of frequency‐dependent selection, female proportion higher or lower than ca. 60% was associated with a reduction or increase in female proportion, respectively, the next year. The rearing of aphid clones in the laboratory indicated that mothers of each clone produced an increasing number of females as maternal size increased. However, the mean male number was not related to maternal size, but varied largely among clones. Given genetic variance in the ability to produce males among clones, selection should favour clones that can produce more numerous males in years with a high female proportion. Population‐level sex allocation to females was on average 71%–73% for three localities and more female‐biased when maternal conditions were better. This tendency was accounted for by the hypothesis of competition among foundresses rather than the hypothesis of local mate competition. We conclude that despite consistent operation of frequency‐dependent selection, the sex ratio continues to fluctuate because environmental conditions always push it away from equilibrium.