Universal behaviors as candidate traditions in wild spider monkeys

Candidate traditions were documented across three communities of wild spider monkeys (Ateles geoffroyi) using an a priori approach to identify behavioral variants and a statistical approach to examine differences in their proportional use. This methodology differs from previous studies of animal traditions, which used retrospective data and relied on the 'exclusion method' to identify candidate traditions. Our a priori approach increased the likelihood that behavior variants with equivalent functions were considered and our statistical approach enabled the proportional use of 'universal' behaviors, i.e., used across all communities, to be examined for the first time in any animal species as candidate traditions. Among universal behaviors we found 14 'community preferred' variants. After considering the extent to which community preferred variants were due to ecological and, to a lesser degree, genetic differences, we concluded that at least six were likely maintained through social learning. Our findings have two main implications: (i) tradition repertoires could be larger than assumed from previous studies using the exclusion method; (ii) the relative use of universal behavior variants can reinforce community membership.     

Traditions in monkeys

Traditions, defined as relatively long‐lasting behavioral practices shared among members of a group partly via social learning, were studied in monkeys, specifically Japanese macaques, before being studied in great apes. Although apes and humans may share some social learning capacities that are absent in monkeys, a complete understanding of the roots of human culture requires attention to the socioecological conditions favoring traditions, however generated, in animals generally and in multiple behavioral domains. Using the four criteria of intergroup variation, observation of the origin and spread of a novel behavior, dissemination patterned according to age or kinship, or individuals' close observation of others' performance of the behavior before engaging in it, over twenty‐five behaviors have been nominated as traditions in free‐ranging monkey populations. Tolerant gregariousness has been proposed to increase the likelihood of the emergence of traditions in any behavioral domain. Omnivory and extractive foraging should favor the emergence of foraging‐related traditions; strong cooperative relationships and flexible coalitionary structure should favor the emergence of social conventions that function to test social bonds. These conditions are taxonomically widespread. Thus, the current restriction of most reported free‐ranging monkey traditions to two taxa (Macaca fuscata and Cebus) is likely to reflect variation in primatologists' research goals, methods, and concepts rather than real interspecific variation in the propensity to generate traditions.     

Understanding Behavioral Traditions in Primates: Are Current Experimental Approaches Too Focused on Food?

Recently, several researchers have highlighted the neglect of social behaviors relative to food-related behaviors in experimental research on social learning in primates, despite the significant number of apparent social traditions reported in the field. Here we aim to highlight the discrepancy between the relative number of nonfood-related behavioral traditions reported in the wild and food-related ones, and the almost exclusive investigation of food-related behaviors in an experimental context. First we discuss aspects of social and communicative customs that make them especially interesting. Then we consider reasons why experimental approaches are crucial to developing a full understanding of behavioral traditions observed in the wild. We report the results of a systematic literature survey in which we assessed the perceived discrepancy quantitatively. We also argue that the existing experimental literature, with its typical reliance on food as a motivator, may not be sufficient to elucidate the mechanisms underlying nonfood traditions, such as social conventions. Finally, we suggest new directions for the experimental investigation of social learning in primates, hoping to stimulate experimental research investigating social and communicative behavioral traditions.     

Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus)

Researchers have identified a variety of cross-site differences in the foraging behavior of free-ranging great apes, most notably among chimpanzees (Pan troglodytes) and more recently orangutans (Pongo pygmaeus), that are not due to obvious genetic or ecological differences. These differences are often referred to as "traditions." What is not known is whether this high level of interpopulation variation in behavior is limited to hominoids. In this study, we use long-term data from three Costa Rican field sites that are geographically close and similar ecologically to identify potential foraging traditions in white-faced capuchins (Cebus capucinus). Foraging traditions are predicted in Cebus because of many behavioral and morphological convergences between this genus and the great apes. The processing techniques used for the same food species were compared across sites, and all differences found were classified as present, habitual, or customary. Proximity data were also analyzed to determine if social learning mechanisms could explain variation in foraging behavior. Of the 61 foods compared, we found that 20 of them are processed differently by capuchins across sites. The differences involve pound, rub, tap, "fulcrum," "leaf-wrap," and "army ant following." For most of the differences with enough data to analyze, the average proximity score of the "matched" dyads (two individuals within a group who shared a "different" processing technique) was statistically higher than the average proximity score of the remaining "unmatched" dyads.     

Interspecific Interactions Between Cebus capucinus and Other Species: Data from Three Costa Rican Sites

Capuchins exhibit considerable cross-site variation in domains such as foraging strategy, vocal communication and social interaction. We report interactions between white-faced capuchins (Cebus capucinus) and other species. We present comparative data for 11 groups from 3 sites in Costa Rica that are ecologically similar and geographically close, thus reducing the likelihood that differences are due solely to genetic or ecological differences. Our aim is to document both the range of variation and common elements across sites and situations. We also consider factors that contribute to the variation or consistency or both, including social learning, local ecology, and temperament. We consider 4 categories of allospecifics: (1) vertebrate prey, (2) potential predators, (3) feeding competitors, and (4) neutral species. Although we cannot rule out local differences in ecology, our data suggest that social learning may account for at least some cross-site differences in behavior toward allospecifics. Our strongest finding is that boldness, aggression and pugnacity are displayed consistently across sites, groups and circumstances, even in interactions with neutral species, which reflects a critical aspect of species-specific temperament in Cebus capucinus that has been evolutionarily developed and reinforced through highly opportunistic foraging, strong predator defense, and active hunting. We suggest directions for future research, particularly in regard to primate temperament as an evolved trait with consequences for fitness.     

Can Traditions Emerge from the Interaction of Stimulus Enhancement and Reinforcement Learning? An Experimental Model

The study of social learning in captivity and behavioral traditions in the wild are two burgeoning areas of research, but few empirical studies have tested how learning mechanisms produce emergent patterns of tradition. Studies have examined how social learning mechanisms that are cognitively complex and possessed by few species, such as imitation, result in traditional patterns, yet traditional patterns are also exhibited by species that may not possess such mechanisms. We propose an explicit model of how stimulus enhancement and reinforcement learning could interact to produce traditions. We tested the model experimentally with tufted capuchin monkeys (Cebus apella), which exhibit traditions in the wild but have rarely demonstrated imitative abilities in captive experiments. Monkeys showed both stimulus enhancement learning and a habitual bias to perform whichever behavior first obtained them a reward. These results support our model that simple social learning mechanisms combined with reinforcement can result in traditional patterns of behavior.     

Intra-community infanticide and forced copulation in spider monkeys: a multi-site comparison between Cocha Cashu, Peru and Punta Laguna, Mexico

We describe two cases of infanticide, two suspected infanticides, and a forced copulation by familiar resident males in two populations of wild spider monkeys (Ateles belzebuth chamek and A. geoffroyi yucatanensis). These are the first known infanticides and forced copulation in spider monkeys. Data were gathered from four neighboring communities of spider monkeys in Manu National Park at the Cocha Cashu Biological Station, Peru and two communities in the Otoch Ma'ax Yetel Kooh Reserve at Punta Laguna, Mexico, during intensive field studies of over 2,000 hr each. These are rare behaviors, but results suggest that mating history and sexual coercion are important in spider monkey social relationships.     

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.     

Success-biased social learning: Cultural and evolutionary dynamics

Success bias is a social learning strategy whereby learners tend to acquire the cultural variants of successful individuals. I develop a general model of success-biased social learning for discrete cultural traits with stochastic payoffs, and investigate its dynamics when only two variants are present. I find that success bias inherently favors rare variants, and consequently performs worse than unbiased imitation (i.e. random copying) when success payoffs are at least mildly stochastic and the optimal variant is common. Because of this weakness, success bias fails to replace unbiased imitation in an evolutionary model when selection is fairly weak or when the environment is relatively stable, and sometimes fails to invade at all. I briefly discuss the optimal strength of success bias, the complicated nature of defining success in social learning contexts, and the value of variant frequency as an important source of information to social learners. I conclude with predictions regarding the prevalence of success bias in different behavioral domains.     

Spider Monkeys (Ateles geoffroyi yucatenensis) Cope with the Negative Consequences of Hurricanes Through Changes in Diet, Activity Budget, and Fission–Fusion Dynamics

Hurricanes can bring about dramatic changes to ecosystems and adversely affect animals that live in them. We monitored behavioral responses in wild spider monkeys (Ateles geoffroyi yucatanensis) in the aftermath of two hurricanes (Emily and Wilma) that moved through the Yucatan peninsula in 2005. We predicted that the monkeys would shift their diets depending on relative food availability and experience a change in the distribution of activity patterns. Because spider monkeys’ social organization is characterized by a high degree of fission–fusion dynamics, we predicted they would form smaller subgroups subsequent to the hurricanes to mitigate competition over limited food resources. We compared their responses in the immediate aftermath of Hurricane Emily and across the dry seasons before and after both hurricanes, to control for seasonal changes, by examining their activity budgets, foods consumed, and subgrouping dynamics. In the immediate aftermath of Hurricane Emily spider monkeys spent less time moving and more time feeding on leaves than before the hurricane and they were in smaller subgroups. In the dry season after both hurricanes the monkeys spent more time resting and less time moving than before the hurricanes, and leaves replaced fruit as their primary food resource. They fused into larger subgroups less often and had smaller subgroup sizes in the dry season after than before the hurricanes. Thus, the high degree of fission–fusion dynamics of spider monkeys was instrumental in affording the behavioral flexibility critical to cope with the negative post-hurricane consequences.     

Testing for personality consistency across naturally occurring behavioral contexts in sanctuary chimpanzees (Pan troglodytes)

Personality is both a reflection of the bio-behavioral profile of individuals and a summary of how they typically interact with their physical and social world. Personality is usually defined as having distinct behavioral characteristics, which are assumed to be consistent over time and across contexts. Like other mammals, primates have individual differences in personality. Although temporal consistency is sometimes measured in primates, and contextual consistency is sometimes measured across experimental contexts, it is rare to measure both in the same individuals and outside of experimental settings. Here, we aim to measure both temporal and contextual consistency in chimpanzees, assessing their personality with behavioral observations from naturally occurring contexts (i.e., real-life settings). We measured personality-based behaviors in 22 sanctuary chimpanzees, in the contexts of feeding, affiliation, resting, and solitude, across two time periods, spanning 4 years. Of the 22 behaviors recorded, about 64% were consistent across two to four contexts and 50% were consistent over time. Ten behaviors loaded significantly onto three trait components: explorativeness, boldness-sociability, and anxiety-sociability, as revealed by factor analysis. Like others, we documented individual differences in the personality of chimpanzees based on reliably measured observations in real-life contexts. Furthermore, we demonstrated relatively strong, but not absolute, temporal, and contextual consistency in personality-based behaviors. We also found another aspect of individual differences in personality, specifically, the extent to which individual chimpanzees show consistency. Some individuals showed contextual and temporal consistency, whereas others show significant variation across behaviors, contexts, and/or time. We speculate that the relative degree of consistency in personality may vary within chimpanzees. It may be that different primate species vary in the extent to which individuals show consistency of personality traits. Our behavioral-based assessment can be used with wild populations, increasing the validity of personality studies, facilitating comparative studies and potentially being applicable to conservation efforts.     

Patterns of behavior across reproductive states of free-ranging female black-handed spider monkeys (Ateles geoffroyi)

Reports on the behavior of spider monkeys (genus Ateles) describe a suite of 5-6 behaviors that are indicative of an estrous female. This study presents hormonal data as an independent measure of reproductive state to determine if these behaviors are associated with any particular reproductive state or stage of the ovarian cycle. Fecal samples collected from 6 free-ranging female black-handed spider monkeys (Ateles geoffroyi) over the course of 11 months were assayed for estrogen (E1C) and progesterone (PdG) metabolites, using an enzyme immunoassay. Behavioral data collected from the same females were analyzed for patterns associated with different reproductive states. A more detailed analysis of behavioral data associated with reproductively cycling periods determined whether each behavior clustered with copulations or a particular phase in the ovarian cycle. Observations of place-sniffing were more frequent for 4 of 5 females when reproductively cycling. Of all copulations observed, 80% occurred when the female participant was reproductively cycling. In addition, the rates of self-clitoral hold and self-clitoral rub behaviors were significantly higher for 2 of 4 and 4 of 5 of females, respectively, when reproductively cycling. No behavior consistently occurred in association with copulations or with any particular phase in the ovarian cycle. Results from this study suggest that the behaviors tested in this paper can provide some information regarding female spider monkey reproductive state (whether or not she is reproductively cycling), but that they are not indicators of estrus in female spider monkeys.     

Use of enclosure space by captive lion-tailed macaques (Macaca silenus) housed in Indian zoos

Captive nonhuman animals use enclosure space differentially. Enclosure features strongly influence this. This study recorded both the enclosure space used by 47 captive lion-tailed macaques housed in 13 zoos across India and the behavior of the macaques. The exhibition of abnormal behaviors, food-related behaviors, and social interactions correlated significantly with the use of the edge zone (the part of the enclosure closest to the visitor area). Animals housed in barren enclosures used the edge zone to a significantly greater percentage than did those housed in complex exhibits. Percentages of autogrooming, social interactions, and food-related behaviors significantly correlated with the use of the enrich zone. Space use studies assist in recognizing areas within the enclosure, which captive animals actively use. Conversely, the studies can identify areas infrequently used and show how to make maximum use of these enclosure areas. Further studies targeting both the increase in percentages of natural behaviors exhibited and use of the enrich zone used the current study on captive lion-tailed macaques for their design.     

Nature Needs Nurture: The Interaction of Hormonal and Social Influences on the Development of Behavioral Sex Differences in Rhesus Monkeys

Thirty years of research on early social and hormonal environments and their relationship to the expression of behavioral sex differences in rhesus monkeys are reviewed. These studies demonstrate that whether aggressive and submissive behaviors are sexually dimorphic depends primarily on the social and not the hormonal environment. Early rearing environments without mothers or allowing brief periods of peer interaction produced higher levels of male aggression and female submission. Presenting behavior was expressed more by females than males in environments with high male aggressivity and female submissiveness. No sex differences in presenting occurred in low aggressivity environments, unless monkeys were reared isosexually, when males presented more than females. Rough and tumble play and foot-clasp mounting were consistently exhibited more by males than females across all rearing environments studied, but rearing environment affected the degree of the sex difference. When reared isosexually males displayed less, and females more, foot-clasp mounting than when heterosexually reared. No social environment increased the low frequency of female rough and tumble play. Suppressing neonatal androgen in males did not effect any sexually dimorphic behavior. Prenatal androgen administration to genetic females masculinized many aspects of their juvenile behavior, consistently increasing rough and tumble play and foot-clasp mounting across different social environments. Thus the sexually dimorphic behaviors which showed the smallest variability across social contexts were the most profoundly affected by the prenatal hormonal environment. These studies demonstrate that the expression of consistent juvenile behavioral sex differences results from hormonally induced predispositions to engage in specific patterns of juvenile behavior whose expression is shaped by the specific social environment experienced by the developing monkey.     

Stress in Yucatan spider monkeys: effects of environmental conditions on fecal cortisol levels in wild and captive populations

In the Yucatán Peninsula, spider monkeys Ateles geoffroyi yucatanensis are generally found in two contrasting conditions: large tracts of conserved forest or small fragments surrounded by human populations. In the present study, we analyzed fecal cortisol levels of spider monkeys to investigate whether environmental conditions have an influence on stress; specifically, we compared fecal cortisol across individuals living in conserved forests, fragmented forests and captive conditions (zoos and pets). Radioimmunoanalysis of fecal samples from 121 individuals indicated significant differences in mean cortisol for A. g. yucatanensis based on habitat type, with the lowest levels found in the conserved forest condition. The higher cortisol levels in both fragmented forest populations and in captive individuals may be the result of metabolic and behavioral stress. The mean male fecal cortisol concentration was significantly higher than that of females, and the fecal cortisol concentration was higher in the dry season compared with the wet season in a conserved habitat. Therefore, we emphasize the importance of considering sex and seasonality when monitoring fecal cortisol concentrations of spider monkeys, and more generally of frugivores, as they face a seasonal variation in food availability. Finally, our results suggest that forest fragmentation may create long-term stressors for spider monkeys, affecting the viability of populations living under such conditions.     

Quantitative trait locus mapping and analysis of heritable variation in affiliative social behavior and co‐occurring traits

Humans exhibit broad heterogeneity in affiliative social behavior. Twin and family studies show that individual differences in core dimensions of social behavior are heritable, yet there are knowledge gaps in understanding the underlying genetic and neurobiological mechanisms. Animal genetic reference panels (GRPs) provide a tractable strategy for examining the behavioral and genetic architecture of complex traits. Here, using males from 50 mouse strains from the BXD GRP, 4 domains of affiliative social behavior—social approach, social recognition, direct social interaction (DSI) (partner sniffing) and vocal communication—were examined in 2 widely used behavioral tasks—the 3‐chamber and DSI tasks. There was continuous and broad variation in social and nonsocial traits, with moderate to high heritability of social approach sniff preference (0.31), ultrasonic vocalization (USV) count (0.39), partner sniffing (0.51), locomotor activity (0.54‐0.66) and anxiety‐like behavior (0.36). Principal component analysis shows that variation in social and nonsocial traits are attributable to 5 independent factors. Genome‐wide mapping identified significant quantitative trait loci for USV count on chromosome (Chr) 18 and locomotor activity on Chr X, with suggestive loci and candidate quantitative trait genes identified for all traits with one notable exception—partner sniffing in the DSI task. The results show heritable variation in sociability, which is independent of variation in activity and anxiety‐like traits. In addition, a highly heritable and ethological domain of affiliative sociability—partner sniffing—appears highly polygenic. These findings establish a basis for identifying functional natural variants, leading to a new understanding typical and atypical sociability.     

Disparate Data Sets Resolve Squirrel Monkey (Saimiri) Taxonomy: Implications for Behavioral Ecology and Biomedical Usage

Squirrel monkeys (Saimiri spp.) are the most commonly used neotropical (platyrrhine) monkeys in biomedical research; however, no consensus exists as to the phylogenetic relationships amongst geographic variants or whether these variants represent species or subspecies. Here we report a strongly supported squirrel monkey phylogeny, congruent across multiple data sets, including new field data and the first molecular (mtDNA) cladogram. These data support species-level classification for the three major groups in this study. Approximately the same amount of molecular divergence exists among Saimiri oerstedii, S. sciureus, and S. boliviensis. The S. sciureus/S. oerstedii ancestor diverged from S. boliviensis and shortly thereafter S. sciureus and S. oerstedii diverged. Until now, lack of a robust taxonomy has hindered exploitation of the massive potential of Saimiri for comparative studies. No other primate genus displays such widely divergent, genetically-based social behaviors. Our taxonomy also provides robust support for previous warnings against the widespread use of hybrid squirrel monkeys as research models.     

Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions

Here we review all published articles and book chapters, as well as unpublished theses and data of Ateles geoffroyi diet to (1) summarize the literature; (2) synthesize general feeding patterns; (3) document plant taxonomic similarity in diet across study sites; and (4) suggest directions for future research and conservation priorities. We found 22 samples from five countries: Mexico, Guatemala, El Salvador, Costa Rica and Panama. Tropical wet forest is the most studied habitat (N=13 samples), followed by tropical dry forest (6) and tropical moist forest (3). Most samples have been carried out in large protected forests. In spite of showing an overall high dietetic diversity (364 species, 76 families), A. geoffroyi concentrated the majority of feeding time on a few species in the families Moraceae and Fabaceae. At all study sites fruits were the most common food item in the diet followed by leaves. Furthermore, a greater variety of food items and less fruit were consumed in forest fragments. These findings suggest that fruit shortage in fragments results in primates using foods of presumably lower energetic content such as leaves. Similarity in diet was higher among groups geographically closer to each other than among distant groups, showing that the floristic and phenological characteristics of the forest can influence diet composition. We conclude that several years of data are required to fully describe the dietary list of A. geoffroyi at any one site, as studies of the same group over different years shared as little as 56% of species. As most populations of A. geoffroyi live in highly fragmented landscapes, it is crucial to carry out studies in these areas to evaluate (1) changes in diet and activity patterns that may negatively affect survival; and (2) habitat attributes that may favor their persistence in altered landscapes.     

Food Transfer in Sichuan Snub-nosed Monkeys (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>)

Food transfer behavior provides a way to distribute food resources among individuals. It is not confined to kin, but also occurs among genetically unrelated individuals. Food transfer among nonkin may result from byproduct mutualism, reciprocal altruism (RA), or tolerated scrounging (TS). Sichuan snub-nosed monkeys (Rhinopithecus roxellana) exhibit a high level of social tolerance, and researchers have observed food transfer behavior in the wild. However, little is known about how tolerant social relations influence food transfer in this species. We recorded food-related interactions and social behavior in a group of captive Sichuan snub-nosed monkeys. Our findings suggest that the monkeys develop partner preference in food transfer behaviors. Moreover, individuals rely primarily on nonharassed approaches to claim food, suggesting that the TS model alone cannot explain their food transfer. Food transfer in this species may be a form of mutualism, in which an individual benefits on an immediate basis by fostering a preferred and tolerant relationship. However, we cannot rule out the possibility of reciprocal altruism. Future studies should record the temporal delay of social exchange to distinguish between mutualism and reciprocal altruism.