A new approach to geostatistical synthesis of historical records reveals capuchin spatial responses to climate and demographic change.

Recent proliferation of GPS technology has transformed animal movement research. Yet, time-series data from this recent technology rarely span beyond a decade, constraining longitudinal research. Long-term field sites hold valuable historic animal location records, including hand-drawn maps and semantic descriptions. Here, we introduce a generalised workflow for converting such records into reliable location data to estimate home ranges, using 30 years of sleep-site data from 11 white-faced capuchin (Cebus imitator) groups in Costa Rica. Our findings illustrate that historic sleep locations can reliably recover home range size and geometry. We showcase the opportunity our approach presents to resolve open questions that can only be addressed with very long-term data, examining how home ranges are affected by climate cycles and demographic change. We urge researchers to translate historical records into usable movement data before this knowledge is lost; it is essential to understanding how animals are responding to our changing world.

Mother of all bonds: Influences on spatial association across the lifespan in capuchins.

In humans, being more socially integrated is associated with better physical and mental health and/or with lower mortality. This link between sociality and health may have ancient roots: sociality also predicts survival or reproduction in other mammals, such as rats, dolphins, and non-human primates. A key question, therefore, is which factors influence the degree of sociality over the life course. Longitudinal data can provide valuable insight into how environmental variability drives individual differences in sociality and associated outcomes. The first year of life-when long-lived mammals are the most reliant on others for nourishment and protection-is likely to play an important role in how individuals learn to integrate into groups. Using behavioral, demographic, and pedigree information on 376 wild capuchin monkeys (Cebus imitator) across 20 years, we address how changes in group composition influence spatial association. We further try to determine the extent to which early maternal social environments have downstream effects on sociality across the juvenile and (sub)adult stages. We find a positive effect of early maternal spatial association, where female infants whose mothers spent more time around others also later spent more time around others as juveniles and subadults. Our results also highlight the importance of kin availability and other aspects of group composition (e.g., group size) in dynamically influencing spatial association across developmental stages. We bring attention to the importance of-and difficulty in-determining the social versus genetic influences that parents have on offspring phenotypes. RESEARCH HIGHLIGHTS: Having more maternal kin (mother and siblings) is associated with spending more time near others across developmental stages in both male and female capuchins. Having more offspring as a subadult or adult female is additionally associated with spending more time near others. A mother's average sociality (time near others) is predictive of how social her daughters (but not sons) become as juveniles and subadults (a between-mother effect). Additional variation within sibling sets in this same maternal phenotype is not predictive of how social they become later relative to each other (no within-mother effect).

Genetic, maternal, and environmental influences on sociality in a pedigreed primate population.

Various aspects of sociality in mammals (e.g., dyadic connectedness) are linked with measures of biological fitness (e.g., longevity). How within- and between-individual variation in relevant social traits arises in uncontrolled wild populations is challenging to determine but is crucial for understanding constraints on the evolution of sociality. We use an advanced statistical method, known as the 'animal model', which incorporates pedigree information, to look at social, genetic, and environmental influences on sociality in a long-lived wild primate. We leverage a longitudinal database spanning 20 years of observation on individually recognized white-faced capuchin monkeys (Cebus capucinus imitator), with a multi-generational pedigree. We analyze two measures of spatial association, using repeat sampling of 376 individuals (mean: 53.5 months per subject, range: 6-185 months per subject). Conditioned on the effects of age, sex, group size, seasonality, and El Niño-Southern Oscillation phases, we show low to moderate long-term repeatability (across years) of the proportion of time spent social (posterior mode [95% Highest Posterior Density interval]: 0.207 [0.169, 0.265]) and of average number of partners (0.144 [0.113, 0.181]) (latent scale). Most of this long-term repeatability could be explained by modest heritability (h2social: 0.152 [0.094, 0.207]; h2partners: 0.113 [0.076, 0.149]) with small long-term maternal effects (m2social: 0.000 [0.000, 0.045]; m2partners: 0.000 [0.000, 0.041]). Our models capture the majority of variance in our behavioral traits, with much of the variance explained by temporally changing factors, such as group of residence, highlighting potential limits to the evolvability of our trait due to social and environmental constraints.

Using an on-site laboratory for fecal steroid analysis in wild white-faced capuchins.

Hormone laboratories located "on-site" where field studies are being conducted have a number of advantages. On-site laboratories allow hormone analyses to proceed in near-real-time, minimize logistics of sample permits/shipping, contribute to in-country capacity-building, and (our focus here) facilitate cross-site collaboration through shared methods and a shared laboratory. Here we provide proof-of-concept that an on-site hormone laboratory (the Taboga Field Laboratory, located in the Taboga Forest Reserve, Costa Rica) can successfully run endocrine analyses in a remote location. Using fecal samples from wild white-faced capuchins (Cebus imitator) from three Costa Rican forests, we validate the extraction and analysis of four steroid hormones (glucocorticoids, testosterone, estradiol, progesterone) across six assays (DetectX® and ISWE, all from Arbor Assays). Additionally, as the first collaboration across three long-term, wild capuchin field sites (Lomas Barbudal, Santa Rosa, Taboga) involving local Costa Rican collaborators, this laboratory can serve as a future hub for collaborative exchange.

Are demographic correlates of white-faced capuchin monkey (Cebus capucinus) "Gargle and Twargle" vocalization rates consistent with the infanticide risk assessment hypothesis?

Zahavi's "Bond Testing Hypothesis" states that irritating stimuli are used to elicit honest information from social partners regarding their attitudes towards the relationship. Two elements of the Cebus capucinus vocal repertoire, the "gargle" and "twargle," have been hypothesized to serve such a bond-testing function. The greatest threat to C. capucinus infant survival, and to adult female reproductive success, is infanticide perpetrated by alpha males. Thus, we predicted that infants (<8 months), pregnant females and females with infants would gargle/twargle at higher rates than the rest of the population, directing these vocalizations primarily to the alpha male. Over 16 years, researchers collected data via focal follows in 11 habituated groups of wild capuchins in Lomas Barbudal, Costa Rica. We found some support for our hypothesis. Infants and females with infants (<8 months) vocalized at higher rates than the rest of the population. Pregnant females did not vocalize at relatively high rates. Infants (age 8-23 months) were the only target group that vocalized more when the alpha male was not their father. Monkeys gargled and twargled most frequently towards the alpha male, who is both the perpetrator of infanticide and the most effective protector against potentially infanticidal males.

The development of sex differences in play in wild white-faced capuchins (Cebus capucinus).

Many mammalian species display sex differences in the frequency of play behavior, yet the animal literature includes few longitudinal studies of play, which are important for understanding the developmental timing of sex differences and the evolutionary functions of play. We analyzed social play, solitary play, and grooming using an 18-year data set on 38 wild white-faced capuchin monkeys (Cebus capucinus) followed since infancy. Rates of each behavior were measured as the proportion of point samples taken during focal follows in which the individual engaged in each behavior. To determine sex differences in these rates, we ran a series of generalized linear mixed models, considering both linear and quadratic effects of age, and chose the optimal model for each of the three behavioral outcomes based on information criteria. Rates of both social play and solitary play decreased with age, with the exception of social play in males, which increased in the early juvenile period before decreasing. Male and female capuchins had different developmental patterns of social play, with males playing more than females during most of the juvenile period, but they did not display meaningful sex differences in solitary play rates. Additionally, males and females had different patterns of grooming over the lifespan: males participated in grooming at low rates throughout their lives, while adult females participated in grooming at much higher rates, peaking around age 11 years before declining. We suggest that male and female white-faced capuchins may adopt alternative social bonding strategies, including different developmental timing and different behaviors (social play for males vs. grooming for females). Our results were consistent with two functional hypotheses of play, the practice and bonding hypotheses. This study demonstrates that play behavior may be critical for the development of sex-specific social strategies and emphasizes the importance of developmental perspectives on social behaviors.

Older, sociable capuchins (Cebus capucinus) invent more social behaviors, but younger monkeys innovate more in other contexts.

An important extension to our understanding of evolutionary processes has been the discovery of the roles that individual and social learning play in creating recurring phenotypes on which selection can act. Cultural change occurs chiefly through invention of new behavioral variants combined with social transmission of the novel behaviors to new practitioners. Therefore, understanding what makes some individuals more likely to innovate and/or transmit new behaviors is critical for creating realistic models of culture change. The difficulty in identifying what behaviors qualify as new in wild animal populations has inhibited researchers from understanding the characteristics of behavioral innovations and innovators. Here, we present the findings of a long-term, systematic study of innovation (10 y, 10 groups, and 234 individuals) in wild capuchin monkeys (Cebus capucinus) in Lomas Barbudal, Costa Rica. Our methodology explicitly seeks novel behaviors, requiring their absence during the first 5 y of the study to qualify as novel in the second 5 y of the study. Only about 20% of 187 innovations identified were retained in innovators' individual behavioral repertoires, and 22% were subsequently seen in other group members. Older, more social monkeys were more likely to invent new forms of social interaction, whereas younger monkeys were more likely to innovate in other behavioral domains (foraging, investigative, and self-directed behaviors). Sex and rank had little effect on innovative tendencies. Relative to apes, capuchins devote more of their innovations repertoire to investigative behaviors and social bonding behaviors and less to foraging and comfort behaviors.

Pay-off-biased social learning underlies the diffusion of novel extractive foraging traditions in a wild primate.

The type and variety of learning strategies used by individuals to acquire behaviours in the wild are poorly understood, despite the presence of behavioural traditions in diverse taxa. Social learning strategies such as conformity can be broadly adaptive, but may also retard the spread of adaptive innovations. Strategies like pay-off-biased learning, by contrast, are effective at diffusing new behaviour but may perform poorly when adaptive behaviour is common. We present a field experiment in a wild primate, Cebus capucinus, that introduced a novel food item and documented the innovation and diffusion of successful extraction techniques. We develop a multilevel, Bayesian statistical analysis that allows us to quantify individual-level evidence for different social and individual learning strategies. We find that pay-off-biased and age-biased social learning are primarily responsible for the diffusion of new techniques. We find no evidence of conformity; instead rare techniques receive slightly increased attention. We also find substantial and important variation in individual learning strategies that is patterned by age, with younger individuals being more influenced by both social information and their own individual experience. The aggregate cultural dynamics in turn depend upon the variation in learning strategies and the age structure of the wild population.

Social and demographic correlates of male androgen levels in wild white-faced capuchin monkeys (Cebus capucinus).

The Challenge Hypothesis, designed originally to explain the patterning of competitive behavior and androgen levels in seasonally breeding birds, predicts that males will increase their androgen levels in order to become more competitive in reproductive contexts. Here we test predictions derived from the Challenge Hypothesis in white-faced capuchin monkeys (Cebus capucinus), a species that has somewhat seasonal reproduction. We analyzed demographic and hormonal data collected over a 5.25-year period, from 18 males in nine social groups living in or near Lomas Barbudal Biological Reserve, Costa Rica. Alpha males had higher androgen levels than subordinates. Contrary to our predictions, neither the number of breeding-age males nor the number of potentially fertile females was obviously associated with androgen levels. Furthermore, male androgen levels were not significantly linked to social stability, as measured by stability of male group membership or recency of change in the alpha male position. Androgen levels changed seasonally, but not in a manner that had an obvious relationship to predictions from the Challenge Hypothesis: levels were generally at their lowest near the beginning of the conception season, but instead of peaking when reproductive opportunities were greatest, they were at their highest near the end of the conception season or shortly thereafter. This lack of correspondence to the timing of conceptions suggests that there may be ecological factors not yet identified that influence ifA levels. We expected that the presence of offspring who were young enough to be vulnerable to infanticide during an alpha male takeover might influence androgen levels, at least in the alpha male, but this variable did not significantly impact results.

Simultaneous measurement of endogenous steroid hormones and their metabolites with LC-MS/MS in faeces of a New World primate species, Cebus capucinus.

We developed and validated a method to measure steroid hormones with liquid chromatography-tandem mass spectrometry (LC-MS/MS) in faecal samples of white-faced capuchins. The method includes the measurement of adrenal and gonadal hormones such as cortisol, testosterone, estrone, progesterone and a number of their faecal metabolites. This method can be used for simultaneous routine measurements of steroids in faecal samples and provides a reference method for the validation of new immunoassays in this matrix. The optimised method consists of an extraction of the dried faecal samples with 80% methanol followed by purification of the extracts by solid phase extraction, solvolytic cleavage of conjugates and liquid-liquid extraction. Extracts were measured by LC-MS/MS with an electrospray interface in positive ionisation mode. Out of 19 steroids spiked into methanol extracts, 14 showed a recovery of 79.8-118.5% with an intra-day precision of 2.5-13.0% and an inter-day precision of 7.2-15.1%. Detection limits for these steroids ranged from 0.3 to 27.0 ng/mL of extract. Five steroids did not fulfil our requirements concerning precision and accuracy and we therefore considered these to not be reliably measurable with this method. While there was no indication of considerable amounts of conjugated forms for most metabolites, 87% of the testosterone was found in the solvolysis fraction, which indicates that the majority of testosterone was conjugated. Therefore, solvolysis turned out to be crucial, especially for the quantification of the total amount of testosterone. The physiological validation of this LC-MS/MS method confirmed known physiologically caused differences in faecal steroid concentrations. This indicates the usefulness of the method in investigating variation in the levels of major steroid hormones in faeces of white-faced capuchins. The possibility to simultaneously measure hormones of the hypothalamic-pituitary-adrenal (HPA) axis and the hypothalamic-pituitary-gonadal (HPG) axis makes this method suitable for dealing with questions concerning the cross talk between those axes.