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.

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.

Capuchin monkey rituals: an interdisciplinary study of form and function.

Many white-faced capuchin monkey dyads in Lomas Barbudal, Costa Rica, practise idiosyncratic interaction sequences that are not part of the species-typical behavioural repertoire. These interactions often include uncomfortable or risky elements. These interactions exhibit the following characteristics commonly featured in definitions of rituals in humans: (i) they involve an unusual intensity of focus on the partner, (ii) the behaviours have no immediate utilitarian purpose, (iii) they sometimes involve 'sacred objects', (iv) the distribution of these behaviours suggests that they are invented and spread via social learning, and (v) many behaviours in these rituals are repurposed from other behavioural domains (e.g. extractive foraging). However, in contrast with some definitions of ritual, capuchin rituals are not overly rigid in their form, nor do the sequences have specific opening and closing actions. In our 9260 h of observation, ritual performance rate was uncorrelated with amount of time dyads spent in proximity but (modestly) associated with higher relationship quality and rate of coalition formation across dyads. Our results suggest that capuchin rituals serve a bond-testing rather than a bond-strengthening function. Ritual interactions are exclusively dyadic, and between-dyad consistency in form is low, casting doubt on the alternative hypothesis that they enhance group-wide solidarity. This article is part of the theme issue 'Ritual renaissance: new insights into the most human of behaviours'.

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.

Development of snake-directed antipredator behavior by wild white-faced capuchin monkeys: I. Snake-species discrimination.

Young animals are known to direct alarm calls at a wider range of species than adults. Our field study examined age-related differences in the snake-directed antipredator behavior of infant, juvenile, and adult white-faced capuchin monkeys (Cebus capucinus) in terms of alarm calling, looking behavior, and aggressive behavior. In the first experiment, we exposed infant and juvenile white-faced capuchins to realistic-looking inflatable models of their two snake predators, the boa constrictior (Boa constrictor) and neotropical rattlesnake (Crotalus durissus) and a white airplane as a novel control. In the second experiment, infants, juveniles, and adults were presented photographic models of a coiled boa constrictor, rattlesnake, indigo snake (Drymarchon corais), a noncapuchin predator, and a white snake-like model. We found that antipredator behavior changed during the immature stage. Infants as young as 4 months old were able to recognize snakes and display antipredator behavior, but engaged in less snake-model discrimination than juveniles. All age classes exhibited a lower response to the white snake-like model, indicating that the absence of color and snake-scale patterns affected snake recognition. Infants also showed a higher level of vigilance after snake-model detection as exhibited by a higher proportion of time spent looking and head cocking at the models. Aggressive antipredator behavior was found in all age classes, but was more prevalent in juveniles and adults than infants. This study adds to the knowledge of development of antipredator behavior in primates by showing that, although alarm calling behavior and predator recognition appear at a very young age in capuchins, snake-species discrimination does not become apparent until the juvenile stage.

Development of snake-directed antipredator behavior by wild white-faced capuchin monkeys: II. Influence of the social environment.

Young animals are known to direct alarm calls at a wider range of animals than adults. If social cues are safer and/or more reliable to use than asocial cues for learning about predators, then it is expected that the development of this behavior will be affected by the social environment. Our study examined the influence of the social environment on antipredator behavior in infant, juvenile, and adult wild white-faced capuchin monkeys (Cebus capucinus) at Lomas Barbudal Biological Reserve in Costa Rica during presentations of different species of model snakes and novel models. We examined (a) the alarm calling behavior of the focal animal when alone versus in the vicinity of conspecific alarm callers and (b) the latency of conspecifics to alarm call once the focal animal alarm called. Focal animals alarm called more when alone than after hearing a conspecific alarm call. No reliable differences were found in the latencies of conspecifics to alarm call based on age or model type. Conspecifics were more likely to alarm call when focal individuals alarm called at snake models than when they alarm called at novel models. Results indicate (a) that alarm calling may serve to attract others to the predator's location and (b) that learning about specific predators may begin with a generalized response to a wide variety of species, including some nonthreatening ones, that is winnowed down via Pavlovian conditioned inhibition into a response directed toward specific dangerous species. This study reveals that conspecifics play a role in the development of antipredator behavior in white-faced capuchins.

Male dominance and reproductive success in wild white-faced capuchins (Cebus capucinus) at Lomas Barbudal, Costa Rica.

Theory and a growing body of empirical evidence suggest that higher ranking males experience reproductive advantages in group-living mammals. White-faced capuchins (Cebus capucinus) exhibit an interesting social system for investigating the relationship between dominance and reproductive success (RS) because they live in multimale multifemale social groups, in which the alpha males can have extraordinarily long tenures (i.e. they coreside with daughters of reproductive age). Genetic paternity was determined from fecal samples for 120 infants born into three social groups of wild C. capucinus at Lomas Barbudal Biological Reserve, Costa Rica. Alpha males produced far more offspring than expected by chance, and significantly high Nonac's B indices (a measure of deviation from a random distribution of RS among potentially breeding individuals) were a feature of six out of eight male tenures. The likelihood of the alpha male siring a particular offspring was predicted by the kin relationship between the mother and the alpha male, as well as the total number of males and females in the group. The almost complete lack of father-daughter inbreeding [Muniz et al., 2006] constitutes an impediment to alpha male reproductive monopolization in this population, particularly toward the end of long alpha male tenures.

Violent coalitionary attacks and intraspecific killing in wild white-faced capuchin monkeys ( Cebus capucinus).

During 12 years of observation, we have observed three confirmed and two inferred lethal coalitionary attacks on adult male white-faced capuchins ( Cebus capucinus) by members of two habituated social groups at Lomas Barbudal Biological Reserve, Costa Rica. In one case, an alpha male was badly wounded and evicted from his group, and when later found by his former groupmates he was attacked by several of them and died less than 24 h later. In two other cases, lone extra-group males were mobbed by adult and immature males of a bisexual group. One victim's abdomen was torn open and he died less than 24 h later. A second victim was quite badly bitten but may have escaped. The fourth and fifth cases resulted from intergroup encounters. One victim lost the use of both arms but may have survived, whereas the other died of unknown causes within an hour of the attack. The observed death rate from coalitionary aggression at our site is approximately the same as that reported for eastern chimpanzees. Because at least three of the five observed incidents involved large coalitions attacking lone victims, they support the general hypothesis that imbalances of power contribute to intraspecific killing in primates. However, the occurrence of lethal coalitional attacks in a species lacking fission-fusion social organization poses a challenge to the more specific version of the imbalance-of-power hypothesis proposed by Manson and Wrangham in 1991 to explain chimpanzee and human intergroup aggression.