Variation in neophilia in seven primate species.

Neophilia is a measure of individuals' attraction to novelty and is thought to provide important fitness benefits related to the acquisition of information and the ability to solve novel problems. Although neophilia is thought to vary across individuals and species, few studies have made direct comparisons to assess the factors that predict this variation. Here we operationalized neophilia as the probability of interacting with novel objects and compared the response to familiar and novel objects in 53 captive individuals belonging to seven different primate species: chimpanzees (Pan troglodytes), bonobos (Pan paniscus), Sumatran orangutans (Pongo abelii), gorillas (Gorilla gorilla), long-tailed macaques (Macaca fascicularis), tufted capuchin monkeys (Sapajus apella), and Geoffroy's spider monkeys (Ateles geoffroyi). Our results showed that individuals were overall more likely to interact with novel than familiar objects. Moreover, we found no evidence that neophilia varied across individuals depending on their sex, age, and dominance rank. However, macaques were overall less likely to interact with objects (regardless of their novelty), as compared to bonobos, orangutans, gorillas, and capuchin monkeys. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

A first exploratory comparison of the behaviour of wolves (Canis lupus) and wolf-dog hybrids in captivity.

Extensive introgression of genes from domesticated taxa may be a serious threat for the genomic integrity and adaptability of wild populations. Grey wolves (Canis lupus) are especially vulnerable to this phenomenon, but there are no studies yet assessing the potential behavioural effects of dog-introgression in wolves. In this study, we conducted a first systematic comparison of admixed (N = 11) and non-admixed (N = 14) wolves in captivity, focusing on their reaction to unfamiliar humans and novel objects, and the cohesiveness of their social groups. When exposed to unfamiliar humans in the experimental task, wolves were more vigilant, fearful and aggressive than admixed wolves, and less likely to approach humans, but also more likely to spend time in human proximity. When exposed to novel objects, wolves were more aggressive than admixed wolves, less likely to spend time in object proximity, and more likely to interact with objects, but also less vigilant and as fearful as admixed wolves. Finally, social networks were more cohesive in wolves than in admixed wolves. Although caution is needed when comparing groups of captive individuals with different life experiences, our study suggests that dog admixture may lead to important behavioural changes in wolves, with possible implications for conservation strategies.

Gestural communication in wild spider monkeys (Ateles geoffroyi).

Gestures play a central role in the communication systems of several animal families, including primates. In this study, we provide a first assessment of the gestural systems of a Platyrrhine species, Geoffroy's spider monkeys (Ateles geoffroyi). We observed a wild group of 52 spider monkeys and assessed the distribution of visual and tactile gestures in the group, the size of individual repertoires and the intentionality and effectiveness of individuals' gestural production. Our results showed that younger spider monkeys were more likely than older ones to use tactile gestures. In contrast, we found no inter-individual differences in the probability of producing visual gestures. Repertoire size did not vary with age, but the probability of accounting for recipients' attentional state was higher for older monkeys than for younger ones, especially for gestures in the visual modality. Using vocalizations right before the gesture increased the probability of gesturing towards attentive recipients and of receiving a response, although age had no effect on the probability of gestures being responded. Overall, our study provides first evidence of gestural production in a Platyrrhine species, and confirms this taxon as a valid candidate for research on animal communication.

A longitudinal comparison of maternal behaviour in German urban humans (Homo sapiens) and captive chimpanzees (Pan troglodytes).

Comparative perspectives are crucial in the study of human development, yet longitudinal comparisons of humans and other primates are still relatively uncommon. Here, we combined theoretical frameworks from cross-cultural and comparative psychology, to study maternal style in 10 mother-infant pairs of German urban humans (Homo sapiens) and 10 mother-infant pairs of captive chimpanzees (Pan troglodytes), during the first year of infants' development. We conducted focal observations of different behaviours (i.e. nursing, carrying, body contact, touching, grooming, restraining, approaching, leaving, rejection, aggression, mutual gaze, object stimulation), during natural interactions. Analyses revealed a more distal maternal style in WEIRD humans than in captive chimpanzees, with different behaviours being generally more common in one of the two species throughout development. For other behaviours (i.e. nursing), developmental trajectories differed between WEIRD humans and captive chimpanzees, although differences generally decreased through infants' development. Overall, our study confirms functional approaches as a valid tool for comparative longitudinal studies.

Maternal Investment Fosters Male but Not Female Social Interactions with Other Group Members in Immature Wild Spider Monkeys (Ateles geoffroyi).

In several species, individuals form long-lasting social relationships with other group members, which provide them with important fitness benefits. In primates, patterns of social relationships are known to differ between sexes, but little is known about how these differences emerge through development or the role that mothers might have in this process. Here, we investigated how sex differences in social behaviour emerge during the first six years of primate life and how sex-biased maternal investment can foster immatures' social development and social interaction with other group members. For this purpose, we observed 20 males and females aged between zero and six years in a wild group of spider monkeys (Ateles geoffroyi) that was male-philopatric and, therefore, expected to show sex-biased maternal investment. Our results showed no sex difference in the social development of offspring with regards to body contact and grooming, but the probability of play was rather constant throughout age for females, whereas, for males, it became higher than females around two years of age, peaking between three and four years of age. Moreover, we found differences between female and male immatures in the importance of maternal investment (which included the time mothers spent nursing, carrying, grooming, touching and playing with their offspring) for their social integration in the natal group. In particular, maternal investment increased the probability of playing with other group members for sons, but not for daughters. Our findings suggest that mothers, through sex-biased maternal investment, might have a crucial function in the social development of spider monkeys, fostering the abilities that young offspring need to thrive as adults. By shedding light on maternal investment and social development in a still understudied primate species, these findings contribute to understanding the evolutionary roots of human maternal care and social development.

Vigilance has mainly a social function in a wild group of spider monkeys (Ateles geoffroyi).

Vigilance is a widespread behavior that allows individuals to socially acquire information and/or effectively detect potential risks posed by predators and conspecifics. In this study, we aimed to investigate how social factors (i.e., subgroup size, number of males and immatures in the subgroup, presence of fission and fusion events, subgroup activity), individual characteristics (i.e., sex, presence of dependent offspring) and possible vulnerability to predation (i.e., being in smaller subgroups or lower in the canopy) explain variation in vigilance behavior in a wild group of spider monkeys (Ateles geoffroyi). We collected vigilance data during focal samples of all adults, subadults and juveniles of the group (N = 38), and ran generalized linear mixed models with a Bayesian approach. We found that the proportion of time both sexes spent in vigilance increased with subgroup size and during fusion events. Individuals also spent more time in vigilance when the subgroup was resting or socializing compared to other activities. Moreover, the proportion of time spent in vigilance increased in subgroups with more immatures. An alternative model with similar fit suggested that the proportion of time spent in vigilance increased in females when subgroups included more adult and subadult males. Overall, these results suggest that our study group mainly directed vigilance toward conspecifics (i.e., social vigilance), probably as a result of the relatively low predation pressure experienced, and contribute to the understanding of the multiple social factors affecting vigilance in group-living primates.

Assessing Eysenck's PEN model to describe personality in chimpanzees.

Questionnaires based on human models can be used to reliably assess personality also in non-human primates. In this study, we used an adapted version of Eysenck's Psychoticism-Extraversion-Neuroticism (PEN) model that focuses on three higher-order personality traits. Extending previous work on a small group of chimpanzees (Pan troglodytes), we tested 37 chimpanzees housed at Fundació Mona (Girona, Spain) and the Leipzig Zoo (Germany). We assessed personality with a 12-item questionnaire, which raters scored using a 7-point Likert scale. To identify the personality traits, we conducted data reduction with Principal Components Analysis and Robust Unweighted Least Squares. The ICCs for the single (3, 1) and average (3, k) ratings indicated substantial agreement between raters. Parallel analyses identified two factors to retain, whereas the scree plot inspection and eigenvalues larger than one rule identified three factors. Factor 1 and 2 in our study were identical to the ones previously described for this species (labelled Extraversion and Neuropsychoticism, respectively) and we also obtained a third factor that could be related to Dominance (Fearless Dominance). Thus, our results confirm the potential of the PEN model to describe chimpanzee personality structure.

Giraffes make decisions based on statistical information.

The ability to make inferences based on statistical information has so far been tested only in animals having large brains in relation to their body size, like primates and parrots. Here we tested if giraffes (Giraffa camelopardalis), despite having a smaller relative brain size, can rely on relative frequencies to predict sampling outcomes. We presented them with two transparent containers filled with different quantities of highly-liked food and less-preferred food. The experimenter covertly drew one piece of food from each container, and let the giraffe choose between the two options. In the first task, we varied the quantity and relative frequency of highly-liked and less-preferred food pieces. In the second task, we inserted a physical barrier in both containers, so giraffes only had to take into account the upper part of the container when predicting the outcome. In both tasks giraffes successfully selected the container more likely to provide the highly-liked food, integrating physical information to correctly predict sampling information. By ruling out alternative explanations based on simpler quantity heuristics and learning processes, we showed that giraffes can make decisions based on statistical inferences.

Corrigendum: Intra-specific variation in the social behavior of Barbary macaques (Macaca sylvanus).

[This corrects the article DOI: 10.3389/fpsyg.2021.666166.].

Yawning and scratching contagion in wild spider monkeys (Ateles geoffroyi).

Behavioural contagion is a widespread phenomenon in animal species, which is thought to promote coordination and group cohesion. Among non-human primates, however, there is no evidence of behavioural contagion in Platyrrhines (i.e. primates from South and Central America) yet. Here, we investigated whether behavioural contagion is also present in this taxon, by assessing yawning and scratching contagion in a wild group (N = 49) of Geoffroy's spider monkeys (Ateles geoffroyi). We conducted focal samples to examine whether individuals observing the triggering event (i.e. a naturally occurring yawning or scratching event in the group) would be more likely to yawn or scratch in the following 3 min, as compared to individuals who did not observe the triggering event. We ran generalized linear mixed models using a Bayesian approach, and found that the probability of yawning and scratching was higher for individuals observing others yawning and scratching, respectively, as compared to individuals who did not observe such an event. Behavioural contagion did not vary depending on the observer's sex, kinship or relationship quality with the individual performing the triggering event. These findings provide the first evidence for yawning and scratching contagion in a wild group of spider monkeys, and importantly contribute to the debate about the evolutionary origins of behavioural contagion in primates.

Innovation across 13 ungulate species: problem solvers are less integrated in the social group and less neophobic.

Innovation is the ability to solve new problems or find novel solutions to familiar problems, and it is known to provide animals with crucial fitness benefits. Although this ability has been extensively studied in some taxa, the factors that predict innovation within and across species are still largely unclear. In this study, we used a novel foraging task to test 111 individuals belonging to 13 ungulate species-a still understudied taxon. To solve the task, individuals had to open transparent and opaque cups with food rewards, by removing their cover. We assessed whether individual factors (neophobia, social integration, sex, age, rank) and socio-ecological factors (dietary breadth, fission-fusion dynamics, domestication, group size) predicted participation and performance in the task. Using a phylogenetic approach, we showed that success was higher for less neophobic and socially less integrated individuals. Moreover, less neophobic individuals, individuals of domesticated species and having higher fission-fusion dynamics were more likely to participate in the task. These results are in line with recent literature suggesting a central role of sociality and personality traits to successfully deal with novel challenges, and confirm ungulates as a promising taxon to test evolutionary theories with a comparative approach.

Face to face interactions in chimpanzee (Pan troglodytes) and human (Homo sapiens) mother-infant dyads.

Human mothers interact with their infants in different ways. In Western, educated, industrialized, rich and democratic (WEIRD) societies, face-to-face interactions and mutual gazes are especially frequent, yet little is known about their developmental trajectories and if they differ from those of other primates. Using a cross-species developmental approach, we compared mother-infant interactions in 10 dyads of urban humans from a WEIRD society (Homo sapiens) and 10 dyads of captive zoo-based chimpanzees (Pan troglodytes), when infants were one, six and 12 months old. Results showed that face-to-face interactions with mutual gaze events were common in both groups throughout the infant's first year of life. The developmental trajectories of maternal and infants' looks partially differed between species, but mutual gaze events were overall longer in humans than in chimpanzees. Mutual gazes were also more frequent in humans, peaking at six months in humans, while increasing with age in chimpanzees. The duration and frequency of mutual gazes varied across contexts in both groups, with mutual gazes being longer during caring/grooming and feeding contexts. These findings confirm that some aspects of early socio-cognitive development are shared by humans and other primates, and highlight the importance of combining developmental and cross-species approaches to better understand the evolutionary roots of parenting behaviour. This article is part of a discussion meeting issue 'Face2face: advancing the science of social interaction'.

Primates unleashed.

Before claiming major differences between the communication systems of humans and other species, it is necessary to (1) overcome methodological limitations in the comparative study of communicative intentions; (2) account for mechanisms other than epistemic vigilance that may also sustain complex forms of communication; and (3) better differentiate between motivational and cognitive factors potentially affecting the emergence of open-ended communication.

Maternal and offspring behavior in free-ranging Japanese and moor macaques: A comparative approach.

Female primates represent the most important social partner for their developing offspring. However, mothers may strongly differ in the way they relate to their offspring (e.g., in terms of two different dimensions: protectiveness and rejection). In this study, we aimed to assess how dominance style predicts (i) changes in maternal behavior through offspring development, and (ii) the link between maternal behavior and offspring behavior. We conducted behavioral observations on 34 free-ranging immatures of two species of macaques with different dominance styles: less tolerant Japanese macaques (JM; Macaca fuscata) and more tolerant moor macaques (MM; Macaca maura). Our results showed that maternal behavior differed between JM and MM: maternal proximity and grooming decreased through offspring development more quickly in MM than in JM, whereas maternal rejection and aggression, which were generally more frequent in JM, decreased with offspring age similarly in both species. In contrast, maternal restraint of offspring decreased similarly with offspring age in both species. Furthermore, dominance style was differentially associated with the link between maternal and offspring behavior: in MM only, maternal grooming predicted an increase of the probability that offspring interacted with partners other than their mothers and engaged in solitary play, whereas maternal rejection predicted a decrease in the occurrence of solitary play. Overall, these results suggest interspecific variation in maternal behavior during offspring's first years of life, and point to the possibility that these differences may have an important role in shaping their behavioral development.

Context and prediction matter for the interpretation of social interactions across species.

Predictions about others' future actions are crucial during social interactions, in order to react optimally. Another way to assess such interactions is to define the social context of the situations explicitly and categorize them according to their affective content. Here we investigate how humans assess aggressive, playful and neutral interactions between members of three species: human children, dogs and macaques. We presented human participants with short video clips of real-life interactions of dyads of the three species and asked them either to categorize the context of the situation or to predict the outcome of the observed interaction. Participants performed above chance level in assessing social situations in humans, in dogs and in monkeys. How accurately participants predicted and categorized the situations depended both on the species and on the context. Contrary to our hypothesis, participants were not better at assessing aggressive situations than playful or neutral situations. Importantly, participants performed particularly poorly when assessing aggressive behaviour for dogs. Also, participants were not better at assessing social interactions of humans compared to those of other species. We discuss what mechanism humans use to assess social situations and to what extent this skill can also be found in other social species.

The social dynamics of complex gestural communication in great and lesser apes (Pan troglodytes, Pongo abelii, Symphalangus syndactylus).

Gestures play an essential role in primate communication. However, little is known about how complexity of gestural use (in terms of repertoire size, intentional use, flexibility and use of gestural sequences) relates to individual and dyadic measures of sociality and whether more complex gestural use is more effective in eliciting a response. We observed 19 captive chimpanzees (Pan troglodytes), 16 Sumatran orangutans (Pongo abelii) and 18 siamangs (Symphalangus syndactylus) to assess the complexity and effectiveness of their gestural use. We found that, beyond interspecies variation, the number of gesture types used in a dyad was higher when individuals had stronger social bonds; the probability of accounting for others' attention increased with age, especially for visual gestures; and sequences were more likely used by younger or socially less integrated individuals. In terms of effectiveness, older individuals and those using fewer sequences were more likely to be responded to, while across dyads, the probability of obtaining a response was higher when both individuals accounted for the other's attention and when they used fewer sequences. Overall, this confirms the link between sociality and complex gestural use and suggests that more complex forms of communication, at least in terms of intentional use, may be more effective at achieving communicative goals. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Cognitive enrichment in a social setting: assessing the use of a novel food maze in sanctuary-housed chimpanzees.

Foraging devices are effective enrichment tools for non-human primates, as they provide both cognitive and manipulative stimulation that may enhance these animals' welfare. We assessed the behavioral effects of a novel tool-based enrichment on 14 chimpanzees (Pan troglodytes) housed at Fundació Mona (Girona, Spain). The device consisted of a vertical maze filled with food rewards, which chimpanzees could extract by using tools. We conducted behavioral observations in two conditions over an approximately 2.5-month period: when the food maze was loaded (12 enrichment days), and when it was empty (12 baseline days). Data were collected using 2-min scan sampling and untimed-event focal sampling during two daily sessions of 80 min each. We expected that the chimpanzees' interest in the enrichment would decrease over time, but that its use would be linked to an increase in the occurrence of species-typical behaviors, a reduction in negative indicators of welfare, and changes in social behaviors. We found that participation widely varied among subjects, being higher in females and decreasing through time. Furthermore, participation was linked to an increase in tool use and a decrease in inactivity, but also to an increase in aggression-related behaviors. In contrast, participation had no effect on the occurrence of abnormal behaviors, social proximity or affiliation-related behaviors. Finally, we detected an increase in self-directed behaviors only when subjects actively interacted with the device. We conclude that, in future studies, these types of devices should be evaluated for longer periods of time and more attention should be paid to individuals' preferences and abilities.

Maternal stress, child behavior and the promotive role of older siblings.

BACKGROUND: In the first years of their lives, children develop the cognitive, social and emotional skills that will provide the foundations for their lifelong health and achievements. To increase their life prospects and reduce the long-term effects of early aversive conditions, it is therefore crucial to understand the risk factors that negatively affect child development and the factors that are instead beneficial. In this study, we tested (i) the effects of different social and environmental stressors on maternal stress levels, (ii) the dynamic relationship between maternal stress and child behavior problems during development, and (iii) the potential promotive (i.e. main) or protective (i.e. buffering) effect of siblings on child behavior problems during development. METHODS: We used longitudinal data from 373 mother-child pairs (188 daughters, 185 sons) from pregnancy until 10 years of age. We assessed maternal stress and child behavior problems (internalizing and externalizing) with validated questionnaires, and then used linear mixed models, generalized linear mixed models and longitudinal cross-lagged models to analyze the data. RESULTS: Our results showed that higher maternal stress levels were predicted by socio-environmental stressors (i.e. the lack of sufficient social areas in the neighborhood). Moreover, prenatal maternal stress reliably predicted the occurrence of behavior problems during childhood. Finally, the presence of older siblings had a promotive function, by reducing the likelihood that children developed externalizing problems. CONCLUSIONS: Overall, our results confirm the negative effects that maternal stress during pregnancy may have on the offspring, and suggest an important main effect of older siblings in promoting a positive child development.

The Habituation Process in Two Groups of Wild Moor Macaques (Macaca maura).

When studying animal behavior in the wild, some behaviors may require observation from a relatively short distance. In these cases, habituation is commonly used to ensure that animals do not perceive researchers as a direct threat and do not alter their behavior in their presence. However, habituation can have significant effects on the welfare and conservation of the animals. Studying how nonhuman primates react to the process of habituation can help to identify the factors that affect habituation and implement habituation protocols that allow other researchers to speed up the process while maintaining high standards of health and safety for both animals and researchers. In this study, we systematically described the habituation of two groups of wild moor macaques (Macaca maura), an Endangered endemic species of Sulawesi Island (Indonesia), to assess the factors that facilitate habituation and reduce impact on animal behavior during this process. During 7 months, we conducted behavioral observations for more than 7,872 encounters and an average of 120 days to monitor how macaque behavior toward researchers changed through time in the two groups under different conditions. We found that both study groups (N = 56, N = 41) became more tolerant to the presence of researchers during the course of the habituation, with occurrence of neutral group responses increasing, and minimum distance to researchers and occurrence of fearful group responses decreasing through time. These changes in behavior were predominant when macaques were in trees, with better visibility conditions, when researchers maintained a longer minimum distance to macaques and, unexpectedly, by the presence of more than one researcher. By identifying these factors, we contribute to designing habituation protocols that decrease the likelihood of fearful responses and might reduce the stress experienced during this process.

Intra-specific Variation in the Social Behavior of Barbary macaques (Macaca sylvanus).

Non-human primates show an impressive behavioral diversity, both across and within species. However, the factors explaining intra-specific behavioral variation across groups and individuals are yet understudied. Here, we aimed to assess how group size and living conditions (i.e., captive, semi-free-ranging, wild) are linked to behavioral variation in 5 groups of Barbary macaques (N=137 individuals). In each group, we collected observational data on the time individuals spent in social interactions and on the group dominance style, along with experimental data on social tolerance over food and neophobia. Our results showed that differences in group size predicted differences in the time spent in social interactions, with smaller groups spending a higher proportion of time in close spatial proximity, but a lower proportion of time grooming. Moreover, group size predicted variation in dominance style, with smaller groups being more despotic. Social tolerance was affected by both group size and living conditions, being higher in smaller groups and in groups living in less natural conditions. Finally, individual characteristics also explained variation in social tolerance and neophobia, with socially integrated individuals having higher access to food sources, and higher-ranking ones being more neophobic. Overall, our results support the view that intra-specific variation is a crucial aspect in primate social behavior and call for more comparative studies to better understand the sources of within-species variation.