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"Schiel, Nicola"
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Hallmarks of social action in the vocal turn-taking of wild common marmosets (Callithrix jacchus)
2026
Conversational turn-taking, the orderly exchange of signals between individuals, is considered an important component of human communication and language. Comparative studies of vocal turn-taking have often been biased toward a limited number of model species and have usually examined only single call types, restricted features of human conversational turn-taking, or captive animals, thereby limiting broader understanding of turn-taking complexity and its evolutionary trajectory. Here we show that wild common marmosets engage in structured vocal exchanges that share several basic features with human conversational turn-taking. We analyzed 1,245 natural vocal interactions and found that individuals can produce multi-turn exchanges with matched call types. Marmosets used different vocalizations when interacting with group members compared to neighboring groups. These interactions were characterized by flexible turn organization, recurring call sequences, relatively short gaps between turns (approximately 1,300 ms), and structured participation involving specific individuals. Altogether, our findings highlight the complexity of vocal interaction in wild common marmosets, providing a broader view of coordination across the whole vocal repertoire and suggesting that elements of human conversational turn-taking may be present in this species and may be shared, at least in part, with other primates.
Journal Article
Wild common marmosets (Callithrix jacchus) employ spatial cognitive abilities to improve their food search and consumption: an experimental approach in small-scale space
by
Schiel Nicola
,
Abreu Filipa
,
Souto, Antonio
in
Animal behavior
,
Callithrix jacchus
,
Cognitive ability
2020
The ability of an animal to integrate and retain spatial information of resources often depends on the spatial memory and the speed at which this memory crystallizes. These become especially important once foragers reach their target area. However, very little is known about how wild common marmosets encode spatial information when feeding rewards are near to each other in a small-scale space. With this in mind, we performed field experiments to test foraging decisions related to a small-scale space setting. Specifically, we tested the (i) short- and (ii) long-term spatial memory, as well as (iii) the ability to remember the spatial location of resources after a single visit (one-trial spatial learning). The study was conducted with four groups of wild common marmosets (Callithrix jacchus) living in a semiarid Caatinga environment. We observed that individuals were able to retain spatial information of food sources on both a short- and long-term basis and to learn the spatial location of these resources after a single visit. We suggest that such abilities during foraging can improve the search for scattered resources with fluctuations of food availability. Presumably, this would be particularly advantageous in Caatinga, with its vegetation exhibiting asynchronous phenological patterns. Altogether, our results demonstrate that common marmosets employ all three studied spatial cognitive abilities to improve their food search and consumption.
Journal Article
Choosing the best way: how wild common marmosets travel to efficiently exploit resources
by
Abreu, Filipa
,
Schiel, Nicola
,
Xavier, Dêverton Plácido
in
Animals
,
Behavioral Sciences
,
Biomedical and Life Sciences
2024
While foraging, animals have to find potential food sites, remember these sites, and plan the best navigation route. To deal with problems associated with foraging for multiple and patchy resources, primates may employ heuristic strategies to improve foraging success. Until now, no study has attempted to investigate experimentally the use of such strategies by a primate in a context involving foraging in large-scale space. Thus, we carried out an experimental field study that aimed to test if wild common marmosets (
Callithrix jacchus
) employ heuristic strategies to efficiently navigate through multiple feeding sites distributed in a large-scale space. In our experiment, we arranged four feeding platforms in a trapezoid configuration with up to 60 possible routes and observe marmosets’ decisions under two experimental conditions. In experimental condition I, all platforms contained the same amount of food; in experimental condition II, the platforms had different amounts of food. According to the number and arrangement of the platforms, we tested two heuristic strategies: the Nearest Neighbor Rule and the Gravity Rule. Our results revealed that wild common marmosets prefer to use routes consistent with a heuristic strategy more than expected by chance, regardless of food distribution. The findings also demonstrate that common marmosets seem to integrate different factors such as distance and quantity of food across multiple sites distributed over a large-scale space, employing a combination of heuristic strategies to select the most efficient routes available. In summary, our findings confirm our expectations and provide important insights into the spatial cognition of these small neotropical primates.
Journal Article
The white-eared opossum failed to understand the parallel strings task: studying a primitive mammal under natural conditions
2020
The present study aimed to investigate if the white-eared opossum under natural conditions is capable of spontaneously solving the parallel string task. The experimental study with this primitive mammal was carried out on fifteen naïve animals of both sexes in northeastern Brazil. The parallel strings task was arranged in apparatuses with a vertical and a horizontal arrangement. A food reward (a slice of banana) was connected at the extremity of one string. A total of 505 videos were recorded using trap cameras. Despite the observed interest in obtaining the bait, the number of attempts to reach it and the use of the strings as support (trying to directly reach the bait in the vertical apparatus), the individuals were unable to pull any of the strings, suggesting that they could not understand the problem. The present study points to the relevance of using the species Didelphis albiventris and other species from this family (e.g., D. virginiana) to broaden our knowledge about the cognitive capacity of mammalian species. In addition, the opossums might represent an advisable path to better understand the evolution of cognition in this group.
Journal Article
Life in a harsh environment: the effects of age, sex, reproductive condition, and season on hair cortisol concentration in a wild non-human primate
by
Abreu, Filipa
,
Bicca-Marques, Júlio César
,
Phillips, Kimberley A.
in
Adults
,
Animal Behavior
,
Anthropology
2020
Hair cortisol concentration (HCC) provides a long-term retrospective measure of hypothalamic–pituitary–adrenal axis activity, and is increasingly used to assess the life history, health and ecology of wild mammals. Given that sex, age, season and pregnancy influence HCC, and that it may indicate ongoing stress, we examined HCC in common marmosets ( Callithrix jacchus ) naturally inhabiting a hot and dry semi-desert like habitat, Caatinga, in northeastern Brazil. We trapped, measured, weighed, marked and collected shaved hair from the back of the neck of 61 wild marmosets during the wet and dry seasons. Using enzyme immunoassay, we found that HCC was higher in the dry season compared with the wet season among all age/sex classes. Females had significantly higher HCC than males, juveniles had higher HCC than adults, and reproductively active adult females and non-pregnant/non lactating adult females did not differ in HCC. There were no interaction effects of sex, age, group, or season on HCC. The magnitude of the effect of this extremely hot and dry environment (average yearly rainfall was only 271 mm) on HCC in common marmosets is difficult to ascertain as these animals are also experiencing a variety of other stressors. However, the elevated HCC seen in common marmosets during the 5–8 month dry season, suggests these primates face an extended period of heat, water and possibly nutritional stress, which appears to result in a high rate of juvenile mortality.
Journal Article
Number of adult females in a group affects infant motor development of a cooperative breeding primate (Callithrix jacchus)
by
Malta, Alexandre
,
Schiel, Nicola
,
De la Fuente, María Fernanda
in
Adults
,
Babies
,
Callithrix jacchus
2022
Callitrichids are small Neotropical primates and, due to their cooperative breeding system, infants are of particular interest in research on social dynamics. Although a few studies have investigated the role of helpers in this type of system, there is still a lack of research in field studies seeking to determine whether there is a relationship between the number of helpers (adults) in a social group and the motor development of infants. With that in mind, four groups of wild marmosets (Callithrix jacchus) were observed and the motor behaviors of 1 to 4 month-old infants were recorded. To investigate the influence of the adult:infant ratio on motor diversity, used as an indicator of motor development, we ran a GLMM with a Gaussian distribution and found that: (i) in groups with fewer adults, 2-month-old infants show earlier motor diversity; (ii) motor diversity increases with age regardless of the ratio of adult males per infant; (iii) in groups with more adult females per infant, the motor diversity of 2-month-old infants is significantly lower compared to 3-month-old infants. Although adult callitrichid males play an important role in the care of their offspring, the presence of females appears to be a key factor in motor development at this early stage in the study groups. In a cooperative breeding system, the lack of helpers seems to drive the development of independence in infants, resulting in earlier development.
Journal Article
Indirect influence of global climate change, mediated by nutrition, on anxiety disorders
by
Albuquerque, Ulysses Paulino
,
do Carmo, Rodrigo Felipe Rodrigues
,
Schiel, Nicola
in
Agribusiness
,
Agricultural production
,
Agriculture
2025
Global climate change has profound direct and indirect impacts on human health, including mental health disorders such as anxiety. In this study, we hypothesize the pathways through which climate change contributes to anxiety disorders, with a specific focus on the indirect effects mediated by nutrition. The direct pathway involves environmental stressors such as rising temperatures and extreme climate events, which elevate anxiety levels through chronic stress and uncertainty about the future. The indirect pathway is shaped by climate-induced food insecurity and other dietary and environmental changes, leading to nutritional deficiencies and gut microbiome alterations that disrupt neurological and physiological processes associated with anxiety. Climate change can reduce agricultural diversity and alter the nutritional composition of food, contributing to deficiencies in key micronutrients (e.g., zinc, iron, and B vitamins) essential for neurotransmitter regulation and brain function. Additionally, the increasing prevalence of ultra-processed foods exacerbates these issues. In contrast, climate-induced pathways, such as heat exposure, dehydration, altered food quality, and increased risks of infectious diseases, also affect the gut microbiome, further impacting mental health. There is a reciprocal influence between the gut microbiome and mental health, and a mediation effect of diet and climate-sensitive environmental factors on mental well-being, with disruptions in microbial diversity linked to higher anxiety risks. We propose an integrative framework that illustrates both pathways and highlights the urgency of policy interventions addressing climate-related changes in the food system to mitigate anxiety disorders. Although there is a complex phenomenon in which the policies and strategies of agrifood systems impact food insecurity, we specifically aim to discuss an overlooked aspect of this phenomenon here. We advocate that the understanding of climate change and nutrition is essential for developing effective public health strategies that incorporate environmental sustainability, food security, and mental health resilience.
Journal Article
Group membership, not diet, structures the composition and functional potential of the gut microbiome in a wild primate
by
Abreu, Filipa
,
Amato, Katherine R.
,
Bicca-Marques, Júlio César
in
Animals
,
Animals, Wild - microbiology
,
Bacteria - classification
2024
The gut microbiome has the potential to buffer temporal variations in resource availability and consumption, which may play a key role in the ability of animals to adapt to a broad range of habitats. We investigated the temporal composition and function of the gut microbiomes of wild common marmosets (
) exploiting a hot, dry environment-Caatinga-in northeastern Brazil. We collected fecal samples during two time periods (July-August and February-March) for 2 years from marmosets belonging to eight social groups. We used 16S rRNA gene amplicon sequencing, metagenomic sequencing, and butyrate RT-qPCR to assess changes in the composition and potential function of their gut microbiomes. Additionally, we identified the plant, invertebrate, and vertebrate components of the marmosets' diet via DNA metabarcoding. Invertebrate, but not plant or vertebrate, consumption varied across the year. However, gut microbiome composition and potential function did not markedly vary across study periods or as a function of diet composition. Instead, the gut microbiome differed markedly in both composition and potential function across marmosets residing in different social groups. We highlight the likely role of factors, such as behavior, residence, and environmental heterogeneity, in modulating the structure of the gut microbiome.
In a highly socially cohesive and cooperative primate, group membership more strongly predicts gut microbiome composition and function than diet.
Journal Article
People socialize ecological information about the environment but may forget their own experiences: a case study of local ecological knowledge about seed-dispersing animals
Local ecological knowledge (LEK) has been increasingly used in the search for efficient strategies to maintain biological diversity. However, considering the rapid environmental changes in ecosystems, such knowledge may have been lost between generations, affecting its potential application. In this study, we adopted the LEK of the potential dispersers of Caryocar coriaceum Wittm. (Caryocaraceae), an endangered plant species of socioeconomic and cultural importance from northeast Brazil, as a model. We evaluated whether there is intergenerational variation in the LEK about the abundance of Dasyprocta prymnolopha (the principal disperser of C. coriaceum) associated with the local practice of hunting. We collected LEK data from 39 hunter-gatherers aged 31 to 84 years, and camera traps were used during two annual C. coriaceum harvests to record its potential dispersers. Our results indicate that the LEK of the potential animal dispersers of C. coriaceum does not vary between generations; it is disseminated and shared between different generations. The strong interactions among people during the C. coriaceum harvest period facilitate the sharing of information about the potential dispersers of this species. Our results show that hunting D. prymnolopha does not depend on perceptions regarding the availability of this resource in the forest, which may be causing overexploitation. Therefore, local knowledge may need to be updated and connected to the recent and rapid environmental changes because people may believe that current environmental conditions are like those of the past. If this is the case, people may be less cooperative with conservation strategies because they are not aware of environmental changes, so measures to update knowledge about environmental conditions may be necessary to encourage effective participation in management and conservation plans.
Journal Article
The Maintenance of Traditions in Marmosets: Individual Habit, Not Social Conformity? A Field Experiment
by
Pesendorfer, Mario B.
,
Schiel, Nicola
,
Range, Friederike
in
Animal cognition
,
Animal experimentation
,
Animals
2009
Social conformity is a cornerstone of human culture because it accelerates and maintains the spread of behaviour within a group. Few empirical studies have investigated the role of social conformity in the maintenance of traditions despite an increasing body of literature on the formation of behavioural patterns in non-human animals. The current report presents a field experiment with free-ranging marmosets (Callithrix jacchus) which investigated whether social conformity is necessary for the maintenance of behavioural patterns within groups or whether individual effects such as habit formation would suffice.
Using a two-action apparatus, we established alternative behavioural patterns in six family groups composed of 36 individuals. These groups experienced only one technique during a training phase and were thereafter tested with two techniques available. The monkeys reliably maintained the trained method over a period of three weeks, despite discovering the alternative technique. Three additional groups were given the same number of sessions, but those 21 individuals could freely choose the method to obtain a reward. In these control groups, an overall bias towards one of the two methods was observed, but animals with a different preference did not adjust towards the group norm. Thirteen of the fifteen animals that discovered both techniques remained with the action with which they were initially successful, independent of the group preference and the type of action (Binomial test: exp. proportion: 0.5, p<0.01).
The results indicate that the maintenance of behavioural patterns within groups 1) could be explained by the first rewarded manipulation and subsequent habit formation and 2) do not require social conformity as a mechanism. After an initial spread of a behaviour throughout a group, this mechanism may lead to a superficial appearance of conformity without the involvement of such a socially and cognitively complex mechanism. This is the first time that such an experiment has been conducted with free-ranging primates.
Journal Article