Choosing the best way: how wild common marmosets travel to efficiently exploit resources.

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.

Temperature and exudativory as drivers of the marmoset (Callithrix spp.) daily activity period.

Primates are affected by fluctuations in ambient temperatures, mostly through thermoregulatory costs and changes in the availability of food. In the present study, we investigate whether the ambient temperature and proxies of food availability affect the activity period of marmosets (Callithrix spp.). We predicted that: (i) at colder sites, marmosets would spend more time at sleeping sites; (ii) midday resting bouts would be longer at hotter sites; (iii) the onset/cessation of activity and resting behavior at midday would be more closely related to temperature than food availability, and (iv) highly exudativorous groups would have higher total levels of resting. We compiled data on the onset and cessation of activity and the time spent resting at midday from seven marmoset studies from sites with a wide range of temperatures. We used generalized linear mixed models to verify the relationship between the dependent variables (lag between dawn and the onset of activities, lag between cessation of activities and dusk, and proportion of resting during midday) and the minimum and maximum temperatures at the respective study sites, together with proxies of food availability (exudativory rates, the amount of habitat available per individual, and net primary productivity) using each sample month as a sampling unit and the identity of the study as a categorical random factor. At colder sites and during colder months, the marmosets left sleeping trees later in the morning and ceased their activities earlier, while at hotter sites and during hotter months, they spent more time resting during midday. More exudativorous groups become active later in the morning, but also ceased their activities later. The abundance of food did not affect the timing of activities. We provide evidence that both low and high temperatures affect marmosets' activities, and that their activity period appears to be more influenced by the thermal environment than food availability.

Navigating in a challenging semiarid environment: the use of a route-based mental map by a small-bodied neotropical primate.

To increase efficiency in the search for resources, many animals rely on their spatial abilities. Specifically, primates have been reported to use mostly topological and rarely Euclidean maps when navigating in large-scale space. Here, we aimed to investigate if the navigation of wild common marmosets inhabiting a semiarid environment is consistent with a topological representation and how environmental factors affect navigation. We collected 497 h of direct behavioral and GPS information on a group of marmosets using a 2-min instantaneous focal animal sampling technique. We found that our study group reused not only long-route segments (mean of 1007 m) but entire daily routes, a pattern that is not commonly seen in primates. The most frequently reused route segments were the ones closer to feeding sites, distant to resting sites, and in areas sparse in tree vegetation. We also identified a total of 56 clustered direction change points indicating that the group modified their direction of travel. These changes in direction were influenced by their close proximity to resting and feeding sites. Despite our small sample size, the obtained results are important and consistent with the contention that common marmosets navigate using a topological map that seems to benefit these animals in response to the exploitation of clustered exudate trees. Based on our findings, we hypothesize that the Caatinga landscape imposes physical restrictions in our group's navigation such as gaps in vegetation, small trees and xerophytic plants. This study, based on preliminary evidence, raises the question of whether navigation patterns are an intrinsic characteristic of a species or are ecologically dependent and change according to the environment.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

Detection of insect prey by wild common marmosets: The effect of color vision.

Most species of New World primates have an unusual color vision pattern that can affect an individual's ability to detect food. Whereas males can only be dichromatic, females can be either dichromatic or trichromatic. Trichromats are expected to have an advantage in detecting conspicuous food whereas dichromats should be better at locating cryptic resources. Here we aimed to understand how color vision phenotype influences insect foraging by five groups of common marmosets living in a semiarid environment. We recorded insect predation events, noting morphotype and color of the captured insect, and the substrate from which it was captured. Color modeling suggested that, for all values of chromatic contrast resulting from comparing the measured insect-substrate pairs, trichromats outperformed dichromats. Females showed an overall higher insect capture rate than males. Females also showed a higher capture rate of conspicuous insects but there was no sex difference for the capture of cryptic insects. When we compared only dichromatic individuals there was no difference between sexes. These findings suggest that differences found in capture rate related not only to sex but also to visual polymorphism and that the latter is a crucial factor determining insect capture rate in common marmosets. Nevertheless, these results should be interpreted with caution because of the small number (three) of dichromat females and the unknown phenotype of the remaining females. Our results support the balancing selection hypothesis, suggesting that the advantage of one phenotype over the other may depend on environmental circumstances. This hypothesis has recently been considered as the most plausible for the maintenance of visual polymorphism in New World primates.

Trait variation and trait stability in common marmosets (Callithrix jacchus) inhabiting ecologically distinct habitats in northeastern Brazil.

Understanding the set of factors that promote and constrain a species' ability to exploit ecologically distinct habitats is central for addressing questions of intraspecific variability in behavior and morphology. In this study, we compared newly collected data with published data on body measurements, group size and composition, daily path length, home range, and reproductive output in wild common marmosets naturally inhabiting two contrasting environments in northeastern Brazil: the Atlantic Forest (AF), which is characterized by high biodiversity and reduced seasonality in food availability and the Caatinga (CAT), which is characterized by a severe hot and dry season lasting from 5 to 11 months, drought-resistant plant species, and reduced primary productivity. Despite marked differences in ecological conditions, CAT marmosets and AF marmosets differed minimally in daily path length, home range, reproductive output, and infant survivorship. CAT marmosets were found to live in smaller groups containing fewer adult females than AF marmosets, and also were characterized by a greater surface area to body mass ratio, a trait that may represent an adaptation to the hot and dry conditions of the Caatinga. We propose that in conjunction with body mass reduction, minor adjustments in behavior, the exploitation of cacti as a source of water and nutrients, and access to exudates as a dependable year-round food resource, common marmosets successfully used the same adaptive pattern to maintain high reproductive output and infant survivorship in exploiting these two ecologically distinct environments.

Group membership, not diet, structures the composition and functional potential of the gut microbiome in a wild primate.

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 (Callithrix jacchus) 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. IMPORTANCE: In a highly socially cohesive and cooperative primate, group membership more strongly predicts gut microbiome composition and function than diet.

Mediterranean diet adherence and nutritional literacy: an observational cross-sectional study of the reality of university students in a COVID-19 pandemic context.

Aim: To evaluate the adherence to the Mediterranean diet (MD) and the level of nutritional literacy (NL) among university students from different academic fields of study, within the context of the COVID-19 pandemic. Methods: A total of 1114 first-year undergraduate students at the University of Lisbon, Portugal, were included in this study. A self-administered online questionnaire was applied that included questions regarding sociodemographic information, the MD measured by the PREDIMED questionnaire (PREvención con DIeta MEDiterránea) and NL assessed using the Newest Vital Sign questionnaire. Results: The average PREDIMED score revealed a low adherence (6.79±2.14 points) to the MD. Notably, students in the Social Sciences and Humanities academic fields showed the highest level of adherence (U=21 071; p<0.05). Within the Health field, there was a greater prevalence of dietary behaviours aligned with the MD, contributing to higher overall adherence scores. Furthermore, 84.1% of the participants demonstrated adequate NL. Interestingly, students in the Exact Sciences and Engineering field demonstrated the highest levels of NL (5.07±1.19), particularly in questions involving mathematical reasoning. Conclusions: Our findings suggest that university students in Lisbon do not follow a MD and are far from the recommendations of this dietary pattern. While most participants showed adequate NL, it is essential to highlight the link between knowledge and application to daily practice. Despite positive literacy levels, there remains a deficit in translating this knowledge into correct dietary practices.

Wild common marmosets (Callithrix jacchus) employ spatial cognitive abilities to improve their food search and consumption: an experimental approach in small-scale space.

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.

Life in a harsh environment: the effects of age, sex, reproductive condition, and season on hair cortisol concentration in a wild non-human primate.

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.