Lévy movements and a slowly decaying memory allow efficient collective learning in groups of interacting foragers.

Many animal species benefit from spatial learning to adapt their foraging movements to the distribution of resources. Learning involves the collection, storage and retrieval of information, and depends on both the random search strategies employed and the memory capacities of the individual. For animals living in social groups, spatial learning can be further enhanced by information transfer among group members. However, how individual behavior affects the emergence of collective states of learning is still poorly understood. Here, with the help of a spatially explicit agent-based model where individuals transfer information to their peers, we analyze the effects on the use of resources of varying memory capacities in combination with different exploration strategies, such as ordinary random walks and Lévy flights. We find that individual Lévy displacements associated with a slow memory decay lead to a very rapid collective response, a high group cohesion and to an optimal exploitation of the best resource patches in static but complex environments, even when the interaction rate among individuals is low.

Group size and mating system predict sex differences in vocal fundamental frequency in anthropoid primates.

Vocalizations differ substantially between the sexes in many primates, and low-frequency male vocalizations may be favored by sexual selection because they intimidate rivals and/or attract mates. Sexual dimorphism in fundamental frequency may be more pronounced in species with more intense male mating competition and in those with large group size, where social knowledge is limited and efficient judgment of potential mates and competitors is crucial. These non-mutually exclusive explanations have not been tested simultaneously across primate species. In a sample of vocalizations (n = 1914 recordings) across 37 anthropoid species, we investigated whether fundamental frequency dimorphism evolved in association with increased intensity of mating competition (H1), large group size (H2), multilevel social organization (H3), a trade-off against the intensity of sperm competition (H4), and/or poor acoustic habitats (H5), controlling for phylogeny and body size dimorphism. We show that fundamental frequency dimorphism increased in evolutionary transitions towards larger group size and polygyny. Findings suggest that low-frequency male vocalizations in primates may have been driven by selection to win mating opportunities by avoiding costly fights and may be more important in larger groups, where limited social knowledge affords advantages to rapid assessment of status and threat potential via conspicuous secondary sexual characteristics.

Barriers and bridges on water management in rural Mexico: from water-quality monitoring to water management at the community level.

Access to sufficient water of suitable quality represents a challenge for achieving several dimensions of sustainable development. Currently, water access is restricted to three of 10 persons globally. In rural areas of Mexico and other low-income countries, coverage could be even less due to the absence of formal supply; thus, rural communities usually perform water management. Surrounding community-based water management, various socio-ecological interactions emerge that determine access to water. Access to water will depend on the obstacles or capacities that arise within the socio-ecological system in which the community is immersed. This work identifies barriers and bridges to water access in a rural environment through mixed methods. The article draws on three case studies in southeastern Mexico by analyzing 90 questionnaires conducted at the household level and three focus groups in parallel with water quality analysis and its relationship with management practices. The barriers and bridges were classified into six water access challenges: (i) access to water in a sufficient quantity, (ii) access to water of adequate quality, (iii) access to water for household crop irrigation, (iv) hygiene and sanitation facilities, (v) collective organization, and (vi) climate variability. The main findings indicate that households' water quantity and quality show deficiencies due to the lack of formal infrastructure and represent a health risk. Water fetching has the highest impact on women and children in poor rural areas, and it is a significant barrier to sustainable development. In contrast, the collective organization proved to be an essential bridge for water access in these communities.

Social complexity as a driving force of gut microbiota exchange among conspecific hosts in non-human primates.

The emergent concept of the social microbiome implies a view of a highly connected biological world, in which microbial interchange across organisms may be influenced by social and ecological connections occurring at different levels of biological organization. We explore this idea reviewing evidence of whether increasing social complexity in primate societies is associated with both higher diversity and greater similarity in the composition of the gut microbiota. By proposing a series of predictions regarding such relationship, we evaluate the existence of a link between gut microbiota and primate social behavior. Overall, we find that enough empirical evidence already supports these predictions. Nonetheless, we conclude that studies with the necessary, sufficient, explicit, and available evidence are still scarce. Therefore, we reflect on the benefit of founding future analyses on the utility of social complexity as a theoretical framework.

Flexible use of contact calls in a species with high fission-fusion dynamics.

The 'social complexity hypothesis' posits that complex social systems (which entail high uncertainty) require complex communicative systems (with high vocal flexibility). In species with fission-fusion dynamics, where the fluid composition of temporary subgroups increases the uncertainty with which group members must manage their social relationships, vocal communication must be particularly flexible. This study assessed whether contact call rates vary with caller and audience characteristics in free-living spider monkeys, as well as with fission and fusion events. Adult females and immature individuals called more when in small audience settings, while audience size did not influence adult males. Adults called more when in the presence of the opposite sex, whereas immatures vocalized more in subgroups composed only by females. Females also called more when with their mature sons. We found higher call rates in periods during which fission and fusion events took place than in periods with more stable compositions and when the composition after a fission or fusion event changed from one sex to two sexes. A flexible use of contact calls allows individuals to identify themselves when they join others, particularly if they are members of the opposite sex. This socio-spatial cohesion function reduces the uncertainty about subgroup composition. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Using natural travel paths to infer and compare primate cognition in the wild.

Within comparative psychology, the evolution of animal cognition is typically studied either by comparing indirect measures of cognitive abilities (e.g., relative brain size) across many species or by conducting batteries of decision-making experiments among (typically) a few captive species. Here, we propose a third, complementary approach: inferring and comparing cognitive abilities through observational field records of natural information gradients and the associated variation in decision-making outcomes, using the ranging behavior of wild animals. To demonstrate the feasibility of our proposal, we present the results of a global survey assessing the availability of long-term ranging data sets from wild primates and the willingness of primatologists to share such data. We explore three ways in which such ranging data, with or without the associated behavioral and ecological data often collected by primatologists, might be used to infer and compare spatial cognition. Finally, we suggest how ecological complexity may be best incorporated into comparative analyses.

Collective Rhythm as an Emergent Property During Human Social Coordination.

The literature on social interactions has shown that participants coordinate not only at the behavioral but also at the physiological and neural levels, and that this coordination gives a temporal structure to the individual and social dynamics. However, it has not been fully explored whether such temporal patterns emerge during interpersonal coordination beyond dyads, whether this phenomenon arises from complex cognitive mechanisms or from relatively simple rules of behavior, or which are the sociocultural processes that underlie this phenomenon. We review the evidence for the existence of group-level rhythmic patterns that result from social interactions and argue that the complexity of group dynamics can lead to temporal regularities that cannot be predicted from the individual periodicities: an emergent collective rhythm. Moreover, we use this interpretation of the literature to discuss how taking into account the sociocultural niche in which individuals develop can help explain the seemingly divergent results that have been reported on the social influences and consequences of interpersonal coordination. We make recommendations on further research to test these arguments and their relationship to the feeling of belonging and assimilation experienced during group dynamics.

Collective Computation in Animal Fission-Fusion Dynamics.

Recent work suggests that collective computation of social structure can minimize uncertainty about the social and physical environment, facilitating adaptation. We explore these ideas by studying how fission-fusion social structure arises in spider monkey (Ateles geoffroyi) groups, exploring whether monkeys use social knowledge to collectively compute subgroup size distributions adaptive for foraging in variable environments. We assess whether individual decisions to stay in or leave subgroups are conditioned on strategies based on the presence or absence of others. We search for this evidence in a time series of subgroup membership. We find that individuals have multiple strategies, suggesting that the social knowledge of different individuals is important. These stay-leave strategies provide microscopic inputs to a stochastic model of collective computation encoded in a family of circuits. Each circuit represents an hypothesis for how collectives combine strategies to make decisions, and how these produce various subgroup size distributions. By running these circuits forward in simulation we generate new subgroup size distributions and measure how well they match food abundance in the environment using transfer entropies. We find that spider monkeys decide to stay or go using information from multiple individuals and that they can collectively compute a distribution of subgroup size that makes efficient use of ephemeral sources of nutrition. We are able to artificially tune circuits with subgroup size distributions that are a better fit to the environment than the observed. This suggests that a combination of measurement error, constraint, and adaptive lag are diminishing the power of collective computation in this system. These results are relevant for a more general understanding of the emergence of ordered states in multi-scale social systems with adaptive properties-both natural and engineered.

Proprioception in Action: A Matter of Ecological and Social Interaction.

The aim of this paper is to provide a theoretical and formal framework to understand how the proprioceptive and kinesthetic system learns about body position and possibilities for movement in ongoing action and interaction. Whereas most weak embodiment accounts of proprioception focus on positionalist descriptions or on its role as a source of parameters for internal motor control, we argue that these aspects are insufficient to understand how proprioception is integrated into an active organized system in continuous and dynamic interaction with the environment. Our strong embodiment thesis is that one of the main theoretical principles to understand proprioception, as a perceptual experience within concrete situations, is the coupling with kinesthesia and its relational constitution-self, ecological, and social. In our view, these aspects are underdeveloped in current accounts, and an enactive sensorimotor theory enriched with phenomenological descriptions may provide an alternative path toward explaining this skilled experience. Following O'Regan and Noë (2001) sensorimotor contingencies conceptualization, we introduce three distinct notions of proprioceptive kinesthetic-sensorimotor contingencies (PK-SMCs), which we describe conceptually and formally considering three varieties of perceptual experience in action: PK-SMCs-self, PK-SMCs-self-environment, and PK-SMC-self-other. As a proof of concept of our proposal, we developed a minimal PK model to discuss these elements in detail and show their explanatory value as important guides to understand the proprioceptive/kinesthetic system. Finally, we also highlight that there is an opportunity to develop enactive sensorimotor theory in new directions, creating a bridge between the varieties of experiences of oneself and learning skills.

Ecological and social determinants of association and proximity patterns in the fission-fusion society of spider monkeys (Ateles geoffroyi).

Some social species exhibit high levels of fission-fusion dynamics (FFD) that improve foraging efficiency. In this study, we shed light on the way that FFD allows animal groups to cope with fluctuations in fruit availability. We explore the relative contribution of fruit availability and social factors like sex in determining association and proximity patterns in spider monkeys. We tested the influence of fruit availability and social factors on the association and proximity patterns using three-year data from a group of spider monkeys in the Yucatan Peninsula of Mexico. We identified subgroup members and estimated their Interindividual distances through instantaneous scan sampling. We evaluated fruit availability by monitoring the phenology of the 10 most important food tree species for spider monkeys in the study site. Social network analyses allowed us to evaluate association and proximity patterns in subgroups. We showed that association patterns vary between seasons, respond to changes in fruit availability, and are influenced by the sex of individuals, likely reflecting biological and behavioral differences between sexes and the interplay between ecological and social factors. In contrast, proximity patterns were minimally affected by changes in fruit availability, suggesting that social factors are more important than food availability in determining cohesion within subgroups.

Horizontal seed dispersal by dung beetles reduced seed and seedling clumping, but did not increase short-term seedling establishment.

Dung beetles are secondary seed dispersers, incidentally moving many of the seeds defecated by mammals vertically (seed burial) and/or horizontally as they process and relocate dung. Although several studies have quantified this ecological function of dung beetles, very few have followed seed fate until seedling establishment, and most of these have focused on the effects of seed burial. We know very little about the effects of horizontal seed movement by dung beetles, though it is generally assumed that it will affect plant recruitment positively through diminishing seed clumping. The objective of our study was to assess the effects of dung beetle activity on the spatial distribution of seeds and seedlings, and on the probability of seedling establishment. In a tropical rainforest in Mexico we carried out two complementary field experiments for each of two tree species (Bursera simaruba and Poulsenia armata), using seeds experimentally imbedded in pig dung and recording their fate and spatial location over time. For both species, dung beetle activity reduced the spatial clumping of seeds and seedlings; however, it did not increase the probability of seedling establishment. We discuss the context- and species-specificity of the combined effects of horizontal and vertical dispersal of seeds by dung beetles, and the need to quantify long-term seedling fates to more accurately determine the effects of seed movement by dung beetles on plant recruitment.

Collective learning from individual experiences and information transfer during group foraging.

Living in groups brings benefits to many animals, such as protection against predators and an improved capacity for sensing and making decisions while searching for resources in uncertain environments. A body of studies has shown how collective behaviours within animal groups on the move can be useful for pooling information about the current state of the environment. The effects of interactions on collective motion have been mostly studied in models of agents with no memory. Thus, whether coordinated behaviours can emerge from individuals with memory and different foraging experiences is still poorly understood. By means of an agent-based model, we quantify how individual memory and information fluxes can contribute to improving the foraging success of a group in complex environments. In this context, we define collective learning as a coordinated change of behaviour within a group resulting from individual experiences and information transfer. We show that an initially scattered population of foragers visiting dispersed resources can gradually achieve cohesion and become selectively localized in space around the most salient resource sites. Coordination is lost when memory or information transfer among individuals is suppressed. The present modelling framework provides predictions for empirical studies of collective learning and could also find applications in swarm robotics and motivate new search algorithms based on reinforcement.

Using multiplex networks to capture the multidimensional nature of social structure.

Network analysis has increasingly expanded our understanding of social structure in primates and other animal species. However, most studies use networks representing only one interaction type, when social relationships (and the emerging social structure) are the result of many types of interactions and their interplay through time. The recent development of tools facilitating the integrated analysis of multiple interaction types using multiplex networks has opened the possibility of extending the insight provided by social network analysis. We use a multiplex representation of interactions among the members of a group of wild Geoffroy's spider monkeys (Ateles geoffroyi), to study their social structure. We constructed a six-layered multiplex network based on three indices of overt social interactions (aggression, embraces, grooming) and three distance-based indices (contact, proximity, and association). With tools provided by the MuxViz software, we assessed the relevance of including all six indices in our analysis, the role of individuals in the network (through node versatility), and the presence of modules and non-random triadic structures or motifs. The multiplex provided information which was not equivalent to any individual layer or to the simple aggregation of layers. Network patterns based on associations did not correspond with those observed for overt-interactions or for the multiplex structure. Males were the most versatile individuals, while multiplex modularity and motifs highlighted the relevance of different interaction types for the overall connectivity of the network. We conclude that the multiplex approach improves on previous methods by retaining valuable information from each interaction type and how it is patterned among individuals.

Predation Attacks on Wild Spider Monkeys (Ateles geoffroyi).

We report 2 cases of predation on an adult and a subadult spider monkey (Ateles geoffroyi) by a puma (Puma concolor) and an unidentified terrestrial predator at the natural protected area of Otoch Ma'ax yetel Kooh, in the Yucatan Peninsula, Mexico. Although spider monkeys are believed to experience overall low predation pressure compared to other primate species, our observations show that predation occurs in the study area and therefore behavioral strategies are likely to be in place to reduce predation risk. Our observations are further evidence that terrestrial predators are a threat for both young and full-grown spider monkeys.

Integrating expert knowledge and ecological niche models to estimate Mexican primates' distribution.

Ecological niche modeling is used to estimate species distributions based on occurrence records and environmental variables, but it seldom includes explicit biotic or historical factors that are important in determining the distribution of species. Expert knowledge can provide additional valuable information regarding ecological or historical attributes of species, but the influence of integrating this information in the modeling process has been poorly explored. Here, we integrated expert knowledge in different stages of the niche modeling process to improve the representation of the actual geographic distributions of Mexican primates (Ateles geoffroyi, Alouatta pigra, and A. palliata mexicana). We designed an elicitation process to acquire information from experts and such information was integrated by an iterative process that consisted of reviews of input data by experts, production of ecological niche models (ENMs), and evaluation of model outputs to provide feedback. We built ENMs using the maximum entropy algorithm along with a dataset of occurrence records gathered from a public source and records provided by the experts. Models without expert knowledge were also built for comparison, and both models, with and without expert knowledge, were evaluated using four validation metrics that provide a measure of accuracy for presence-absence predictions (specificity, sensitivity, kappa, true skill statistic). Integrating expert knowledge to build ENMs produced better results for potential distributions than models without expert knowledge, but a much greater improvement in the transition from potential to realized geographic distributions by reducing overprediction, resulting in better representations of the actual geographic distributions of species. Furthermore, with the combination of niche models and expert knowledge we were able to identify an area of sympatry between A. palliata mexicana and A. pigra. We argue that the inclusion of expert knowledge at different stages in the construction of niche models in an explicit and systematic fashion is a recommended practice as it produces overall positive results for representing realized species distributions.

Quantifying uncertainty due to fission-fusion dynamics as a component of social complexity.

Groups of animals (including humans) may show flexible grouping patterns, in which temporary aggregations or subgroups come together and split, changing composition over short temporal scales, (i.e. fission and fusion). A high degree of fission-fusion dynamics may constrain the regulation of social relationships, introducing uncertainty in interactions between group members. Here we use Shannon's entropy to quantify the predictability of subgroup composition for three species known to differ in the way their subgroups come together and split over time: spider monkeys (Ateles geoffroyi), chimpanzees (Pan troglodytes) and geladas (Theropithecus gelada). We formulate a random expectation of entropy that considers subgroup size variation and sample size, against which the observed entropy in subgroup composition can be compared. Using the theory of set partitioning, we also develop a method to estimate the number of subgroups that the group is likely to be divided into, based on the composition and size of single focal subgroups. Our results indicate that Shannon's entropy and the estimated number of subgroups present at a given time provide quantitative metrics of uncertainty in the social environment (within which social relationships must be regulated) for groups with different degrees of fission-fusion dynamics. These metrics also represent an indirect quantification of the cognitive challenges posed by socially dynamic environments. Overall, our novel methodological approach provides new insight for understanding the evolution of social complexity and the mechanisms to cope with the uncertainty that results from fission-fusion dynamics.

How Survey Design Affects Monkey Counts: A Case Study on Individually Recognized Spider Monkeys (Ateles geoffroyi).

The fast movement and high degree of fission-fusion dynamics of spider monkeys (Ateles spp.) make them notoriously difficult to survey. We examined which aspects of survey design affect spider monkey sightings along transects in a group of individually recognized spider monkeys (Ateles geoffroyi) in Punta Laguna, Yucatan, Mexico. We calculated the number of monkeys and subgroups sighted per transect walk. Using generalized linear models, we found no effect of the number of observers, transect type (new vs. existing), walking speed, or time of day on individual monkey counts or subgroup counts. Recounting of individuals was relatively rare and occurred when transects were walked relatively slowly. We missed more young than adult monkeys. The group composition based on survey data was similar to the known group composition. Based on our findings we recommend that surveys performed on relatively flat terrain be conducted at speeds similar to or faster than the moving speed of spider monkeys to minimize recounting of individuals and that young:adult female ratios based on survey data be interpreted as conservative indicators of population health. The novel methods presented to determine sources of bias in population estimates are applicable to a wide range of primates that are difficult to survey.

Seasonal Changes in Socio-Spatial Structure in a Group of Free-Living Spider Monkeys (Ateles geoffroyi).

Ecological and social factors influence individual movement and group membership decisions, which ultimately determine how animal groups adjust their behavior in spatially and temporally heterogeneous environments. The mechanisms behind these behavioral adjustments can be better understood by studying the relationship between association and space use patterns of groups and how these change over time. We examined the socio-spatial patterns of adult individuals in a free-ranging group of spider monkeys (Ateles geoffroyi), a species with high fission-fusion dynamics. Data comprised 4916 subgroup scans collected during 325 days throughout a 20-month period and was used to evaluate changes from fruit-scarce to fruit-abundant periods in individual core-area size, subgroup size and two types of association measures: spatial (core-area overlap) and spatio-temporal (occurrence in the same subgroup) associations. We developed a 3-level analysis framework to distinguish passive associations, where individuals are mostly brought together by resources of common interest, from active association, where individuals actively seek or avoid certain others. Results indicated a more concentrated use of space, increased individual gregariousness and higher spatio-temporal association rates in the fruit-abundant seasons, as is compatible with an increase in passive associations. Nevertheless, results also suggested active associations in all the periods analyzed, although associations differed across seasons. In particular, females seem to actively avoid males, perhaps prompted by an increased probability of random encounters among individuals, resulting from the contraction of individual core areas. Our framework proved useful in investigating the interplay between ecological and social constraints and how these constraints can influence individual ranging and grouping decisions in spider monkeys, and possibly other species with high fission-fusion dynamics.

Sexual selection on male vocal fundamental frequency in humans and other anthropoids.

In many primates, including humans, the vocalizations of males and females differ dramatically, with male vocalizations and vocal anatomy often seeming to exaggerate apparent body size. These traits may be favoured by sexual selection because low-frequency male vocalizations intimidate rivals and/or attract females, but this hypothesis has not been systematically tested across primates, nor is it clear why competitors and potential mates should attend to vocalization frequencies. Here we show across anthropoids that sexual dimorphism in fundamental frequency (F0) increased during evolutionary transitions towards polygyny, and decreased during transitions towards monogamy. Surprisingly, humans exhibit greater F0 sexual dimorphism than any other ape. We also show that low-F0 vocalizations predict perceptions of men's dominance and attractiveness, and predict hormone profiles (low cortisol and high testosterone) related to immune function. These results suggest that low male F0 signals condition to competitors and mates, and evolved in male anthropoids in response to the intensity of mating competition.