Microbes influence a wide range of host social behaviors and vice versa. So far, however, the mechanisms underpinning these complex interactions remain poorly understood. In social animals, where individuals share microbes and interact around foods, the gut microbiota may have considerable consequences on host social interactions by acting upon the nutritional behavior of individual animals. Here we illustrate how conceptual advances in nutritional ecology can help the study of these processes and allow the formulation of new empirically testable predictions. First, we review key evidence showing that gut microbes influence the nutrition of individual animals, through modifications of their nutritional state and feeding decisions. Next, we describe how these microbial influences and their social consequences can be studied by modelling populations of hosts and their gut microbiota into a single conceptual framework derived from nutritional geometry. Our approach raises new perspectives for the study of holobiont nutrition and will facilitate theoretical and experimental research on the role of the gut microbiota in the mechanisms and evolution of social behavior.

Individual bees exhibit complex movement patterns to efficiently exploit small areas within larger plant populations. How such individual spatial behaviours scale up to the collective level, when several foragers visit a common area, has remained challenging to investigate, both because of the low resolution of field movement data and the limited power of the statistical descriptors to analyse them. To tackle these issues we video recorded all flower visits (N = 6205), and every interaction on flowers (N = 628), involving foragers from a bumblebee (Bombus terrestris) colony in a large outdoor flight cage (880 m²), containing ten artificial flowers, collected on five consecutive days, and analysed bee movements using networks statistics. Bee-flower visitation networks were significantly more modular than expected by chance, indicating that foragers minimized overlaps in their patterns of flower visits. Resource partitioning emerged from differences in foraging experience among bees, and from outcomes of their interactions on flowers. Less experienced foragers showed lower activity and were more faithful to some flowers, whereas more experienced foragers explored the flower array more extensively. Furthermore, bees avoided returning to flowers from which they had recently been displaced by a nestmate, suggesting that bees integrate memories of past interactions into their foraging decisions. Our observations, under high levels of competition in a flight cage, suggest that the continuous turnover of foragers observed in colonies can led to efficient resource partitioning among bees in natural conditions.

Parasites alter the physiology and behaviour of their hosts. In domestic honey bees, the microsporidia Nosema ceranae induces energetic stress that impairs the behaviour of foragers, potentially leading to colony collapse. Whether this parasite similarly affects wild pollinators is little understood because of the low success rates of experimental infection protocols. Here, we present a new approach for infecting bumblebees (Bombus terrestris) with controlled amounts of N. ceranae by briefly exposing individual bumblebees to parasite spores before feeding them with artificial diets. We validated our protocol by testing the effect of two spore dosages and two diets varying in their protein to carbohydrate ratio on the prevalence of the parasite (proportion of PCR-positive bumblebees), the intensity of parasites (spore count in the gut and the faeces), and the survival of bumblebees. Overall, insects fed a low-protein, high-carbohydrate diet showed the highest parasite prevalence (up to 70%) but lived the longest, suggesting that immunity and survival are maximised at different protein to carbohydrate ratios. Spore dosage did not affect parasite infection rate and host survival. The identification of experimental conditions for successfully infecting bumblebees with N. ceranae in the lab will facilitate future investigations of the sub-lethal effects of this parasite on the behaviour and cognition of wild pollinators.

Central place foraging pollinators tend to develop multi-destination routes (traplines) to exploit patchily distributed plant resources. While the formation of traplines by individual pollinators has been studied in detail, how populations of foragers use resources in a common area is an open question, difficult to address experimentally. We explored conditions for the emergence of resource partitioning among traplining bees using agent-based models built from experimental data of bumblebees foraging on artificial flowers. In the models, bees learn to develop routes as a consequence of feedback loops that change their probabilities of moving between flowers. While a positive reinforcement of movements leading to rewarding flowers is sufficient for the emergence of resource partitioning when flowers are evenly distributed, the addition of a negative reinforcement of movements leading to unrewarding flowers is necessary when flowers are patchily distributed. In environments with more complex spatial structures, the negative experiences of individual bees on flowers favour spatial segregation and efficient collective foraging. Our study fills a major gap in modelling pollinator behaviour and constitutes a unique tool to guide future experimental programs.