The effect of idiosyncrasy on aggregation in group-living organisms.

We use a minimalistic mathematical model with a limited number of parameters to evaluate the impact of interindividual differences in the collective decision-making of a group. As it turns out, in most cases, heterogeneous groups are more efficient in their decision-making than homogenous ones, especially when considering small group sizes. In reality, being different disfavours the emergence of an hysteresis and a collective threshold which are characteristics of such cooperative species while keeping inter-attractions the same between individuals. Finally, when the cooperativity becomes very large, we observe an explosion of accessible stable states.

Schooling in habitats with aggregative sites: The case of tropical tuna and floating objects.

Many marine and terrestrial species live in groups, whose sizes and dynamics can vary depending on the type and strength of their social interactions. Typical examples of such groups in vertebrates are schools of fish or flocks of bird. Natural habitats can encompass a wide range of spatial heterogeneities, which can also shape the structure of animal groups, depending on the interplay between the attraction/repulsion of environmental cues and social interactions. A key issue in modern applied ecology and conservation is the need to understand the relationship between these ethological and ecological scales in order to account for the social behaviour of animals in their natural environments. Here, we introduce a modeling approach which studies animal groups within heterogeneous habitats constituted by a set of aggregative sites. The model properties are investigated considering the case study of tropical tuna schools and their associative behavior with floating objects, a question of global concern, given the thousands of floating objects deployed by industrial tropical tuna fisheries worldwide. The effects of increasing numbers of aggregative sites (floating objects) on tuna schools are studied. This study offers a general modeling framework to study social species in their habitats, accounting for both ethological and ecological drivers of animal group dynamics.

Food dissemination in ants: robustness of the trophallactic network against resource quality.

Insect societies are often composed of many individuals, achieving collective decisions that depend on environmental and colonial characteristics. For example, ants are able to focus their foraging effort on the most rewarding food source. While this phenomenon is well known, the link between the food source quality and the intranidal food dissemination networks and its dynamics has been neglected. Here, we analysed the global dynamics of food dissemination in Camponotus cruentatus workers, after feeding on a low (0.1 mol l-1) or on a high (1 mol l-1) sucrose concentration food source. We also analysed the trophallaxis activity at the individual level and built the complete network of trophallaxis. The results reveal that the dynamics of food dissemination and the structure of the trophallaxis network are robust and independent of the food concentration. We discuss these results in the light of recent advances in the study of efficiency in food management in ants.

Symmetry breaking and inter-clonal behavioural variability in a slime mould.

Cells are dynamic systems capable of switching from isotropic growth to polarized growth even in the absence of any pre-existing external asymmetry. Here, we study this process of symmetry breaking in the acellular slime mould Physarum polycephalum. In these experiments, slime moulds could grow on two identical opposed sources of calcium. We highlighted a positive correlation between growth dynamic, level of symmetry breaking and calcium concentration. We identified three populations of slime moulds within our clonal lineage with similar symmetry breaking behaviours but different motility characteristics. These behavioural differences between slime moulds emerged in the absence of any environmental differences. Such behavioural plasticity could generate cellular diversity, which can be critical for survival.

Same length, different shapes: ants collectively choose a straight foraging path over a bent one.

In socials insects, exploration is fundamental for the discovery of food resources and determines decision-making. We investigated how the interplay between the physical characteristics of the paths leading to food sources and the way it impacts the behaviour of individual ants affects their collective decisions. Colonies of different sizes of Lasius niger had access to two equal food sources through two paths of equal length but of different geometries: one was straight between the nest and the food source, and the other involved an abrupt change of direction at the midway point (135°). Both food sources were discovered simultaneously, but the food source at the end of the straight path was preferentially exploited by ants. Based on experimental and theoretical results, we show that a significantly shorter duration of nestbound travel on the straight path, which rapidly leads to a stronger pheromone trail, is at the origin of this preference.

Interspecific shared collective decision-making in two forensically important species.

To date, the study of collective behaviour has mainly focused on intraspecific situations: the collective decision-making of mixed-species groups involving interspecific aggregation-segregation has received little attention. Here, we show that, in both conspecific and heterospecific groups, the larvae of two species (Lucilia sericata and Calliphora vomitoria, calliphorid carrion-feeding flies) were able to make a collective choice. In all groups, the choice was made within a few minutes and persisted throughout the period of the experiment. The monitoring of a focal individual within a group showed that these aggregations were governed by attractive and retentive effects of the group. Furthermore, the similarity observed between the conspecific and heterospecific groups suggested the existence of shared aggregation signals. The group size was found to have a stronger influence than the species of necrophagous larvae. These results should be viewed in relation to the well-known correlation between group size and heat generation. This study provides the first experimental examination of the dynamics of collective decision-making in mixed-species groups of invertebrates, contributing to our understanding of the cooperation-competition phenomenon in animal social groups.

Evidence of self-organization in a gregarious land-dwelling crustacean (Isopoda: Oniscidea).

How individuals modulate their behavior according to social context is a major issue in the understanding of group initiation, group stability and the distribution of individuals. Herein, we investigated the mechanisms of aggregation behavior in Porcellio scaber, a terrestrial isopod member of the Oniscidea, a unique and common group of terrestrial crustaceans. We performed binary choice tests using shelters with a wide range of population densities (from 10 to 150 individuals). First, the observed collective choices of shelters strengthen the demonstration of a social inter-attraction in terrestrial isopods; especially, in less than 10 min, the aggregation reaches its maximal value, and in less than 100 s, the collective choice is made, i.e., one shelter is selected. In addition, the distribution of individuals shows the existence of (1) quorum rules, by which an aggregate cannot emerge under a threshold value of individuals, and (2) a maximum population size, which leads to a splitting of the populations. These collective results are in agreement with the individual's probability of joining and leaving an aggregate attesting to a greater attractiveness of the group to migrants and greater retention of conspecifics with group size. In this respect, we show that the emergence of aggregation in terrestrial isopods is based on amplification mechanisms. And lastly, our results indicate how local cues about the spatial organization of individuals may favor this emergence and how individuals spatiotemporally reorganize toward a compact form reducing the exchange with the environment. This study provides the first evidence of self-organization in a gregarious crustacean, similar as has been widely emphasized in gregarious insects and eusocial insects.

Behavioural Contagion Explains Group Cohesion in a Social Crustacean.

In gregarious species, social interactions maintain group cohesion and the associated adaptive values of group living. The understanding of mechanisms leading to group cohesion is essential for understanding the collective dynamics of groups and the spatio-temporal distribution of organisms in environment. In this view, social aggregation in terrestrial isopods represents an interesting model due to its recurrence both in the field and in the laboratory. In this study, and under a perturbation context, we experimentally tested the stability of groups of woodlice according to group size and time spent in group. Our results indicate that the response to the disturbance of groups decreases with increases in these two variables. Models neglecting social effects cannot reproduce experimental data, attesting that cohesion of aggregation in terrestrial isopods is partly governed by a social effect. In particular, models involving calmed and excited individuals and a social transition between these two behavioural states more accurately reproduced our experimental data. Therefore, we concluded that group cohesion (and collective response to stimulus) in terrestrial isopods is governed by a transitory resting state under the influence of density of conspecifics and time spent in group. Lastly, we discuss the nature of direct or indirect interactions possibly implicated.

Group personality during collective decision-making: a multi-level approach.

Collective decision-making processes emerge from social feedback networks within a group. Many studies on collective behaviour underestimate the role of individual personality and, as a result, personality is rarely analysed in the context of collective dynamics. Here, we show evidence of sheltering behaviour personality in a gregarious insect (Periplaneta americana), which is characterized by a collective personality at the group level. We also highlight that the individuals within groups exhibited consistent personality traits in their probability of sheltering and total time sheltered during the three trials over one week. Moreover, the group personality, which arises from the synergy between the distribution of behaviour profiles in the group and social amplifications, affected the sheltering dynamics. However, owing to its robustness, personality did not affect the group probability of reaching a consensus. Finally, to prove social interactions, we developed a new statistical method that will be helpful for future research on personality traits and group behaviour. This approach will help to identify the circumstances under which particular group compositions may improve the fitness of individuals in gregarious species.

The aggregation of tuna around floating objects: what could be the underlying social mechanisms?

Several empirical and theoretical studies have shown how the exploitation of food sources, the choice of resting sites or other types of collective decision-making in heterogeneous environments are facilitated and modulated by social interactions between conspecifics. It is well known that many pelagic fishes live in schools and that this form of gregarious behavior provides advantages in terms of food intake and predator avoidance efficiency. However, the influence of social behavior in the formation of aggregations by tuna under floating objects (FOBs) is poorly understood. In this work, we investigated the collective patterns generated by different theoretical models, which either include or exclude social interactions between conspecifics, in the presence of two aggregation sites. The resulting temporal dynamics and distributions of populations were compared to in situ observations of tuna behavior. Our work suggests that social interactions should be incorporated in aggregative behavior to reproduce the temporal patterns observed in the field at both the individual and the group level, challenging the common vision of tuna aggregations around FOBs. Our study argues for additional data to further demonstrate the role of social behavior in the dynamics of these fish aggregations. Understanding the interplay between environmental and social factors in the associative behavior of fish with FOBs is necessary to assess the consequences of the widespread deployment of artificial FOBs by fishermen.

Impact of living with kin/non-kin on the life history traits of Tetranychus urticae (Acari: Tetranychidae).

In many vertebrates and invertebrates, living in a group may influence the life history traits, physiology and behaviour of its individual members, whereas genetic relatedness affects social interactions among individuals in a group. The two-spotted spider mite Tetranychus urticae is characterised by a communal organization, in which silk production plays a key role. A silken web protects the colony against biotic and abiotic agents such as predators, competitors, humidity, wind, rain and acaricides. To evaluate the potential costs and benefits of being associated with genetically distant vs genetically close individuals in T. urticae, we assessed various fitness indicators (faecal pellet production, fecundity, death rate) in pure and mixed groups of two distinct populations of T. urticae: a red-form population from Tunisia and a green-form population from Belgium. If genetic origin had no influence, the values of fitness indicators in mixed groups composed of green and red individuals, would be intermediate between those of the pure green-form and red-form groups. Our results show that in a mixed group, faecal pellet production and death rate were statistically similar to the values obtained in the pure group of green-form individuals. Therefore, our study suggests that strain recognition ability may occur in T. urticae and that the genetic background of an individual may have a great impact on several of its life history traits.

Collective regulatory stock management and spatiotemporal dynamics of the food flow in ants.

The organization of complex societies requires constant information flow between individuals. The shape of the food web organizes itself according to the spatial distribution of the individuals and of the stocks. To understand how the spatial organization of the food stocks changes with the colony needs, we monitored the flow of radiolabeled sugar solution inside an ant nest at different degrees of starvation. The spatial dynamics of the food flow revealed stable patterns and fine-tuning regulation of the feeding process. The complex collective regulatory stock management task can be reproduced by a surprising simple model that integrates a positive and a negative feedback proportional to the number of ants that already received food. Spatial analysis of the food distribution showed that sucrose is heterogeneously stocked among individuals and also heterogeneously consumed. Furthermore, we observed a regular spatial structure, leading to centralization of the stocks: heavily loaded individuals being at the center of the cluster and weakly loaded individuals at its periphery. The centralization of both resources and information in self-organized systems might be a widespread phenomenon that deserves further studies.

Emergence and retention of a collective memory in cockroaches.

The stability of collective decisions-making in social systems is crucial as it can lead to counterintuitive phenomena such as collective memories, where an initial choice is challenged by environmental changes. Many social species face the challenge to perform collective decisions under variable conditions. In this study, we focused on situations where isolated individuals and groups of the American cockroach (Periplaneta americana) had to choose between two shelters with different luminosities that were inverted during the experiment. The darker shelter was initially preferred, but only groups that reached a consensus within that shelter maintain their choice after the light inversion, while isolated individuals and small groups lacked site fidelity. Our mathematical model, incorporating deterministic and probabilistic elements, sheds light on the significance interactions and their stochasticity in the emergence and retention of a collective memory.

Leader-based and self-organized communication: modelling group-mass recruitment in ants.

For collective decisions to be made, the information acquired by experienced individuals about resources' location has to be shared with naïve individuals through recruitment. Here, we investigate the properties of collective responses arising from a leader-based recruitment and a self-organized communication by chemical trails. We develop a generalized model based on biological data drawn from Tetramorium caespitum ant species of which collective foraging relies on the coupling of group leading and trail recruitment. We show that for leader-based recruitment, small groups of recruits have to be guided in a very efficient way to allow a collective exploitation of food while large group requires less attention from their leader. In the case of self-organized recruitment through a chemical trail, a critical value of trail amount has to be laid per forager in order to launch collective food exploitation. Thereafter, ants can maintain collective foraging by emitting signal intensity below this threshold. Finally, we demonstrate how the coupling of both recruitment mechanisms may benefit to collectively foraging species. These theoretical results are then compared with experimental data from recruitment by T. caespitum ant colonies performing group-mass recruitment towards a single food source. We evidence the key role of leaders as initiators and catalysts of recruitment before this leader-based process is overtaken by self-organised communication through trails. This model brings new insights as well as a theoretical background to empirical studies about cooperative foraging in group-living species.

Social prophylaxis through distant corpse removal in ants.

Living in groups raises important issues concerning waste management and related sanitary risks. Social insects such as ants live at high densities with genetically related individuals within confined and humid nests, all these factors being highly favorable for the spread of pathogens. Therefore, in addition to individual immunity, a social prophylaxis takes place, namely, by the removal of risky items such as corpses and their rejection at a distance from the ant nest. In this study, we investigate how Myrmica rubra workers manage to reduce encounters between potentially hazardous corpses and nestmates. Using both field and laboratory experiments, we describe how the spatial distribution and the removal distance of waste items vary as a function of their associated sanitary risks (inert item vs. corpse). In the field, corpse-carrying ants walked in a rather linear way away from the nest entrance and had an equal probability of choosing any direction. Therefore, they did not aggregate corpses in dedicated areas but scattered them in the environment. In both field and laboratory experiments, ants carrying corpses dropped their load in more remote-and less frequented-areas than workers carrying inert items. However, for equidistant areas, ants did not avoid dropping corpses at a location where they perceived area marking as a cue of high occupancy level by nestmates. Our results suggest that ants use distance to the nest rather than other occupancy cues to limit sanitary risks associated with dead nestmates.

Shape transition during nest digging in ants.

Nest building in social insects is among the collective processes that show highly conservative features such as basic modules (chambers and galleries) or homeostatic properties. Although ant nests share common characteristics, they exhibit a high structural variability, of which morphogenesis and underlying mechanisms remain largely unknown. We conducted two-dimensional nest-digging experiments under homogeneous laboratory conditions to investigate the shape diversity that emerges only from digging dynamics and without the influence of any environmental heterogeneity. These experiments revealed that, during the excavation, a morphological transition occurs because the primary circular cavity evolves into a ramified structure through a branching process. Such a transition is observed, whatever the number of ants involved, but occurs more frequently for a larger number of workers. A stochastic model highlights the central role of density effects in shape transition. These results indicate that nest digging shares similar properties with various physical, chemical, and biological systems. Moreover, our model of morphogenesis provides an explanatory framework for shape transitions in decentralized growing structures in group-living animals.

The silk road of Tetranychus urticae: is it a single or a double lane?

Tetranychus urticae (Acari: Tetranychidae) is a phytophagous mite that forms huge colonies. All active members of a colony (immatures and matures, females and males) spin silken threads. These mites construct a common web that protects the colony from external aggression. The silk coverage is well-known to provide advantages to the colony but very little is known about the characteristics of the threads themselves. Here is the first quantification of the diameter of silken threads spun by two different stages (adult females and larvae) and its relationship with body size of the spinning individuals. Moreover, we observed how silk was deposited on the substrate through their two pedipalps. Threads were observed by means of transmission electron and fluorescence microscopy. Silken threads spun by larvae (0.055 ± 0.018 µm) were significantly thinner than threads spun by adult females (0.111 ± 0.038 µm). In the first step of the silk depositing behaviour, the mite attached the thread to the substrate by putting its pedipalps in contact with the surface (adhesion, double silken threads). When walking, silken threads became detached from the substrate and spitted up (silken threads were free). Finally, silken threads adhered to the surface. The presence of single and double threads makes thread diameter highly variable.

Testing for collective choices in the two-spotted spider mite.

Silk is a vector for collective behaviour in many spinning arthropods, including social spiders, social caterpillars, and some spider mites. In this study, the potential for silk-mediated collective choices is evaluated for the two-spotted spider mite Tetranychus urticae. This subsocial mite lives in large colonies on plants, sheltered under a collectively spun silk web. The silk has an attractive and arresting effect. We test whether the silk trails left by the spider mites can give rise to the collective choice of a path. The experiment consists in offering two identical paths to a group of migrating mites. Our results show that the presence of a silk trail influences the mites, but not sufficiently to systematically provoke a collective choice. In order to determine the trail following potential of T. urticae, we parameterise a theoretical trail following model to fit our experiments and those found in the literature. Our prediction is that even after a large number of mites have passed (200), a systematic collective choice of path should not be expected under the tested conditions. Our results, combined with what is known from the literature, allow us to propose a general scenario for the dispersal behaviour of T. urticae.

Does a high social status confer greater levels of trust from groupmates? An experimental study of leadership in domestic horses.

In collective movements, specific individuals may emerge as leaders. In this study on the domestic horse (Equus ferus caballus), we conducted experiments to establish if an individual is successfully followed due to its social status (including hierarchical rank and centrality). We first informed one horse about a hidden food location and recorded by how many it was followed when going back to this location. In this context, all horses lead their groupmates successfully. In a second step, we tested whether group members would trust some leaders more than others by removing the food before the informed individual led the group back to the food location. In addition, two control initiators with intermediate social status for which the food was not removed were tested. The results, confirmed by simulations, demonstrated that the proportions of followers for the unreliable initiator with highest social status are greater than the ones of the unreliable initiator with lowest social status. Our results suggest an existing relationship between having a high social status and a leadership role. Indeed, the status of a leader sometimes prevail at the detriment of the accuracy of the information, because an elevated social status apparently confers a high level of trust.

A Data-Driven Simulation of the Trophallactic Network and Intranidal Food Flow Dissemination in Ants.

Food sharing can occur in both social and non-social species, but it is crucial in eusocial species, in which only some group members collect food. This food collection and the intranidal (i.e., inside the nest) food distribution through trophallactic (i.e., mouth-to-mouth) exchanges are fundamental in eusocial insects. However, the behavioural rules underlying the regulation and the dynamics of food intake and the resulting networks of exchange are poorly understood. In this study, we provide new insights into the behavioural rules underlying the structure of trophallactic networks and food dissemination dynamics within the colony. We build a simple data-driven model that implements interindividual variability and the division of labour to investigate the processes of food accumulation/dissemination inside the nest, both at the individual and collective levels. We also test the alternative hypotheses (no variability and no division of labour). The division of labour, combined with inter-individual variability, leads to predictions of the food dynamics and exchange networks that run, contrary to the other models. Our results suggest a link between the interindividual heterogeneity of the trophallactic behaviours, the food flow dynamics and the network of trophallactic events. Our results show that a slight level of heterogeneity in the number of trophallactic events is enough to generate the properties of the experimental networks and seems to be crucial for the creation of efficient trophallactic networks. Despite the relative simplicity of the model rules, efficient trophallactic networks may emerge as the networks observed in ants, leading to a better understanding of the evolution of self-organisation in such societies.