Nest Entrances, Spatial Fidelity, and Foraging Patterns in the Red Ant Myrmica rubra: A Field and Theoretical Study.

The nest architecture of social insects deeply impacts the spatial distribution of nestmates their interactions, information exchanges and collective responses. In particular, the number of nest entrances can influence the interactions taking place beyond the nest boundaries and the emergence of collective structures like foraging trails. Here, we investigated in the field how the number of nest entrances impacted the foraging dynamics of Myrmica rubra ant colonies. We located the nest entrances where recruitment occurred towards sugar feeders placed in their surroundings. The nests showed one or multiple entrance(s) aggregated in clusters spaced by at least 15 cm. Foragers from colonies with two clusters of entrances were distributed more homogeneously among the feeders than those of colonies with one cluster. In addition, foragers always returned to the first discovered feeder and demonstrated a high fidelity to their original entrance. Finally, a multi-agent model highlighted that additional entrances and clusters of entrances delayed the mobilisation of workers but favoured the simultaneous exploitation of several sources, which was further enhanced by the spatial fidelity of foragers. Multiple nest entrances seem to be a way for medium-sized colonies to benefit from advantages conferred by polydomy while avoiding associated costs to maintain social cohesion.

Multiple nest entrances alter foraging and information transfer in ants.

The ecological success of ants relies on their ability to discover and collectively exploit available resources. In this process, the nest entrances are key locations at which foragers transfer food and information about the surrounding environment. We assume that the number of nest entrances regulates social exchanges between foragers and inner-nest workers, and hence influences the foraging efficiency of the whole colony. Here, we compared the foraging responses of Myrmica rubra colonies settled in either one-entrance or two-entrance nests. The total outflows of workers exploiting a sucrose food source were similar regardless of the number of nest entrances. However, in the two-entrance nests, the launching of recruitment was delayed, a pheromone trail was less likely to emerge between the nest and the food source, and recruits were less likely to reach the food target. As a result, an additional entrance through which information could transit decreased the efficiency of social foraging and ultimately led to a lower amount of retrieved food. Our study confirms the key-role of nest entrances in the transfer of information from foragers to potential recruits. The influence of the number of entrances on the emergence of a collective trail also highlights the spatially extended impact of the nest architecture that can shape foraging patterns outside the nest.

Bidirectional interactions facilitate the integration of a robot into a shoal of zebrafish Danio rerio.

Many studies on collective animal behavior seek to identify the individual rules that underlie collective patterns. However, it was not until the recent advancements of micro-electronic and embedded systems that scientists were able to create mixed groups of sensor-rich robots and animals and study collective interactions from the within a bio-hybrid group. In recent work, scientists showed that a robot-controlled lure is capable of influencing the collective decisions of zebrafish Danio rerio shoals moving in a ring and a two-room setup. Here, we study a closely related topic, that is, the collective behavior patterns that emerge when different behavioral models are reproduced through the use of a robotic lure. We design a behavioral model that alternates between obeying and disobeying the collective motion decisions in order to become socially accepted by the shoal members. Subsequently, we compare it against two extreme cases: a reactive and an imposing decision model. For this, we use spatial, directional and information theoretic metrics to measure the degree of integration of the robotic agent. We show that our model leads to similar information flow as in freely roaming shoals of zebrafish and exhibits leadership skills more often than the open-loop models. Thus, in order for the robot to achieve higher degrees of integration in the zebrafish shoal, it must, like any other shoal member, be bidirectionally involved in the decision making process. These findings provide insight on the ability to form mixed societies of animals and robots and yield promising results on the degree to which a robot can influence the collective decision making.

Collective departures and leadership in zebrafish.

In social animals, morphological and behavioural traits may give to some individuals a stronger influence on the collective decisions, even in groups assumed to be leaderless such as fish shoals. Here, we studied and characterized the leadership in collective movements of shoals of zebrafish Danio rerio by observing groups of 2, 3, 5, 7 and 10 zebrafish swimming in a two resting sites arena during one hour. We quantified the number of collective departures initiated by each fish and the number of attempts that they made. To do so, we developed an automated pipeline that analysed the individual trajectories generated by the tracking software. For all shoal sizes, the leadership was distributed among several individuals. However, it was equally shared among all the fish in some shoals while other groups showed a more asymmetrical sharing of the initiation of collective departures. To quantify this distribution, we computed the entropy associated with the time series of the identity of all initiators for each experiment and confirmed the presence of a continuum between a homogeneous and a heterogeneous distribution of the leadership. While some fish led more departures than others, an individual analysis showed that all fish had actually the same success rate to lead the shoal out of a resting site after an attempt. Thus, some individuals monopolized the leadership by attempting more often than others to exit a resting site. Finally, we highlight that the intra-group ranking of a fish for the initiative is correlated to its intra-group ranking for the average speed with mobile individuals more prone to lead the shoal. These results demonstrate that the collective behaviour of a shoal can be mainly driven by a subset of individuals even in the absence of higher influence of a fish on its congeneers.

Loose social organisation of AB strain zebrafish groups in a two-patch environment.

We study the collective behaviour of zebrafish shoals of different numbers of individuals (1, 2, 3, 5, 7, 10 and 20 AB zebrafish Danio rerio) in a constraint environment composed of two identical square rooms connected by a corridor. This simple set-up is similar to a natural patchy environment. We track the positions and the identities of the fish and compute the metrics at the group and at the individual levels. First, we show that the number of fish affects the behaviour of each individual in a group, the cohesion of the groups, the preferential interactions and the transition dynamics between the two rooms. Second, during collective departures, we show that the rankings of exit correspond to the topological organisations of the fish prior to their collective departure. This spatial organisation appears in the group a few seconds before a collective departure. These results provide new evidences on the spatial organisation of the groups and the effect of the number of fish on individual and collective behaviours in a patchy environment.

How mimetic should a robotic fish be to socially integrate into zebrafish groups?

Biomimetic robots are promising tools in animal behavioural studies. If they are socially integrated in a group of animals, they can produce calibrated social stimuli to test the animal responses. However, the design of such social robots is challenging as it involves both a luring capability including appropriate robot behaviours, and the acceptation of the robots by the animals as social companions. Here, we investigate the integration of a biomimetic robot driven by biomimetic behavioural models into a group of zebrafish (Danio rerio). The robot behaviours are based on a stochastic model linking zebrafish visual perception to individual behaviour and calibrated experimentally to correspond to the behaviour of zebrafish. We show that our robot can be integrated into a group of zebrafish, mimic their behaviour and exhibit similar collective dynamics compared to fish-only groups. This study shows that an autonomous biomimetic robot was enhanced by a biomimetic behavioural model so that it can socially integrate into groups of fish.

Collective behaviour in vertebrates: a sensory perspective.

Collective behaviour models can predict behaviours of schools, flocks, and herds. However, in many cases, these models make biologically unrealistic assumptions in terms of the sensory capabilities of the organism, which are applied across different species. We explored how sensitive collective behaviour models are to these sensory assumptions. Specifically, we used parameters reflecting the visual coverage and visual acuity that determine the spatial range over which an individual can detect and interact with conspecifics. Using metric and topological collective behaviour models, we compared the classic sensory parameters, typically used to model birds and fish, with a set of realistic sensory parameters obtained through physiological measurements. Compared with the classic sensory assumptions, the realistic assumptions increased perceptual ranges, which led to fewer groups and larger group sizes in all species, and higher polarity values and slightly shorter neighbour distances in the fish species. Overall, classic visual sensory assumptions are not representative of many species showing collective behaviour and constrain unrealistically their perceptual ranges. More importantly, caution must be exercised when empirically testing the predictions of these models in terms of choosing the model species, making realistic predictions, and interpreting the results.

Strain differences in the collective behaviour of zebrafish (Danio rerio) in heterogeneous environment.

Recent studies show differences in individual motion and shoaling tendency between strains of the same species. Here, we analyse collective motion and response to visual stimuli in two morphologically different strains (TL and AB) of zebrafish. For both strains, we observed 10 groups of 5 and 10 zebrafish swimming freely in a large experimental tank with two identical landmarks (cylinders or discs) for 1 h. We tracked the positions of the fish by an automated tracking method and compute several metrics at the group level. First, the probability of the presence shows that both strains avoid free space and are more likely to swim in the vicinity of the walls of the tank and the landmarks. Second, the analysis of landmarks occupancy shows that AB zebrafish are more present in their vicinity than TL ones and that both strains regularly transit from one to the other one with no preference on the long duration. Finally, TL zebrafish show a higher cohesion than AB zebrafish. Thus, environmental heterogeneity and duration of the trials allow to reveal individual and collective behavioural variabilities among different strains of zebrafish. These results provide a new insight into the need to take into account individual variability of zebrafish strains for studying collective behaviour.

A stochastic vision-based model inspired by zebrafish collective behaviour in heterogeneous environments.

Collective motion is one of the most ubiquitous behaviours displayed by social organisms and has led to the development of numerous models. Recent advances in the understanding of sensory system and information processing by animals impels one to revise classical assumptions made in decisional algorithms. In this context, we present a model describing the three-dimensional visual sensory system of fish that adjust their trajectory according to their perception field. Furthermore, we introduce a stochastic process based on a probability distribution function to move in targeted directions rather than on a summation of influential vectors as is classically assumed by most models. In parallel, we present experimental results of zebrafish (alone or in group of 10) swimming in both homogeneous and heterogeneous environments. We use these experimental data to set the parameter values of our model and show that this perception-based approach can simulate the collective motion of species showing cohesive behaviour in heterogeneous environments. Finally, we discuss the advances of this multilayer model and its possible outcomes in biological, physical and robotic sciences.

Group recruitment in ants: who is willing to lead?

In social species, food exploitation is a challenging cooperative task that requires communication and coordination with some individuals that are more influential in the final foraging process. Among recruiters of the ant Tetramorium caespitum that have discovered food, some individuals act as leaders that physically guide groups of recruits until they reach the food source. Here, we discovered that highly motivated recruiters that focus their recruiting activity on areas close to the nest entrance and that perform a high number of contacts with nestmates in a short period of time are more likely to lead a group of followers on their next foraging trip. Based on the individual tracking of recruiters, we also show that the probability to lead a group is homogeneously distributed and that no specialisation into leadership occurs even over successive foraging trips. Instead of a permanent leadership, a distributed leadership that is mainly based on the motivation level of recruiters appears as an efficient way to process information and make collective decisions. Finally, we discuss how heterogeneity among group members in their access to information, their motivation to recruit or the social context of recruitment can be coupled to self-organising processes and can ultimately lead to adaptive collective patterns.

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.