Bringing a Time–Depth Perspective to Collective Animal Behaviour (original) (raw)

The field of collective animal behaviour examines how relatively simple, local interactions between individuals in groups combine to produce global-level outcomes. Existing mathematical models and empirical work have identified candidate mechanisms for numerous collective phenomena but have typically focused on one-off or short-term performance. We argue that feedback between collective performance and learning – giving the former the capacity to become an adaptive, and potentially cumulative, process – is a currently poorly explored but crucial mechanism in understanding collective systems. We synthesise material ranging from swarm intelligence in social insects through collective movements in vertebrates to collective decision making in animal and human groups, to propose avenues for future research to identify the potential for changes in these systems to accumulate over time. What Are Collective Behaviours and How Do They Arise? Some of the most impressive biological phenomena emerge out of interactions among members of animal groups. Bird flocks, fish schools, and insect swarms perform highly coordinated collective movements that can encompass thousands of individuals, producing complex group-level patterns that are difficult to predict from the behaviour of isolated individuals only. Animal groups are also able to solve problems that are beyond the capacities of single individuals [1]; ant colonies, for example, tackle certain types of optimisation problems so effectively that they have inspired an entire field of computer science [2]. Despite the appearance of synchronised organisation, it is increasingly well understood that no central control acts on the collective as a whole; instead, the global patterns result from simple, local interactions among the group's neighbouring members – a form of biological self-organisation [3] (see Glossary). Recent years have seen a proliferation of both empirical and theoretical work on the mechanistic underpinnings of collective animal behaviour [4], with self-organisation emerging as a major principle in various contexts including collective motion [5], decision making [6] and construction [7], activity synchronisation [8], and the spontaneous emergence of leader–follower relations [9]. Nonetheless, a rigorous adaptive framework is yet to be applied to collective animal behaviour; little is known about the nature of the selective forces that act at the level of the individual behavioural rules to shape pattern formation at group level. Over shorter timescales, and crucially for this review, no major synthesis has yet examined collective behaviour from a time–depth perspective; we do not know: (i) what changes group-level organisation might undergo over the course of repeated executions of collective tasks; (ii) to what extent solutions arrived at collectively are retained (learned), either at the individual or at the collective level, with the potential to influence future interactions; or (iii) what effect changes in group composition, due to natural demographic processes, have on whether solutions are 'inherited' from previous generations.