Intermittent collective dynamics emerge from conflicting imperatives in sheep herds

Abstract

Among the many fascinating examples of collective behavior exhibited by animal groups, some species are known to alternate slow group dispersion in space with rapid aggregation phenomena induced by a sudden behavioral shift at the individual level. We study this phenomenon quantitatively in large groups of grazing Merino sheep under controlled experimental conditions. Our analysis reveals strongly intermittent collective dynamics consisting of fast, avalanche-like regrouping events distributed on all experimentally accessible scales. As a proof of principle, we introduce an agent-based model with individual behavioral shifts, which we show to account faithfully for all collective properties observed. This offers, in turn, an insight on the individual stimulus/ response functions that can generate such intermittent behavior. In particular, the intensity of sheep allelomimetic behavior plays a key role in the group's ability to increase the per capita grazing surface while minimizing the time needed to regroup into a tightly packed configuration. We conclude that the emergent behavior reported probably arises from the necessity to balance two conflicting imperatives: (i) the exploration of foraging space by individuals and (ii) the protection from predators offered by being part of large, cohesive groups. We discuss our results in the context of the current debate about criticality in biology.sheep herds | collective behavior | self-organization | computational modeling | Allelomimetism T he social interactions and behavioral mechanisms involved in the coordination of collective movements in animal groups largely determine the animals' ability to display adapted responses when they face challenges, such as finding, efficiently, food sources (1-4) or safe resting places (5-7) or avoiding predators (8-13). Thus, the diversity of collective motion patterns observed in groupliving species reflects the multiple forms of interactions individuals use for coordinating their behavioral actions (14,15). Deciphering these interactions, their relation with the patterns emerging at the collective level, and their connections with the physiological and ecological constraints peculiar to each group-living species is crucial to understanding the evolution of collective phenomena in biological systems (16-18). So far, only a handful of quantitative datasets have been gathered for large animal groups (19-21). Most of them have focused on elementary cases where the prevailing biological imperative seems to be group cohesion, either to gain protection from potential predators, such as for the spontaneous collective motion exhibited by starling flocks (19,22) and some fish schools (23-25), or for reproductive purposes, as in swarms of midges (21,26).One important and, so far, often neglected aspect of collective motion is the existence of individual-level behavioral shifts, which, in turn, may trigger a transition at the collective level. For instance, in many species of fish, groups regularly alternate between a swarming state, in wh...

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