Subcritical escape waves in schooling fish

Sci Adv. 2022 Jun 24;8(25):eabm6385. doi: 10.1126/sciadv.abm6385. Epub 2022 Jun 22.

Abstract

Theoretical physics predicts optimal information processing in living systems near transitions (or pseudo-critical points) in their collective dynamics. However, focusing on potential benefits of proximity to a critical point, such as maximal sensitivity to perturbations and fast dissemination of information, commonly disregards possible costs of criticality in the noisy, dynamic environmental contexts of biological systems. Here, we find that startle cascades in fish schools are subcritical (not maximally responsive to environmental cues) and that distance to criticality decreases when perceived risk increases. Considering individuals' costs related to two detection error types, associated to both true and false alarms, we argue that being subcritical, and modulating distance to criticality, can be understood as managing a trade-off between sensitivity and robustness according to the riskiness and noisiness of the environment. Our work emphasizes the need for an individual-based and context-dependent perspective on criticality and collective information processing and motivates future questions about the evolutionary forces that brought about a particular trade-off.