Group living is ubiquitous among animals [1, 2], but the exact benefits of group living experienced by individual groupmates is related to their spatial location within the overall group [3-5]. Individual variation in behavioral traits and nutritional state is known to affect interactions between individuals and their social group [6, 7], but physiological mechanisms underpinning collective animal behavior remain largely unexplored [8]. Here, we show that while fish at the front of moving groups are most successful at capturing food items, these individuals then show a systematic, post-feeding movement toward the rear of groups. Using observations of fish feeding in groups coupled with estimates of metabolic rate in fish consuming different meal sizes, we demonstrate that the magnitude of this shift in spatial position is directly related to the aerobic metabolic scope remaining after accounting for energetic costs of digestion. While previous work has shown that hungry individuals occupy anterior positions in moving groups [9, 10], our results show that the metabolic demand of food processing reduces the aerobic capacity available for locomotion in individuals that eat most, thus preventing them from maintaining leading positions. This basic trade-off between feeding and locomotor capacity could fundamentally dictate the spatial position of individuals within groups, perhaps obviating the role of individual traits in determining spatial preferences over shorter timescales (e.g., hours to days). This may be a general constraint for individuals within animal collectives, representing a key, yet overlooked, mediator of group functioning that could affect leadership, social information transfer, and group decision making.
Keywords: aerobic scope; collective behavior; ecophysiology; foraging; leadership; metabolic rate; sociality; teleost fish.
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