Several ecologically and commercially important fish species spend the winter in a state of minimum feeding activity and at lower risk of predation. To enable this overwintering behaviour, energetic reserves are generated prior to winter to support winter metabolism. Maintenance metabolism in fish scales with body size and increases with temperature, and the two factors together determine a critical threshold size for passive overwintering below which the organism is unlikely to survive without feeding. This is because the energetic cost of metabolism exceeds maximum energy reserves. In the present study, we estimated the energetic cost of overwintering from a bioenergetic model. The model was parameterised using respirometry-based measurements of standard metabolic rate in buried A. tobianus (a close relative to A. marinus) at temperatures from 5.3 to 18.3 degrees C and validated with two independent long-term overwintering experiments. Maximum attainable energy reserves were estimated from published data on A. marinus in the North Sea. The critical threshold size in terms of length (L(th)) for A. marinus in the North Sea was estimated to be 9.5 cm. We then investigated two general predictions: (1) Fish smaller than L(th) display winter feeding activity, and (2) size at maturation of iteroparous species is larger than L(th) to ensure sufficient energy reserves to accommodate both the metabolic cost of passive overwintering and reproductive investments. Both predictions were found to be consistent with data on size at maturation and total body energy in December and February.