The paradox of the pelagics: why bluefin tuna can go hungry in a sea of plenty

Large marine predators such as tunas and sharks play an important role in structuring marine food webs. Their future populations depend on the environmental conditions they en counter across life history stages and the level of human exploitation. Standard predator-prey relationships suggest favorable conditions (high prey abundance) should result in successful foraging and reproductive output. Here, we demonstrate that these assumptions are not invariably valid across species, and that somatic condition of Atlantic bluefin tuna Thunnus thynnus in the Gulf of Maine declined in the presence of high prey abundance. We show that the paradox of declining bluefin tuna condition during a period of high prey abundance is explained by a change in the size structure of their prey. Specifically, we identified strong correlations between bluefin tuna body condition, the relative abundance of large Atlantic herring Clupea harengus, and the energetic payoff resulting from consuming different sizes of herring. This correlation is consistent with optimal foraging theory, explaining why bluefin tuna condition suffers even when prey is abundant. Furthermore, optimal foraging principles explain a shift in traditional bluefin tuna foraging areas, toward regions with a higher proportion of large herring. Bluefin tuna appear sensitive to changes in the size spectrum of prey rather than prey abundance, impacting their distribution, reproduction and economic value. Fisheries managers will now face the challenge of how to manage for high abundance of small pelagic fish, which benefits benthic fishes and mammalian predators, and maintain a robust size structure beneficial for top predators with alternative foraging strategies.