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The twilight zone contains the largest biomass of the world’s ocean. Identifying its role in the trophic supply and contaminant exposure of marine megafauna constitutes a critical challenge in the context of global change. The white shark (Carcharodon carcharias) is a threatened species with some of the highest concentrations of neurotoxin methylmercury (MeHg) among marine top predators. Large white sharks migrate seasonally from coastal habitats, where they primarily forage on pinnipeds, to oceanic offshore habitats. Tagging studies suggest that while offshore, white sharks may forage at depth on mesopelagic species, yet no biochemical evidence exists. Here, we used mercury isotopic composition to assess the dietary origin of MeHg contamination in white sharks from the Northeast Pacific Ocean. We estimated that a minimum of 72% of the MeHg accumulated by white sharks originates from the consumption of mesopelagic prey, while a maximum of 25% derives from pinnipeds. In addition to highlighting the potential of mercury isotopes to decipher the complex ecological cycle of marine predators, our study provides evidence that the twilight zone constitutes a crucial foraging habitat for these large predators, which had been suspected for over a decade. Climate change is predicted to expand the production of mesopelagic MeHg and modify the mesopelagic biomass globally. Considering the pivotal role of the twilight zone is therefore essential to better predict both MeHg exposure and trophic supply to white sharks, and effectively protect these key vulnerable predators.

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