Educated predators make strategic decisions to eat defended prey according to their toxin content

Animals often eat foods containing toxins to benefit from the nutrients that they contain. Understanding how animals balance the costs of eating toxins with the benefits of gaining nutrients is important for understanding the evolution of antipredator defenses, particularly aposematism and mimicry. In this study, we tested whether predators could learn to use color signals to make strategic decisions about when to include prey that varied in their toxin content in their diets. We gave European starlings (Sturnus vulgaris) daily sessions of sequentially presented mealworms (Tenebrio molitor). There were 3 types of mealworm which were made discriminable using color signals: undefended mealworms injected with water, mildly defended mealworms injected with 1% quinine solution, and moderately defended mealworms injected with 3% quinine solution. Birds learned to eat more undefended than defended prey and more mildly than moderately defended prey. Crucially, when we manipulated the birds' energetic states using food restriction, we found that they increased the number of defended prey that they ate but maintained their relative preferences. Birds made state-dependent decisions based upon their knowledge of the amount of toxin prey contained and their current energetic need. Our results provide novel insights into the evolution of aposematic signals and also demonstrate that we may need to develop new models of the evolution of mimicry based on the state-dependent behavior of predators. Our data also have broader implications for the study of nutrient-toxin trade-offs across a range of different ecological scenarios.