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Avian predators readily learn to associate the warning coloration of aposematic prey with the toxic effects of ingesting them, but they do not necessarily exclude aposematic prey from their diets. By eating aposematic prey ‘educated’ predators are thought to be trading-off the benefits of gaining nutrients with the costs of eating toxins. However, while we know that the toxin content of aposematic prey affects the foraging decisions made by avian predators, the extent to which the nutritional content of toxic prey affects predators' decisions to eat them remains to be tested. Here, we show that European starlings (Sturnus vulgaris) increase their intake of a toxic prey type when the nutritional content is artificially increased, and decrease their intake when nutritional enrichment is ceased. This clearly demonstrates that birds can detect the nutritional content of toxic prey by post-ingestive feedback, and use this information in their foraging decisions, raising new perspectives on the evolution of prey defences. Nutritional differences between individuals could result in equally toxic prey being unequally predated, and might explain why some species undergo ontogenetic shifts in defence strategies. Furthermore, the nutritional value of prey will likely have a significant impact on the evolutionary dynamics of mimicry systems.

Predators that have learned to associate warning coloration with toxicity often continue to include aposematic prey in their diet in order to gain the nutrients and energy that they contain. As body size is widely reported to correlate with energetic content, we predicted that prey size would affect predators' decisions to eat aposematic prey. We used a well-established system of wild-caught European starlings, Sturnus vulgaris, foraging on mealworms, Tenebrio molitor, to test how the size of undefended (water-injected) and defended (quinine-injected) prey, on different coloured backgrounds, affected birds’ decisions to eat defended prey. We found that birds ate fewer defended prey, and less quinine, when undefended prey were large compared with when they were small, but that the size of the defended prey had no effect on the numbers eaten. Consequently, we found no evidence that the mass of the defended prey or the overall mass of prey ingested affected the amount of toxin that a predator was willing to ingest, and instead the mass of undefended prey eaten was more important. This is a surprising finding, challenging the assumptions of state-dependent models of aposematism and mimicry, and highlighting the need to understand better the mechanisms of predator decision making. In addition, the birds did not learn to discriminate visually between defended and undefended prey based on size, but only on the basis of colour. This suggests that colour signals may be more salient to predators than size differences, allowing Batesian mimics to benefit from aposematic models even when they differ in size.

Aposematic prey warn predators of their toxicity using conspicuous signals. However, predators regularly include aposematic prey in their diets, particularly when they are in a poor energetic state and in need of nutrients. We investigated whether or not an environmental factor, ambient temperature, could change the energetic state of predators and lead to an increased intake of prey that they know to contain toxins. We found that European starlings, Sturnus vulgaris, increased their consumption of mealworm, Tenebrio molitor, prey containing quinine (a mild toxin) when the ambient temperature was reduced below their thermoneutral zone from 20 °C to 6 °C. The birds differed in their sensitivity to changes in ambient temperature, with heavier birds increasing the number of toxic prey they ate more rapidly with decreasing temperature compared to birds with lower body mass. This could have been the result of their requiring more nutrients at lower temperatures or being better able to detoxify quinine. Taken together, our results suggest that conspicuous coloration may be more costly at lower temperatures, and that aposematic prey may need to invest more in chemical defences as temperatures decline. Our study also provides novel insights into what factors affect birds' decisions to eat toxic prey, and demonstrates that selection pressures acting on prey defences can vary with changing temperature across days, seasons, climes, and potentially in response to climate change.