Carotenoid-dependent sexual coloration is one of the best-studied sexual signals, but how the honesty of such signals is maintained remains uncertain. The main hypotheses focus on acquisition limits and physiological use of carotenoids in immune function and regulating oxidative stress. A hypothesis that has received less attention states that carotenoids can also be detrimental, depending on an animal's state. Hence, carotenoid-dependent signals may be a handicap, signaling the ability to evade or tolerate detrimental effects of carotenoids. To investigate this hypothesis, we examined the effects of carotenoid supplementation on subsequent reproduction in zebra finches in 2 different foraging environments ("easy" and "hard"), thereby generating variation in physiological state. We find support for context-dependent negative effects of carotenoid supplementation on subsequent laying latency and on total number of eggs laid: carotenoids had a detrimental effect in the "easy" conditions and a beneficial effect in the "hard" conditions. Thus, our results support the hypothesis that carotenoids can have context-dependent detrimental effects. Dissecting the relative contribution of the different mutually nonexclusive honesty mechanisms-acquisition, physiological benefits, and context-dependent detrimental effects of carotenoids-maintaining carotenoid-dependent signal honesty will be an exciting challenge.