In uniparental intermittent incubators, incubating parents must simultaneously regulate both the temperature of the clutch and their own energy level. To examine energetic consequences of providing different thermal environments for clutches of different sizes, a dynamic model was constructed in which energy level of an incubating European Starling (Sturnus vulgaris) and temperature of its clutch were simultaneously described. Adult energy balance after a day of incubation decreased as mean clutch temperature increased, such that the debt accrued while maintaining a clutch within the optimal developmental temperature range (36–39°C) was predicted to be prohibitively high, despite the prediction that the mean basal metabolic rate (BMR) required to maintain this temperature was <2 BMR. Thus, this model can explain our observation that starlings maintained their eggs at 32–33°C, well below the developmental optimum. Consistent with empirical studies, our model predicted that the metabolic demand of incubation increases with clutch size. That increase was predicted to affect adult energy balance and hence cost of incubation when starlings maintained their clutches at optimal temperatures, but not at the lower temperatures actually observed. Hence, clutch-size-dependent variation in incubation demands may be unlikely to influence optimal number of eggs that a starling should lay. However, exact relationship between clutch size and adult energy debt depended on the nature of the relationship between clutch size and clutch thermal properties and on mean incubation temperature. Thus, consequences of clutch size for the cost of incubation are not clearly predictable, and caution may be required when using experimental clutch enlargements to manipulate reproductive costs.