Although previously disputed, it is now clear that the demands from avian incubation put parents under considerable energetic stress, sometimes to an extent where the costs of incubation constrain clutch size evolution. However, the behavioural mechanisms involved in manifesting such costs remain largely unknown. We manipulated the demands of incubation by enlarging and reducing clutch size during 2 years in a pied flycatcher, Ficedula hypoleuca, population in southern Sweden, and measured the resulting effects on incubation temperature and incubation behaviour. In addition, we assessed possible effects on later reproductive stages by restoring clutch size prior to hatching and subsequently monitoring female nest provisioning and nestling growth rate. The length of both attentive and inattentive bouts, as well as the total time spent incubating, was longer for females incubating enlarged clutches. These females also maintained eggs at lower temperatures, but only at the beginning of incubation. Thus, increased incubation demands were met by investing more time in incubation, but females were still not able to maintain incubation temperature at the same level as control females. Furthermore, females paid costs of increased incubation demands in terms of a longer incubation period in both years, and reduced nestling production in one, but did not appear to transfer any additional costs to their nestlings. We conclude that costs of incubation are context dependent, and suggest that the demands from incubation may be important in brood size determination in this species, at least in deteriorating ambient conditions. (C) 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.