Feeding rates influence reproductive output in many kinds of animals, but we need to understand the timescale of this influence before we can compare reproductive energy allocation to energy intake. A central issue is the extent to which reproduction is fuelled by long-term energy stores (“capital” breeding) versus recently-acquired resources (“income” breeding). Our data on free-living aspic vipers show that there is no simple answer to this question: reproductive frequency is determined by long-term energy stores, offspring size is influenced by maternal food intake immediately before ovulation, and litter size is influenced by both long-term stores and short-term energy acquisition. Thus, offspring size in free-living vipers reflects the mother's energy balance over the preceding year (via a trade-off between litter size and offspring size) as well as her energy balance in the current breeding season. Hence, different components of a given reproductive output (litter) are not only functionally linked, but also respond to different temporal scales of prey availability. A female's body size has little effect on her reproductive output. Attempts to quantify reproductive energy allocation must take into account the fact that different reproductive traits (such as offspring size versus number) may respond to energy availability over different timespans. Thus, although the aspic viper is a typical “capital breeder” in terms of its reliance on stored reserves for maternal “decisions” concerning reproductive frequency, it is to some degree a facultative “income breeder” with respect to the determination of offspring size and litter size.