Upon nutrient deprivation, cells are thought to suppress biosynthesis but activate catabolic pathways to provide alternative energy sources and nutrients. However, here we provide evidence that in adult male C. elegans, both biosynthesis and degradation activities, including ribosome biogenesis and turnover, are enhanced during early starvation and appear to depend on the availability of intestinal lipid stores. Upon depletion of the intestinal lipids, further food deprivation results in a significant reduction in metabolic activity in the starved male worms. Our data show that adult C. elegans exhibits a two-phase metabolic response to starvation stress: an initial phase with enhanced metabolic activity that rapidly exhausts the lipid stores, followed by a phase with low metabolic activity, which outlasts the life of fed control worms. DAF-2 insulin/IGF-1 receptor signaling to the RAS pathway is required for the starvation-induced ribosome biogenesis and rapid lipid depletion in the initial phase of starvation.