Phototrophic Cnidaria are mixotrophic organisms that can complement their het- erotrophic diet with nutrients assimilated by their algal endosymbionts. Metabolic mod- els suggest that the translocation of photosynthates and their derivatives from the algae may be sufficient to cover the metabolic energy demands of the host. However, the im- portance of heterotrophy to the nutritional budget of these holobionts remains unclear. Here, we report on the long-term survival of the photosymbiotic anemone Aiptasia in the absence of heterotrophic food sources. Following one year of heterotrophic starva- tion, these anemones remained fully viable but showed an 85 % reduction in biomass compared to their regularly fed counterparts. This shrinking was accompanied by a re- duction in host protein content and algal density, indicative of severe nitrogen limitation. Nonetheless, isotopic labeling experiments combined with NanoSIMS imaging revealed that the contribution of algal-derived nutrients to the host metabolism remained unaf- fected due to an increase in algal photosynthesis and more efficient carbon translocation. Taken together, our results suggest that, on a one- year timescale, heterotrophic feeding is not essential to fulfilling the energy requirements of the holobiont. But, while symbi- otic nutrient cycling effectively retains carbon in the holobiont over long time scales, our data suggest that heterotrophic feeding is a critical source of nitrogen required for holobiont growth under oligotrophic conditions.