Population level metabolic rates are by definition the sum of the individual metabolic rates within a population. Several studies have used estimates of individual metabolic rates to scale up metabolic activity of individuals to populations or whole communities. However, for aquatic single-celled organisms, individual metabolic rate is related to percapita resource availability, and accounting for this fact is essential for obtaining accurate estimates of population- or community-level metabolism. We frame the problem with a simple model of resource division that predicts per capita metabolic rate should decline with increasing density. We allow the magnitude of density-dependence to be adjusted by intraspecific competition, from perfectly dependent to completely independent of density. Our results demonstrate that per-capita metabolic rate of single-celled eukaryotes is indeed inversely related to density via the per-capita availability of resources, and this has a significant effect on population-level metabolic rates. Suppression of individual metabolic rate occurred up to an order of magnitude, and although this magnitude of suppression has been seen in starved protists, our results indicate that a broad continuum of density-dependence governs the resource-dependent variability in metabolic rates for these organisms. The species we used cover a range of resource acquisition modes and phylogenies, suggesting that density-dependence of metabolic rate may be widespread in aquatic unicells.