Hypotheses that relate body size to energy use are of particular interest in community ecology and macroecology because of their potential to facilitate quantitative predictions about species interactions and to clarify complex ecological patterns. One prominent size-energy hypothesis, the energetic equivalence hypothesis, proposes that energy use from shared, limiting resources by populations or size classes of foragers will be independent of body size. Alternative hypotheses propose that energy use will increase with body size, decrease with body size, or peak at an intermediate body size. Despite extensive study, however, size-energy hypotheses remain controversial, due to a lack of directly-measured data on energy use, a tendency to confound distinct scaling relationships, and insufficient attention to the ecological contexts in which predicted relationships are likely to occur. Our goal, therefore, was to directly evaluate size-energy hypotheses while clarifying how results would differ with alternate methods and assumptions. We comprehensively tested size-energy hypotheses in a vertebrate frugivore guild in a tropical forest in Madagascar. Our test of size-energy hypotheses, which is the first to examine energy intake directly, was consistent with the energetic equivalence hypothesis. This finding corresponds with predictions of metabolic theory and models of energy distribution in ecological communities, which imply that body size does not confer an advantage in competition for energy among populations or size classes of foragers. This result was robust to different assumptions about energy regulation. Our results from direct energy measurement, however, contrasted with those obtained with conventional methods of indirect inference from size-density relationships, suggesting that size-density relationships do not provide an appropriate proxy for size-energy relationships as has commonly been assumed. Our research also provides insights into mechanisms underlying local size-energy relationships and has important implications for predicting species interactions and for understanding the structure and dynamics of ecological communities.