Plants assimilate carbon primarily via the Calvin-Benson cycle. Two companion papers report evidence for anaplerotic carbon flux into this cycle. To estimate flux rates in Helianthus annuus leaves based on gas exchange measurements, we here expanded Farquhar-von Caemmerer-Berry photosynthesis models by terms accounting for anaplerotic respiration and energy recycling. In line with reported isotope evidence (companion papers), we found relative increases in anaplerotic flux as intercellular CO2 concentrations, Ci, decrease below a change point. At Ci=136 and 202 ppm, we found absolute rates of 2.99 and 2.39 μmol Ru5P m−2 s−1 corresponding to 58.3 and 28.2% of net CO2 assimilation, 13.1 and 10.7% of ribulose 1,5-bisphosphate regeneration, and 22.2 and 15.8% of Rubisco carboxylation (futile carbon cycling), respectively. Anaplerotic respiration governs total day respiration with contributions of 81.3 and 77.6%, and anaplerotic relative to photorespiratory CO2 release amounts to 63.9 and 67%, respectively. Furthermore, anaplerotic flux significantly increases absolute ATP demands and ATP-to-NADPH demand ratios of photosynthesis and may explain increasing sucrose-to-starch carbon partitioning ratios with decreasing Ci. We propose that anaplerotic flux can occur under both Rubisco and RuBP-limited growth conditions. Overall, our work introduces the anaplerotic pathway as central component in carbon and energy metabolism of C3 plants.