Summary1. Animals commonly experience variation in both food quality and metabolic requirements, and must regulate their food intake to maintain energy balance. 2. We exposed captive whitebellied (Cinnyris talatala) and amethyst (Chalcomitra amethystina) sunbirds (Nectariniidae) to different nectar sugar concentrations (0AE25, 0AE5 and 1 M sucrose), i.e. food qualities, and ambient temperatures (5, 15 and 25°C), i.e. energy requirements, to examine the effects on food intake, feeding patterns and body mass of the birds. 3. Both species compensated for decreased dietary sugar concentration by increasing food intake. While whitebellied sunbirds showed a constant sugar intake over the range of diet concentrations, amethyst sunbirds ingested less sugar on 0AE25 M than on 0AE5 M sucrose. During acute short-term exposure to 5°C, birds increased food and thus sugar intake on all diet concentrations by almost 27%, compared to the similar intake at 15 and 25°C. Despite increased food consumption, all birds lost more body mass at 5 and 15°C than at 25°C. 4. Adjustment of food intake in both species took place via changes in feeding frequency, with the duration of feeding events unchanged. 5. Apparent sugar assimilation in whitebellied sunbirds was >99%, irrespective of diet concentration and temperature. A chemical reactor model of digestive capacity based on measurements of intestinal hydrolytic capacity mostly underestimated the maximal food intake of whitebellied sunbirds in the cold, but predicted higher maximal intake for amethyst sunbirds than observed on most diet concentrations. 6. We conclude that physiological constraints impose upper limits on compensatory feeding in sunbirds. These constraints are mainly digestive at low temperature and osmoregulatory on dilute diets, while the combination of both stresses leads to additional metabolic costs. 7. The moderate mass loss of both species when exposed to these energy challenges suggests that behavioural changes and ⁄ or hypothermia may be used to reduce energy expenditure.