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Carbon turnover differs between tissues within an animal, but the extent to which ecologically relevant increases in metabolism affect carbon turnover rates is largely unknown. We tested the energy expenditure and protein turnover hypotheses that predict increased carbon turnover, either in association with increased daily energy expenditure, or in concert with tissue-specific increased protein metabolism. We used stable-isotope-labeled diets to quantify the rate of carbon turnover in 12 different tissues for three groups of zebra finches (Taeniopygia guttata): cold-exposed birds kept at ambient temperatures below their thermoneutral zone, exercised birds that were flown for 2 h per day in a flight arena, and control birds that were kept at ambient temperatures within their thermoneutral zone and that were not exercised. We found that increases in metabolism associated with cold-exposure but not exercise produced measurable increases in carbon turnover rate of, on average, 2.4±0.3 days for pectoral muscle, gizzard, pancreas and heart, even though daily energy intake was similar for exercised and cold-exposed birds. This evidence does not support the energy expenditure hypothesis, and we invoke two physiological processes related to protein metabolism that can explain these treatment effects: organ mass increase and tissue-specific increase in activity. Such changes in carbon turnover rate associated with cold temperatures translate into substantial variation in the estimated time window for which resource use is estimated and this has important ecological relevance.