SUMMARYNorthern cardinals (Cardinalis cardinalis) are faced with energetically expensive seasonal challenges that must be met to ensure survival, including thermoregulation in winter and reproductive activities in summer. Contrary to predictions of life history theory that suggest breeding metabolic rate should be the apex of energetic effort, winter metabolism exceeds that during breeding in several temperate resident bird species. By examining whole-animal, tissue and cellular function, we ask whether seasonal acclimatization is accomplished by coordinated phenotypic plasticity of metabolic systems. We measured summit metabolism (V O2,sum ), daily energy expenditure (DEE) and muscle oxidative capacity under both winter (December to January) and breeding (May to June) conditions. We hypothesize that: (1) rates of energy utilization will be highest in the winter, contrary to predictions based on life history theory, and (2) acclimatization of metabolism will occur at multiple levels of organization such that birds operate with a similar metabolic ceiling during different seasons. We measured field metabolic rates using heart rate telemetry and report the first daily patterns in avian field metabolic rate. Patterns of daily energy use differed seasonally, primarily as birds maintain high metabolic rates throughout the winter daylight hours. We found that DEE and V O2,sum were significantly greater and DEE occurred at a higher fraction of maximum metabolic capacity during winter, indicating an elevation of the metabolic ceiling. Surprisingly, there were no significant differences in mass or oxidative capacity of skeletal muscle. These data, highlighting the importance of examining energetic responses to seasonal challenges at multiple levels, clearly reject life history predictions that breeding is the primary energetic challenge for temperate zone residents. Further, they indicate that metabolic ceilings are seasonally flexible as metabolic effort during winter thermoregulation exceeds that of breeding. Supplementary material available online at

The annual cycle of a migrating bird involves metabolically distinct stages of substantial fatty acid storage and periods of increased fatty acid mobilization and utilization, and thus requires a great deal of phenotypic flexibility. Specific mechanisms directing stage transitions of lipid metabolism in migrants are largely unknown. This study characterized the role of the PPARs ( peroxisome proliferatoractivated receptors) in regulating migratory adiposity of the gray catbird (Dumetella carolinensis). Catbirds increased adipose storage during spring and autumn migration and showed increased rates of basal lipolysis during migration and tropical overwintering. Expression of the PPAR target genes involved in fat uptake and storage, FABPpm and PLIN3, increased during pre-migratory fattening. We found significant correlation between PPARγ and target gene expression in adipose but little evidence that PPARα expression levels drive metabolic regulation in liver during the migratory cycle.

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Phenotypic flexibility across the annual cycle allows birds to adjust to fluctuating ecological demands. Varying energetic demands associated with time of year have been demonstrated to drive metabolic and muscle plasticity in birds, but it remains unclear what molecular mechanisms control this flexibility. We sampled gray catbirds at five stages across their annual cycle: tropical overwintering (January), northward spring (late) migration (early May), breeding (mid June), the fall pre-migratory period (early August) and southward fall (early) migration (end September). Across the catbird's annual cycle, cold-induced metabolic rate (V O2summit) was highest during migration and lowest during tropical wintering. Flight muscles exhibited significant hypertrophy and/or hyperplasia during fall migratory periods compared with breeding and the fall pre-migratory period. Changes in heart mass were driven by the tropical wintering stage, when heart mass was lowest. Mitochondrial content of the heart and pectoralis remained constant across the annual cycle as quantified by aerobic enzyme activities (CS, CCO), as did lipid catabolic capacity (HOAD). In the pectoralis, transcription factors PPARα, PPARδ and ERRβ, coactivators PGC-1α and β, and genes encoding proteins associated with fat uptake (FABPpm, Plin3) were unexpectedly upregulated in the tropical wintering stage, whereas those involved in fatty acid oxidation (ATGL, LPL, MCAD) were downregulated, suggesting a preference for fat storage over utilization. Transcription factors and coactivators were synchronously upregulated during pre-migration and fall migration periods in the pectoralis but not the heart, suggesting that these pathways are important in preparation for and during early migration to initiate changes to phenotypes that facilitate long-distance migration.