es transport from storage sites to working muscles difficult. Birds have a suite of adaptations in lipid mobilization and oxidation that allow them to utilize fat at roughly 10 times the capacity of mammals. During migration, these capabilities are further enhanced, allowing for a high degree of efficiency in fat utilization and storage. For example, several studies have shown that migrating birds have increased levels of lipid transport proteins, which move fat from subcutaneous stores to muscle. During premigratory fattening and during refueling at stopover sites, evidence suggests that birds select food sources with higher fat content, particularly unsaturated fats that are used more efficiently, as a form of “natural doping.” Several research groups are currently investigating how general this behavior is among migratory birds, as well as the nuts and bolts of burning different types of fat during flight.
All long-distance migrants, whether flying by day or night, must cope with energetic demands. Diurnal birds that migrate nocturnally, however, must regulate these physiological changes in accordance with the reorganization of their circadian rhythms. A circadian clock in every animal controls food acquisition and energy utilization. These clocks are intertwined with metabolic pathways in a complex fashion at the cellular level. The molecular circadian clock is a negative feedback loop constructed of so-called clock genes and clock proteins, detailed in the sidebar on the opposite page.
The network of interactions between the molecular clock and metabolic hormones is extremely complex. The links between lipid metabolism and the molecular clock are the subject of intense research because of their implications for the causes of metabolic disorders in humans. Recent evidence also points to an important role of the liver clock in regulating metabolism during avian migration, which is not surprising, given that migratory birds without pathological effects remarkably resemble humans with metabolic disorders known to be associated with changes in the liver.
In a recent study by one of us (Bartell) on blackcaps (Sylvia atricapilla) exhibiting Zugunruhe, the liver circadian clock fundamentally changes. In particular, timing of molecular clock components is altered, and the rhythms of many clock proteins fluctuate between higher maxima and lower minima. The circadian clock in the liver becomes stronger and more dominant as greater emphasis is placed on metabolism for flight as opposed to other behaviors or physiological processes. This study was conducted using birds that spontaneously exhibited Zugunruhe under constant day length, indicating that the changes in the liver clock are brought about by internal circannual cues. Because birds exhibiting migratory behavior do not eat at night, the changes in the liver clock and in liver metabolic pathway regulation are not due to differences in feeding time or to differences in the nutrient content of their food.
In migrating birds, feeding remains a daytime activity, but energy-requiring flight switches to nighttime. Very few studies consider such time-of-day effects, and instead focus on global changes in metabolism associated with migration. The study on blackcaps exhibiting Zugunruhe mentioned above suggests that during the day, the clock in the liver primes the bird’s body for more efficient nocturnal flight by inducing increases in PPARγ (see Sidebar: Circadian Regulation of Fat Metabolism, above left). Conversely, during the night, the liver clock ramps up the energy-burning process to power flight by inducing increases in PPARα. Thus, the birds’ circadian and circannual clocks are integral components to their extreme migratory physiology and behavior, referred to as migratory syndrome.
These experiments underscore the complex relationship between the circadian clock, fat metabolism and migration. We don’t yet fully understand this system or how it changes during migration. Clearly, an internal circannual clock controls seasonal changes in both fatty acid metabolism and the l