ectin, another hormone that, like leptin, is produced by adipose cells that make up body fat. This hormone exerts effects on metabolic activity via two different adiponectin receptors. Adiponectin promotes glucose and fatty acid mobilization and metabolism, so levels of this molecule are usually higher in lean animals. Like numerous other metabolic factors, adiponectin is rhythmically expressed in a circadian manner (see Figure 8, below). Work from our laboratory shows that when white-throated sparrows (Zonotrichia albicollis) migrate, peak levels of adiponectin are shifted from daytime to nighttime. Furthermore, adiponectin receptors in the liver of migrating birds increase in abundance during the night. Changing the adiponectin rhythm, in combination with increased levels of the receptors, promotes energy utilization during the night when birds are flying.
The initiation and duration of the fattening period is correlated with migration distance: The longer the migratory route, the more fat birds amass. How are they even able to get off the ground? The gain in body mass is partially offset by a premigratory reduction in digestive organ sizes, and bulking up flight muscles helps power the extra load. Still, the body condition of a premigratory bird is in stark contrast to the human athlete preparing for extended physical activity, for whom excess weight is undesirable. The premigratory increase in body mass, body-fat percentage, and levels of glucose and lipids in blood plasma are hallmarks of human obesity and metabolic syndrome, the constellation of metabolic imbalances associated with increased risk of diabetes and cardiovascular disease. By human standards, premigratory birds are obese, diabetic and likely to drop dead of a heart attack at any moment. However, unlike mammals, birds are exceptionally good at burning fat for energy, and their bodies are extremely resistant to metabolic disorders.
Fat provides the greatest energy per unit mass, making it an ideal fuel for flying animals. But its insolubility makes 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 t