Avian Migration: The Ultimate Red-Eye Flight
Birds that migrate at night enter a state of sleepless mania and gorge on foods by day, behaviors mediated by their biological clocks
Why Fly by Night?
Why do so many species of diurnal birds migrate at night? Humans, another typically day-active species, take red-eye flights because they offer certain advantages. Red-eye tickets are cheaper, the crowds are smaller and the flight schedule allows the maximal amount of time spent at a destination. A recent study by Guy Beauchamp at University of Montreal compared diurnal and nocturnal migration in all North American bird species to identify factors associated with daily migration. The results suggest that daytime travel is beneficial for highly social species that travel in large flocks and rely on visual cues to stick together. Advantages proposed for nocturnal migration include predator avoidance, minimized thermal stress, reduced evaporative water loss and lower energetic costs due to decreased air turbulence. These benefits are thought to be proportionally greater in smaller birds, and indeed, most small avian species migrate at night. In addition, flying at night frees up daylight hours for foraging.
Energy, Metabolism and Clocks
Migration is analogous to an extreme endurance sport, but even the most impressive human athletic endeavors pale in comparison to bird migration. The Badwater Ultramarathon, one of the most extreme endurance races, covering 135 miles from Death Valley to Mt. Whitney, is nominal in light of the migration of the bar-tailed godwit (Limosa lapponica), which makes a nonstop, eight-day journey of 6,800 miles. To be fair, more energy is expended moving a unit of mass by running than by flying the same distance. Nevertheless, birds are hardly loafing. Aerobically speaking, flight is high-intensity exercise requiring 70 to 90 percent of their maximal aerobic capacity. Unlike human endurance athletes, birds have no access to external sources of water, electrolytes or food during exercise. Humans need external fuel sources during long-term, high-intensity exercise because mammals preferentially burn carbohydrates to provide energy, and these reserves are rapidly used up. The body switches to a lipid fuel source after carbohydrate stores are depleted, but the fat-burning process is inefficient, limiting our ability to exercise continuously even if we have excess fat to burn. In contrast, migrating birds preferentially use fat for energy, and each bird bulks up before its long flight.
The accumulation and internal storage of fuel is necessary for long-distance avian migration. Songbirds double their body mass to prepare for migration, mostly due to increased subcutaneous fat stores. Premigratory fattening is controlled by a circannual timer in many species. Photoperiod and food availability also serve as cues to stimulate fattening. In some species, a change in metabolic efficiency prompts fat accumulation, even without increased food intake. For the most part, however, seasonal changes in appetite and satiety lead to increased food intake, accounting for a significant amount of the body mass in many species. The hypothalamic region of the brain controls appetite and satiety, and seasonal increases in neurotransmitters in the hypothalamus (for example, one called neuropeptide Y) are associated with seasonal hyperphagia in birds.
In mammals, a major signal for satiety, which basically indicates, “Stop eating, you’re full,” is a hormone called leptin. This hormone may be involved in seasonal changes in eating, fat storage and lipid utilization in migratory birds. Strangely, the gene that encodes leptin is absent from the avian genome. However, research from Christopher Guglielmo at University of Western Ontario shows that birds are responsive to leptin: They possess a functional receptor for the hormone, and injecting leptin has dramatic effects on their metabolism. Do birds make use of a signal other than leptin that serves to indicate the levels of fat stores? The answer is probably yes. One candidate is adiponectin, 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 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 liver clock, and these changes are associated with migratory state. Further work is needed to unravel the causal relationships.